Time-course transcriptomics analysis reveals key responses ...€¦ · energy and then resume...

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Time-course transcriptomics analysis reveals key responses of 2

submerged deepwater rice to flooding 3

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Short title: Transcriptomics of deepwater rice 6

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All author names and affiliations 8

Anzu Minami1, Kenji Yano1, Rico Gamuyao1, Keisuke Nagai1, Takeshi Kuroha1, Madoka 9

Ayano1, Masanari Nakamori1, Masaya Koike1, Yuma Kondo1, Yoko Niimi1, Keiko 10

Kuwata2, Takamasa Suzuki3,4, Tetsuya Higashiyama3,4,5, Yumiko Takebayashi6, Mikiko 11

Kojima6, Hitoshi Sakakibara 6, 7, Atsushi Toyoda8, Asao Fujiyama8, Nori Kurata9, 12

Motoyuki Ashikari1 and Stefan Reuscher1 13

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1 Bioscience and Biotechnology Center, Nagoya University, Furo-cho, Chikusa-ku, 15

Nagoya, Aichi 464-8601, Japan 16

2 Institute of Transformative Bio-Molecules (WPI-ITbM), Nagoya University, Furo-cho, 17

Chikusa-ku, Nagoya, Aichi 464-8602, Japan 18

3 Graduate School of Science, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi 19

464-8602, Japan 20

4 ERATO Higashiyama Live-Holonics Project, Nagoya University, Furo-cho, Chikusa-ku, 21

Nagoya, Aichi 464-8602, Japan 22

5 Institute of Transformative Bio-Molecules (WPI-ITbM), Nagoya University, Furo-cho, 23

Chikusa-ku, Nagoya 464-8601, Japan 24

Plant Physiology Preview. Published on February 23, 2018, as DOI:10.1104/pp.17.00858

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6 RIKEN Center for Sustainable Resource Science, 1-7-22 Suehiro-cho, Tsurumi-ku, 25

Yokohama, 230-0045, Japan 26

7 Graduate School of Bioagricultural Sciences, Nagoya University, Furo-cho, Chikusa-27

ku, Nagoya, Aichi 464-8601, Japan 28

8 Center for Information Biology, National Institute of Genetics, Mishima, 411-8540, 29

Japan 30

9 Genetic Strains Research Center, National Institute of Genetics, Mishima, 411-8540, 31

Japan 32

Corresponding authors’ details 33

Anzu Minami: Bioscience and Biotechnology Center, Nagoya University, Furo-cho, 34


Stefan Reuscher: Bioscience and Biotechnology Center, Nagoya University, Furo-cho, 36


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One sentence summary 39

Comparative transcriptomics and targeted analyses provide insights into the roles of 40

phytohormone synthesis, signaling and turnover during submergence-induced internode 41

elongation in deepwater rice. 42

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Author contributions 44

A.M., M.ASHIKARI and S.R. designed this work and wrote the manuscript. A.M. 45

prepared all plant materials, made cDNA libraries and performed physiological 46

experiments. A.M., K.N., T.K., M.AYANO, M.N, M.KOIKE, Y.K. and Y.N. isolated RNA. 47



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T.S. and T.H. performed transcriptome sequencing and S.R. analyzed the data. A.M. 48

and K.Y. performed additional data analysis. A.T., A.F. and N.K. provided C9285 49

genomic sequence data and S.R performed C9285 genome targeted de novo assembly. 50

K.Y. performed promoter element enrichment analysis. K.K. carried out proteomics 51

analysis. Y.T., M.KOJIMA. and H.S. analyzed hormone concentrations. R.G. provided 52

many critical suggestions, did final editing and proofreading of the manuscript. 53

54

Funding information 55

This work was supported by JST Core Research for Evolutional Science and 56

Technology, a MEXT Grant-in-Aid for Scientific Research on Innovative Areas 57

(22119007 and 17H06473) and JICA-JST SATREPS, by JSPS Grand-in Aid for Young 58

Scientists (B) Grant Number 17K15136 to A.M. and by a JST ERATO Grant 59

(JPMJER1004) to T.H. 60

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Present addresses 63

Kenji Yano: Faculty of Agriculture, Tokyo University, 1-1-1 Yayoi, Bunkyo, 113-8657 64

Tokyo, Japan 65

Rico Gamuyao: Department of Ophthalmology, Johns Hopkins University School of 66

Medicine, Baltimore, MD 21287, USA 67

Takeshi Kuroha: Department of Developmental Biology and Neurosciences, Graduate 68

School of Life Sciences, Tohoku University, Sendai 980-8578, Japan 69



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Takamasa Suzuki: College of Bioscience and Biotechnology, Chubu University, 70

Matsumoto-cho, Kasugai, Aichi, 478-8501, Japan 71

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Corresponding author email 73

Anzu Minami: [email protected] 74

Stefan Reuscher: [email protected] 75

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ABSTRACT 78 79

Water submergence is an environmental factor that limits plant growth and survival. 80

Deepwater rice (Oryza sativa) adapts to submergence by rapidly elongating its 81

internodes and thereby maintaining its leaves above the water surface. We performed a 82

comparative RNA sequencing transcriptome analysis of the shoot base region, including 83

basal nodes, internodes and shoot apices of seedlings at two developmental stages 84

from two varieties with contrasting deepwater growth responses. A transcriptomic 85

comparison between deepwater rice C9285 and non-deepwater rice Taichung 65 86

revealed both similar and differential expression patterns between the two genotypes 87

during submergence. The expression of genes related to gibberellin biosynthesis, 88

trehalose biosynthesis, anaerobic fermentation, cell wall modification and transcription 89

factors that include ethylene-responsive factors was significantly different between the 90

varieties. Interestingly, in both varieties the jasmonic acid content at the shoot base 91

decreased during submergence, while exogenous jasmonic acid inhibited 92

submergence-induced internode elongation in C9285, suggesting that jasmonic acid 93

plays a role in the submergence response of rice. Furthermore, a targeted de novo 94

transcript assembly revealed transcripts that were specific to C9285, including 95

submergence-induced biotic stress-related genes. Our multifaceted transcriptome 96

approach using the rice shoot base region illustrates a differential response to 97

submergence between deepwater and non-deepwater rice. Jasmonic acid metabolism 98

appears to participate in the submergence-mediated internode elongation response of 99

deepwater rice. 100

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INTRODUCTION 102

103 Submergence stress is harmful to plants. In addition to causing O2- and CO2-deficient 104

conditions by restricting environmental gas exchange, submergence reduces the light 105

available for photosynthesis, perturbs cellular energy generation and disrupts ionic 106

balance (Bailey-Serres and Voesenek, 2008; Bailey-Serres and Voesenek; Voesenek 107

and Bailey-Serres, 2015). The mechanism of the submergence response has been well-108

studied using rice (Oryza sativa), two diverging Rumex species (R. acetosa and R. 109

palustris) and Arabidopsis thaliana, and several global analyses using transcriptomic or 110

metabolomic approaches to examine submergence or hypoxia/anoxia stress have been 111

reported (Lasanthi-Kudahettige et al., 2007; Magneschi and Perata, 2009; Narsai et al., 112

2009; Mustroph et al. 2009, 2010; Lakshmanan et al., 2013; van Veen et al., 2013; 113

Narsai et al., 2015; Rivera-Contreras et al., 2016). 114

Rice is the most important staple crop in Asia and water availability is a crucial 115

factor for rice cultivation. In tropical Southeast Asia, rice is produced in paddy fields with 116

water-controlling irrigation systems using rivers, lakes, ponds and swamps. However, in 117

some parts of South and Southeast Asia, such as Bangladesh, India, Thailand, Vietnam, 118

and Cambodia, the paddy fields are frequently submerged during the rainy season. The 119

general cultivated rice cannot survive in these submergence-prone areas, but some 120

cultivars such as floating or deepwater rice can grow and survive in such conditions 121

even under several month-long periods of deep flooding. 122

The adaptation of plants to submergence stress involves two different opposing 123

mechanisms, the ‘quiescence strategy (e.g. Rice SUB1 varieties, Arabidopsis ecotypes, 124

Rumex acetosa)’ and ‘escape strategy (e.g. deepwater/floating rice varieties, Rumex 125



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palustris)’ (Jackson, 2008; Bailey-Serres et al. 2012; Loreti et al., 2016). Submergence-126

tolerant rice such as FR13A survives flooded conditions for a few weeks through the 127

‘quiescence strategy’ wherein the plants temporarily cease shoot elongation to conserve 128

energy and then resume growth when the water recedes. Quantitative trait loci (QTL) 129

mapping revealed that the SUBMERGENCE1 (SUB1) locus regulates the ‘quiescence 130

strategy’ (Xu et al., 2006; Fukao et al., 2006). The SUB1 locus on chromosome 9 131

contains a cluster of three group VII ethylene response factor (ERF) genes (SUB1A, 132

SUB1B and SUB1C) and the presence of the SUB1A-1 allele restricts underwater shoot 133

growth and confers submergence tolerance. SUB1A-1 suppresses ethylene production, 134

leading to the suppression of gibberellin (GA) synthesis and GA responsiveness 135

mediated by the negative regulators in GA signaling, SLENDER RICE-1 (SLR1) and 136

SLR like-1 (SLRL1) (Fukao et al., 2006; Fukao and Bailey-Serres, 2008). Moreover, 137

SUB1A-1 activates the expression of various genes, including other ERF genes and 138

genes encoding transcription factors, reactive oxygen species scavengers, and 139

enzymes involved in brassinosteroid synthesis and several metabolic pathways 140

facilitating survival during the quiescent period (Fukao et al., 2006, Fukao et al., 2011; 141

Jung et al., 2010; Schmitz et al., 2013; Tamang and Fukao, 2015). 142

Conversely, the ‘escape strategy’ involves stem elongation to keep the leaves 143

above the water surface. This typically involves metabolic activation and the 144

mobilization of energy reserves to drive elongation growth (Figure 1A). Utilizing this 145

strategy, deepwater rice rapidly elongates its internodes (~20 to 25 cm per day) and 146

reaches a length of several meters in deep water (Catling, 1992; Kende et al., 1998). 147

The deepwater rice cultivar C9285 from Bangladesh belongs to the Japonica varietal 148



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group (Wang et al. 2013) and shows strong internode elongation in response to 149

submergence (Hattori et al., 2009). Our previous QTL mapping showed that the 150

submergence-induced elongation in C9285 is caused by three major QTLs located on 151

chromosomes 1, 3 and 12 and two minor QTL on chromosome 2 and 4 (Hattori et al., 152

2009, Nagai et al. 2012). The major QTL on chromosome 12 contains the two ERF 153

family genes named SNORKEL1 and SNORKEL2 (SK1/2) which are positive regulators 154

of internode elongation. During submergence, the gaseous hormone ethylene 155

accumulates, triggering SK1/2 gene expression in C9285. Although the downstream 156

factors directly regulated by SK1/2 are still unknown, it is clearly established that 157

internode elongation in deepwater rice requires active GA biosynthesis (Ayano et al, 158

2014; Nagai et al., 2014). 159

Both the underwater ‘quiescence strategy’ and ‘escape strategy’ involve ethylene 160

signaling and regulation by strategy-specific group VII ERFs (ERF-VII): SUB1A limits 161

stem elongation underwater whereas SK1/2 promotes the submergence-induced 162

elongation. The molecular mechanisms of SUB1A-mediated ‘quiescence strategy’ have 163

been well-studied (Bailey-Serres, 2010; Voesenek and Bailey-Serres, 2015) and SUB1-164

related gene expression profiles during submergence have been analyzed (Jung et al., 165

2010, Fukao et al., 2011). However, there is little information about the responses of 166

deepwater rice under the ‘escape strategy’. In this study, we explored the transcriptional 167

responses to submergence of the deepwater rice cultivar C9285. We aimed to compare 168

the transcriptional responses associated with phytohormone signaling, regulation of 169

gene expression and energy metabolism following submergence of two contrasting rice 170

varieties (deepwater and non-deepwater rice) at different leaf developmental stages to 171



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better understand the mechanism involved in the ‘escape strategy’. Our findings expose 172

temporal and genotype-specific responses to submergence and implicate a role for 173

jasmonic acid (JA) catabolism in the pronounced submergence-induced internode 174

elongation of deepwater rice. 175

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RESULTS 177

178

Transcriptome profiles of deepwater rice and non-deepwater rice plants exposed 179

to submergence 180

181

To investigate the gene expression dynamics of deepwater rice in response to 182

submergence, we compared the transcriptome profiles between the deepwater rice 183

Oryza sativa cv. C9285 and non-deepwater rice Oryza sativa cv. Taichung 65 (T65) 184

(Supplemental Figure 1). The internodes of C9285 plants can elongate in response to 185

submergence once plants reach the the six-leaf stage (6LS) (Ayano et al., 2014). 186

Hence for the transcriptome analysis, C9285 and T65 plants at the 6LS were used for 187

expression profiling. We also included submerged C9285 plants at the four-leaf stage 188

(4LS), which cannot respond to submergence by elongation yet. The plants were 189

completely submerged for 0, 1, 3, 6, 12 and 24 hours (h) and we sampled the shoot 190

base region of the stem, as this region in C9285 plants rapidly elongates in response to 191

submergence. Per sample, on average 8.04 x 106 single-end reads were generated, of 192

which an average of 6.83 x 106 reads could be mapped to the transcripts annotated in 193

the Oryza sativa L. ssp. Japonica cv. Nipponbare reference genome (Kawahara et al., 194

2013). The average rates of mapped reads for C9285 and T65 samples in the 195

Nipponbare reference genome were 84.8% and 86.1%, respectively (Supplemental 196

Table 1). After quality control and filtering, we detected 27,812 expressed genes in at 197

least one sample (Supplemental Data Set 1). 198

For global comparison of the transcriptomes derived from all 18 tissue 199

samples, we performed a principal component analysis (PCA). The first two principal 200



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components (PC1 and PC2) accounted for 48% of the total variance (Figure 1B). PC1 201

accounted for 26% of all variance in the data and clearly separated the T65 samples 202

(T65 6LS) from the C9285 samples at two different stages (C9285 4LS and C9285 203

6LS). Among the T65 6LS samples, only the sample from the 24 h submergence 204

treatment showed lower PC1 values closer to the C9285 samples. PC2 (accounting for 205

22% of all variance) separated the samples based on duration of submergence 206

treatment. That is, each genotype showed higher and lower PC2 values reflecting the 207

samples submerged for shorter and longer periods, respectively. The results from the 208

