The SnRK1 kinase as central mediator of energy signalling ... · limitation, plants react to...

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Update on SnRK1 Signalling 1

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The SnRK1 kinase as central mediator of energy signalling between different organelles1 3

Bernhard Wurzinger2, Ella Nukarinen2, Thomas Nägele2, Wolfram Weckwerth2,3, and Markus Teige2,4 4

2Molecular Systems Biology, Faculty of Life Sciences, University of Vienna, Althanstr. 14, A-1090 5

Vienna, Austria; 3Vienna Metabolomics Center (VIME), University of Vienna 6

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Author contributions: 8

B.W., E.N., and M.T. drafted and wrote the article, T.N., and W.W. revised the article. 9

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Abstract 11

The evolutionary conserved SnRK1 kinase complex is a key regulator in adjusting cellular metabolism 12

during starvation, stress conditions and growth promoting conditions. Over the last two decades 13

extensive genetic evidence for a widespread SnRK1 signalling network has accumulated. It is now 14

well established that SnRK1 is a central integrator of energy signalling. However, little is known about 15

connections between the cytoplasmic and nuclear localized SnRK1 and plastids and mitochondria as 16

the main energy producing compartments in the cell. Here we review recent findings indicating how 17

SnRK1 affects metabolic adaptation including plastidial and mitochondrial functions. Special 18

emphasis is put on identified direct targets of SnRK1, which would eventually enable cross talk with 19

organelles. In this context a number of transcription factors are emerging as mediators of SnRK1 20

signalling, potentially linking SnRK1 activity to organellar functions. Furthermore, many SnRK1 targets 21

act in various hormonal signalling pathways, which are at least partly localized in plastids. With this 22

review, we summarize the current knowledge on SnRK1 organelle interaction and provide ideas on 23

the potential molecular mechanisms governing these interactions. 24

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Summary: 26

SnRK1 is a central integrator of energy signalling in different subcellular locations with emerging roles 27

in organellar and hormone metabolism. 28

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Key words 30

1 This work has been funded by the Austrian Science Fund (FWF) with project P 28491 (to MT) and I 2071 (to TN and WW) as well as by the EU in the framework of the Marie Curie ITNs CALIPSO (GA ITN 2013 ITN-607 607) and MERIT (GA ITN 2010-264 474). 4address correspondence to: [email protected]

Plant Physiology Preview. Published on January 8, 2018, as DOI:10.1104/pp.17.01404

Copyright 2018 by the American Society of Plant Biologists

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SnRK1 kinase, metabolic regulation, stress response, organellar energy metabolism 31

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Abbreviations 35

ABA, abscisic acid; AMPK, AMP-activated protein kinase; AKIN10/11, Arabidopsis Kinase 10/11 36

(kinase subunits of the SnRK1 complex); BCAA, branched-chain amino acid; bHLH, basic helix-loop-37

helix; bZIP, basic leucine zipper; CDPK, calcium-dependent protein kinase; DCMU, 3-(3,4-38

dichlorophenyl)-1,1-dimethylurea; ETC, electron transport chain; ETF, electron transfer flavoprotein; 39

ETFQO, ETF ubiquinone oxidoreductase; F2KP, fructose-2,6-bisphosphatase ; JA, jasmonic acid; LHC, 40

light-harvesting complex; MPK, mitogen-activated protein kinase; PS, photosystem; ROS, reactive 41

oxygen species; SNF1, sucrose non-fermenting kinase 1; SnRK1, SNF1-related protein kinase 1; T6P, 42

Trehalose 6-phosphate 43

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Metabolic reprogramming by SnRK1 kinase activity under different growth and stress conditions 45

Already under optimal growth conditions plants need to continuously adjust their metabolic balance 46

between autotrophic growth based on photosynthesis during the day and respiration during the 47

night. At daytime, sugars and other metabolites are produced by photosynthesis in chloroplasts and 48

further distributed to be used in other metabolic pathways at different cellular compartments or 49

transported to non-photosynthetic sink tissues. During the night, starch and sugars supply carbon 50

equivalents for respiration providing the necessary energy for further growth and metabolic 51

activities. Additionally, metabolic reprogramming is required for plants to adjust their metabolism to 52

diverse biotic and abiotic environmental stimuli. This often leads to a stop of plant growth involving a 53

reduction in ribosomal protein synthesis, and in parallel, accumulation of protective metabolites or 54

defence compounds. This switching of cellular energy metabolism is mediated by the activity of the 55

evolutionary conserved AMPK/SNF1/SnRK1 kinase complex (Baena-Gonzalez and Sheen, 2008; 56

Broeckx et al., 2016). The heterotrimeric SNF1-related protein kinase 1 (SnRK1) is the plant 57

orthologue of the yeast SNF1 (sucrose non-fermenting 1) kinase and the mammalian AMPK (AMP-58

activated protein kinase). In Arabidopsis, AKIN10 and AKIN11, the kinase subunits of the SnRK1 59

complex, were found to regulate the expression of more than 600 target genes in response to 60

starvation or nutrient signals in protoplasts (Baena-Gonzalez et al., 2007). However, being a protein 61

kinase, direct targets of SnRK1 need to be measured by phospho-proteomics. To this end, we applied 62

a quantitative phospho-proteomic approach combined with proteomics and metabolomics to 63

identify in vivo targets of SnRK1 and to uncover the related metabolic reprograming using SnRK1 64

mutants under energy starvation (Nukarinen et al., 2016). This study revealed hundreds of changed 65

phosphoproteins and a very pronounced SnRK1-dependent reprogramming of metabolism including 66

sugars. 67

Besides being the universal fuel of life, sugars also act as important developmental signals. 68

Accordingly, all biological systems have evolved homeostatic mechanisms to regulate their sugar 69

levels. For example, the level of glucose functions as ancient and conserved regulatory signal 70



3

controlling gene expression and primary and secondary metabolism, as well as growth and 71

development (Sheen, 2014; Wingler et al., 2017). Plants have three known glucose-modulated 72

master regulators: HEXOKINASE1, a direct glucose sensor (Moore et al., 2003; Li et al., 2016); the 73

energy sensing protein kinase SnRK1, which is inhibited by sugars (Baena-Gonzalez and Sheen, 2008); 74

and the TARGET OF RAPAMYCIN (TOR) kinase, which is activated by glucose (Xiong et al., 2013). 75

These major regulators of energy metabolism are evolutionary highly conserved and the 76

protokinases can be found in all three domains of life (Roustan et al., 2016). In response to energy 77

deficits the AMPK/SNF1/SnRK1 kinases restore energy homeostasis by switching on ATP-producing 78

catabolic pathways (such as glycolysis and fatty acid oxidation), while in parallel switching off 79

biosynthetic and other non-essential ATP-consuming metabolic- and growth processes. SnRK1 plays a 80

central role in the regulation of starch metabolism. In the moss Physcomitrella patens it was 81

observed that a SNF1a/b double knockout revealed reduced starch mobilisation in response to 82

darkness (Thelander et al., 2004). Similarly, Baena-González et al. (2007) found that virus-induced 83

gene silencing of AKIN10/11 impaired starch mobilisation also in Arabidopsis during the night. 84

