Short Title: Root Secondary Growth and Phosphorus ......2017/11/08 · Jonathan P. Lynch, Email:...

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Short Title: Root Secondary Growth and Phosphorus Acquisition

Corresponding Author Details: Jonathan P. Lynch, Email: [email protected], Tel.: +1 8148632256 Article Title: Reduction in Root Secondary Growth as a Strategy for Phosphorus Acquisition

Authors: Christopher F. Strock, Laurie Morrow de la Riva, Jonathan P. Lynch

Authors’ Affiliation: Department of Plant Science, The Pennsylvania State University, University Park, PA USA

One-sentence summary: Reduced root secondary growth decreases

maintenance and construction costs, allowing greater root elongation and soil exploration, thereby improving P acquisition and plant growth under P stress.

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Authors’ Contributions: C.S. performed all of the experiments, analyzed the data, and wrote the article with contributions of all the authors; L.R. carried out the original screening and foundational research for these published data; J.L. conceived the hypotheses, and supervised the design, experimentation, analysis, and reporting.

Funding Information: This project was supported by the USAID Climate Resilient Beans Feed the Future Legume Innovation Laboratory and the National Institute of Food and Agriculture, U.S. Department of Agriculture, Hatch project 4582.

Present Address: 221 Tyson Bldg., University Park, PA 16802

Corresponding Author Email: [email protected]

Plant Physiology Preview. Published on November 8, 2017, as DOI:10.1104/pp.17.01583

Copyright 2017 by the American Society of Plant Biologists

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Abstract 1

We tested the hypothesis that reduced root secondary growth of dicotyledonous 2

species improves phosphorus acquisition. Functional-structural modeling in 3

SimRoot indicates that in common bean (Phaseolus vulgaris), reduced root 4

secondary growth reduces root metabolic costs, increases root length, improves 5

phosphorus capture, and increases shoot biomass in low phosphorus soil. 6

Observations from the field and greenhouse confirm that under phosphorus 7

stress, resource allocation is shifted from secondary to primary root growth, 8

genetic variation exists for this response, and reduced secondary growth 9

improves phosphorus capture from low phosphorus soil. Under low phosphorus 10

in greenhouse mesocosms, genotypes with reduced secondary growth had 39% 11

smaller root cross sectional area, 60% less root respiration, 27% greater root 12

length, 78% greater shoot phosphorus content, and 68% greater shoot mass 13

than genotypes with advanced secondary growth. In the field under low 14

phosphorus, these genotypes had 43% smaller root cross sectional area, 32% 15

greater root length, 58% greater shoot phosphorus content, and 80% greater 16

shoot mass than genotypes with advanced secondary growth. Secondary growth 17

eliminated arbuscular mycorrhizal associations as cortical tissue was destroyed. 18

These results support the hypothesis that reduced root secondary growth is an 19

adaptive response to low phosphorus availability and merits investigation as a 20

potential breeding target. 21

Introduction 22

Most soils on earth have suboptimal phosphorus (P) availability for plant growth 23

(Vance et al. 2003; Lynch & Brown 2008; Lynch 2011), as it is only available to 24

plants as inorganic P (Pi), and is rarely present in concentrations greater than 25

several M in soil solution (Bieleski 1973). Diffusion of P in soil is greatly 26

outpaced by plant uptake, resulting in the formation of P depletion zones around 27

roots (Hinsinger et al. 2005). Due to the limited availability and slow movement of 28

P in soil, one of the most effective strategies of increasing P uptake is to increase 29

the volume of soil explored by the root system. This accounts for the increase in 30



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the root:shoot ratio under P stress (Fohse et al. 1988). Although increasing 31

resource allocation to root growth improves P acquisition, unbalanced root 32

development reduces overall plant growth due to the increased metabolic cost of 33

added root tissue (Nielsen et al. 1998, 2001; Lambers et al. 2006). Over 50% of 34

daily carbon fixation may be consumed by the root system, with P stressed 35

plants allocating a larger fraction of their daytime net carbon assimilation than 36

non-stressed plants (Van der Werf et al. 1988; Lambers et al. 1996; Nielsen et al. 37

1998, 2001). This cost consists of three main components: the growth of new 38

root tissue, ion uptake and assimilation, and maintenance of existing root tissue 39