PCA analysis suggest that there are different gene expression patterns between the two 209

rice genotypes dependent and independent of submergence treatment. Furthermore, 210

the expression profiles become variable depending on the duration of submergence 211

treatment but were less affected by the leaf developmental stage in C9285 plants. In 212

addition, a more targeted attempt at isolating genes specifically induced by 213

submergence at the 4LS, but not at the 6LS in C9285 plants found only 36 such genes 214

(see Supplemental Results) 215

Submergence induced expression changes for a large number of genes in 216

both genotypes (Supplemental Table 2 and Supplemental Figure 2A and 2B). To group 217

genes with similar expression profiles, we performed k-means clustering of all 27,812 218

expressed genes. We empirically chose k = 40 for k-means clusters and manually 219

grouped the clusters into four major groups; (1) higher expression in C9285 plants 220

(1,019 genes) (Supplemental Data Set 2), (2) higher expression in T65 plants (1,205 221

genes) (Supplemental Data Set 3), (3) induced expression in both C9285 and T65 222

plants (2,683 genes), and (4) repressed expression in both C9285 and T65 plants 223



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(4,125 genes), excluding clusters which contained genes with no discernable pattern of 224

expression (Figure 2A). In addition, to achieve a better separation of submergence-225

responsive genes, we next performed k-means clustering (k = 20) for each genotype 226

separately (Supplemental Data Sets 4 to 7). In C9285 samples, five (B6, B9, B11, B12 227

and B16) and four (B7, B8, B15 and B17) clusters contained submergence-induced and 228

-repressed genes, respectively (Figure 2B). A total of 2,429 genes in B6, B12 and B16 229

clusters showed the strongest expression around 12 h submergence and a total of 775 230

early responsive genes were classified into B9 and B11 clusters. In T65 samples, five 231

clusters (C1, C3, C5, C13 and C17) contained a total of 4,563 submergence-induced 232

genes and most of the genes showed relatively slow response to submergence except 233

for the 374 early responsive genes in C5 and C17 clusters (Figure 2C). In cluster C2, 234

the expression of 514 genes in T65 plants was repressed by submergence. We 235

evaluated the biological function of genes enriched in each group of clusters based on 236

the MAPMAN ontology (Thimm et al., 2004; 237

http://mapman.gabipd.org/web/guest/mapman). The hierarchical enrichment analysis of 238

MAPMAN bins of genes with higher expression in C9285 or T65 plants (P < 0.05) and 239

the data of submergence-changed genes in C9285 or T65 plants (P < 0.05) are shown 240

in Supplemental Table 3 and Supplemental Table 4, respectively (described in 241

Supplemental Results). Selected enriched MAPMAN bins were then chosen for further 242

analysis. 243

244


http://mapman.gabipd.org/web/guest/mapman)


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Different expression pattern of genes related to plant hormone biosynthesis 245

during submergence in both genotypes 246

247

Kende et al. (1998) proposed a model describing the relationship among the three 248

phytohormones ethylene, abscisic acid (ABA) and gibberellin (GA) in regulating rapid 249

internode elongation of deepwater rice. During submergence, the reduced diffusion of 250

ethylene causes its accumulation, which then triggers the ethylene signaling cascade, 251

leading to the reduction of ABA content and increase of GA content (Kende et al., 1998; 252

Fukao and Bailey-Serres, 2008). To investigate the genes related with hormone 253

biosynthesis that are regulated during submergence, we compared the expression level 254

of hormone biosynthetic genes between C9285 and T65 plants. 255

Ethylene is produced from its precursor, S-adenosylmethionine (SAM) derived 256

from the Yang cycle through two steps (Yang and Hoffman, 1984; Wang et al., 2002). 257

The first step is catalyzed by ACC synthase (ACS) converting the SAM into 1-258

aminocyclopropane-1-carboxylic acid (ACC) while the second step involves ACC 259

oxidase (ACO) which converts the ACC to ethylene (Ruduś et al. 2013) (Figure 3A). The 260

reaction catalyzed by ACS is the major rate-limiting step of ethylene biosynthesis and 261

ACO also probably becomes the rate-limiting enzyme at low oxygen and high ethylene 262

conditions (Yang and Hoffman, 1984, Kende, 1993). Rice has six putative ACS 263

(OsACS1-6) genes (Rzewuski and Sauter, 2008), but only OsACS6 expression was 264

detected in our dataset showing a similar expression pattern during submergence in 265

both genotypes. In contrast, all seven rice ACO transcripts [OsACO1-7 in Rzewuski and 266

Sauter (2008)] were detected. In both genotypes OsACO1, 2, 3 and 7 showed 267

moderate-to-high expression levels while OsACO4, 5 and 6 were expressed only at 268



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very low levels. OsACO7 was markedly induced by submergence in both genotypes, 269

showing slightly higher expression in C9285 than in T65. The expression profile of 270

genes involved in ethylene signaling were mostly similar in both C9285 and T65 plants 271

(Supplemental Figure 3A), which coincides with the similar increased levels of ethylene 272

during submergence in both genotypes (Hattori et al., 2009). 273

GA is the key hormone for submergence-induced stem elongation and 274

particularly the concentration of bioactive GA1 and GA4 increases in submerged C9285 275

plants (Hattori et al., 2009). GA biosynthesis starts from the conversion of trans-geranyl-276

geranyl diphosphate (GGDP) followed by four enzymatic steps to generate GA12 (Figure 277

3B) (Richards et al., 2001; Yamaguchi, 2008). In the later biosynthetic steps, the 278

conversion of GA12 to GA53 is catalyzed by GA13 oxidase (GA13ox) (Magome et al., 279

2013), and both GA12 and GA53 are catalyzed through two parallel pathways (the early–280

13-hydroxylation (13-OH) and non-13-OH pathways) by GA20 oxidase (GA20ox). 281

GA20ox catalyzes the conversion of GA12 and GA53 into the bioactive GA precursors 282

GA9 and GA20, respectively. Finally, GA3 oxidase (GA3ox) converts GA9 and GA20 into 283

the bioactive GA forms GA4 and GA1. The expression pattern of genes encoding the 284

enzymes before the catalytic step of GA13ox was not prominently different between 285

C9285 and T65 plants. GA20ox is the key enzyme of bioactive GA synthesis and rice 286

has four putative GA20ox genes (OsGA20ox1 to 4) (Sakamoto et al., 2004). The 287

transcripts of three OsGA20ox genes were detected in our dataset and only one of the 288

OsGA20ox genes, OsGA20ox2, was strongly expressed 1 h after submergence (>15-289

fold increase) in C9285 (Figure 3B). On the other hand, in T65, the expression level of 290

OsGA20ox2 was considerably lower (1.5 cpm in T65 vs. 72 cpm in C9285 1 h after 291



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submergence). OsGA20ox1 and OsGA20ox4 were expressed at low levels (less than 292

2.5 cpm) in both genotypes during submergence. Among the two GA3ox genes in rice, 293

only OsGA3ox2 expression was detected in both genotypes, showing a slight increase 294

after submergence. GA is inactivated by GA2ox and CYP714D1/EUI1 enzymes 295

(Sakamoto et al., 2004, Zhu et al., 2006). Among the eleven putative OsGA2ox genes in 296

rice, the expression of eight OsGA2ox was detected and the expression patterns were 297

mostly similar between the two genotypes. In our data, the expression of 298

CYP714D1/EUI1, which inactivates GA12, GA9 and GA4, could not be detected. We also 299

investigated the expression profiles of GA signaling-related genes during submergence 300

and found that SLENDER RICE-LIKE 1 (SLRL1) is expressed after submergence in 301

both genotypes, although SLENDER1 (SLR1) was not induced by submergence 302

(Supplemental Figure 3B). However, the results remain elusive because GA 303

homeostasis tightly interacts with GA metabolism and GA signaling pathways, which are 304

controlled by feed-back and feed-forward regulations and various environmental factors 305

(Sun, 2011; Hedden, 2012). 306

ABA is a negative regulator of stem elongation during submergence 307

corresponding with the decrease of ABA content in both submerged genotypes (Hattori 308

et al., 2009, Hoffmann-Benning and Kende, 1992). In higher plants, the ABA precursor 309

β-carotene is synthesized from isopentenyl pyrophosphate through the plastidial 310

methylerythritol phosphate pathway (Endo et al., 2014). β-carotene is catalyzed by 311

several enzymes and eventually converted into ABA (Figure 3C). The 9-cis-312

epoxycarotenoid dioxygenase (NCED) is a rate-limiting enzyme in ABA biosynthesis 313

and, in rice, NCED is putatively encoded by five genes (OsNCED1 to 5) (Zhu et al., 314



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2009). OsNCED1, 2 and 5 genes were detected in our dataset and the expression of 315

OsNCED2 reduced in both genotypes 1 h after submergence. Additionally, in the rice 316

genome, there are three genes that encode the ABA inactivating enzyme, ABA 8’-317

hydroxylase (ABA8ox). In our data, the OsABA8ox1 and 2 genes in both genotypes 318

showed transiently increased expression after 1 h submergence. The genes involved in 319

ABA signaling were similar expressed in both C9285 and T65 plants (Supplemental 320

Figure 3C). 321

Hoffman-Benning and Kende (1992) showed that ABA negatively regulates 322

GA-mediated stem elongation by experiments with excised stem sections of the 323

deepwater rice variety Habiganj Aman II. To test the effect of ABA on the GA activity in 324

whole plants, C9285 plants were grown from seeds for 18 days in shallow water 325

containing either GA3, ABA or a combination of both GA3 and ABA. Treatment with GA3 326

increased the total plant height and internode length compared to untreated plants 327

(Figure 3D). While treatment with ABA alone had no observable effect, treatment with 328

combined ABA and GA3 reduced the GA-induced elongation of C9285 plants. 329

Jasmonic acids (JAs) control plant growth, development and responses to 330

abiotic and biotic stresses. JAs are derived from α-linolenic acid (LA), which is released 331

from galactolipids of chloroplast membranes by fatty acid desaturase (FAD) and 332

phospholipase A1 (PLA1) including defective in anther dehiscence1 (DAD1) 333

(Wasternack and Hause, 2013) (Figure 4A). LA is converted to 3-oxo-2-(2’-pentenyl)-334

cyclopentane-1-octanoic acid (OPC-8) through the action of several enzymes including 335

lipoxygenase (LOX), allene oxide synthase (AOS), allene oxide cyclase (AOC) and 12-336

oxo-phytodienoic acid reductase3 (OPR3). After the three steps of β-oxidation, OPC-8 337



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is converted into jasmonoyl-CoA (JA-CoA) and then cleaved to (+)-7-iso-jasmonoyl [(+)-338

7-iso-JA] by thioesterase. Finally, (+)-7-iso-jasmonoyl-isoleucine (JA-IIe), which is a 339

ligand binding a co-receptor of JA receptors, is catalyzed by jasmonate resistant1 340

(JAR1) in the cytosol. Through the activity of the members of the CYP94 family, JA-IIe is 341

inactivated through hydroxylation. The putative JA-inactivating CYP94C4 gene showed 342

higher expression during submergence compared to before submergence in both 343

genotypes. In addition, endogenous JA levels decreased after 24 h of submergence in 344

both genotypes (Figure 4B). To examine the effect of JA on the submergence response, 345

we submerged C9285 plants in water containing 50 µM methyl-jasmonate and 346

measured the total internode length after three days of treatment (Figure 4C). 347

Surprisingly, treatment with JA remarkably inhibited the submergence-induced internode 348

elongation. 349

350

Deepwater treatment has genotype-specific effects on trehalose metabolism and 351

fermentation-related pathways 352

353

We further investigated the expression of genes in other relevant pathways to 354

understand the metabolic adaptation of deepwater rice under submergence. 355

Comparative analysis of metabolic pathways using the MAPMAN software showed that 356

genes related to the metabolism of trehalose (Supplemental Figure 4A) and 357

fermentation (Supplemental Figure 4B) were induced in response to 1 h submergence 358

in C9285 plants. Expression of genes in the NO3-generating pathway (Supplemental 359

Figure 4C) was also up-regulated after submergence, but their absolute expression was 360

at very low levels. 361



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362

Trehalose is a disaccharide that functions in carbon metabolism and tolerance 363

to biotic and abiotic stresses (Lunn et al., 2014). In plants, trehalose is synthesized in a 364

two-step process from UDP-glucose (UDPG) and glucose-6-phosphate （Glu6P） by the 365

subsequent actions of trehalose-6-phosphate synthases (TPS) and trehalose-6-366

phosphate phosphatases (TPP) and the degradation of trehalose is catalyzed by 367

trehalase (TRE) (Figure 5A, Ponnu et al., 2011). In our dataset, we detected the 368

expression of trehalose metabolism-related genes including 13 TPS (out of 14), 7 TPP 369

(out of 13) and one TRE (Ge et al., 2008). Some TPS genes clearly responded to 370

submergence in C9285 plants. Notably, three TPS genes (OsTPS12, OsTPS13, 371

OsTPS14) were strongly induced in response to submergence in C9285 plants but not 372

in T65 plants (Figure 5B). OsTPP1 and OsTPP11 showed elevated expression in 373

response to submergence in C9285 plants while OsTPP2 expression was induced at a 374

relatively low level in T65 after submergence (Figure 5C). In the case of TRE, the 375

expression pattern was similar in both genotypes (Figure 5D). 376

Under anaerobic conditions, oxygen is limited for aerobic respiration and plant 377

cells implement anaerobic respiration (glycolysis and fermentation) for energy 378

production instead (Perata et al., 1998; Fukao and Bailey-Serres, 2004, Bailey-Serres 379

and Vosencnek, 2008; Miro and Ismail, 2013). The glycolysis pathway generates ATP 380

and the following fermentation steps produce NAD+ for maintenance of glycolysis and 381

some metabolites. Fermentation converts the glycolysis-derived pyruvate into other 382

metabolites such as alanine, lactate, ethanol and acetate (Figure 6A). Alanine is 383

synthesized from pyruvate and glutamate by the alanine aminotransferase (AlaAT) while 384



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lactate is formed by the reduction of pyruvate via lactate dehydrogenase (LDH). 385

Pyruvate decarboxylase (PDC) converts pyruvate to acetaldehyde. To detoxify 386

acetaldehyde, alcohol dehydrogenase (ADH) or acetaldehyde dehydrogenase (ALDH) 387

subsequently catalyzes the conversion of acetaldehyde to ethanol or acetate, 388

respectively. Interestingly, we found that the two LDH genes (LDH-A and LDH-B) were 389

strongly and specifically induced 1 h after submergence in C9285 but not in T65 plants 390

(Figure 6B). Among other fermentation-related genes, the OsAlaAT1, OsPDC1, 2 and 3, 391