However, it is important to note that SnRK1 can have quite different roles in source and sink tissues. 85

For example, opposite effects have been observed in starch metabolism where overexpression of 86

AKIN10 in Arabidopsis leaves led to reduced glucose-induced starch accumulation in seedlings 87

(Jossier et al., 2009), while SnRK1 overexpression increased starch accumulation in potato tubers 88

(McKibbin et al., 2006). A first mechanistic insight into AKIN10-dependent starch mobilisation came 89

from the observation that a luciferase reporter gene was specifically activated by AKIN10 co-90

expression via the α-amylase Amy3-SRC promoter (Lin et al., 2014). The tissue-specific differential 91

expression of SnRK1-interacting negative regulators (SKINs) offers a way to explain the seemingly 92

contradictory influence of SnRK1 on starch metabolism in different tissues (Lin et al., 2014). 93

However, in conclusion it becomes evident, that not all modulators of SnRK1 activity under different 94

conditions in different tissues have been identified yet. Overall, it is clear that SnRK1 can be activated 95

by very diverse abiotic and biotic stress conditions that directly or indirectly cause an energy deficit 96

by affecting photosynthesis, respiration, or carbon allocation, and the activity of the SnRK1 kinase 97

complex is repressed by sugars (Baena-González et al., 2007). Still, the exact mechanisms of this 98

inhibition as well as the identity of other inhibitors remain unclear (Emanuelle et al., 2016). The 99

kinase subunits AKIN10 and AKIN11 are found in the nucleus and the cytosol, and additionally, a 100

chloroplast localization of AKIN10 has been reported (Fragoso et al., 2009) but could not be 101

confirmed (Bayer et al., 2012). Nevertheless, the regulation of photosynthesis is intimately linked to 102

energy metabolism and accordingly functional links between AKIN10/11 activity and chloroplast 103

functions have been reported. For example, AKIN10 is activated by 3-(3,4-dichlorophenyl)-1,1-104

dimethylurea (DCMU) treatment (Baena González et al., 2007), which blocks electron transport at 105

photosystem II (PSII), thus leading to energy deprivation by inhibiting photosynthesis. Moreover, 106

many photosynthetic genes were found to be regulated transcriptionally depending on SnRK1 107

activity mediated by trehalose-6-phosphate (T6P) (Zhang et al., 2009). The role of sugar signalling and 108

SnRK1 activity is discussed in detail in another update review of this issue (Wingler et al., 2017). 109

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SnRK1 in metabolic- and hormone signalling under stress conditions 112



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SnRK1 activation is also triggered by hypoxia leading to suppression of mitochondrial aerobic 113

respiration resulting in cellular energy deprivation (Im et al., 2014; Cho et al., 2016). Flooding stress 114

or hypoxia lead to a reduced availability of O2 as the final electron acceptor in the mitochondrial 115

electron transport chain (mETC), causing a rapid decrease in the cellular ATP:ADP ratio (Bailey-Serres 116

and Voesenek, 2008). Cells cope with this energy crisis by relying primarily on glycolysis and 117

fermentation to generate ATP and regenerate NAD+, respectively. To overcome this critical energy 118

limitation, plants react to hypoxia and flooding stress by limiting protein synthesis and maintaining 119

translation of a subset of cellular mRNAs, many of which encode enzymes involved in anaerobic 120

metabolism and reactive oxygen species (ROS) scavenging as well as the mobilization of storage 121

compounds such as starch. This includes also amino acid and nitrogen metabolism for example at the 122

level of nitrate reductase (NR) activity or amino acids fuelling the citric acid cycle. Such conditions 123

could even lead to ATP-import by mitochondria, mediated by Ca2+-regulated importers (Stael et al., 124

2011). Following the submergence-induced hypoxia, the subsequent exposure to oxygen during 125

reoxygenation produces a burst of ROS. Recently it was shown that ROS inhibit SnRK1 kinase activity, 126

which would be consistent with a termination of hypoxia-induced SnRK1 signalling at the beginning 127

of the reoxygenation phase (Wurzinger et al., 2017). This reoxygenation phase involves also a rapid 128

accumulation of jasmonates (JAs) and increased transcript levels of JA biosynthesis genes. Mutants 129

deficient in JA biosynthesis and signalling were found to be sensitive to reoxygenation, which was 130

linked to the function of the basic helix-loop-helix (bHLH) transcription factor (TF) MYC2, a key 131

regulator of JA-signalling (Yuan et al., 2017). MYC2 overexpression enhanced the tolerance to post-132

hypoxic stress, and myc2 knockout mutants showed increased sensitivity to reoxygenation. In a 133

previous study it was shown that AKIN10 overexpression resulted in decreased MYC2 protein levels 134

which could be counteracted by addition of proteasome inhibitor MG132. The authors demonstrated 135

that AKIN10 and MYC2 physically interact and identified the serine which when phosphorylated is 136

crucial for proteasomal degradation of MYC2 (Im et al., 2014). 137

Plants activate ethylene signalling in response to flooding stress to initiate enhanced hypocotyl 138

growth leading to the emergence of shoots (Bailey-Serres and Voesenek, 2008; Sasidharan and 139

Voesenek, 2015). A comparison of transcriptional responses to darkness in air and under submerged 140

conditions revealed a common early transcriptional and posttranscriptional response signature that 141

was conserved primarily across Arabidopsis genotypes (van Veen et al., 2016). The common set of 142

downregulated genes (shared between negative clusters of ethylene and shade) was highly enriched 143

in photosynthesis-related proteins, thus indicating a transient downregulation of photosynthesis 144

during enhanced growth to induce accelerated shoot elongation to bring leaf tips from the water 145

layer into the air (Sasidharan and Voesenek, 2015). Overall, this low-energy escape syndrome (LOES) 146

shows a remarkable overlap with shade avoidance responses (Das et al., 2016). Notably, both 147

ethylene signalling and SnRK1 kinase activity were reported to have a role in flooding-induced 148

hypoxia tolerance in plants. A functional link between ethylene signalling, photosynthesis and 149

AKIN10 activity was recently reported (Kim et al., 2017a). It was shown that PSII activity is involved in 150

the regulation of ethylene-inducible Arabidopsis hypocotyl growth in the light. A lack of ethylene 151

responsiveness in etr1 mutants causes PSII inefficiency, leading to cellular energy deprivation and 152

activation of AKIN10 expression. This, in turn, suppresses ethylene-inducible hypocotyl growth in the 153

light. 154

The important regulatory function of SnRK1 for sugar- and nitrate metabolism and its connection to 155

ABA signalling has been shown in a number of biochemical analyses of SnRK1 mutants (Jossier et al., 156