(Nielsen et al. 1998; Fan et al. 2003). Nielsen et al. (1998) found that in common 40

bean under P deficit, the proportion of total root respiration allocated to 41

maintenance accounts for approximately 90% of total root respiration. The 42

functional-structural model Simroot has estimated that the cost of maintenance 43

respiration of the root system constitutes 40% of the total growth reduction under 44

P stress (Postma & Lynch 2011). Consequently, the greatest opportunity to 45

reduce the metabolic burden of the root system lies in moderating maintenance 46

costs. 47

To improve the balance between soil exploration and consumption of growth 48

limiting resources, a decrease in root secondary growth would reduce the carbon 49

cost of producing and maintaining root length (Lynch 1995). It has been 50

hypothesized that this may be an adaptive strategy to improve the metabolic 51

efficiency of soil foraging under P stress, where roots will favor primary growth 52

(elongation) over secondary growth (radial thickening) to achieve greater 53

exploration of soil domains that have not been depleted of P (Lynch & Brown 54

2008; De la Riva & Lynch 2010; Lynch 2007, 2011). 55

Previous observations of root systems under P stress provide evidence for the 56

importance of root diameter in a diversity of plant species. In the sedge Carex 57

coriacea, specific root length (SRL, i.e. root length per mass of root tissue) was 58

negatively correlated with P availability, with a 30% reduction in root diameter 59

from high P to low P (Powell 1974). In a study of the root morphology of 60



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temperate pasture species, a reduction in root diameter, root mass density, and 61

an increase in SRL were observed under P stress (Hill 2006). Reduced lateral 62

root diameter has also been described under low P in water hyacinth (Eichhornia 63

crassipes) and maize (Zea mays L.) (Xie & Yu 2003; Zhu & Lynch 2004). 64

Nevertheless, observations of reductions in root diameter under P stress have 65

not been made within root classes, and published reductions in root diameter of 66

the entire root system may be the product of a greater proportion of higher-order 67

lateral roots, rather than the effects of altered secondary growth. To determine if 68

reduction of secondary growth is an adaptive response, an explicit study of 69

secondary growth within root classes under P stress is required (Lynch & Brown 70

2008). 71

During secondary growth, periclinal cellular divisions and differentiation of 72

secondary tissues at the vascular cambium and phellogen cause the splitting and 73

destruction of the epidermis, cortex, and endodermis. While the production of the 74

periderm replaces these primary tissues and helps to protect the vasculature of 75

the root, the bulk of secondary thickening is driven by the production of 76

secondary xylem elements and parenchyma internal to the vascular cambium 77

(Dikison 2008). This elimination of the primary tissues and proliferation of 78

secondary tissue are observed in transverse sections as the loss of the 79

epidermis, cortex, and endodermis, expansion of the stele, and an increase in 80

the abundance and size of metaxylem vessels (Fig. S1). Under P deficiency, 81

observed changes in root anatomy of a variety of species include smaller root 82

diameter, stele diameter, fewer and smaller epidermal cells and metaxylem 83

vessels, reduced percent stele area, and fewer cortical cells, and xylem vessels 84

(Fohse et al. 1991; Fan et al. 2003; Liu et al. 2004; Sarker et al. 2015). 85

In this study, we utilize functional-structural modeling as well as empirical 86

observations of plants grown in controlled environment mesocosms and in the 87

field to explore the effect of reduced secondary growth of roots on P acquisition. 88

Our goals were to test the hypotheses that 1) secondary growth is suppressed by 89

P stress, 2) genetic variation exists for this response, and 3) reduced secondary 90



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growth of roots improves P acquisition. We address these hypotheses by first 91

utilizing the functional-structural plant model SimRoot to determine the 92

relationship between secondary growth of roots and P acquisition, followed by 93

greenhouse and field studies to validate in silico results. 94

The common bean (Phaseolus vulgaris L.) was used to test these hypotheses 95

due to observed genotypic variation in phosphorus acquisition and metabolic 96

efficiency of roots under P stress (Nielsen et al. 2001; Beebe et al. 2006; De la 97