Os05g0469800, OsADH1 and 2, and OsALDH2a appeared to increase after 392

submergence in both genotypes whereas the genes in ALDH1 family seemed to show 393

variable expression pattern during submergence. 394

395

Submergence induces differential expression profiles of genes related to cell wall 396

formation between C9285 and T65 plants 397

398

Under the non-submerged condition, genes related with cell wall formation and 399

secondary metabolic pathways showed higher expression in C9285 plants compared to 400

T65 plants (Supplemental Figure 5A to 5D). The plant cell wall provides mechanical 401

strength, regulates growth, serves as a barrier to diffusion, and protects the plant 402

against pathogens. The cell wall-related transcripts with higher expression in C9285 403

plants encoded cell wall modification proteins α- and β-expansins (EXPAs and EXPBs), 404

xyloglucan endotransglycosylases/hydrolases (XTHs), pectin esterases (PMEs) and 405

structural cell wall proteins [fasciclin-like arabinogalactans (FLAs) and extensins] 406

(Figure 7A). In T65 plants, almost all genes responded to submergence and the 407

expression level finally reached that of C9285 within 24 h submergence. In C9285 408



20

plants, several genes were strongly induced by submergence, especially the genes 409

EXPB6, EXPB7, OsXTH23, OsXTH1 and two PMEs (Os01g0880300 and 410

Os01g0312500), three FLAs (FLA7, FLA6 and FLA2) and two extensins 411

(Os02g0138000 and Os01g0594300) remarkably responded to submergence in C9285 412

plants. 413

Under non-submerged conditions, genes involved in flavonoid, anthocyanin, 414

and phenylpropanoid metabolism, as well as in the biosynthesis of lignin and simple 415

phenols (e.g., laccases involved in lignin polymerization), were expressed higher in 416

C9285 compared to T65 (Supplemental Figure 5C). Lignin is a complex polymer of 417

monolignols and strengthens the cell wall as a component of secondary cell walls. Thus, 418

cell wall lignification probably functions in the suppression of rapid growth in deepwater 419

rice resulting in a slow rate of elongation of its stems in non-submerged conditions 420

(Sauter and Kende 1992). We investigated the transcriptional responses of lignin 421

biosynthesis-related genes to submergence and focused on genes encoding 422

coniferyl/sinapyl alcohol dehydrogenase (CAD/SAD), which catalyzes the final step of 423

monolignol biosynthesis (Supplemental Figure 6A). In C9285 plants, among the 11 424

CAD/SAD genes (out of a total of 12 genes in the genome), OsCAD1, OsCAD2, 425

OsCAD8B and OsCAD8C were highly expressed in non-submerged conditions and, 426

except for OsCAD1, showed decreased expression in response to submergence 427

(Figure 7B). The OsCAD1 showed a similar expression level in both genotypes while 428

the other CAD genes in T65 maintained lower expression levels during submergence. 429

To determine whether the decrease in expression of CAD genes affects lignin 430

biosynthesis in elongating internodes of C9285 plants, we measured the lignin content 431



21

of the C9285 stem including (1) nodes from different positions, (2) non-elongated 432

internodes (an internode that already stopped elongating) and (3) newly-elongated 433

internode (newly elongating internode during submergence) (Figure 7C). Under non-434

submerged condition, the basal node, non-elongated internode, and the 2nd and 3rd 435

nodes showed similar lignin content (Figure 7D). The total lignin content in the basal 436

and 2nd nodes did not change after 2 days of submergence (Figure 7D, 7E). On the 437

other hand, the 3rd node on the internode newly-elongated after 2 days of submergence 438

exhibited a lower lignin content (Figure 7E). The total lignin content in the non-439

elongating internode was not affected by 2 days of submergence while the content of 440

the newly-elongated internodes was lower than that of the non-elongated internode. 441

These results suggest that suppression of lignin biosynthesis through the reduction of 442

CAD transcripts contributes to the elongation of internodes in C9285 plants. In 443

agreement with this, the lignin content in the basal nodes of T65 plants did not change 444

during submergence (Supplemental Figure 6B). 445

446

Expression of ERF transcription factor genes in response to submergence 447

448

The MAPMAN overrepresentation analysis revealed that transcription factor (TF) genes 449

from the AP2/EREBP family were significantly enriched among genes induced by 450

submergence in both genotypes (Supplemental Table 4A and 4B). To investigate the 451

response of all TF genes to submergence, the genes in our dataset were categorized 452

according to the Plant Transcription Factor Database v3.0 (Oryza sativa ssp. Japonica) 453

(plantTFDB; http://planttfdb.cbi.pku.edu.cn/; Jin et al., 2014) (Supplemental Data Set 8, 454

Supplemental Figure 7 and Supplemental Results). Interestingly, those clusters 455



22

contained a total of 10 ethylene response factor (ERF) genes (Supplemental Figure 7). 456

The ERFs belong to the AP2/EREBP superfamily which is a plant-specific transcription 457

factor family with three sub-families, (1) AP2 family proteins containing two repeated 458

AP2 DNA-binding domains, (2) ERF family proteins containing a single AP2 domain and 459

(3) RAV family proteins containing a B3 DNA-binding domain and a single AP2 domain 460

(Riechmann and Meyerowitz, 1998; Sakuma et al., 2002; Nakano et al., 2006). Nakano 461

et al. (2006) divided the rice ERF family (total of 139 genes) into 15 subfamilies 462

including 28 subgroups. In our dataset, we categorized the ERF genes into these 463

subgroups. Among all TFs in our dataset, 115 were found to be ERF genes including 41, 464

10, and 64 genes with increased, decreased and unchanged expression during 465

submergence, respectively (Supplemental Table 5). The ERF genes from subgroups IIa, 466

IIIc, VIIa, VIIb, IXa, Xa, Xb, Xc and XI predominately showed an increased expression in 467

response to submergence in C9285 plants while those of subgroups IIIe and Va showed 468

decreased expression under submergence treatment. Supplemental Figure 8 shows 469

expression profiles of the submergence-induced ERF genes. The SUB1 locus encodes 470

three ERF transcription factor genes (SUB1A, 1B and 1C) (Xu et al., 2006); however, 471

the genome of C9285 contains only Sub1B and Sub1C but does not have Sub1A 472

(Hattori et al., 2009). In C9285 plants, SUB1B (OsERF#063) and SUB1C (OsERF#073) 473

increased 3.2-fold and 2.7-fold 1 h after submergence, respectively (Supplemental 474

Figure 8A). The expression of SK1 and SK2 genes, which are positive regulators of 475

internode elongation in C9285 plants and absent in T65 plants, was also remarkably 476

increased 5.3-fold and 3.2-fold by submergence, respectively (Supplemental Figure 8B). 477

478

479



23

GCC-box like promoter elements are enriched in the promoters of genes 480

specifically expressed in C9285 plants 481

482

483

Using k-means clustering, we isolated 189 genes which are specifically expressed in 484

C9285 plants (Supplemental Data Set 9). Their putative promoter regions (1 kb 485

upstream from the transcriptional start site) were constructed by aligning reads from 486

genomic DNA of C9285 plants to the Oryza sativa ssp. Japonica cv. Nipponbare 487

reference genome. The constructed promoter sequences were then analyzed for 488

enriched DNA sequence motifs using Multiple EM for Motif Elicitation (MEME) suite. We 489

found two GCC-box like elements (GCGGCGGCGG and CGCCGCCGCC) enriched in 490

sequence among the analyzed promoter sequences (Supplemental Figure 9). The 491

consensus DNA-binding motif (GCCGCC) is known to be recognized by the ERF 492

proteins (Hao et al. 1998; Fujimoto et al., 2000). 493

494

Identification and analysis of differentially expressed genes unique to 495

C9285. 496

497

Although about 85% of C9285 RNA-Seq reads could be mapped to the Nipponbare 498

reference genome (Supplemental Table 1), there is a possibility that C9285 has 499

additional genes missing in the reference genome, such as SK1 and SK2. Hence, we 500

performed a targeted de novo assembly of transcripts to detect C9285-specific 501

transcripts (Supplemental Figure 10 and Supplemental Methods). We used 47,978,704 502

paired-end reads from genomic DNA of C9285 (ca. 20x coverage) to assemble C9285-503

specific genomic regions and quantified transcripts detected in those regions using 504



24

RNA-Seq reads. We then restricted our analysis to those transcripts which are either 505

expressed at high levels, are strongly induced by submergence, or have an interesting 506

annotation. In total, 86 transcribed loci on 33 genomic contigs were found to be either 507

putatively unique to C9285 or sufficiently different from the Nipponbare reference so that 508

mapping with standard parameter failed to produce alignments (Supplemental Data 509

Sets 10, 12 to 14). 510

Among those 86 loci, two encoded the full-length SK1 and SK2 transcripts. 511

The genomic contigs that contained the SK1 (contig_21; 5,776 bp) and SK2 (contig_8; 512

12,025 bp) loci aligned almost perfectly with parts of the BAC clone that was used for 513

map-based cloning of SK1 and SK2 (Hattori et al., 2009). When we quantified the 514

expression of SK1 and SK2 genes from those contigs, we found the typical early 515

increase of transcriptional activity 1 h after submergence with subsequent decline 516

(Supplemental Figure 8B). This shows that our targeted assembly strategy was able to 517

correctly identify unique C9285 transcripts, including their genomic sequence and their 518

expression patterns. We found 11 novel transcripts that had at least two-fold higher 519

expression level after 1 h submergence (Figure 8). Except for SK1 and SK2, most of 520

those transcripts did not encode well-characterized proteins. Instead, a sequence 521

comparison using blastp reported at least six pathogen- or disease-related proteins. The 522

remaining three proteins were annotated as domain of unknown function, 523

retrotransposon-related and SAM-dependent methyl transferase. 524

525

526

527



25

528

529

DISCUSSION 530

The overall goal of this study was to understand the transcriptional responses 531

associated with the ‘escape strategy’ of the deepwater rice C9285 during submergence. 532

Cataloguing the whole transcriptome through an RNA-seq approach revealed 533

differences in gene expression between deepwater rice (C9285) and non-deepwater 534

rice (T65) plants, as well as unique and common responses to submergence in the two 535

genotypes. The results of our comprehensive transcriptome analysis contribute to the 536

finding of key genes regulating the metabolic pathways during submergence in rice. 537

538

Transcripts associated with ethylene, GA, and ABA metabolism are differentially 539

expressed in response to submergence 540

Previous studies have demonstrated that the hormones ethylene, gibberellin 541

(GA), and abscisic acid (ABA) modulate the internode elongation response of 542

submerged deepwater rice (Kende et al., 1998). Among the ethylene biosynthesis 543

genes, it is reported that OsACS1, OsACS5, and OsACO1 were increased by 544

submergence in deepwater rice (Mekhedow and Kende 1996; Zarembinski and 545

Theologis 1997; van Der Straeten et al. 2001). On the other hand, in our data, OsACO7 546

transcript and protein accumulated during submergence in both genotypes (Figure 3A, 547

Supplemental Figure 11A). Ethylene accumulation in submerged deepwater rice is 548

attributed to the decrease in ethylene diffusion and enhancement of ethylene 549

biosynthesis (Métraux and Kende (1983). Our previous study showed that ethylene 550



26

accumulation is a common occurrence in both C9285 and T65 plants (Hattori et al., 551

2009). Our transcript analysis supports that OsACO7 is involved in ethylene 552

accumulation in both genotypes during submergence. OsACO7 has not been reported 553

to participate in ethylene biosynthesis during submergence, although most previous 554

studies used non-deepwater rice varieties. 555

Under submergence condition, the accumulated ethylene enhances GA 556

accumulation for the promotion of internode elongation in deepwater rice (Métraux and 557

Kende, 1983, 1984; Raskin and Kende, 1984b; Kende et al., 1998). Interestingly, unlike 558

ethylene biosynthesis, the activation of GA biosynthesis occurs only in C9285 plants 559

(Hattori et al. 2009). In our data, OsGA20ox2 (also known as SD1) expression levels 560

were strongly and specifically induced by submergence in C9285, but not in T65 (Figure 561

3B). GA20ox2 is a key locus for GA production and its increased expression is thus 562

most likely responsible for the higher GA1 and GA4 accumulation in submerged C9285 563

plants (Supplemental Figure 12F, Hattori et al., 2009, Ayano et al., 2014). In the case of 564

the submergence-tolerant rice with SUB1A, SUB1A suppresses GA signaling through 565

accumulation of GA signaling repressors, SLR1 and SLRL1, leading to restricted 566

elongation of stems and leaves under submergence (Fukao and Bailey-Serres, 2008; 567

Colebrook et al., 2014). Thus, the absence of SUB1A in the deepwater rice C9285 may 568

explain the accumulation of bioactive GA levels promoting the elongation of stems and 569

leaves during submergence. It has been reported that the GA-induced genes, Oryza 570

sativa Growth Regulating Factor1 (OsGRF1) and a GA stimulated transcript (GAST)-like 571

gene, OsGSR1, enhance the stem elongation in rice (van der Knaap et al., 2000; Ben-572

Nissan et al., 2004; Choi et al, 2004; Wang et al., 2009). Interestingly, two GAST-like 573



27

genes (Os05g0376800 and OsGSR1) were expressed higher in C9285 plants during 574

submergence, although OsGRF1 was not induced during submergence in our dataset 575

(Supplemental Figure 11B and 11C), suggesting that the GAST-like genes may be 576

involved in GA-induced stem elongation during submergence in C9285 plants. 577

The content of ABA, which has the antagonistic effect to GA on internode 578

elongation, decreased under submergence and ethylene treatments (Hoffman-Benning 579

and Kende, 1992; Azuma et al.,1995; Benschop et al., 2006; Yang and Choi, 2006; 580

Weiss and Ori, 2007; Saika et al., 2007; Fukao and Bailey-Serres, 2008a; Hattori et al., 581

2009; Chen et al., 2010). The decrease in ABA content is a common response to 582

submergence in both T65 and C9285 plants (Hattori et al. 2009). Our data revealed that 583

transcript levels of OsNCED2, encoding one of the rate-limiting enzymes in ABA 584

biosynthesis decreased, and OsABA8ox1 and OsABA8ox2 encoding ABA inactivation 585

enzymes were up-regulated in both genotypes during submergence (Figure 3C), 586

indicating that the decrease in ABA content may be explained by the changes in 587

expression level of genes related to ABA metabolism in both genotypes. 588

589

Jasmonic acid is a novel regulatory factor associated with stem elongation in 590

deepwater rice 591

Kende et al. (1998) reported that ethylene, ABA and GA are key regulators of 592

internode elongation in deepwater rice. In this study, we demonstrated that 593

submergence regulated the endogenous jasmonic acid (JA) content in node samples of 594

rice and JA inhibited the submergence-induced internode elongation in C9285 plants 595

(Figure 4). CYP94C2b encodes a cytochrome P450 enzyme and was involved in the 596