5

2009). Mechanistically this connection was further underpinned by the identification of two clade A 157

type 2C protein phosphatases (PP2Cs), both established repressors of the abscisic acid (ABA) 158

hormonal pathway, as interactors and negative regulators of the SnRK1 catalytic subunit causing its 159

de-phosphorylation (Rodrigues et al., 2013). However, the ABA core signalling pathway is mainly 160

regulated by the activation of SnRK2 kinases resulting in rapid responses, including the regulation of 161

ion channels resulting in stomatal closure, and gene expression via AREB TFs to modulate plant 162

growth to respond to the stress condition (Munemasa et al., 2015; Fujita et al., 2013). Under osmotic 163

stress conditions, ABA does also control the activity of the starch amylases BAM1 and AMY3 in leaves 164

through the AREB/ABF-SnRK2 kinase-signalling pathway (Thalmann et al., 2016). Moreover, SnRK1 165

has also been identified as regulator of the MYC2 TF in the regulation of ABA responsive elements 166

(Im et al., 2014), and a further functional link between SnRK1 and ABA signalling was provided in a 167

study of sucrose responses in apple where the overexpression of the C2-domain ABA Insensitive 168

Protein1 (MdCAIP1) was found to cause insensitivity towards ABA (Liu et al., 2017a). This phenotype 169

was abolished in presence of active MdSnRK1 which was shown to directly phosphorylate MdCAIP1 170

and thereby rendering it a target for 26S-proteasomal degradation. Another link to JA signalling was 171

provided by the report that MdSnRK1.1 interacted with the MdJAZ18 protein, which acts as a 172

repressor of JA signalling. MdSnRK1.1 phosphorylated MdJAZ18 to facilitate its 26S proteasome-173

mediated degradation (Liu et al., 2017b). Under conditions of sucrose over supply and without JA, 174

MdJAZ18 binds to the transcription factor MdbHLH3 rendering it inactive towards anthocyanin 175

biosynthesis gene activation. In their study, the authors describe a direct phosphorylation of 176

MdJAZ18 by MdSnRK1, which subsequently leads to degradation of MdJAZ18 by the 26S-proteasome 177

(Liu et al., 2017b). All together, these data do nicely illustrate the intense crosstalk among the 178

ethylene, JA and ABA signalling pathways and indicate that SnRK1 acts as one key regulator in these 179

interconnections. 180

SnRK1 as regulator of developmental transitions 181

Light does not only drive photosynthesis and thereby energy metabolism, it serves also as important 182

signal for many developmental switches during the life cycle of a plant. At the end of the life cycle, 183

plants undergo senescence, which is a coordinated redistribution of resources such as nitrogen from 184

the source (i.e. chloroplasts) to sink tissues such as seeds. Ethylene signalling is a key regulator of 185

senescence and involves a set of transcription factors including ETHYLENE INSENSITIVE3 (EIN3). 186

AKIN10 directly interacts, phosphorylates and antagonistically modulates EIN3 activity. Consistently, 187

DCMU-treatment of plants slows down senescence progression through destabilization of EIN3 in 188

Arabidopsis (Kim et al., 2017b). Plant leaf senescence involves autophagy (Liu and Bassham, 2012), 189

and recently AKIN10 was identified as a positive regulator of plant autophagy. Transgenic Arabidopsis 190

lines overexpressing AKIN10 show delayed leaf senescence and increased tolerance to nutrient 191

starvation and abiotic stresses, and a functional autophagy pathway was found to require AKIN10 192

activity (Baena-Gonzalez et al., 2007; Chen et al., 2017, Soto-Burgos and Bassham, 2017). Moreover, 193

phosphorylation of ATG1 (AUTOPHAGY RELATED GENE 1), the plant orthologue of mammalian ULK1, 194

was enhanced when AKIN10 was overexpressed indicating that the mechanism of autophagy 195

activation is conserved between plants and animals (Chen et al. 2017). This is consistent with the 196

results that similarly to overexpression of AKIN10 and reduced expression of AKIN10 and AKIN11, 197

also a decreased and increased T6P content delays and accelerates senescence, respectively (Baena-198

Gonzalez et al., 2007; Wingler et al., 2012). 199



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Another level of complexity to these regulatory circuits is added by the circadian regulation of gene 200

expression, which is evident for the nuclear encoded photosynthesis genes such as chlorophyll 201

binding proteins (Harmer et al., 2000). Sugar is the major outcome of photosynthesis and recently a 202

link between ethylene- and sugar-signalling and the circadian clock was established by the finding 203

that ethylene shortens the circadian period, depending on sucrose and the circadian clock evening-204

element GIGANTEA (GI) (Haydon et al., 2017). These findings reveal that sucrose affects the stability 205

of circadian oscillator proteins and can mask the effects of ethylene on the circadian system 206

identifying novel molecular pathways for input of sugar to the Arabidopsis circadian network. A 207

functional link between the circadian clock and AKIN10 was found by the observation that elevated 208

AKIN10 expression delayed the peak expression of GI under diurnal conditions, and it lengthened the 209

clock period specifically under light conditions (Shin et al., 2017). Previously, it has also been shown 210

that inhibition of photosynthesis and thereby of the endogenous oscillations in sugar levels mediates 211

a metabolic feedback to the clock through the morning-expressed gene PSEUDO-RESPONSE 212

REGULATOR 7 (PRR7), and that prr7 mutants are insensitive to the effects of sucrose on the circadian 213

period (Haydon et al., 2013). 214

Sugar metabolism and the allocation of sugars between tissues is intimately associated with 215

flowering transition in plants. A functional link between the regulation of flowering time, sugar levels 216

and SnRK1 activity became evident from the observations that overexpression of AKIN10 delayed 217

flowering (Baena-González et al., 2007) and the finding that a loss of TPS1 causes extremely late 218

flowering in Arabidopsis, even under otherwise inductive environmental conditions (Wahl et al., 219

2013). More recently, a direct link between SnRK1 and the regulation of flowering time was shown in 220

a study reporting that AKIN10 interacts with the INDETERMINATE DOMAIN (IDD)-containing TF IDD8 221

in the nucleus and phosphorylates IDD8 primarily at two serine (Ser) residues, Ser-178 and Ser-182 222

(Jeong et al., 2015). IDD8 regulates flowering time by modulating sugar metabolism and transport 223

under sugar-limiting conditions in Arabidopsis. The phosphorylated serine residues in IDD8 reside in 224

the fourth zinc finger (ZF) domain that mediates DNA binding and protein-protein interactions. The 225