Riva & Lynch 2010; Henry et al. 2010; Miguel et al. 2015). Common bean is also 98

an important food security crop in Africa and Latin America, where its productivity 99

is often limited by low P availability. 100

Results 101

Phenotypic Classification 102

Total cross sectional area (TCSA) (mm2) of the root and the percent stele area 103

from greenhouse grown root segments were used to categorize genotypes into 104

two phenotypic groups that were used as a factor in data analysis; genotypes 105

with a mean TCSA < 0.5 mm2 and < 50% stele in the basal segment at time of 106

flowering (46 DAP) were classified as having reduced secondary growth 107

(“reduced”) (DG6, DG35, L8814, L8863). Genotypes with a mean TCSA > 0.5 108

mm2 and > 50% stele in the basal segment at flowering were categorized as 109

having advanced secondary growth (“advanced”) (DG23, DG51, L8843, L8857). 110

Effects of Reducing Secondary Growth in Silico 111

When root secondary growth was reduced by 50% (intermediate phenotype), by 112

40 DAP under P stress (4 mol/L available P) root respiration per g was reduced 113

by 14%, total root length was increased by 7%, P acquisition increased by 9%, 114

and shoot mass increased by 17% from the “advanced” phenotype (Figs. 1, S2). 115

In the “reduced” phenotype where roots had no secondary growth, root 116

respiration was reduced by 12%, total root length was increased by 14%, net P 117

acquisition increased by 15%, and the shoot mass increased by 31% from the 118



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“advanced” phenotype (Figs. 1, S3). In environments with greater P availability, 119

root respiration rate was suppressed and root length increased to a greater 120

degree, but the impact of these root parameters on improving P capture and 121

shoot biomass was less pronounced (Fig. 1). When P availability was more 122

strongly stratified with depth, the benefits to reducing secondary growth became 123

less pronounced (Fig. S4). 124

Plant Growth in Mesocosms 125

Under high P in mesocosms, no genotypic differences in shoot size and shoot P 126

were observed, while under P stress, reduced genotypes had 68% greater shoot 127

mass and 78% greater shoot P than advanced genotypes by 46 DAP (Figs. 2, 3). 128

Under high P there were no phenotypic differences in root mass, while under P 129

stress, reduced genotypes had significantly greater root mass than advanced 130

genotypes (Fig. S5). Within each treatment, no phenotypic differences in 131

root:shoot ratios were observed (Fig. S5). Allometric analysis revealed that root 132

mass had a hyperallometric relationship to shoot size under both P treatments 133

(Table 1). All genotypes had statistically similar basal root whorl number, basal 134

root number, and adventitious root number. 135

By 46 DAP under P stress, reduced genotypes had 56% greater specific root 136

length and 27% greater basal root length than advanced genotypes, while in the 137

high P treatment, both phenotypic groups had statistically similar specific root 138

length and basal root length (Fig. 3). Although a trend of thinner lateral roots and 139

greater net lateral root length were observed for the reduced genotypes under P 140

stress, statistical analysis did not reveal a significant genotypic effect at p < 0.05 141

(Fig. S6). Under P stress, specific root length and basal root length were both 142

positively correlated with shoot P content by 32 DAP, while in the high P 143

treatment no relationship was observed. 144

Plant Growth in the Field 145

Under high P in the field, no genotypic differences in shoot size and shoot P 146

content were observed, while in the P stress treatment, reduced genotypes had 147



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80% greater shoot mass, 62% greater leaf number, and 58% greater shoot P 148

than advanced genotypes by 49 DAP (Fig. 4). Under P stress, reduced 149

genotypes had 32% greater root length density in the top 40cm of soil than 150

advanced genotypes, while under high P no genotypic differences were 151

detectable (Fig. 4). Root length density in the top 40 cm was positively correlated 152

with total shoot P under P stress while no relationship was observed under high 153

P (Fig. 5). Root length density in the top 40 cm of soil had a hyperallometric 154

relationship with shoot size under P stress, but not under high P (Table 1). All 155

genotypes had statistically similar basal root whorl number, basal root number, 156

adventitious root number, and basal root growth angle. 157

Root Anatomy 158

In mesocosms, total cross sectional area (TCSA), percent stele, metaxylem 159

vessel number, total metaxylem vessel area, and hydraulic conductance 160

increased significantly from 18 to 46 DAP and from the apical to the basal end of 161

the root in both P treatments (Figs. 6, S7, S8, S9, S10). Phosphorus stress 162

significantly reduced these anatomical phenes in both greenhouse and field-163

grown roots (Fig. 7). Differences in TCSA between reduced and advanced 164

genotypes were statistically detectable by 18 DAP under P stress (Fig. 6). 165

Phosphorus treatment, temporal, and phenotypic effects were most detectable in 166

the basal segment, where the greatest secondary growth had occurred. In this 167

segment at 46 DAP, reduced genotypes displayed 29% smaller percent stele 168

area, 21% fewer metaxylem number, 48% less metaxylem area, and 52% less 169

hydraulic conductance than advanced genotypes under P stress (Figs. 7, S7, S8, 170