28

inactivation of JA-Ile (Kurotani et al., 2015). Our data showed that CYP94C4, which is a 597

major expressed CYP94C gene, showed increased expression levels during 598

submergence in both genotypes. Thus, the increase in CYP94C4 might regulate the 599

decrease in endogenous JA content. The decrease in JA is a common response to 600

submergence in both genotypes, like the changes in ethylene and ABA contents during 601

submergence. The non-deepwater rice T65 at 6LS has no ability to elongate its 602

internodes even in the case of GA treatment (Nagai et al., 2014), suggesting that the 603

changes in JA contents in T65 plants does not affect the stem elongation. 604

Studies on cross-talk between JA and GA signaling pathways have shown that 605

GA antagonistically functions in JA signaling pathways involved in plant growth and 606

development processes in Arabidopsis (Hou et al., 2013, Wasternack and Hause, 607

2013). In addition, Yang et al. (2012) showed that JA-mediated growth inhibition in rice 608

was caused by changes in the levels of DELLA repressors and interference with GA-609

signaling. Our data suggest that GA-mediated internode elongation in deepwater rice 610

requires suppression of JA function through the reduction of JA content in 611

submergence. 612

613

614

C9285 and T65 plants differentially express trehalose and fermentation 615

metabolism-related genes 616

Trehalose, which accumulates in response to various stresses, acts as a 617

carbon source and an osmoprotectant by stabilizing the proteins and membranes 618

against the stresses (Krasensky and Jonak, 2012). On the other hand, trehalose-6-619

phosphate (Tre6P), a precursor of trehalose, functions as a signaling metabolite which 620



29

coordinates carbon assimilation, starch synthesis, nitrogen metabolism, growth and 621

development (Schluepmann et al., 2003; Martins et al., 2013; Lunn et al., 2014; Yadav 622

et al., 2014; Figueroa et al., 2016; Figueroa and Lunn, 2016). The change in 623

Tre6P/sucrose ratio is an important homeostatic mechanism of plants under stress 624

conditions and thus Tre6P also acts as a signal for sucrose status through negative 625

feedback regulation of sucrose levels (Yadav et al., 2014; Figueroa and Lunn, 2016). In 626

rice, overexpression of OsTPS1 or OsTPP1 enhanced the tolerance to abiotic stresses, 627

leading to the expression of stress-related genes (Ge et al., 2008; Li et al., 2011). 628

OsTPP7 (OsTPP11 in this paper) also enhances the anaerobic germination tolerance in 629

young rice by regulating the trehalose content and Tre6P/sucrose homeostasis in sugar 630

signaling, but not the Tre6P content (Kretzschmar et al., 2015). In our data, although 631

several OsTPS genes including OsTPS1, OsTPP1 and OsTPP11 were expressed by 632

submergence in both genotypes, the expression of OsTPS12, 13, and 14 was 633

dramatically induced by submergence in C9285 but maintained at a lower level in T65 634

(Figure 5B). This result implies that trehalose metabolism during submergence is 635

differentially regulated between C9285 and T65 and that trehalose and trehalose-6-636

phosphate (Tre6P) may be accumulating more in submerged C9285 plants, contributing 637

to the ability of deepwater rice to withstand and adapt to submergence stress. In 638

submerged SUB1A-1 containing M202(SUB1) rice seedlings and anoxic coleoptiles, the 639

trehalose biosynthesis pathway is activated (Jung et al., 2010), suggesting that such a 640

pathway is also being utilized by the deepwater rice as part of metabolic adaptation to 641

submergence. 642



30

Under low oxygen condition, glycolysis is predominantly channeled to 643

fermentation pathways (instead of aerobic respiration) which is necessary for cell 644

survival to produce energy and recycle carbon for other pathways (Gibbs and 645

Greenway, 2003; Voesenek et al., 2006). Our data exhibited the increased expression 646

of fermentation-related genes, pyruvate decarboxylases (PDCs), alcohol 647

dehydrogenases a and 2 (ADH1 and ADH2) and acetaldehyde dehydrogenase2a 648

(ALDH2a), during submergence in both genotypes (Figure 6B). A functional SUB1 locus 649

regulates the gene expression and enzyme activities of PDC and ADH during 650

submergence (Fukao et al., 2006). Thus, a SUB1A-1 containing rice, Flood Resistant 651

13A (FR13A), accumulates less aldehydes because high expression of ADH enhances 652

the detoxification of acetaldehyde into the neutral and diffusible ethanol (Singh et al., 653

2001, Xu et al., 2006). Submergence also induces the expression of ALDH2a, but not 654

ALDH1, in coleoptiles of rice (Nakazono et al. 2000). Our results imply that the 655

fermentation pathway is active in both genotypes and that the enzymes ADH and 656

ALDH2a is likely involved in removing toxic alcohol and acetaldehyde in response to low 657

oxygen during submergence (Figure 6A). 658

The increased expression of alanine aminotransferase1 gene (OsAlaAT1) 659

(Figure 6B) further supports that the active fermentation pathway in C9285 and T65 also 660

generates alanine. These results are consistent with the increased activities of AlaAT, 661

PDC and ADH in the flooded coleoptile of rice (Oryza sativa L. cv. Nipponbare) (Kato-662

Noguchi, 2006); however, in their study, the activity of lactate dehydrogenase (LDH), 663

and lactate content were similar both in the presence and absence of oxygen. In our 664

dataset, the transcripts of two LDH genes in C9285 plants were strongly upregulated 665



31

after submergence, compared to T65 plants (Figure 6B). Formation of lactate leads to a 666

decrease in cytosolic pH and the initial acidification of the cytoplasm helps to achieve 667

optimum activity of PDC, which in turn promotes the switch from lactate to ethanol 668

fermentation (Kennedy et al., 1992; Roberts et al. 1994; Magneschi and Perata, 2009). 669

Hence, it is possible that the abundance of LDH transcripts results in higher 670

accumulation of lactate in the cytoplasm and a stronger lactate-dependent reduction of 671

cytosolic pH favoring ethanol fermentation more in C9285 than in T65 plants. Recently, 672

Lee et al. (2015) reported that lactate binds to NDRG3, an oxygen-regulated protein, 673

and activates Raf-ERK signaling for promoting cell growth and angiogenesis during 674

hypoxia in human cells, suggesting that lactate in plant cells might function as a 675

signaling molecule in a similar signaling pathway in response to hypoxia. 676

677

Cell wall synthesis and modification genes are differentially expressed in C9285 678

plants in response to submergence 679

Genes with a differential response to submergence between C9285 and T65 680

plants were enriched in the cell wall-related category (Supplemental Figure 2C). 681

Additionally, genes encoding cell wall-related proteins such as expansins (EXPs), 682

xyloglucan endotransglycosylases/hydrolases (XTHs), pectin methylesterases (PMEs), 683

and structural cell wall proteins [fasciclin-like arabinogalactans (FLAs) and extensins] 684

were categorized as submergence-induced genes in both genotypes (Supplemental 685

Table 4A and 4B) and showed higher expression in C9285 plants under non-submerged 686

condition (Figure 7A). Elongating cells require relaxation of cell walls involving cell wall 687

loosening factors such as expansins. Expansin activity increases under acidic condition, 688



32

which is controlled by plasma membrane H+-ATPase activity via auxin-induced SMALL 689

AUXIN UP-RNA (SAUR) proteins (Perrot-Rechenmann 2010, Spartz et al., 2014). In 690

deepwater rice, a positive correlation was observed between the expression of EXPs 691

and acid-induced cell wall extensibility, and they may be functioning in internode 692

elongation (Cho and Kende, 1997a; Cho and Kende, 1997b; Lee and Kende 2001). The 693

EXPs together with XTHs control fiber orientation and viscoelastic properties of the 694

matrix facilitating cell wall expansions (Cosgrove, 2000, Van Sandt et al., 2007). XTH 695

activity possibly enhances the EXP activity during the shade avoidance elongation 696

response in S. longipes (Sasidharan et al., 2008). In rice, XTHs could function in the cell 697

wall formation of the vascular bundles in elongating stems (Hara et al., 2013). 698

PMEs catalyze the demethylesterification of pectin, a galacturonic acid-rich cell 699

wall polymer resulting in the formation of a gel-like structure of polymers and thereby 700

increase wall porosity and extension of cells (Jolie et al., 2010). Jeong et al. (2015) 701

investigated that high PME activity was detected in germinating shoots that actively 702

undergo cell elongation. The cell wall is also regulated by structural cell wall proteins, 703

for instance, the arabinogalactan proteins (AGPs) which are involved in elongation and 704

growth of Arabidopsis and cucumber (van Hengel and Roberts, 2002; Park et al., 2003). 705

We found that that the expression of several genes related to cell wall loosening were 706

induced. These genes might contribute to cell wall reconstruction and increased cell 707

wall extensibility, leading to further enhancement of rapid internode elongation of C9285 708

plants during submergence. 709

Accumulation of lignin is part of the cell wall modifications that lead to an 710

increase in mechanical strength but also inhibits cell elongation. In C9285 plants, the 711



33

expression of several CAD genes, encoding key enzymes that catalyze the final step in 712

monolignol synthesis, decreased during submergence (Figure 7B), leading to a reduced 713

lignin content in newly-elongated internode during submergence. (Figure 7E). 714

Peroxidase genes showed differential expression pattern between both 715

genotypes under submergence (Supplemental Figure 2C and supplemental results) and 716

were classified as submergence-induced genes (Supplemental Tables 4A and 4B). 717

Interestingly, the expression levels of the peroxidase genes were higher in C9285 plants 718

than in T65 plants during early submergence condition (Supplemental Figure 6C). 719

Peroxidases are involved in lignification, stress defense, and regulation of reactive 720

oxygen species production (Shigeto and Tsutsumi, 2016). In addition, hydroxyl radicals 721

(・OH) produced by peroxidases may also function in cell wall loosening and cell 722

elongation as in maize roots (Liszkay et al., 2004). Thus, submergence-responsive 723

peroxidases probably function in cell wall loosening and lignification of elongating 724

internodes in C9285 plants. 725

726

Ethylene response factor genes are differentially regulated in submerged C9285 727

and T65 plants 728

Ethylene response factors (ERFs) are major downstream components of the 729

ethylene signaling pathway. In our analysis, among the 115 detected ERF family 730

transcripts, 39 genes in Ib, IIa, IIIc, VII, VIIIa, IXa, X and XI subgroups were up-731

regulated and 10 genes in IIIe and Va subroups were down-regulated by submergence 732

in C9285 plants, respectively (Supplemental Table 5), indicating that ethylene signaling 733

is an important regulatory pathway for the response of deepwater rice to submergence. 734



34

Interestingly, among all 15 members of the Group VII ERF family, 12 genes 735

including SUB1B (OsERF#063) and SUB1C (OsERF#073) were induced by 736

submergence in C9285 plants (Supplemental Table 5; Supplemental Figure 8A). 737

Members of Group VII ERF family act as oxygen sensors under hypoxic conditions by 738

the N-end rule pathway for protein degradation in Arabidopsis (Gibbs et al., 2011, 739

Licausi et al., 2011; Gasch et al., 2016) and function in multiple stress tolerances such 740

as drought, cold, pathogen attack, salinity, osmotic stress, and submergence in various 741

plants (Licausi et al., 2010; Mizoi et al., 2002; Gibbs et al., 2015, Papdi et al., 2015). We 742

found the other 3 genes (OsERF#70, #71, #72) encoding a CMVII-4 motif, which is 743

predicted to be a phosphorylation site of mitogen activated protein kinases (MPKs) 744

(Nakano et al., 2006), showed non-responsive expression to submergence in C9285 745

plants (Supplemental Figure 13). MPKs phosphorylate a large of transcription factors 746

including ERFs (Popescu et al., 2009) and the MPK-induced phosphorylations in rice 747

ERFs enhance their transcriptional activities and environmental stress tolerances 748

(Cheong et al., 2003; Schmidt et al., 2013). Recently, it was reported that OsMPK3 749

phosphorylated SUB1A-1 to control shoot elongation in a SUB1A-1-dependent manner, 750

although the phosphorylation site was not located in the CMVII-4 motif (Singh and 751

Sinha, 2016). In C9285 plants, all members of Group VII ERFs that encode proteins 752

without the phosphorylation sites were induced by submergence and the submergence-753

induced expression level of some Group VII ERFs (OsERF#59, 61, 63, 64, 66 and 67) 754

was higher during submergence compared to T65 plants (Supplemental Figure 13). 755

These results suggest that phosphorylation-independent Group VII ERFs may be 756

important for the submergence-induced stress response in deepwater rice, although 757



35

there is still the possibility that submergence induces phosphorylation of the ERFs by 758

MAP kinases. 759

Other submergence-induced ERFs in subgroups IIa and VIIIa encode proteins 760

that contain an ERF-associated amphiphilic repression (EAR) motif (DLNxxP), which 761

acts as a transcriptional repressor domain (Fujimoto et al., 2000; Ohta et al., 2001). As 762

EAR-containing transcription factors regulate various stress responses (Kazan, 2006; 763

Dong and Liu, 2010; Licausi et al., 2013), the submergence-induced ERFs might be 764

involved in negatively regulating the expression of dispensable genes for submergence 765

response. 766

In our data, Group IIIc, IXa and X ERFs also showed up-regulated expression 767

in response to submergence (Supplemental Table 5). In Arabidopsis, the group IIIc, IXa 768

and X ERFs function in tolerance to environmental stresses such as freezing, salt and 769

dehydration (e.g. cold-binding factor/dehydration responsive element binding1 770

[CBF/DREB1] protein) (Dubouzet et al., 2003), the ethylene-jasmonic acid signaling 771

pathway (Lorenzo et al., 2003, Champion et al., 2009) and the response to ABA and 772

various stresses (Pandey et al., 2005; Zhu et al., 2010), respectively. In the case of the 773

Group XI ERFs, this family exists in rice but not in Arabidopsis, indicating that these 774

genes have rice-specific functions. 775

A Group IIIe ERF, TINY, functions in the reduction of cell expansion and 776

differentiation leading to a dwarf phenotype in Arabidopsis (Wilson et al., 1996). In 777

C9285 plants, two Group IIIe ERF family genes were down-regulated by submergence, 778

suggesting that the Group IIIe ERFs possibly affects cell expansion during 779

submergence. Arabidopsis ERF11 in group VIIIa represses ethylene biosynthesis genes 780