AKIN10-mediated phosphorylation of IDD8 reduced its transcriptional activation ability but did not 226

affect the subcellular localization and DNA-binding property of IDD8. Similarly, the phosphorylation 227

of the bZIP transcription factor bZIP63 by AKIN10 at two evolutionary conserved Ser residues was 228

found to regulate its (hetero-) dimerization status and thereby target gene specificity upon low-229

energy stress (Mair et al., 2015), and a phosphorylation of bZIP63 in its DNA binding domain was also 230

shown to impair its DNA binding ability (Kirchler et al., 2010). 231

Metabolic signals via regulation of enzymes as targets of SnRK1 232

As outlined before, the switching of cellular metabolism is a hallmark of SnRK1 signalling and has 233

been clearly demonstrated in vivo by a recent study on SnRK1 mutants under energy starvation 234

combining quantitative phospho-proteomics and metabolomics (Nukarinen et al., 2016). Such a 235

reprogramming of cellular (energy) metabolism by SnRK1 can, in principle, be achieved by two 236

different modes of action: (i) by a direct phosphorylation of metabolic enzymes, resulting either in an 237

altered enzymatic activity or protein stability; or (ii) by changing transcript levels of key enzymes for 238

metabolic pathways. In fact, various examples for both possibilities have been reported as recently 239

reviewed in (Broeckx et al., 2016). Key metabolic enzymes in the cytosol such as sucrose phosphate 240

synthase (SPS), nitrate reductase (NR), trehalose 6-phosphate synthase 5 (TPS5) or HMG-CoA 241

reductase (HMGR) have been identified as direct targets of SnRK1 in vitro (Jossier et al., 2009; 242

Robertlee et al., 2017), and in vivo (Nukarinen et al., 2016). Quantitative phospho-proteomics 243



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revealed altered phosphorylation levels of SnRK1 target sites in planta using an artificial miRNA 244

knock-down approach to silence both, AKIN10 as well as AKIN11 (Nukarinen et al., 2016). It should be 245

noted here, that those metabolic enzymes are also targeted by other kinases such as CDPKs or MAP-246

kinases and therefore seem to present a central hub for regulation and potential cross-talk of 247

different signalling pathways (Huber et al., 2002; Chardin et al., 2017). Additionally, the use of 248

untargeted quantitative phospho-proteomics revealed the unexpected identification of several 249

differentially phosphorylated sites in organellar proteins, most prominently the chloroplast, which 250

was at first sight surprising (Table 1). However, considering that chloroplasts and mitochondria are 251

the key organelles of energy metabolism in plant cells such a link comes not completely unexpected. 252

Still it immediately raises the question of how this connection is functioning at a mechanistic level. As 253

the AKIN10/11 kinases are not localized within these organelles, this connection must be mediated 254

by other signals instead. Of course, sugars or intermediates of energy metabolism would be prime 255

candidates for such a connection. In fact, many changes in metabolite levels have been reported in 256

the context of either SnRK1 function or downstream targets, such as bZIP transcription factors. The 257

bZIP TF bZIP63 was recently identified as direct in planta target of SnRK1 under energy deprivation 258

(Mair et al., 2015) and was also found to be differentially phosphorylated in SnRK1 mutants 259

(Nukarinen et al., 2016). bZIP63 is a member of group C bZIP TFs, which form heterodimers with 260

group S bZIP TFs such as bZIP1, bZIP11, or bZIP53. These bZIP TFs are known for their role in sugar 261

signalling and amino acid metabolism under low-energy stress, salt stress or during dark-induced 262

senescence (Hanson et al., 2008; Alonso et al., 2009; Weltmeier et al., 2009; Dietrich et al., 2011; 263

Hartmann et al., 2015). In these studies it was commonly observed that the level of primary 264

carbohydrates, proline and branched-chain amino acids (BCAAs) was strongly regulated by different 265

combinations of bZIP TFs. For example, a bzip1 bzip53 double mutant was found to be affected in the 266

coordination of BCAA catabolism under salt stress conditions, indicating a central function of these 267

bZIPs in amino acid breakdown (Hartmann et al., 2015). Also mutants being defective in the bZIP63 268

TF showed increased levels of many proteinogenic amino acids, particularly under conditions of 269

energy deprivation (Mair et al., 2015). Simultaneously, concentration of the TCA cycle intermediates 270

citrate, 2-oxoglutarate and malate were found to be significantly increased in bzip63 plants. In 271

addition to effects on amino acid degradation, these findings point to a role of bZIP63 in coordinating 272

subcellular metabolism. The malate shuttle across the chloroplast envelope is essential for the 273

transport of 2-oxoglutarate and glutamate between cytosol and chloroplast (Facchinelli and Weber, 274

2011), and thereby automatically also affects mitochondrial metabolism. Hence, it is interesting to 275

speculate that SnRK1 coordinates the subcellular C/N balance not only by phosphorylating NR, SPS or 276

F2KP, but also via transcriptional control mediated by bZIP63 leading to allocation of organic and 277

amino acids between multiple compartments. 278

During energy-limiting conditions such as extended darkness, alternative substrates are required to 279

fuel mitochondrial respiration. This can be achieved by oxidation of amino acids, which can then 280

either be further oxidized in the tricarboxylic acid cycle or be used to generate electrons that can be 281

directly transferred to the mitochondrial electron transport chain via the electron transfer 282

flavoprotein/ubiquinone oxidoreductase (ETF/ETFQO) system (Araujo et al., 2010). Particularly the 283

breakdown of BCAAs has recently gained more attention leading to the conclusion that ETF/ETFQO is 284

an essential pathway to donate electrons to the mETC and that amino acids are alternative 285

substrates to maintain respiration under carbohydrate starvation (Cavalcanti et al., 2017). A 286

functional link to SnRK1 via bZIP TFs has been suggested based on the observation that different bZIP 287

TFs of the group C and S were found to regulate amino acid breakdown, particularly proline and 288



8

BCAAs (Hanson et al., 2008; Dietrich et al., 2011; Hartmann et al., 2015). ETFQO can directly fuel 289

electrons to the mETC, and has recently been identified as direct target gene regulated by bZIP63 290

(Pedrotti et al., 2018), thereby providing the first functional link between SnRK1 and mitochondrial 291

energy metabolism (Figure 1). 292

Anterograde signals to organelles via phosphorylation of transcription factors by SnRK1? 293

Currently, increasing evidence is accumulating for communication networks between organelles that 294

are regulated in part by retrograde (=organelle to nucleus) signals (Chan et al., 2016; Kmiecik et al., 295

2016; de Souza et al., 2017). In contrast, anterograde (=nucleus to organelle) signals mainly regulate 296

biogenesis of the organelles as well as maintenance, for example in repair processes during stress 297

situations. This topic is further discussed in another review of this special issue focussing on 298

mitochondrial retrograde signals (Wagner et al., 2018). The finding that bZIP63 is a direct regulator of 299

ETFQO and thereby affects mitochondrial electron transport (Pedrotti et al., 2018) and the 300

identification of several differentially phosphorylated proteins in chloroplasts and mitochondria in 301