S9, S10). At 49 DAP in the field, reduced genotypes had 43% smaller TCSA, 171

26% fewer metaxylem number, 41% reduced metaxylem area, and 55% less 172

hydraulic conductance than advanced genotypes under P stress (Figs. 8, S10). 173

Allometric analysis indicates that differences in secondary growth of roots 174

(TCSA, percent stele, metaxylem area, metaxylem number) were not driven by 175

differences in plant size in either the greenhouse or the field (Table 1). Under P 176

stress a negative relationship between basal TCSA and total shoot P was 177



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observed, but under high P, no significant association between basal TCSA and 178

shoot P was detected (Fig. 9). 179

In mesocosms under P stress, TCSA of the basal segment was negatively 180

correlated with basal root length at all time points, while under high P no 181

relationship was statistically observable (Fig. 9). Similarly, at 49 DAP under P 182

deficit in the field basal TCSA was negatively correlated with root length density 183

in the top 40 cm of soil (Fig. 5). This association between the allocation of 184

resources from secondary growth to primary growth can be represented by the 185

ratio of basal TCSA:total basal root length. Mean TCSA:total basal root length at 186

46 DAP in the greenhouse was greater for genotypes classified as advanced 187

than for most genotypes in the reduced group with the exception of L8863 (Fig. 188

S12). Genotypes in the advanced group had mean TCSA:RL > 0.1 while 189

genotypes in the reduced group had a mean TCSA:RL of < 0.1. 190

Root Respiration 191

By 46 DAP in the greenhouse, reduced genotypes had 60% less basal segment 192

respiration, 47% less middle segment respiration, and 69% less apical segment 193

respiration than advanced genotypes under P deficit (Fig. 10). There was a 194

strong positive relationship between respiration rate per unit length and TCSA in 195

all P treatments and time points (Fig. 9). By 32 DAP under P stress, respiration 196

per unit length of all segments was negatively correlated with basal root length, 197

and by 46 DAP (Fig. S13), respiration per unit length of all locations was 198

negatively correlated with shoot mass (Fig. S14). These relationships between 199

root respiration and root length and shoot mass were not present in the high P 200

treatment (Figs. S13, S14). 201

Root Construction Costs 202

Root P concentration decreased significantly with root segment age in the high P 203

treatment but was consistent for all root segments in P-stressed plants (Fig. 204

S15). Nitrogen (N) concentration was significantly greater in the growing root tips 205

than in older root segments and was significantly greater in P stressed roots than 206



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in roots grown under high P (Fig. S15B). Carbon (C) concentration was 207

statistically similar for root segments in all P treatments, time points, and 208

positions along the root. There was no effect of P treatment on the C:H ratio of 209

roots and no detectable change in the C:H ratio among locations, but C:H ratio 210

significantly increased at the basal segment over time. Phosphorus stress 211

significantly reduced C:N and C:N increased with root segment age. These 212

increases in C:N were driven by a reduction in N, not changes in C. No 213

statistically observable differences in the elemental concentration of roots were 214

observed between advanced and reduced genotypes. 215

Mycorrhizal Synergism with Secondary Growth 216

Despite observed genotypic differences in secondary growth, no statistically 217

detectable genotypic differences in mycorrhizal symbiosis were observed under 218

P stress. While roots grown under P stress had significantly greater 219

mycorrhization of the basal-most segment, roots grown under high P displayed 220

the opposite pattern of symbiosis with the least abundance of mycorrhizal 221

structures in the basal segment (Fig. 11C). Basal segments from the P stress 222

treatment had 367% greater cortical tissue area than basal segments in the high 223

P treatment and across both P treatments there was a significant positive 224

relationship between cortical tissue area and symbiosis (Fig. 11A, 11B, 11D). 225

Discussion 226

SimRoot predicted that reducing secondary growth of roots reduces metabolic 227

costs, liberates resources for greater primary growth and thereby augments the 228

total quantity of P captured. These predictions were confirmed by in vivo 229

observations under P stress in the greenhouse and field. These results confirm 230

the hypotheses that 1) in low P soil, roots of this dicot species favor primary 231

growth over secondary growth (Figs. 4, 5, 7, 8, 9), 2) genetic variation exists for 232

this response (Figs. 3, 4, 5, 6, 8, S11, S12), and 3) and the reallocation of 233

resources from secondary to primary growth improves P acquisition (Figs. 1, 3, 5, 234