36

but promotes cell elongation by promoting GA accumulation and inhibition of DELLA 781

function (Li et al., 2011; Zhou et al., 2016). In rice, OsEATB (OsERF#102) in group Xb 782

and OsERF3 (OsERF#075) in group VIIIa negatively regulates internode elongation (Qi 783

et al., 2011; Zhang et al., 2013), respectively. In C9285 plants, OsEATB was not 784

expressed and OsERF3 was not differentially expressed during submergence 785

(Supplemental Figure 11D), suggesting that the two negative regulators do not 786

participate in GA-mediated internode elongation during submergence in C9285 plants. 787

The SUB1A up-regulates the transcriptional expression level of 12 ERF family 788

genes (Jung et al., 2010). Although the SUB1A gene is not present in C9285 genome 789

(Hattori et al., 2009), the six SUB1A-dependent expressed genes (i.e., OsERF#025, 790

#066, #067, #068, #076 and #077) were also induced by submergence in C9285 plants 791

(Supplemental Figure 8A). All SUB1A downstream ERF genes belong to IIIc, VIIa and 792

VIIIa subfamilies. This indicates that these genes are also regulated by other factors in 793

C9285 plants and may also indicate that their expression is not directly associated with 794

internode elongation in deepwater rice. 795

The ERF transcription factors bind to the promoter regions of their target genes 796

such as pathogen-related (PR) genes through recognition of a GCC box cis-regulatory 797

sequence (GCCGCC; core motif) (Ohme-Takagi and Shinshi, 1995; Hao et al., 1998, 798

Solano et al., 1998). Our in-silico analysis showed that the two GCC-box like motifs 799

(G/CCGGCGGCGG) and (CGCCGCCGCC) were enriched in the promoter region of 800

genes with higher expression in C9285 plants (Supplemental Figure 9), suggesting that 801

these genes with GCC-box like motifs are preferentially regulated by ERFs. Some 802

submergence-induced ERF genes showed higher expression in C9285 than those of 803



37

T65 plants before and after submergence (Supplemental Figure 8A). This result 804

suggests that the ERF genes in C9285 are associated with the constitutively higher 805

expression of their putative downstream target genes. Recently, Gasch et al. (2016) 806

identified a novel hypoxia-responsive promoter element (HRPE) which is a binding site 807

of ERF VIIs, RELATED TO AP2 (RAP) 2.2 and RAP2.12, the key regulators of N-end 808

rule pathway in Arabidopsis. However, we did not identify the HRPE motif in our 809

promoter analysis of C9285-enriched genes. The O2 levels in underwater nodes could 810

be much higher than expected for two reasons: (i) diffusion from the water layer into the 811

node, and (ii) underwater photosynthesis. Under submergence with light illumination, O2 812

concentration of deepwater rice initially dropped but recovered within 90 min by its 813

underwater photosynthesis (Stünzi and Kende, 1989). Thus, our data may not be 814

suitable to study hypoxia, since we collected all samples under light condition. 815

816

A model for the transcriptional response of deepwater rice to submergence 817

We propose a model for submergence responses during the “escape strategy” in 818

the deepwater rice C9285 (Supplemental Figure 14). Submergence subjects the plant 819

cells to multiple stresses such as limitation of gas diffusion, lower light intensity, high risk 820

of pathogen infection and decreased oxygen uptake. To avoid critical damage from 821

submergence, C9285 plants have evolved to rapidly elongate their internodes and 822

leaves. We revealed that changes in contents of the plant hormones, ethylene, ABA, GA 823

and JA during submergence were transcriptionally regulated. Ethylene signaling leads 824

to biotic and abiotic stress tolerances by changing the expression of many genes and 825

plant hormone levels (Müller and Munné-Bosch, 2015) and our data exhibited largely 826



38

changes in the putative downstream components of ethylene signaling during 827

submergence. We also proposed that JA is a novel regulator for submergence-induced 828

internode elongation in C9285 plants. In deepwater rice, GA has an important role in 829

elongation response because GA treatment induces the expression of cell wall-related 830

genes such as expansins and changes the activity of CAD (Sauter and Kende 1992, 831

Cho and Kende 1997c). We found that C9285-specific accumulation of active GAs was 832

probably controlled by the expression of GA20ox2 during submergence (Figure 3B) and 833

the cell wall-related genes showed higher expression in C9285 plants (Figure 7A). 834

Furthermore, the reduced lignin content in C9285 plants may also facilitate the 835

elongation of internodes under submerged condition. Overall modifications in cell wall 836

metabolism may also be contributing to the rapid internode elongation of deepwater 837

rice. Among the transcription factor genes, the ERF family genes were especially 838

expressed at high levels during submergence in C9285 plants. Interestingly, genes 839

specifically expressed in C9285 plants contain the GCC-box like motifs which are 840

recognized by ERFs. This indicates that ethylene signaling and the transcriptional 841

response pathway via ERFs could be a key factor for submergence response in C9285 842

plants. In fact, the rice ETHYLENE INSENSITIVE3-like 1 (OsEIL1), which is the master 843

regulator of ethylene signaling, binds to the promoter region of ethylene/submergence-844

induced ERF transcription factors, SNORKEL1 and SNORKEL2 (SK1/2), that positively, 845

but not exclusively, regulate internode elongation in C9285 plants (Hattori et al., 2009). 846

Since we could not find any C9285-specific novel submergence-induced TFs in the 847

C9285 genome by our de-novo assembly analysis and the presence of SK1/2 alone 848



39

does not lead to a full stem elongation response, additional TFs in coordination with 849

SK1/2 are most likely involved. 850

In Rumex palustris, genes associated with photomorphogenesis and shade 851

avoidance seem to regulate underwater elongation response (van Veen et al. 2013). In 852

our data, the expression pattern of light signaling regulated genes in C9285 plants did 853

not show any obvious genotype or submergence-specific pattern (Supplemental Figure 854

15). The genes involved in fermentation and trehalose metabolic pathways responded 855

to submergence in both C9285 and T65 plants, and we found that TPSs and LDHs were 856

preferentially expressed during submergence in C9285 plants (Figure 5 and 6), 857

suggesting that these metabolic activities increase more strongly in C9285 plants during 858

submergence, compared to normal rice such as T65 plants, resulting in adaptation to 859

long-term submergence. 860

Our experiments showed that many pathogenesis related proteins (PR-861

proteins) were preferentially expressed in each rice variety (Supplemental Table 3) and 862

several genes encoding disease resistance proteins were identified as C9285-unique 863

transcripts (Figure 8). Waterlogged conditions increase the risk of pathogen infection in 864

plants (Tamang and Fukao. 2015). Accordingly, rice in paddy fields have protection 865

mechanisms that prevent damage rendering them vulnerable to pathogens (Hsu et al., 866

2013). Therefore, these C9285-specific genes might function as a pathogen defense 867

pathway during partial long-term submergence in C9285 plants. 868

Our studies identified genotype-specific responsive genes to submergence in 869

C9285 plants and assumed that the putative key genes would be associated with 870

submergence-induced physiological responses in C9285 plants. Furthermore, we 871



40

showed that ethylene is one of the main drivers of submergence responses and JA is a 872

new negative regulator of submergence-induced internode elongation in C9285 plants. 873

The network involving submergence-induced changes and genetic factors complexly 874

regulate underwater elongation and adaptation in deepwater rice. 875

876



41

877

METHODS 878

Plant material and cultivation 879

A deepwater rice cultivar (C9285, Oryza sativa) and a non-deepwater rice cultivar 880

(Taichung 65, T65, Oryza sativa ssp. Japonica) were used. Rice seeds were incubated 881

at 60˚C for 10 min followed by pre-germination at 29˚C in water for 3 to 4 days. 882

Afterwards, germinated seeds were transferred to plastic pots containing soil mixture 883

(Mikawa Baido, AICHI Mederu, Nishio, JAPAN) and grown in a greenhouse in Nagoya, 884

Japan in June with a natural light cycle of ca. 14 h light / 10 h dark. For deepwater 885

treatment, rice seedlings that reached the indicated leaf stages (4LS and 6LS) were 886

completely submerged for 1, 3, 6, 12 and 24 h (Supplemental Figure 1A). To avoid 887

differences in gene expression between samples due to circadian rhythms, 888

submergence treatments were initiated at different times of the day and all samples 889

were collected in the afternoon, although varying durations of underwater- and above 890

water photosynthesis causes change in the availability of photosynthates. After 891

submergence treatment, 5 mm of the shoot base region containing internodes, nodes, 892

the shoot apex and basal regions of leaves were sampled and rapidly frozen in liquid 893

nitrogen and stored at -80˚C until RNA extraction (Supplemental Figure 1B). 894

895

RNA extraction, sequencing and read mapping 896

For each RNA extraction frozen tissues from one individual plant were homogenized 897

and up to 100 mg were used. Total RNA of each sample was isolated using the RNeasy 898

Plant Mini Kit (Qiagen, Hilden, Germany) with the RNase-Free DNase Set (Qiagen). 899



42

RNA purity was checked using a NanoDrop spectrophotometer (Thermo-Fisher) and 900

RNA was quantified using a QuantiFluor RNA system (Promega) and an EnSpire 901

Multimode Plate Reader (PerkinElmer). For HiSeq library construction, 2 µg of total RNA 902

was used with the llumina TruSeq RNA Sample Preparation Kit v2 (Illumina) according 903

to the manufacturer's instructions. Agencourt AMPure XP beads (Beckman Coulter) 904

were used to remove small DNA fragments. The clustering of index-coded samples was 905

performed on a cBot Cluster Generation System using the TruSeq SR Cluster Kit v2-906

cBot-GA (Illumia) and the TruSeq SBS Kit v5-GA (Illumia). After cluster generation, the 907

library preparations were sequenced on an Illumina Genome Analyzer IIx and 36 bp 908

single-ended reads were generated. Reads were mapped to the IRGSP 1.0 reference 909

transcripts of Oryza sativa ssp. Japonica cv. Nipponbare (Goff et al., 2002) using bowtie 910

(version 0.12.7) (Langmead et al., 2009) with the “—all –best –strata” options 911

(Supplemental Table 1) and read counts were quantified using PostgreSQL and a 912

custom PHP script. 913

914

Data analysis 915

Statistical data analysis was performed using R. The “edgeR” package was used to 916

normalize raw count data and generate counts per million (cpm) values. (Robinson et 917

al., 2010). Transcripts with less than 10 averaged counts in at least 1 condition were 918

removed from the dataset and only the strongest expressed isoform per transcript was 919

used for analysis. To determine differentially expressed genes, a negative binominal 920

generalized log-linear model was used (function “glmFit”) with each genotype and time 921

point after submergence defined as one group. Then, likelihood-ratio tests (function 922



43

“glmLRT”) were performed to compare between groups or to test for interactions 923

between genotype and submergence treatment. The Bonferoni-Holm method was used 924

to correct for multiple testing (function “topTags”). PCA was performed using the 925

“prcomp” function with scaled and centered cpm data as the input. k-means clustering 926

was performed using the “MBClusterSeq” package with a negative binomial model and 927

the EM algorithm (Si et al., 2014). The number of clusters was varied between 10 and 928

100 in intervals of 10 and empirically k = 40 (for all samples) or k = 20 (for samples from 929

one genotype only) was chosen as the most appropriate number of clusters. 930

Hierarchical clustering of transcription factor genes was performed using the “dist” and 931

“hclust” functions. The distance matrix was calculated using Euclidian distance and 932

clustering was performed using the “average” algorithm. 933

Gene set enrichment analysis was based on the MAPMAN ontology and 934

mappings (RAPDB locus ID to MAPMAN bin) were obtained from 935

http://www.mapman.gabipd.org (Ramsak et al., 2014). Significant enrichment of bins 936

was determined using Fisher’s Exact test and corrections for multiple testing were done 937

by the Bonferroni-Holm method using the R functions “fisher.test” and “p.adjust”, 938

respectively. Separate analyses were performed for the first three hierarchy levels of the 939

MAPMAN ontology. 940

Metabolic maps were based on a combination of RAPDB, KEGG (Kanehisa et 941

al., 2015), MAPMAN and in-house annotations. Data visualization was performed using 942

ggplot2 (Wickham, 2009). 943

944



44

ABA and GA3 treatments of whole plants 945

Germinated seeds of C9285 plants were sown in plastic pots filled with soil and then 946

grown in a phytotron at 25˚C with a 14-h photoperiod. When the plants were grown at 947

the 4 LS, they were transferred to new plastic containers for hormone treatment. For 948

hormone treatment, plants were watered with either 10 µM ABA (Sigma-Aldrich), 10 µM 949

Gibberellin A3 (Wako) or a combination of both into the containers. The water level in 950

each container was controlled to keep the hormone concentration during the treatment. 951

Plant height and internode length were measured after 18-day treatment. Internode 952

length was calculated using the total length of all internodes. 953

954

JA treatment of whole plants during submergence 955

Germinated seeds of C9285 plants were sown in plastic pots filled with soil and then 956

grown in a controlled environment chamber at 25˚C with a 14 h photoperiod. When the 957

plants reached the 6 LS they were submerged in water with or without 50 µM methyl 958

jasmonate (Wako) for 3 days. Total internode length was calculated as the sum of the 959

length of all internodes. 960

961

Measurement of plant hormone contents 962

The concentrations of endogenous hormones were measured using UPLC-MS/MS 963

(UPLC-Xevo TQ-S; Waters, Maple Street, Milford, MA, USA) as described in Kojima et 964

al. (2009). 965

966



45

Measurement of lignin content 967

Nodes and internodes were sampled from C9285 and T65 plants at the 6LS or 7LS 968

before and after submergence treatment for 2 days. Lignin content was determined by 969

the thio-glycolic acid method according to Suzuki et al. (2009). 970

971

Promoter motif enrichment analysis 972

Transcripts were clustered into 6 groups based on expression in C9285 and T65 plants 973

(6LS) at 0 h, 1 h, 3 h, 6 h, 12 h and 24 h after submergence using k-means clustering 974

as described above. For tentative construction of a C9285 genome, all reads obtained 975

from whole-genome sequencing of C9285 were mapped against the IRGSP-1.0 976

pseudomolecules using bwa-mem with the -M option (Li and Durbin, 2009). Mapped 977

reads were re-aligned using RealignerTargetCreator and indelRealigner from the GATK 978

software suite (DePristo et al., 2011). To identify SNPs and INDELs, UnifiedGenotyper 979

of GATK was used with the -glm BOTH option. The C9285 genome sequence was 980

tentatively constructed by modifying the IRGSP-1.0 genome with the identified variants 981

of C9285 by custom Perl scripts. DNA sequences 1 kb upstream of the translational 982

start sites from the C9285 genome were regarded as promoter regions and used for 983

motif enrichment analysis. CENSOR was used to mask low-complexity regions in the 984

promoter sequences (Kohany et al., 2006). The MEME suite was used to find enriched 985