AKIN10/11 mutants (Nukarinen et al., 2016) prompted us to screen further for target genes of those 302

transcription factors, which have been identified as SnRK1 targets. In addition to the already 303

mentioned EIN3, MYC2, IDD8 and bZIP63, we included here also Wrinkled1 (WRI1), a member of the 304

plant-specific APETALA2 (AP2) family, and the B3-domain TF FUSCA3 (FUS3), for both of which also a 305

direct interaction with AKIN10 has been shown recently. WRI1 was found to be a central regulator of 306

oil synthesis and flowering time and in Brassica BnWRI1 accelerated flowering and enhanced oil 307

accumulation in both seeds and leaves without leading to a visible growth inhibition (Li et al., 2015). 308

WRI1 is also a positive regulator of glycolysis and lipid biosynthesis in Arabidopsis, and recently, 309

phosphorylation of WRI1 by AKIN10 was shown to result in its proteasomal degradation (Zhai et al., 310

2017). This AKIN10-dependent degradation of WRI1 provides a homeostatic mechanism that favours 311

lipid biosynthesis when intracellular sugar levels are elevated and AKIN10 is inhibited. FUS3, a 312

member of the AFL (ABI3/FUS3/LEC2) subfamily of B3 TFs, is a master regulator of seed maturation 313

and hormonal responses during late embryogenesis and germination (Carbonero et al., 2017). 314

AKIN10 was identified as a FUS3-interacting protein and it was reported that AKIN10 physically 315

interacts with and phosphorylates FUS3 at its N-terminal region which delays degradation of FUS3 316

(Tsai and Gazzarrini, 2012). Through their interaction SnRK1 and FUS3 were shown to work 317

synergistically in ABA signalling thereby influencing developmental phase transition and lateral organ 318

growth. 319

To screen the Arabidopsis genome for binding sites in the promoter region of target genes of those 320

TFs, which are directly targeted by SnRK1, we used the AthaMap web tool (www.athamap.de) (Hehl 321

et al., 2016). To specifically assess the extent of how much SnRK1 anterograde signalling could affect 322

plastidial and mitochondrial proteins, we focussed on nuclear-encoded targets of those TFs with a 323

known or clearly predicted localization in plastids or mitochondria according to SUBA 4.0 324

(http://suba.live), (Hooper et al., 2017). This analysis uncovered a remarkable list of nuclear encoded 325

organellar proteins with important functions in mitochondria and chloroplasts (suppl. Table 1). These 326

potential targets of the SnRK1 targeted TFs include a number of well-known key regulators for 327

organellar protein import and biogenesis as well as organellar maintenance and repair: ALB3, TIM, 328

TIC, and TOC proteins or the FtsH proteases which are required for PSII repair. Moreover, a number 329

of nuclear-encoded subunits of PSI and PSII and components of the light-harvesting systems were 330

among those proteins as well as different Tetratricopeptide repeat (TPR)-like superfamily proteins, 331

which are involved in organellar RNA processing or ribosomal proteins or t-RNA synthetases. Finally, 332


http://www.athamap.de/

http://suba.live/


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also several metabolic enzymes or components involved in electron transport or redox processes 333

were found, once more supporting the hypothesis, that these TFs could indeed mediate an important 334

functional role of SnRK1 signalling to chloroplasts and mitochondria. As the protein kinases inside the 335

chloroplast, e.g. the state-transition kinases STN7 and STN8 or the chloroplast Casein Kinase II 336

(cpCKII) respond to changes in the metabolic state or redox conditions (Link, 2003; Rochaix, 2013), 337

changes in the electron flow and organellar redox state might also trigger changes in their activity, 338

which would in turn explain the observed differences in phosphorylation levels of organellar proteins 339

in the SnRK1 mutants. A similar scenario has been proposed before for other TFs involved in 340

retrograde signalling (Kmiecik et al., 2016). In fact recently evidence for this scenario was provided by 341

the finding that ABI4, a central TF involved in different chloroplast retrograde signalling pathways, 342

was phosphorylated by the MAP kinase MPK6 in a Ca2+-dependent manner (Guo et al., 2016). 343

Strikingly, MPK6 was recently also found to be regulated by SnRK1 under hypoxia conditions (Cho et 344

al., 2016). 345

Conclusions 346

The advances of sensitivity in mass spectrometry-based analysis of protein modification combined 347

with targeted enrichment strategies of phosphorylated proteins allowed a quantitative 348

determination of the phosphorylation status of SnRK1 targets in an in vivo context. Combined with 349

the analysis of mutants including inducible double knockout/knockdown mutants of AKIN10/11 this 350

enabled to assess the level of regulation of metabolism by the SnRK1 kinase under different 351

environmental conditions revealing an altered phosphorylation state of several metabolic enzymes. 352

This explains one part of SnRK1 action in metabolic reprogramming by direct regulation of enzyme 353

activities. The second part however, the regulation of transcription is mediated by regulation of 354

transcription factors, which are very low-abundant proteins. Accordingly, such an analysis will be 355

difficult to be achieved using mass spectrometry-based approaches. Nevertheless, for the bZIP TF 356

bZIP63, a difference in phosphorylation level could be observed by this method. As several other TFs 357

have been identified as interactors or direct phosphorylation targets of SnRK1, based mostly on in 358

vitro studies, further studies of those will be needed in the future using complementary approaches, 359

for example using target genes of those TFs as functional readout (see outstanding questions). 360

Hence, the lists of potential targets summarized here can present a valuable starting point for future 361

research. This is particularly true for the third aspect, which has been highlighted in this review: the 362

role of SnRK1 in the regulation of organellar functions. Our analysis uncovered a remarkable list of 363

nuclear-encoded chloroplast and mitochondrial proteins with key functions for organellar biogenesis 364

and metabolism. Functional testing of those proteins in SnRK1 mutants will reveal if the hypothesis 365

proposed here is correct. 366

Finally, it becomes obvious that SnRK1 fulfils different functions in different plant tissues. For 367

example its involvement in FUS3 dependent ABA signalling during developmental phase transition is 368

restricted due to FUS3 expression in seeds, cotyledons, hypocotyls, leaf primordia and shoot apical 369

meristems (Tsai and Gazzarrini, 2012) whereas SnRK1 action in autophagy via interaction with ATG1 370

may very well take place in all tissues of the plant (Chen et al, 2017). These points are of course also 371

due for other kinases such as CDPKs (Simeunovic et al., 2016). This has also been observed for other 372

examples mentioned in this review demonstrate how important it is to interpret SnRK1 connections 373

to other signalling networks in a tissue-dependent context in order to draw valid conclusions about 374

its functions in planta. 375



10

376

377

Supplemental Material 378

Suppl. Table 1. Predicted targets of transcription factors physically interacting with AKIN10. 379

380

Acknowledgements 381

Work in the authors’ lab has been funded by the Austrian Science Fund (FWF) with project P 28491 382

(to MT) and I 2071 (to TN/WW), as well as by the EU in the framework of the Marie Curie ITNs 383