9, S2). 235



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Because SimRoot does not explicitly consider beneficial aspects of secondary 236

root growth such as axial water transport (Valenzuela-Estrada et al. 2008), 237

mechanical support of the shoot, or resistance to herbivores and pathogens 238

(Eissenstat 1992; Valenzuela-Estrada et al. 2008), reduced secondary growth is 239

unconditionally beneficial for improving root length and P acquisition in silico. In 240

vivo, secondary growth is a constitutive characteristic of dicot roots, and the 241

inverse relationship between secondary growth and P acquisition predicted by 242

the model is only present under P stress. Under high P, plants are able to 243

acquire adequate P to support the production of less efficient roots without 244

reducing plant growth. The observation that secondary growth is inhibited only 245

under P stress would suggest that increased root diameter affords increased 246

fitness in fertile environments. 247

Despite possible drawbacks to reduced root diameter, reallocation of resources 248

among different tissues is a hallmark adaptive response to P deficiency (Fohse et 249

al. 1988). This concept is evident in the present study through the greater 250

allometric scaling coefficient for root mass under P stress compared to high P 251

conditions, demonstrating a shift in resources from shoot growth to soil 252

exploration. Although there was an increase in root:shoot ratio under P stress, 253

there was no phenotypic difference for this metric within the P stress treatment. 254

While the relative investment of resources to roots of both phenotypic groups 255

was comparable, the allocation of those resources within the root system of 256

reduced and advanced groups differed. This shift in allocation of resources within 257

the root system is evidenced by the reduction in root diameter and metabolic cost 258

per length of root, and increase in total root length of the reduced genotypes 259

under P stress. Genotypic variation in metabolic efficiency of P. vulgaris roots 260

under P stress has been previously reported in a study by Nielsen et al. (2001), 261

where there was no difference in daily carbon allocated to roots of P-efficient and 262

P-inefficient genotypes of P. vulgaris, but P-efficient genotypes were able to 263

maintain a larger root system per unit of carbon respired than inefficient 264

genotypes. Further evidence for a genetic component to root etiolation is 265

reported in a QTL study by Beebe et al. (2006) for root architectural phenes 266



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using the same DxG RILs as in the present study. This work found that these 267

DxG RILs displayed genetic variation in P accumulation per unit root length and 268

two significant QTLs for P accumulation under P stress were identified in the 269

same regions as QTLs for root length and for specific root length, with joint QTL 270

analysis uncovering a positive relationship between specific root length and P 271

accumulation under P stress (Beebe et al. 2006). 272

The observed effect of P deficit on root length at 18 DAP suggests that the 273

reduction of secondary growth in root segments at later time points may be in 274

part the ancillary effect of shifts in allocation of resources to primary growth. The 275

regulation of root elongation under P deficiency has been previously described 276

and attributed to ethylene signaling pathways in Arabidopsis (Ma et al. 2003). In 277

P. vulgaris, ethylene production is greater in roots grown under P stress and 278

serves to maintain root elongation under P stress while ethylene inhibits 279

elongation under high P conditions (Borch et al. 1999; Liao et al. 2001). 280

Additionally, the reduction in root diameter and respiration rate at the root apex 281

under P stress indicates that the differences in secondary growth are not strictly 282

the result of the gradual accrual of differences in secondary growth in older 283

segments of root over time, but are initiated at the root apex. The anatomy of 284

these thinner apical segments from the P stress treatment did not manifest as an 285

isometric reduction in both cortex and vascular tissue, rather, we observed 286

thinner apical segments that had reduced cortex area, but comparable stele 287

area, metaxylem number, and metaxylem area to apical segments in the high P 288

treatment (Fig. S16). These P stressed root apices in reduced genotypes achieve 289

smaller TCSA and decreased respiration through reduction in cortical tissue 290

while maintaining the same amount of vasculature necessary for axial transport. 291

Unlike roots in the high P treatment, where P concentration of root tissue 292

decreased with secondary growth, under P stress, root P concentration remained 293

stable over time. This may indicate that the P stress was substantial and the P 294

concentration in root tissue was being sustained at the minimal level required to 295

maintain living tissue. While no phenotypic differences in nutrient concentrations 296