DNA sequence motifs using following parameters: -dna -nmotifs 10 -maxw 10 (Bailey 986

and Elkan, 1994). 987

988



46

Accession numbers 989

All reads used in this manuscript can be found in the DNA Database of Japan (DDBJ) 990

under bioproject PRJDB5294 (C9285 RNA-Seq reads) and bioproject PRJDB5300 991

(C9285 genomic reads). 992

993

SUPPLEMENTAL DATA 994

Supplemental Figure 1. Schematic overview of the experimental setup and 995

transcriptome sequencing. 996

Supplemental Figure 2. Significance analysis using a generalized log-linear model. 997

Supplemental Figure 3. Expression of genes related to ethylene, gibberellin and 998

abscisic acid signaling during submergence. 999

Supplemental Figure 4. Overview of MapMan visualization of differentially expressed 1000

genes in C9285 plants after 1 h of submergence. 1001

Supplemental Figure 5. Overview of MapMan visualization of differentially expressed 1002

genes in C9285 and T65 plants under non-submerged condition. 1003

Supplemental Figure 6. Expression of lignin biosynthesis genes during submergence. 1004

Supplemental Figure 7. Clustering of transcription factor genes according to expression 1005

in C9285 relative to T65 plants. 1006

Supplemental Figure 8. Submergence-induced AP2/EREBP family genes in C9285 1007

plants. 1008

Supplemental Figure 9. Enriched sequence motifs in the promoters of genes that are 1009

differentially expressed in C9285 plants. 1010

Supplemental Figure 10. Analysis pipeline to detect novel C9285 transcripts. 1011



47

Supplemental Figure 11. Submergence responses related to plant hormones 1012

Supplemental Figure 12. Isolation of genes specifically induced by submergence in 1013

C9285 4LS plants. 1014

Supplemental Figure 13. Expression of Group VII ERF genes during submergence. 1015

Supplemental Figure 14. A molecular model for the submergence response in the 1016

deepwater rice C9285. 1017

Supplemental Figure 15. Expression of light signaling genes during submergence. 1018

1019

Supplemental Table 1. Summary of read mapping statistics. 1020

Supplemental Table 2. Number of genes with significantly different expression in 1021

pairwise comparisons. 1022

Supplemental Table 3. Enriched MAPMAN bins among genes preferentially expressed 1023

in C9285 or T65 plants. 1024

Supplemental Table 4. Enriched MAPMAN bins among genes induced or repressed by 1025

submergence in either genotype. 1026

Supplemental Table 5. Response to submergence of rice ERF subfamily genes in 1027

C9285 plants. 1028

1029

Supplemental Results 1030

Supplemental Methods 1031

Supplemental References 1032

1033



48

Supplemental Data Set 1. Gene expression data, annotations and results of whole 1034

transcriptome analysis. 1035

Supplemental Data Set 2. Genes specifically or preferentially expressed in C9285 1036

samples. 1037

Supplemental Data Set 3. Genes specifically or preferentially expressed in T65 1038

samples. 1039

Supplemental Data Set 4. Genes with submergence-induced expression in C9285 1040

samples. 1041

Supplemental Data Set 5. Genes with submergence-induced expression in T65 1042

samples 1043

Supplemental Data Set 6. Genes with submergence-repressed expression in C9285 1044

samples. 1045

Supplemental Data Set 7. Genes with submergence-repressed expression in T65 1046

samples. 1047

Supplemental Data Set 8. Analyses of transcription factor-encoding genes. 1048

Supplemental Data Set 9. List of 189 genes specifically expressed in C9285 plants. 1049

Supplemental Data Set 10. Expression of genes in de novo assembled C9285 genomic 1050

regions. 1051

Supplemental Data Set 11. 36 genes responding to submergence in C9285 at the 6 1052

leaf-stage, but not in C9285 at the 4 leaf-stage. 1053

Supplemental Data Set 12. C9285 unique genomic contigs. 1054

Supplemental Data Set 13. C9285 unique transcripts. 1055

Supplemental Data Set 14. C9285 unique proteins. 1056



49

1057



50

ACKNOWLEDGMENTS 1058

We thank Dr. KO Hirano for assisting with lignin quantification and Dr. MASAHIRO 1059

FUJITA for providing C9285 genomic sequencing data. Seeds of C9285 used in this 1060

study was distributed from the National Institute of Genetics supported by the National 1061

Bioresource Project, AMED, JAPAN. 1062

1063

1064



51

1065

FIGURE LEGENDS 1066

1067

Figure 1. Submergence response of deepwater rice and non-deepwater rice. 1068

(A) Deepwater rice can survive and escape from submerged condition by rapid 1069

elongation of stems (internodes) and leaves while non-deepwater rice cannot 1070

elongate internodes during submergence. (B) Principal component analysis of 18 1071

RNA-Seq samples from C9285 and T65 submerged at different leaf stages (LS) 1072

and time points. A plot of all transcriptome samples along the first two principal 1073

components (PC) is shown. The percentage of variation explained is indicated at 1074

each axis. Colors indicate samples from different genotypes and LS. Each data 1075

point represents averaged data from three independent time series and one 1076

individual plant was sampled for each data point.. 1077

1078

Figure 2. Clustering analysis of the transcriptome of C9285 and T65 plants after 1079

submergence. 1080

Heatmap representations of expression data from selected clusters in both 1081

C9285 and T65 at six-leaf stage (C9286 6LS and T65 6LS) (A), and from clusters 1082

only in C9285 6LS (B) or T65 6LS (C) plants are shown. The clusters in the 1083

figure derived from Supplemental Dataset S1 were manually arranged. Rows 1084

represent clusters of genes generated by k-means clustering. Columns represent 1085

samples from different time points after submergence. Colors represent the 1086

average expression profile for each cluster with red showing high and blue 1087



52

showing low expression, respectively. Before averaging within each cluster, 1088

expression of each gene was normalized to its average expression across all 1089

samples and transformed to log2 values. Numbers on the left side of each panel 1090

show the assigned cluster IDs and the number of genes in each cluster is in 1091

parenthesis. The total number of clusters was k = 40 in (A) and k = 20 in (B) and 1092

(C). 1093

1094

Figure 3. Ethylene, gibberellin, and abscisic acid metabolism during 1095

submergence. 1096

Schematic overview of ethylene (A), gibberellin (GA) (B) and abscisic acid (ABA) 1097

(C) metabolism alongside heatmaps showing expression of relevant genes are 1098

shown. Each row represents one gene, columns represent samples from different 1099

time points after submergence and colors represent gene expression levels as 1100

log2 transformed counts per million values (cpm). Lower levels of expression are 1101

represented in blue and higher expression in yellow. ACS, ACC-synthase; AAO3, 1102

ABA-aldehyde oxidase; ABA8ox, ABA-8’ oxidase; ACC, 1-aminocyclopropane-1-1103

carboxylic acid; ACO, ACC-oxidase; CPS, copalyl-phosphate synthase; CYP714, 1104

cytochrome P714; GAXox, GA-X oxidase; GGDP, geranyl-geranyl diphosphate; 1105

KAO, ent-kaurenoic acid oxidase; KO, ent-kaurene oxidase; KS, ent-kaurene 1106

synthase; NCED, 9-cis-epoxycarotenoid dioxygenase; SAM, S-adenosyl 1107

methionine; ZEP1, zeaxanthin epoxidase 1. Asterisks indicates genes with 1108

significant difference (FDR < 0.05) at more than 4 time points between C9285 1109



53

and T65 samples and < or > indicate the direction of the difference relative to 1110

C9285. (D) Effect of ABA and GA3 on plant height and total internode length. 1111

C9285 4LS plants were grown in shallow-water containing 10 µM GA3 and/or 10 1112

µM ABA for 18 days. Bars represent the average of at least seven biological 1113

replicates and error bars show standard errors. Asterisks show significant 1114

differences (P < 0.05) between the indicated treatments as calculated by 1115

Student’s t tests. 1116

1117

Figure 4. Jasmonic acid metabolism during submergence. 1118

(A) Schematic overview of jasmonic acid (JA) metabolism alongside heatmaps 1119

showing expression of relevant genes are shown. Each row represents one 1120

gene, columns represent samples from different time points after submergence 1121

and colors represent gene expression levels as log2 transformed counts per 1122

million values (cpm). Lower levels of expression are represented in blue and 1123

higher expression in yellow. FDA, fatty acid desaturase; DAD1, defective in 1124

anther dehiscence1; PLA, phospholipase A1; LOX, lipoxygenase; 13(S)-HPOT, 1125

(13S)-hydroperoxyoctadecatrienoic acid; AOS, allene oxide synthase; 12, 13-1126

EOT, 12,13(S)-epoxy-octadecatrienoic acid; AOC, allene oxide cyclase; OPDA, 1127

cis-(+)-12-oxophytodienoic acid; OPR, 12-oxo-phytodienoic acid reductase; 1128

OPC-8, OPC-8, 3-oxo-2-(2’-pentenyl)-cyclopentane-1-octanoic acid; OPCL1, 1129

acyl-activating enzyme; ACX, acyl-CoA oxidase; MFP, multifunctional protein; 1130

KAT, 3-keto-acyl-CoA thiolase; TS2, tasselseed2; JA-CoA, jasmonoyl-CoA; (+)-7-1131



54

iso-JA, (+)-7-iso-jasmonoyl; JAR1, jasmonate resistant1; JA-lle, (+)-7-iso-1132

jasmonoly-L-isoleucine; CYP94, cytochrome P94. Asterisks indicates genes with 1133

significant difference (FDR < 0.05) at more than 4 time points between C9285 1134

and T65 samples and < or > indicate the direction of the difference relative to 1135

C9285. (B) Endogenous JA level in the shoot base regions of C9285 and T65 1136

plants during submergence for 24 hours. Bars represent the average of at least 1137

five biological replicates and error bars represent standard errors. Asterisk show 1138

significant difference (P < 0.05) between C9285 and T65 samples as calculated 1139

by Student’s t tests. (C) Jasmonic acid inhibits internode elongation during 1140

submergence. C9285 6LS plants were submerged under water containing 50 µM 1141

metyl jasmonate (Me-JA) for 3 days. Bars represent the average of at least 1142

twelve biological replicates and error bars show standard errors. Asterisk show 1143

significant difference (P < 0.05) between the indicated treatments as calculated 1144

by Student’s t tests. 1145

1146

Figure 5. Expression of trehalose metabolism-related genes during 1147

submergence. 1148

(A) Schematic overview of the trehalose metabolic pathway. Glu6P, glucose-6-1149

phosphate; Tre6P, trehalose-6-phosphate; UDPG, UDP-glucose. (B) to (D) 1150

Expression of genes involved in trehalose metabolism during submergence in 1151

C9285 6LS (black) and T65 6LS (orange) plants at the indicated time points after 1152

submergence. Data points show expression levels as average cpm in three 1153



55

biological replicates and error bars show standard deviation. (B) TPS; trehalose-1154

6-phosphate synthase, (C) TPP; trehalose-6-phosphate phosphatase, (D) TRE; 1155

trehalase. Black and orange asterisks indicate significant differences (P < 0.05) 1156

from 0 h at each time point for C9285 and T65 samples, respectively. Daggers 1157

indicate significant differences (FDR < 0.05) between C9285 and T65 samples. 1158

P-values were calculated using likelihood ratio tests and corrected for multiple 1159

testing by the Bonferoni-Holm method. 1160

1161

Figure 6. Expression of fermentation-related genes during submergence. 1162

(A) Schematic overview of three fermentation pathways. (B) Expression of genes 1163

related to fermentation during submergence in 6LS C9285 (black) and 6LS T65 1164

(orange) plants at the indicated time points after submergence is shown. Data 1165

points show expression levels as average cpm in three biological replicates and 1166

error bars show standard deviation. Panels have been arranged to reflect the 1167

different possibilities of anaerobic energy production. PEP; 1168

phosphoenolpyruvate, ADH; aldehyde dehydrogenase, AlaAT; alanine-1169

aminotransferase, ALDH; alcohol dehydrogenase, LDH; lactate dehydrogenase, 1170

PDC; pyruvate decarboxylase. Black and orange asterisks indicate significant 1171

differences (P < 0.05) from 0 h at each time point for C9285 and T65 samples, 1172

respectively. Daggers indicate significant differences (P < 0.05) between C9285 1173

and T65 samples. P-values were calculated using likelihood ratio tests and 1174

corrected for multiple testing by the Bonferoni-Holm method. 1175



56

1176

Figure 7. Effect of submergence on the expression of cell wall formation-related 1177

genes. 1178

(A) Expression pattern of cell wall-related genes during 24 h of submergence. 1179

The gene expression levels in C9285 6LS and T65 6LS samples are indicated by 1180

log2-fold changes at each time point (0 h, 1 h, 3 h, 12 h and 24 h) relative to that 1181

of T65 samples before submergence. Genes with a maximal cpm value of more 1182

than 15 are shown. AGP, arabinogalactan protein; PME, pectin esterase; XTH, 1183

xyloglucan endotransglycosylases/hydrolase. (B) Changes in expression of 11 1184

coniferyl/sinapyl alcohol dehydrogenase (CAD) genes during submergence for 1185

24 h. Data points show expression levels as average cpm in three biological 1186

replicates and error bars show standard deviation. (C) Sampled regions of 1187

internodes for lignin quantification. C9285 plants at the seven-leaf stage (7LS) 1188

that have already formed internodes were submerged for 2 days (2 d). Photos of 1189

stems before (0 d) and after (2 d) submergence treatment of C9285 plants at the 1190

7LS are shown. Red arrowheads indicate stem nodes. (D, E) Lignin content in 1191

the nodes and internodes before (D) and after (E) 2 d submergence of C9285 1192

plants at 7LS. Bars represent averages of at least six biological replicates and 1193

error bars represent standard errors. Different letters indicate significant (P < 1194

0.05) differences according to the Tukey-Kramer test. 1195

1196

Figure 8. Submergence-induced transcripts from C9285-unique loci. 1197



57

Expression from selected loci which are presumably absent in the IRGSP1.0 1198

reference genome is shown. Each row represents one locus, columns represent 1199

samples from different time points after submergence and colors represent gene 1200

expression levels as log2 transformed counts per million values (cpm) normalized 1201

to the average expression in all samples of different time points. Genes that have 1202

an at least two-fold increase in expression after submergence in C9285 6 LS 1203

plants are shown. Complete expression data from C9285-unique transcripts can 1204

be found in Supplemental Dataset 10 and sequence data is provided in 1205

Supplemental Datasets 12 to 14. 1206

1207

1208



58

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Deepwater rice Non-deepwater rice Deepwater rice Non-deepwater rice

Figure 1. Submergence response of deepwater rice and non-deepwater rice. (A) Deepwater rice can survive and escape from submerged condition by rapid elongation of stems (internodes) and leaves while non-deepwater rice cannot elongate internodes during submergence. (B) Principal component analysis of 18 RNA-Seq samples from C9285 and T65 submerged at different leaf stages (LS) and time points. A plot of all transcriptome samples along the first two principal components (PC) is shown. The percentage of variation explained is indicated at each axis. Colors indicate samples from different genotypes and LS. Each data point represents averaged data from three biological replicates.