CALIPSO (GA ITN 2013 ITN-607 607) and MERIT (GA ITN 2010-264 474). 384

385



11

Table 1. Mitochondrial and plastid proteins differentially phosphorylated in an AKIN10 dependent manner. 1) 386

proteins found to be significantly (P < 5%) differentially phosphorylated in leaves between AKIN10 knockout, 387

wild type and overexpressor plants after 2h of extended night treatment (Nukarinen et al., 2016). 2) proteins 388

found to be significantly (P < 5%) differentially phosphorylated in leaves between AKIN10 wild type and knock-389

down plants at one or more time-points within a time-series along the transition into extended night 390

(Nukarinen et al., 2016). 391

Gene Identifier Annotation

Plastid

1) AT3G53460 CP29, chloroplast RNA-binding protein 29 1) AT5G35630 GS2, glutamine synthetase 2 1) AT3G46780 PTAC16, plastid transcriptionally active 16 1) AT3G03710 PNP1, polyribonucleotide nucleotidyltransferase 1) AT4G15530 PPDK, pyruvate orthophosphate dikinase 1) AT1G67090 RBCS1A, ribulose bisphosphate carboxylase small chain 1A 1) AT2G47450 CAO, chloroplast signal recognition particle component 1) AT4G13670 PTAC5, plastid transcriptionally active 5 1) AT1G68830 STN7, STT7 homolog STN7 1) AT4G02510 TOC159, translocon at the outer envelope membrane of chloroplasts 159 2) AT3G08940 LHCB4.2 (CP29.2), light harvesting complex photosystem II 2) AT2G46820 PSAP, PTAC8 photosystem I P subunit 2) AT2G35980 NHL10, NDR1/HIN1-like protein 10 2) AT3G02150 PTF1, plastid transcription factor 1 2) AT4G18480 CHLI1, magnesium-chelatase subunit ChlI-1 2) AT4G22890 PGRL1A, PGR5-like protein 1A 2) AT5G20720 CPN20, 20 kDa chaperonin

Mito

cho

nd

ria

1) AT5G66760 SDH1-1, succinate dehydrogenase 1-1 1),2) AT5G26860 LON1, ion protease 1

1) AT4G27585 SLP1, SPFH/Band 7/PHB domain-containing membrane-associated protein family 1) AT3G25140 GAUT8, galacturonosyltransferase 8 2) AT5G14780 FDH, FDH formate dehydrogenase

392

393



12

Figure Legend 394

395

Figure 1. Different modes of metabolic regulation by SnRK1. SnRK1 regulates cytosolic metabolism directly by 396

phosphorylation of metabolic enzymes and can also indirectly affect organellar metabolism via phosphorylation 397

of transcription factors in the nucleus that regulate expression of nuclear-encoded organellar proteins. This in 398

turn will then affect the proteomic state within the organelles. The phosphorylation status of several plastid 399

and mitochondria proteins is altered by yet unknown mechanisms in response to SnRK1 activity changes. 400

Transcription factors directly phosphorylated by SnRK1 are predicted to bind to nuclear encoded plastid and 401

mitochondria genes eventually altering their transcription. The thereby altered metabolic state might be 402

directly transduced into plastids and mitochondria or indirect, via transcriptional regulation. 403

404

405

406

407

408



13

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616



ADVANCES

• The sucrose non-fermenting-related kinase 1 (SnRK1) is an evolutionary conserved central regulator of cellular metabolism related to energy metabolism and stress responses. Its role as direct regulator of key enzymatic activities in the cytosol, as well as its role as regulator of transcriptional responses, has been well-described. However, only recently, a number of different transcription factors have been identified as direct SnRK1 targets in plants, and functional consequences of their phosphorylation is starting to become understood.

• In addition to cellular targets of the SnRK1 complex in the cytosol and the nucleus, SnRK1 was recently also shown to affect different metabolic events and even phosphorylation patterns in chloroplasts and mitochondria.

• Analysis of potential target genes of SnRK1 regulated transcription factors indicates a substantial impact of those TFs on different organellar functions.



OUTSTANDING QUESTIONS

• The list of SnRK1 regulated target genes is still incomplete, particularly regarding TFs. Moreover, for most of them, it needs to be shown whether or not a reported phosphorylation of a TF by SnRK1 does result in an altered regulation of transcription of its target genes.

• A potential effect on the transcriptional regulation of nuclear-encoded organellar proteins by SnRK1 via phosphorylation of TFs as discussed here is so far mostly based on the prediction of their target genes. Therefore, future research should focus on testing these connections functionally in planta to address their role in connecting/coordinating energy metabolism between the organelles and the cytosol.

• Crosstalk between SnRK1 and other kinases such as CDPKs or MAPKs merging at identical targets has been reported for some metabolic enzymes, for example nitrate reductase (NR) or sucrose phosphate synthase (SPS). However, these data are so far restricted to identification of specific phosphorylation sites in particular target proteins and have not been systematically studied. Furthermore, according to the emerging data, such studies should also be extended to TFs.

• SnRK1 phenotypes are obviously pleiotropic. Thus, more emphasis on tissue-specific analysis will be required to correctly asses the role of SnRK1 in signaling networks in their relevant natural environment.



BOX 1. SnRK1 Kinases (SNF1-Related Kinases)

The SNF1 (SUCROSE NON-FERMENTING1) kinase has first been described in yeast as a central regulator of energy metabolism in response to nutritional signals. This kinase is evolutionarily conserved and its orthologues, the AMPK (AMP-ACTIVATED PROTEIN KINASE) in mammals and the SnRK1 (SNF1-RELATED KINASE1) in plants, have been characterized in great detail (Baena-Gonzalez and Sheen, 2008; Emanuelle et al., 2016; Broeckx et al., 2016). They are structurally and functionally related and function as heterotrimeric complex composed of an α-catalytic and β- and γ-regulatory subunits. In Arabidopsis, the catalytic subunits are encoded by AKIN10 (SnRK1α1), AKIN11 (SnRK1α2), and AKIN12 (SnRK1α3). AKIN10 and AKIN11 appear to be partially redundant as double mutants could not be recovered, while AKIN12 is hardly expressed (Baena-Gonzalez et al., 2007). SnRK1 kinase activity is induced by starvation conditions and leads to a metabolic switch from anabolic to energy-saving catabolic pathways, as well as autophagy or general stress responses. However, the exact mechanistic details of SnRK1 activation are still not fully understood (Crozet et al., 2014; Emanuelle et al., 2016). Plants harbor two other SnRK kinase families in addition to SnRK1: SnRK2 with 10 members and SnRK3s with 25 members in Arabidopsis (Hrabak et al., 2003). The 10 SnRK2 kinases have been found to be mainly involved in abiotic stress responses and turned out to be key regulators in ABA signaling (Cutler et al., 2010), while the 25 SnRK3s are also referred to as CBL-interacting protein kinases (CIPKs) and have been found to be involved in response to a wide range of stimuli (Kudla et al., 2010).