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of roots were observed between reduced and advanced groups under P stress, 297

advanced genotypes have greater root diameter and therefore greater total 298

nutrient content per length compared to reduced genotypes. In addition to the 299

smaller respiration rate per length of thinner roots, this savings in construction 300

costs is another avenue for conservation of resources in reduced genotypes 301

under P stress. Furthermore, as secondary growth progresses, the vascular 302

tissue expands and the living cortex is destroyed, thereby shifting the 303

physiological role of roots from resource capture to axial transport (McCully, 304

1999). While reduced genotypes had diminished axial conductance, the delayed 305

transition into the role of axial transport may allow roots to acquire more 306

resources from the surrounding soil for a greater length of time. 307

In addition to the possible benefit of greater direct nutrient uptake by the root, 308

retarded stele development and maintenance of cortical tissue in roots under P 309

stress has a synergistic effect on P uptake through the preservation of arbuscular 310

mycorrhizal associations that colonize the cortex. While it is well known that P 311

availability suppresses mycorrhizal associations in ways unrelated to secondary 312

growth, the significant relationship between cortical area and fungal colonization 313

across P treatments suggests that secondary growth inhibits arbuscular 314

mycorrhizal relationships. These results reinforce Brundrett (2002) who has 315

suggested that plant species with less root cortical volume sacrifice the capacity 316

for arbuscular mycorrhizal associations, and Valenzuela-Estrada et al. (2008), 317

who observed this in Vaccinium, where roots with greater radial growth and 318

reduced specific root length had less mycorrhizal colonization. 319

While suppression of secondary growth appears to facilitate mycorrhizal 320

symbiosis, it may also increase the vulnerability of roots to soil pathogens and 321

herbivores. Although there was no greater incidence of disease observed in roots 322

of reduced genotypes, in soils where pathogens and herbivores are prevalent, 323

roots with advanced secondary growth may have greater longevity than those 324

with reduced secondary growth. This relationship between anatomical 325

development and disease has demonstrated in Malus domestica, where 326



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pathogen colonization is closely linked to the senescence and loss of the root 327

cortex (Emmet et al. 2014). Although P limitation alone does not diminish root 328

survivorship in P. vulgaris grown in sand culture, in the field where soil biota are 329

present, up to 49% of roots are lost by late pod filling (Fisher et al. 2002). 330

These results support growing evidence that root phenes and phene states that 331

reduce the metabolic cost of soil exploration are adaptive in resource-poor soil 332

environments (Chimungu et al. 2014a,b; Lynch 2014; Saengwilai et al. 2014; 333

Chimungu et al. 2015; Miguel et al. 2015; Schneider et al. 2017). In this context, 334

root anatomical phenes merit attention as breeding targets for more stress 335

tolerant crops. 336

Conclusions 337

These results support the hypothesis that reduced root secondary growth 338

increases resources available for primary growth, thereby increasing the total 339

volume of soil explored and acquisition of soil resources. Although all P. vulgaris 340

genotypes tested favor primary growth of roots over secondary growth under P 341

stress, genotypes differ in the intensity of this response. Genotypes with reduced 342

secondary growth had suppressed anatomical development, reduced metabolic 343

and construction costs per length of root, greater soil exploration, and greater P 344

acquisition than genotypes with advanced secondary growth. These results 345

demonstrate the adaptive significance of reduced secondary growth under P 346

stress, but further work to determine the influence of reduced hydraulic 347

conductance in roots with reduced secondary growth on water capture in drying 348

soils would be of merit, as well as a targeted investigation into the relationship 349

between secondary growth and the colonization of arbuscular mycorrhizal. 350

Further research may elucidate if a reduction in root secondary growth improves 351

soil resource capture under drought and other nutrient deficiencies. 352

Materials & Methods 353

Germplasm 354



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Previous work by De la Riva and Lynch (2010) identified two genotypes of P. 355

vulgaris contrasting in P acquisition and root development under P stress. DOR 356

364 is a high yielding genotype developed by breeders at CIAT (Cali, Colombia) 357

(CIAT 1996, p.22-38). Despite exhibiting a strong reduction in secondary growth 358

of roots under low P conditions, it has been identified as being P inefficient due to 359

other components of the root phenotype (Liao et al. 2004). G19833 is a Peruvian 360

landrace from the Andean gene pool (Beebe et al. 1997). This genotype displays 361

less reduction in secondary growth of roots than DOR 364 under P stress (De la 362

Riva & Lynch 2010), but is classified as P efficient due to the contribution of other 363

beneficial root phenes (phene is to phenotype as gene is to genotype (York et al. 364