Figure 2. Clustering analysis of the transcriptome of C9285 and T65 plants after submergence. Heatmap representations of expression data from selected clusters in both C9285 and T65 at six-leaf stage (C9286 6LS and T65 6LS) (A), and from clusters only in C9285 6LS (B) or T65 6LS (C) plants are shown. The clusters in the figure derived from Supplemental Dataset S1 were manually arranged. Rows represent clusters of genes generated by k-means clustering. Columns represent samples from different time points after submergence. Colors represent the average expression profile for each cluster with red showing high and blue showing low expression, respectively. Before averaging within each cluster, expression of each gene was normalized to its average expression across all samples and transformed to log2 values. Numbers on the left side of each panel show the assigned cluster IDs and the number of genes in each cluster is in parenthesis. The total number of clusters was k = 40 in (A) and k = 20 in (B) and (C).

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Figure 3. Ethylene, gibberellin, and abscisic acid metabolism during submergence.Schematic overview of ethylene (A), gibberellin (GA) (B) and abscisic acid (ABA) (C) metabolism alongside heatmaps showing expression of relevant genes are shown. Each row represents one gene, columns represent samples from different time points after submergence and colors represent gene expression levels as log2transformed counts per million values (cpm). Lower levels of expression are represented in blue and higher expression in yellow. ACS, ACC-synthase; AAO3, ABA-aldehyde oxidase; ABA8ox, ABA-8’ oxidase; ACC, 1-aminocyclopropane-1-carboxylic acid; ACO, ACC-oxidase; CPS, copalyl-phosphate synthase; CYP714, cytochrome P714; GAXox, GA-X oxidase; GGDP, geranyl-geranyl diphosphate; KAO, ent-kaurenoic acid oxidase; KO, ent-kaurene oxidase; KS, ent-kaurene synthase; NCED, 9-cis-epoxycarotenoid dioxygenase; SAM, S-adenosylmethionine; ZEP1, zeaxanthin epoxidase 1. Asterisks indicates genes with significant difference (FDR < 0.05) at more than 4 time points between C9285 and T65 samples. Among genes with asterisks, < or > indicates the lower or higher gene expression levels in C9285 plants than that in T65 plants, respectively. (D) Effect of ABA and GA3 on plant height and total internode length. C9285 4LS plants were grown in shallow-water containing 10 µM GA3 and/or 10 µM ABA for 18 days. Bars represent the average of at least seven biological replicates and error bars show standard errors. Asterisks show significant differences (P < 0.05) between the indicated treatments as calculated by Student’s t tests.

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Figure 4. Jasmonic acid metabolism during submergence. (A) Schematic overview of jasmonic acid (JA) metabolism alongside heatmaps showing expression of relevant genes are shown. Each row represents one gene, columns represent samples from different time points after submergence and colors represent gene expression levels as log2 transformed counts per million values (cpm). Lower levels of expression are represented in blue and higher expression in yellow. FDA, fatty acid desaturase; DAD1, defective in anther dehiscence1; PLA, phospholipase A1; LOX, lipoxygenase; 13(S)-HPOT, (13S)-hydroperoxyoctadecatrienoic acid; AOS, allene oxide synthase; 12, 13-EOT, 12,13(S)-epoxy-octadecatrienoic acid; AOC, allene oxide cyclase; OPDA, cis-(+)-12-oxophytodienoic acid; OPR, 12-oxo-phytodienoic acid reductase; OPC-8, OPC-8, 3-oxo-2-(2’-pentenyl)-cyclopentane-1-octanoic acid; OPCL1, acyl-activating enzyme; ACX, acyl-CoA oxidase; MFP, multifunctional protein; KAT, 3-keto-acyl-CoA thiolase; TS2, tasselseed2; JA-CoA, jasmonoyl-CoA;(+)-7-iso-JA, (+)-7-iso-jasmonoyl; JAR1, jasmonate resistant1; JA-lle, (+)-7-iso-jasmonoly-L-isoleucine; CYP94, cytochrome P94. Asterisks indicates genes with significant difference (FDR < 0.05) at more than 4 time points between C9285 and T65 samples. < or > indicates the lower or higher gene expression levels in C9285 plants than that in T65 plants, respectively. (B) Endogenous JA level in the shoot base regions of C9285 and T65 plants during submergence for 24 hours. Bars represent the average of at least five biological replicates and error bars represent standard errors. Asterisk show significant difference (P < 0.05) between C9285 and T65 samples as calculated by Student’s t tests. (C) Jasmonic acid inhibites internode elongation during submergence. C9285 6LS plants were submerged under water containing 50 µM metyl jasmonate (Me-JA) for 3 days. Bars represent the average of at least twelve biological replicates and error bars show standard errors. Asterisk show significant difference (P < 0.05) between the indicated treatments as calculated by Student’s t tests.

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Figure 6. Expression of fermentation-related genes during submergence.(A) Schematic overview of three fermentation pathways. (B) Expression of genes related to fermentation during submergence in 6LS C9285 (black) and 6LS T65 (orange) plants at the indicated time points after submergence is shown. Data points show expression levels as average cpm in three biological replicates and error bars show standard deviation. Panels have been arranged to reflect the different possibilities of anaerobic energy production. PEP; phosphoenolpyruvate, ADH; aldehyde dehydrogenase, AlaAT; alanine-aminotransferase, ALDH; alcohol dehydrogenase, LDH; lactate dehydrogenase, PDC; pyruvate decarboxylase. Black and orange asterisks indicate significant bdifferences (P < 0.05) from 0 h at each time point for C9285 and T65 samples, respectively. Daggers indicate significant differences (P < 0.05) between C9285 and T65 samples. P-values were calculated using likelihood ratio tests and corrected for multiple testing by the Bonferoni-Holm method.

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Figure 7. Effect of submergence on the expression of cell wall formation-related genes. (A) Expression pattern of cell wall-related genes during 24 h of submergence. The gene expression levels in C9285 6LS and T65 6LS samples are indicated by log2-fold changes at each time point (0 h, 1 h, 3 h, 12 h and 24 h) relative to that of T65 samples before submergence. Genes with a maximal cpm value of more than 15 are shown. AGP, arabinogalactan protein; PME, pectin esterase; XTH, xyloglucan endotransglycosylases/hydrolase. (B) Changes in expression of 11 coniferyl/sinapyl alcohol dehydrogenase (CAD) genes during submergence for 24 h. Data points show expression levels as average cpm in three biological replicates and error bars show standard deviation. (C) Sampled regions of internodes for lignin quantification. C9285 plants at the seven-leaf stage (7LS) that have already formed internodes were submerged for 2 days (2 d). Photos of stems before (0 d) and after (2 d) submergence treatment of C9285 plants at the 7LS are shown. Red arrowheads indicate stem nodes. (D, E) Lignin content in the nodes and internodes before (D) and after (E) 2 d submergence of C9285 plants at 7LS. Bars represent averages of at least six biological replicates and error bars represent standard errors. Different letters indicate significant (P < 0.05) differencesaccording to the Tukey-Kramer test.

2nd node 3rd node

B

tota

l lig

nin

cont

ent (

% d

ry w

eigh

t)

D

C

E

1 cm

0 dbasal node

2 d

newly-elongated intermode

non-elongated internode

A

0

1

2

3

4

5

6

7

0

1

2

3

4

5

6

7

basalnode

2nd+3rdnode

non-elongatedinternode

basalnode

2ndnode


3rdnode

newlyelongatedinternode

2nd node

3rd node

basal node

tota

l lig

nin

cont

ent (

% d

ry w

eigh

t) 0 d 2 d

C9285 6LS T65 6LS C9285 6LS T65 6LSC9285

max cpm

α-expansinβ-expansin

XTH

PME

AGP-like

extensin-like

0 1 3 6 12 24 0 1 3 6 12 24

EXPA6 (23.26)EXPLA3 (25.47)EXPLA2 (28.02)EXPA5 (29.65)EXPLA1 (41.01)EXPA3 (47.24)EXPA2 (66.36)EXPA4 (91.77)EXPA7 (95.97)

EXPB17 (17.14)EXPB16 (18.51)EXPB7 (20.68)EXPB12 (32.76)EXPB6 (42.4)EXPB3 (205.69)EXPB4 (518.98)

XTH12 (7.76)XTH28 (11.53)XTH19 (29.16)XTH2 (31.35)XTH24 (36.15)XTH21 (37.16)XTH1 (45.29)XTH27 (64.75)XTH17 (101.83)XTH3 (140.51)XTH23 (162.11)XTH11 (226.32)XTH10 (460.38)

PME3 (21.62)PME29 (24.53)PME7 (83.85)

FLA4 (20.24)FLA5 (26.73)FLA24 (36.75)FLA11 (41.68)FLA16 (41.91)FLA1 (48.26)FLA2 (51.13)FLA6 (73.41)FLA7 (102.53)FLA3 (130.15)

OS01G0594300 (16.42)OS04G0670100 (18.23)OS02G0138000 (18.46)OS01G0180000 (21.72)OS07G0176500 (24.16)OS05G0180300 (27.48)OS02G0616100 (37.23)OS04G0505200 (90.09)


submergence time point (h)-2 0 2 4

C9285max cpm

A

B C

D E

1 cm

newlyelongated internode


2nd node

3rd node

basal nodebasal node

2nd node

3rd node1

cm

DW 0 d DW 2 d

Tota

l lig

nin

cont

ent

(% d

ry w

eigh

t)

012345678

basalnode

2nd+3rdnode


Tota

l lig

nin

cont

ent

(% d

ry w

eigh

t)

0

1

2

3

4

5

6

7

basalnode

2ndnode


3rdnode


C9285 6LS T65 6LS

0 1 3 6 12 24 0 1 3 6 12 240

20

40

60


expr

essi

on (c

pm)

CAD1

CAD2

CAD3

CAD4

CAD6

CAD7

CAD8A

CAD8B

CAD8C

CAD8D

CAD9

DW 0 d DW 2 d

log2 FCrelative to T65 0 h

EXPA11 96EXPA2 92EXPA13 66EXPA5 47EXPA12 41EXPA25 30EXPA6 28EXPA21 25EXPA7 23

EXPB4 519EXPB3 206EXPB6 42EXPB12 33EXPB7 21EXPB16 19EXPB17 17

XTH10 460XTH11 226XTH23 162XTH3 141XTH17 102XTH27 65XTH1 45XTH21 37XTH24 36XTH2 31XTH19 29 submergence time point (h)


C9285 6LS T65 6LSC9285

max cpm

α-e

xpansin

β-e

xpansin

XT

H

PM

EA

GP

-likeexte

nsin

-like

0 1 3 6 12 24 0 1 3 6 12 24

EXPA6 (23.26)EXPLA3 (25.47)EXPLA2 (28.02)EXPA5 (29.65)EXPLA1 (41.01)EXPA3 (47.24)EXPA2 (66.36)EXPA4 (91)EXPA7 (95)



PME3 (21.62)PME29 (24.53)PME7 (83.85)



-2 0 2 4

C9285A

B C

D E

1 c

m



2nd node

3rd node


2nd node

3rd node

1 c

m

DW 0 d DW 2 d

Tota

l lig

nin

conte

nt

(% d

ry w

eig

ht)

012345678

basalnode

2nd+3rdnode


Tota

l lig

nin

conte

nt

(% d

ry w

eig

ht)

0

1

2

3

4

5

6

7

basalnode

2ndnode


3rdnode


C9285 6LS T65 6LS

0 1 3 6 12 24 0 1 3 6 12 240

20

40

60


exp

ress

ion

(cp

m)

CAD1

CAD2

CAD3

CAD4

CAD6

CAD7

CAD8A

CAD8B

CAD8C

CAD8D

CAD9

DW 0 d DW 2 d


0 1 3 6 12 24

C9285 6LS T65 6LS

0 1 3 6 12 24 0 1 3 6 12 24



C9285 6LS T65 6LSC9285

max cpm


XTH

PM

EA

GP

-likeextensin-like

0 1 3 6 12 24 0 1 3 6 12 24




PME3 (21.62)PME29 (24.53)PME7 (83.85)



-2 0 2 4

C9285A

B C

D E

1 cm



2nd node

3rd node


2nd node

3rd node

1 cm

DW 0 d DW 2 d

Tota

l lig

nin

cont

ent

(% d

ry w

eigh

t)

012345678

basalnode

2nd+3rdnode


Tota

l lig

nin

cont

ent

(% d

ry w

eigh

t)

0

1

2

3

4

5

6

7

basalnode

2ndnode


3rdnode


C9285 6LS T65 6LS

0 1 3 6 12 24 0 1 3 6 12 240

20

40

60


expr

essi

on (c

pm)

CAD1

CAD2

CAD3

CAD4

CAD6

CAD7

CAD8A

CAD8B

CAD8C

CAD8D

CAD9

DW 0 d DW 2 d


0 1 3 6 12 24

C9285 6LS T65 6LS

0 1 3 6 12 24 0 1 3 6 12 24

Os01g0880300 84Os10g0407000 25Os01g0312500 22

FLA3 130FLA7 103FLA6 73FLA2 51FLA1 48FLA16 42FLA11 42FLA24 37FLA5 27FLA4 20

Os04g0505200 90Os02g0616100 37Os05g0180300 27Os07g0176500 24Os01g0180000 22Os02g0138000 18Os04g0670100 18Os01g0594300 16

C9Max (cpm)





C9285 6LS T65 6LSC9285

max cpm

α-e

xpansin

β-e

xpansin

XT

H

PM

EA

GP

-likeexte

nsin

-like

0 1 3 6 12 24 0 1 3 6 12 24




PME3 (21.62)PME29 (24.53)PME7 (83.85)



-2 0 2 4

C9285A

B C

D E

1 c

m



2nd node

3rd node


2nd node

3rd node

1 c

m

DW 0 d DW 2 d

Tota

l lig

nin

conte

nt

(% d

ry w

eig

ht)

012345678

basalnode

2nd+3rdnode


Tota

l lig

nin

conte

nt

(% d

ry w

eig

ht)

0

1

2

3

4

5

6

7

basalnode

2ndnode


3rdnode


C9285 6LS T65 6LS

0 1 3 6 12 24 0 1 3 6 12 240

20

40

60


exp

ress

ion

(cp

m)