Parsed CitationsAlonso R, Onate-Sanchez L, Weltmeier F, Ehlert A, Diaz I, Dietrich K, Vicente-Carbajosa J, Droge-Laser W (2009) A pivotal role of thebasic leucine zipper transcription factor bZIP53 in the regulation of Arabidopsis seed maturation gene expression based onheterodimerization and protein complex formation. Plant Cell 21: 1747-1761

Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Araujo WL, Ishizaki K, Nunes-Nesi A, Larson TR, Tohge T, Krahnert I, Witt S, Obata T, Schauer N, Graham IA, Leaver CJ, Fernie AR(2010) Identification of the 2-hydroxyglutarate and isovaleryl-CoA dehydrogenases as alternative electron donors linking lysinecatabolism to the electron transport chain of Arabidopsis mitochondria. Plant Cell 22: 1549-1563


Baena-Gonzalez E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energysignalling. Nature 448: 938-942


Baena-Gonzalez E, Sheen J (2008) Convergent energy and stress signaling. Trends Plant Sci 13: 474-482Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Bailey-Serres J, Voesenek LA (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 59: 313-339Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Bayer RG, Stael S, Rocha AG, Mair A, Vothknecht UC, Teige M (2012) Chloroplast-localized protein kinases: a step forward towards acomplete inventory. J Exp Bot 63: 1713-1723


Broeckx T, Hulsmans S, Rolland F (2016) The plant energy sensor: evolutionary conservation and divergence of SnRK1 structure,regulation, and function. J Exp Bot 67: 6215-6252


Carbonero P, Iglesias-Fernandez R, Vicente-Carbajosa J (2017) The AFL subfamily of B3 transcription factors: evolution and function inangiosperm seeds. J Exp Bot 68: 871-880


Cavalcanti JHF, Quinhones CGS, Schertl P, Brito DS, Eubel H, Hildebrandt T, Nunes-Nesi A, Braun HP, Araujo WL (2017) Thedifferential impact of amino acids on OXPHOS system activity following carbohydrate starvation in Arabidopsis cell suspensions.Physiol Plant


Chan KX, Phua SY, Crisp P, McQuinn R, Pogson BJ (2016) Learning the Languages of the Chloroplast: Retrograde Signaling andBeyond. Annu Rev Plant Biol 67: 25-53


Chardin C, Schenk ST, Hirt H, Colcombet J, Krapp A (2017) Review: Mitogen-Activated Protein Kinases in nutritional signaling inArabidopsis. Plant Sci 260: 101-108


Chen L, Su ZZ, Huang L, Xia FN, Qi H, Xie LJ, Xiao S, Chen QF (2017) The AMP-Activated Protein Kinase KIN10 Is Involved in theRegulation of Autophagy in Arabidopsis. Front Plant Sci 8: 1201



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http://www.ncbi.nlm.nih.gov/pubmed?term=Cho HY%2C Wen TN%2C Wang YT%2C Shih MC %282016%29 Quantitative phosphoproteomics of protein kinase SnRK1 regulated protein phosphorylation in Arabidopsis under submergence%2E J Exp Bot 67%3A 2745%2D2760&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Crozet P%2C Margalha L%2C Confraria A%2C Rodrigues A%2C Martinho C%2C Adamo M%2C Elias CA%2C Baena%2DGonzalez E %282014%29 Mechanisms of regulation of SNF1%2FAMPK%2FSnRK1 protein kinases%2E Front Plant Sci 5%3A 190&dopt=abstract

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http://scholar.google.com/scholar?as_q=Mechanisms of regulation of SNF1/AMPK/SnRK1 protein kinases.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Crozet&as_ylo=2014&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Cutler SR%2C Rodriguez PL%2C Finkelstein RR%2C Abrams SR %282010%29 Abscisic acid%3A emergence of a core signaling network%2E Annu Rev Plant Biol 61%3A 651%2D679&dopt=abstract

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http://scholar.google.com/scholar?as_q=Abscisic acid: emergence of a core signaling network&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Cutler&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Das D%2C St Onge KR%2C Voesenek LA%2C Pierik R%2C Sasidharan R %282016%29 Ethylene%2D and Shade%2DInduced Hypocotyl Elongation Share Transcriptome Patterns and Functional Regulators%2E Plant Physiol 172%3A 718%2D733&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Das D, St Onge KR, Voesenek LA, Pierik R, Sasidharan R (2016) Ethylene- and Shade-Induced Hypocotyl Elongation Share Transcriptome Patterns and Functional Regulators. Plant Physiol 172: 718-733

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http://www.ncbi.nlm.nih.gov/pubmed?term=de Souza A%2C Wang JZ%2C Dehesh K %282017%29 Retrograde Signals%3A Integrators of Interorganellar Communication and Orchestrators of Plant Development%2E Annu Rev Plant Biol 68%3A 85%2D108&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=de Souza A, Wang JZ, Dehesh K (2017) Retrograde Signals: Integrators of Interorganellar Communication and Orchestrators of Plant Development. Annu Rev Plant Biol 68: 85-108

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Hartmann L, Pedrotti L, Weiste C, Fekete A, Schierstaedt J, Gottler J, Kempa S, Krischke M, Dietrich K, Mueller MJ, Vicente-CarbajosaJ, Hanson J, Droge-Laser W (2015) Crosstalk between Two bZIP Signaling Pathways Orchestrates Salt-Induced MetabolicReprogramming in Arabidopsis Roots. Plant Cell 27: 2244-2260


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Haydon MJ, Mielczarek O, Robertson FC, Hubbard KE, Webb AA (2013) Photosynthetic entrainment of the Arabidopsis thalianacircadian clock. Nature 502: 689-692


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Hrabak EM, Chan CW, Gribskov M, Harper JF, Choi JH, Halford N, Kudla J, Luan S, Nimmo HG, Sussman MR, Thomas M, Walker-Simmons K, Zhu JK, Harmon AC (2003) The Arabidopsis CDPK-SnRK superfamily of protein kinases. Plant Physiol 132: 666-680


Huber SC, MacKintosh C, Kaiser WM (2002) Metabolic enzymes as targets for 14-3-3 proteins. Plant Mol Biol 50: 1053-1063Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Im JH, Cho YH, Kim GD, Kang GH, Hong JW, Yoo SD (2014) Inverse modulation of the energy sensor Snf1-related protein kinase 1 onhypoxia adaptation and salt stress tolerance in Arabidopsis thaliana. Plant Cell Environ 37: 2303-2312


Jeong EY, Seo PJ, Woo JC, Park CM (2015) AKIN10 delays flowering by inactivating IDD8 transcription factor through proteinphosphorylation in Arabidopsis. BMC Plant Biol 15: 110


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Kim GD, Cho YH, Yoo SD (2017)b Regulatory Functions of Cellular Energy Sensor SNF1-Related Kinase1 for Leaf Senescence Delay www.plantphysiol.orgon August 27, 2019 - Published by Downloaded from