2013; Serebrovsky 1925) including a shallow basal root angle (Bonser et al. 365

1996), high basal root whorl number (Miguel et al. 2013), and long, dense root 366

hairs (Yan et al. 2004). DOR 364 and G19833 were selected for their contrasting 367

P efficiency and root characteristics and crossed to generate a population of 368

recombinant inbred lines (RILs). The DOR 354 x G19833 (DG) RIL population 369

was then screened for variation in root secondary growth under P stress and four 370

genotypes were selected for their observed differences in secondary growth. 371

These genotypes include DG 6 (reduced secondary growth), DG 35 (reduced 372

secondary growth), DG 23 (advanced secondary growth), DG 51 (advanced 373

secondary growth). Additionally, genotypes from the L88 RIL population 374

(developed by J. Kelly, Michigan State University), generated from a cross 375

between drought resistant B98311 and P-efficient TLP 19 (Frahm et al. 2004), 376

were selected for their differences in secondary growth of roots under low P. 377

These genotypes include L88-14 (reduced secondary growth), L88-63 (reduced 378

secondary growth), L88-43 (advanced secondary growth) and L88-57 (advanced 379

secondary growth). A multiline study by Henry et al. (2010) further supports the 380

purported contrast in secondary growth between these genotypes where under 381

low P in the field, L88-14 had thinner roots and more roots per root core while 382

L88-57 had thicker roots and less roots per core. 383

In Silico Study 384



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The functional-structural plant model SimRoot is able to integrate parameters of 385

root growth, nutrient uptake, and resource allocation from in vivo studies to 386

model the relationship between root growth and performance of P. vulgaris 387

(Postma et al. 2017). To investigate the relationship between secondary growth 388

in roots and P acquisition efficiency, root systems of P. vulgaris were modeled 389

with three different secondary growth rates; root systems with no secondary 390

growth (Reduced), root systems with 50% the secondary growth rates observed 391

under high P conditions (Intermediate), and root systems with the same 392

secondary growth rates observed under high P conditions (Advanced). All other 393

plant properties were held constant in all simulations. For each level of 394

secondary growth, P availability was varied from 0.17 to 5 kg ha-1 across 13 395

levels. Here, phosphorus concentration represents the quantity available to the 396

plant in the soil solution, and the buffer capacity of the soil (ratio between the 397

dissolved and absorbed fraction) is held constant. In total, 39 simulations (3 398

secondary growth rates x 13 P levels) were run on the Pennsylvania State 399

University clusters (http://rcc.its.psu.edu/hpc/systems). Starting from germination, 400

plant growth was simulated for 40 days and root growth was permitted to grow 401

within a 60 x 60cm by 1.5 m deep soil volume. Any roots that intersected the 402

boundary of the soil environment were mirrored back to maintain a total root 403

length similar to that of field conditions. 404

In SimRoot, carbon used for growth comes from either seed reserves or 405

photosynthesis. The model is inclusive of multiple components of metabolic costs 406

stemming from respiration, nitrogen fixation, nutrient uptake, and production of 407

exudates. Root system architecture is represented by a network of root nodes 408

and is modeled in three dimensions. Shoot growth is simulated non-geometrically 409

and is represented by integral parameters such as leaf area and dry shoot mass. 410

Phosphorus uptake at each root node is parameterized using the Barber-411

Cushman model and integrated over the length of the root system (Barber and 412

Cushman 1981). When P availability is inadequate to satisfy optimal growth, leaf 413

area expansion, photosynthesis, and root growth are inhibited. Inter-root 414

competition for P is simulated in one dimension by the Barber-Cushman model 415


http://rcc.its.psu.edu/hpc/systems


16

and is dependent on the average root density within 1 cm of the root (Postma & 416

Lynch 2011). In SimRoot, sink strength of a given organ is based on the resource 417

requirements for potential growth and maintenance of the tissue. The growth rate 418

of all root classes, leaves, and stem tissue is based on empirical data. Roots of 419

greater thickness have greater longitudinal potential growth rates and 420

consequently have greater sink strength (Pages 2000). Resources required for 421

secondary growth are determined by the volumetric increase associated with 422

class, location, and age of each root segment. Respiration is a function of the 423

root segment biomass and age. Further information on SimRoot, can be found in 424