CAD1

CAD2

CAD3

CAD4

CAD6

CAD7

CAD8A

CAD8B

CAD8C

CAD8D

CAD9

DW 0 d DW 2 d


0 1 3 6 12 24

C9285 6LS T65 6LS

0 1 3 6 12 24 0 1 3 6 12 24

C9Max (cpm)



C9285 6LS T65 6LSC9285

max cpm


XTH

PM

EA

GP

-likeextensin-like

0 1 3 6 12 24 0 1 3 6 12 24




PME3 (21.62)PME29 (24.53)PME7 (83.85)



-2 0 2 4

C9285A

B C

D E

1 cm



2nd node

3rd node


2nd node

3rd node1

cm

DW 0 d DW 2 d

Tota

l lig

nin

cont

ent

(% d

ry w

eigh

t)

012345678

basalnode

2nd+3rdnode


Tota

l lig

nin

cont

ent

(% d

ry w

eigh

t)

0

1

2

3

4

5

6

7

basalnode

2ndnode


3rdnode


C9285 6LS T65 6LS

0 1 3 6 12 24 0 1 3 6 12 240

20

40

60


expr

essi

on (c

pm)

CAD1

CAD2

CAD3

CAD4

CAD6

CAD7

CAD8A

CAD8B

CAD8C

CAD8D

CAD9

DW 0 d DW 2 d


0 1 3 6 12 24

C9285 6LS T65 6LS

0 1 3 6 12 24 0 1 3 6 12 24



C9285 6LS T65 6LSC9285

max cpm


XTH

PM

EA

GP

-likeextensin-like

0 1 3 6 12 24 0 1 3 6 12 24




PME3 (21.62)PME29 (24.53)PME7 (83.85)



-2 0 2 4

C9285A

B C

D E

1 cm



2nd node

3rd node


2nd node

3rd node

1 cm

DW 0 d DW 2 d

Tota

l lig

nin

cont

ent

(% d

ry w

eigh

t)

012345678

basalnode

2nd+3rdnode


Tota

l lig

nin

cont

ent

(% d

ry w

eigh

t)

0

1

2

3

4

5

6

7

basalnode

2ndnode


3rdnode


C9285 6LS T65 6LS

0 1 3 6 12 24 0 1 3 6 12 240

20

40

60


expr

essi

on (c

pm)

CAD1

CAD2

CAD3

CAD4

CAD6

CAD7

CAD8A

CAD8B

CAD8C

CAD8D

CAD9

DW 0 d DW 2 d


0 1 3 6 12 24

C9285 6LS T65 6LS

0 1 3 6 12 24 0 1 3 6 12 24submergence time point (h)


C9285 6LS T65 6LSC9285

max cpm


XTH

PM

EA

GP

-likeextensin-like

0 1 3 6 12 24 0 1 3 6 12 24




PME3 (21.62)PME29 (24.53)PME7 (83.85)



-2 0 2 4

C9285A

B C

D E1

cm



2nd node

3rd node


2nd node

3rd node

1 cm

DW 0 d DW 2 d

Tota

l lig

nin

cont

ent

(% d

ry w

eigh

t)

012345678

basalnode

2nd+3rdnode


Tota

l lig

nin

cont

ent

(% d

ry w

eigh

t)

0

1

2

3

4

5

6

7

basalnode

2ndnode


3rdnode


C9285 6LS T65 6LS

0 1 3 6 12 24 0 1 3 6 12 240

20

40

60


expr

essi

on (c

pm)

CAD1

CAD2

CAD3

CAD4

CAD6

CAD7

CAD8A

CAD8B

CAD8C

CAD8D

CAD9

DW 0 d DW 2 d


0 1 3 6 12 24

C9285 6LS T65 6LS

0 1 3 6 12 24 0 1 3 6 12 24

XTH

β-ex

pans

inα-

expa

nsin

fasc

iclin

-like

AG

Pex

tens

in-li

ke



C9285 6LS T65 6LSC9285

max cpm


XTH

PM

EA

GP

-likeextensin-like

0 1 3 6 12 24 0 1 3 6 12 24




PME3 (21.62)PME29 (24.53)PME7 (83.85)



-2 0 2 4

C9285A

B C

D E

1 cm



2nd node

3rd node


2nd node

3rd node

1 cm

DW 0 d DW 2 d

Tota

l lig

nin

cont

ent

(% d

ry w

eigh

t)

012345678

basalnode

2nd+3rdnode


Tota

l lig

nin

cont

ent

(% d

ry w

eigh

t)

0

1

2

3

4

5

6

7

basalnode

2ndnode


3rdnode


C9285 6LS T65 6LS

0 1 3 6 12 24 0 1 3 6 12 240

20

40

60


expr

essi

on (c

pm)

CAD1

CAD2

CAD3

CAD4

CAD6

CAD7

CAD8A

CAD8B

CAD8C

CAD8D

CAD9

DW 0 d DW 2 d


0 1 3 6 12 24

C9285 6LS T65 6LS

0 1 3 6 12 24 0 1 3 6 12 24

PM

E

a a aa

aa

bb



Figure 8. Submergence-induced transcripts from C9285-unique loci.Expression from selected loci which are presumably absent in the IRGSP1.0 reference genome is shown. Each row represents one locus, columns represent samples from different time points after submergence and colors represent gene expression levels as log2 transformed counts per million values (cpm) normalized to the average expression in all samples of different time points. Genes that have an at least two-fold increase in expression after submergence in C9285 6 LS plants are shown. Complete expression data from C9285-unique transcripts can be found in Supplemental Dataset 10 and sequence data is provided in Supplemental Datasets 12 to 14.

contig_31:434-1084contig_22:1359-2511contig_23:2082-5157contig_14:1058-2399contig_12:7770-10275contig_3:7545-12614contig_7:4617-9033contig_22:2607-4832contig_13:2616-6249contig_24:803-5067contig_8:9243-11357contig_20:2230-5386contig_28:769-3481contig_2:4464-6707contig_17:810-6158contig_21:785-1970contig_29:1648-2639

0 1 3 6 12 24submergence time point (h)

-2 -1 0 1

average log2 FC

relative to row mean

con�glength pep�delength(bp) (AA)2921 272 OsI_30077NB-ARCdomainprotein5576 257 SK1ethyleneresponsefactor6299 974 XP_006663590RPM1-likediseaseresistanceprotein16325 681 OsJ_13717DUFprotein3549 306 XP_004952393thauma�n-likeprotein1b5788 378 XP_006660338RGA4-likediseaseresistanceprotein12025 259 SK2ethyleneresponsefactor5091 104 OSJNBa0019J05.12RT-LTRrelatedprotein9804 611 OsI_14912puta�veSAM-dependentmethyltransferase5753 512 EMT18893DiseaseresistanceproteinRPM12074 1042 XP_006657081LRRreceptorkinase,EFR-like15513 810 NBS-LRRtypeprotein10276 835 puta�veRNAhelicase9621 140 puta�veTy1-copiaretrotransposonprotein5223 239 Cysteine-richreceptor-likeproteinkinase85753 147 DiseaseresistanceproteinRPM12453 172 OsI_30538,hypothe�calprotein

descrip�on



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http://www.ncbi.nlm.nih.gov/pubmed?term=Ayano M%2C Kani T%2C Kojima M%2C Sakakibara H%2C Kitaoka T%2C Kuroha T%2C Angeles%2DShim RB%2C Kitano H%2C Nagai K%2C Ashikari M %282014%29 Gibberellin biosynthesis and signal transduction is essential for internode elongation in deepwater rice%2E Plant Cell Environ%2E 37%3A 2313�??2324%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Ayano M, Kani T, Kojima M, Sakakibara H, Kitaoka T, Kuroha T, Angeles-Shim RB, Kitano H, Nagai K, Ashikari M (2014) Gibberellin biosynthesis and signal transduction is essential for internode elongation in deepwater rice. Plant Cell Environ. 37: 2313?2324.

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ayano&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Gibberellin biosynthesis and signal transduction is essential for internode elongation in deepwater rice&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Gibberellin biosynthesis and signal transduction is essential for internode elongation in deepwater rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ayano&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Azuma T%2C Hirano T%2C Deki Y%2C Uchida N%2C Yasua T%2C Yamaguchi T %281995%29 Involvement of the decrease in levels of abscisic acid in the internodal elongation of submerged floating rice%2E J Plant Physiol 146%3A 323�??328%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Azuma T, Hirano T, Deki Y, Uchida N, Yasua T, Yamaguchi T (1995) Involvement of the decrease in levels of abscisic acid in the internodal elongation of submerged floating rice. J Plant Physiol 146: 323?328.

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Azuma&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Involvement of the decrease in levels of abscisic acid in the internodal elongation of submerged floating rice&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Involvement of the decrease in levels of abscisic acid in the internodal elongation of submerged floating rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Azuma&as_ylo=1995&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Bailey TL%2C Elkan C %281994%29 Fitting a mixture model by expectation maximization to discover motifs in biopolymers%2E Proc Int Conf Intell Syst Mol Biol 2%3A 28�??36%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2: 28?36.

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Bailey&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Fitting a mixture model by expectation maximization to discover motifs in biopolymers&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Fitting a mixture model by expectation maximization to discover motifs in biopolymers&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Bailey&as_ylo=1994&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Bailey%2DSerres J%2C Voesenek%2C Laurentius A C J %282008%29 Flooding stress%3A acclimations and genetic diversity%2E Annu Rev Plant Biol 59%3A 313�??339%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Bailey-Serres J, Voesenek, Laurentius A C J (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 59: 313?339.

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Bailey-Serres&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Flooding stress: acclimations and genetic diversity&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Flooding stress: acclimations and genetic diversity&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Bailey-Serres&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Bailey%2DSerres J%2C Voesenek%2C Laurentius A C J %282010%29 Life in the balance%3A a signaling network controlling survival of flooding%2E Curr Opin Plant Biol 13%3A 489�??494%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Bailey-Serres J, Voesenek, Laurentius A C J (2010) Life in the balance: a signaling network controlling survival of flooding. Curr Opin Plant Biol 13: 489?494.

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http://www.ncbi.nlm.nih.gov/pubmed?term=Laudert D%2C Pfannschmidt U%2C Lottspeich F%2C Holl�nder%2DCzytko H%2C Weiler%2C EW %281996%29 Cloning%2C molecular and functional characterization of Arabidopsis thaliana allene oxide synthase %28CYP 74%29%2C the first enzyme of the octadecanoid pathway to jasmonates%2E Plant Mol%2E Biol%2E 31%3A 323%2D335%2E&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Mizoi J%2C Ohori T%2C Moriwaki T%2C Kidokoro S%2C Todaka D%2C Maruyama K%2C Kusakabe K%2C Osakabe Y%2C Shinozaki K%2C Yamaguchi%2DShinozaki K %282013%29 GmDREB2A%3B2%2C a canonical DEHYDRATION%2DRESPONSIVE ELEMENT%2DBINDING PROTEIN2%2Dtype transcription factor in soybean%2C is posttranslationally regulated and mediates dehydration%2Dresponsive element%2Ddependent gene expression%2E Plant Physiol 161%3A 346�??361%2E&dopt=abstract

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Zarembinski TI, Theologis A (1997) Expression characteristics of OS-ACS1 and OS-ACS2, two members of the 1-aminocyclopropane-1-carboxylate synthase gene family in rice (Oryza sativa L. cv. Habiganj Aman II) during partial submergence. Plant Mol Biol 33: 71–77.


Zhang H, Zhang J, Quan R, Pan X, Wan L, Huang R (2013) EAR motif mutation of rice OsERF3 alters the regulation of ethylenebiosynthesis and drought tolerance. Planta 237: 1443–1451.

Pubmed: Author and Title www.plantphysiol.orgon June 23, 2020 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

http://www.ncbi.nlm.nih.gov/pubmed?term=Wang KL%2DC%2C Li H%2C Ecker JR %282002%29 Ethylene biosynthesis and signaling networks%2E Plant Cell 14 Suppl%3A S131%2D151%2E&dopt=abstract

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http://search.crossref.org/?page=1&rows=2&q=Zhang H, Zhang J, Quan R, Pan X, Wan L, Huang R (2013) EAR motif mutation of rice OsERF3 alters the regulation of ethylene biosynthesis and drought tolerance. Planta 237: 1443?1451.

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http://scholar.google.com/scholar?as_q=EAR motif mutation of rice OsERF3 alters the regulation of ethylene biosynthesis and drought tolerance&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhou X%2C Zhang Z%2DL%2C Park J%2C Tyler L%2C Yusuke J%2C Qiu K%2C Nam EA%2C Lumba S%2C Desveaux D%2C McCourt P%2C Kamiya Y%2C Sun T%2DP %282016%29 The ERF11 Transcription Factor Promotes Internode Elongation by Activating Gibberellin Biosynthesis and Signaling%2E Plant Physiol 171%3A 2760�??2770%2E&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zhou&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The ERF11 Transcription Factor Promotes Internode Elongation by Activating Gibberellin Biosynthesis and Signaling&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The ERF11 Transcription Factor Promotes Internode Elongation by Activating Gibberellin Biosynthesis and Signaling&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhou&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhu G%2C Ye N%2C Zhang J %282009%29 Glucose%2Dinduced delay of seed germination in rice is mediated by the suppression of ABA catabolism rather than an enhancement of ABA biosynthesis%2E Plant Cell Physiol 50%3A 644�??651%2E&dopt=abstract

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http://scholar.google.com/scholar?as_q=Glucose-induced delay of seed germination in rice is mediated by the suppression of ABA catabolism rather than an enhancement of ABA biosynthesis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhu&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

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http://scholar.google.com/scholar?as_q=The Arabidopsis AP2/ERF transcription factor RAP2&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The Arabidopsis AP2/ERF transcription factor RAP2&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhu&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zhu Y%2C Nomura T%2C Xu Y%2C Zhang Y%2C Peng Y%2C Mao B%2C Hanada A%2C Zhou H%2C Wang R%2C Li P%2C Zhu X%2C Mander LN%2C Kamiya Y%2C Yamaguchi S%2C He Z %282006%29 ELONGATED UPPERMOST INTERNODE encodes a cytochrome P450 monooxygenase that epoxidizes gibberellins in a novel deactivation reaction in rice%2E Plant Cell 18%3A 442�??456%2E&dopt=abstract

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http://scholar.google.com/scholar?as_q=ELONGATED UPPERMOST INTERNODE encodes a cytochrome P450 monooxygenase that epoxidizes gibberellins in a novel deactivation reaction in rice&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhu&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1


Time-course transcriptomics analysis reveals key responses ...€¦ · energy and then resume...

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Transcript of Time-course transcriptomics analysis reveals key responses ...€¦ · energy and then resume...