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http://www.ncbi.nlm.nih.gov/pubmed?term=Jeong EY%2C Seo PJ%2C Woo JC%2C Park CM %282015%29 AKIN10 delays flowering by inactivating IDD8 transcription factor through protein phosphorylation in Arabidopsis%2E BMC Plant Biol 15%3A 110&dopt=abstract

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http://scholar.google.com/scholar?as_q=AKIN10 delays flowering by inactivating IDD8 transcription factor through protein phosphorylation in Arabidopsis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Jeong&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Jossier M%2C Bouly JP%2C Meimoun P%2C Arjmand A%2C Lessard P%2C Hawley S%2C Grahame Hardie D%2C Thomas M %282009%29 SnRK1 %28SNF1%2Drelated kinase 1%29 has a central role in sugar and ABA signalling in Arabidopsis thaliana%2E Plant J 59%3A 316%2D328&dopt=abstract

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http://scholar.google.com/scholar?as_q=SnRK1 (SNF1-related kinase 1) has a central role in sugar and ABA signalling in Arabidopsis thaliana&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Jossier&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kim GD%2C Cho YH%2C Yoo SD %282017%29a Phytohormone ethylene%2Dresponsive Arabidopsis organ growth under light is in the fine regulation of Photosystem II deficiency%2Dinducible AKIN10 expression%2E Sci Rep 7%3A 2767&dopt=abstract

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http://scholar.google.com/scholar?as_q=a Phytohormone ethylene-responsive Arabidopsis organ growth under light is in the fine regulation of Photosystem II deficiency-inducible AKIN10 expression.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kim&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1


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Kmiecik P, Leonardelli M, Teige M (2016) Novel connections in plant organellar signalling link different stress responses andsignalling pathways. J Exp Bot 67: 3793-3807


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Li L, Sheen J (2016) Dynamic and diverse sugar signaling. Curr Opin Plant Biol 33: 116-125Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Li Q, Shao J, Tang S, Shen Q, Wang T, Chen W, Hong Y (2015) Wrinkled1 Accelerates Flowering and Regulates Lipid Homeostasisbetween Oil Accumulation and Membrane Lipid Anabolism in Brassica napus. Front Plant Sci 6: 1015


Lin CR, Lee KW, Chen CY, Hong YF, Chen JL, Lu CA, Chen KT, Ho TH, Yu SM (2014) SnRK1A-interacting negative regulators modulatethe nutrient starvation signaling sensor SnRK1 in source-sink communication in cereal seedlings under abiotic stress. Plant Cell 26:808-827


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Liu XJ, An XH, Liu X, Hu DG, Wang XF, You CX, Hao YJ (2017b) MdSnRK1.1 interacts with MdJAZ18 to regulate sucrose-inducedanthocyanin and proanthocyanidin accumulation in apple. J Exp Bot 68: 2977-2990


Liu Y, Bassham DC (2012) Autophagy: pathways for self-eating in plant cells. Annu Rev Plant Biol 63: 215-237Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Mair A, Pedrotti L, Wurzinger B, Anrather D, Simeunovic A, Weiste C, Valerio C, Dietrich K, Kirchler T, Nagele T, Vicente Carbajosa J,Hanson J, Baena-Gonzalez E, Chaban C, Weckwerth W, Droge-Laser W, Teige M (2015) SnRK1-triggered switch of bZIP63 dimerizationmediates the low-energy response in plants. Elife 4


McKibbin RS, Muttucumaru N, Paul MJ, Powers SJ, Burrell MM, Coates S, Purcell PC, Tiessen A, Geigenberger P, Halford NG (2006)Production of high-starch, low-glucose potatoes through over-expression of the metabolic regulator SnRK1. Plant Biotechnol J 4: 409-418

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http://www.ncbi.nlm.nih.gov/pubmed?term=Kim GD%2C Cho YH%2C Yoo SD %282017%29b Regulatory Functions of Cellular Energy Sensor SNF1%2DRelated Kinase1 for Leaf Senescence Delay through ETHYLENE%2D INSENSITIVE3 Repression%2E Sci Rep 7%3A 3193&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Kirchler T%2C Briesemeister S%2C Singer M%2C Schutze K%2C Keinath M%2C Kohlbacher O%2C Vicente%2DCarbajosa J%2C Teige M%2C Harter K%2C Chaban C %282010%29 The role of phosphorylatable serine residues in the DNA%2Dbinding domain of Arabidopsis bZIP transcription factors%2E Eur J Cell Biol 89%3A 175%2D183&dopt=abstract

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http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kirchler&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The role of phosphorylatable serine residues in the DNA-binding domain of Arabidopsis bZIP transcription factors&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 role of phosphorylatable serine residues in the DNA-binding domain of Arabidopsis bZIP transcription factors&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kirchler&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kmiecik P%2C Leonardelli M%2C Teige M %282016%29 Novel connections in plant organellar signalling link different stress responses and signalling pathways%2E J Exp Bot 67%3A 3793%2D3807&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kmiecik P, Leonardelli M, Teige M (2016) Novel connections in plant organellar signalling link different stress responses and signalling pathways. J Exp Bot 67: 3793-3807

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kmiecik&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Novel connections in plant organellar signalling link different stress responses and signalling pathways&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=Novel connections in plant organellar signalling link different stress responses and signalling pathways&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kmiecik&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kudla J%2C Batistic O%2C Hashimoto K %282010%29 Calcium signals%3A the lead currency of plant information processing%2E Plant Cell 22%3A 541%2D563&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Kudla J, Batistic O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. Plant Cell 22: 541-563

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http://scholar.google.com/scholar?as_q=Calcium signals: the lead currency of plant information processing&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

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http://www.ncbi.nlm.nih.gov/pubmed?term=Li L%2C Sheen J %282016%29 Dynamic and diverse sugar signaling%2E Curr Opin Plant Biol 33%3A 116%2D125&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Li L, Sheen J (2016) Dynamic and diverse sugar signaling. Curr Opin Plant Biol 33: 116-125

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Li&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Dynamic and diverse sugar 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=Dynamic and diverse sugar signaling&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Li&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Li Q%2C Shao J%2C Tang S%2C Shen Q%2C Wang T%2C Chen W%2C Hong Y %282015%29 Wrinkled1 Accelerates Flowering and Regulates Lipid Homeostasis between Oil Accumulation and Membrane Lipid Anabolism in Brassica napus%2E Front Plant Sci 6%3A 1015&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Lin CR%2C Lee KW%2C Chen CY%2C Hong YF%2C Chen JL%2C Lu CA%2C Chen KT%2C Ho TH%2C Yu SM %282014%29 SnRK1A%2Dinteracting negative regulators modulate the nutrient starvation signaling sensor SnRK1 in source%2Dsink communication in cereal seedlings under abiotic stress%2E Plant Cell 26%3A 808%2D827&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Link G %282003%29 Redox regulation of chloroplast transcription%2E Antioxid Redox Signal 5%3A 79%2D87&dopt=abstract

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