Postma and Lynch (2011). Overview of SimRoot parameterization is available in 425

the supplementary files (SimRoot Parameterization) and files used to generate 426

this simulation are available at (https://doi.org/10.5281/zenodo.998950). 427

Greenhouse Study 428

This study was conducted in a greenhouse located at The Pennsylvania State 429

University, University Park, Pennsylvania, USA (40.801955° N, -77.862544° W). 430

Plants were grown from April through May 2016 under a 16:8 (light:dark) 431

photoperiod and max/min temperature of 34°C/20°C. Mid-day photosynthetic 432

active radiation (PAR) was approximately 900-1000 mol photons m-2 s-1. Natural 433

light was supplemented from 0600 to 2200 h with 110mol photons m-2 s-1 from 434

LED Illumitex ES2 lights (Illumitex, Inc., Austin, TX, USA). A Complete 435

Randomized Block Design was utilized with two P levels; P stress and high P. 436

The experiment was run for a total of 46 days with destructive measurements 437

taken from all genotypes in all treatments at 18, 32, and 46 days after planting 438

(DAP). Each genotype at each time point and treatment had four replications. 439

Seeds were surface sterilized in a 25% NaOCl solution for 2 minutes, rinsed in 440

deionized water and germinated in 0.5 mM CaSO4 in the dark at 28°C for 24 hrs. 441

Uniform seedlings were transplanted to the greenhouse in opaque, 20 L 442

mesocosms 30 cm in diameter and 44 cm in height, wrapped in silver duct tape 443

to enhance reflectiveness. Mesocosms were filled with a mixture of 40% coarse 444

grade A perlite (Whittemore Co., Inc., Lawrence, MA, USA), 30% medium grade 445


https://doi.org/10.5281/zenodo.998950


17

sand (Quikrete Co, Inc., Atlanta, GA, USA), 20% low P soil (Ap2 Hagerstown silt 446

loam (fine, mixed, semi-active, mesic Typic Hapludalf) Available P = 12 ppm) 447

sieved through 6mm mesh, and 10% D3 coarse grade A vermiculite (Whittemore 448

Co., Inc., Lawrence, MA, USA). The soil was incorporated to replicate features 449

found under field conditions such as the presence of organic matter, soil biota, 450

and oxide surfaces that serve to buffer P availability. Mesocosms designated as 451

being part of the high P treatment received 40 g granular triple superphosphate 452

(25% P) incorporated into the media at the time of mixing. Mesocosms assigned 453

to the low P treatment did not receive any supplemental P. Other nutrients were 454

supplied through drip irrigation once daily. At each irrigation event, high and low 455

P mesocosms received 400 ml of nutrient solution. This nutrient solution 456

contained 1.5 mM KNO3, 1.2 mM Ca(NO3)2, 0.4 mM NH4NO3, 0.025 mM MgCl2, 457

0.5 mM MgSO4, 0.3 mM K2SO4, 0.3 mM (NH4)2SO4, 5 M Fe-EDTA, 1.5 M 458

MnSO4, 1.5 M ZnSO4, 0.5 M CuSO4, 0.15 M (NH4)6Mo7O24, and 0.5 M 459

Na2B4O7. The pH of the nutrient solution was adjusted as needed at every other 460

irrigation event to 5.8 with KOH and HCl. 461

At 18, 32, and 46 DAP destructive shoot measurements were taken including leaf 462

number, dry shoot biomass, and leaf tissue P content. Dry mass was determined 463

from tissues dried at 65°C for 7 d. Leaf P content was measured 464

spectrophotometrically after ashing leaf tissue at 500°C for 16 h (Murphy & Riley 465

1962). 466

The root system of each plant was extracted, washed, and basal root whorl 467

number, basal root number, adventitious root number, root respiration rate, root 468

P content, specific root length, basal root length, and anatomical phenes were 469

measured. Root respiration rates were determined immediately after washing for 470

two, 10 cm segments taken from representative basal roots at the 10 cm nearest 471

to the hypocotyl (basal), 10 cm at the middle of the root axis (middle), and 10 cm 472

from the growing tip back (apical) (Fig. S17). To relate differences in respiration 473

rates to secondary growth of the primary root axis, lateral roots were removed 474

from these segments with a razor prior to respiration measurements. Respiration 475



18

rates were measured using a Li-Cor 6400 gas exchange system with a modified 476

respiration chamber (Li-Cor, Lincoln, NE, USA). Measurements were performed 477

under ambient greenhouse conditions with the sealed chamber being submerged 478

in a water bath kept at 28°C and baseline sample chamber and reference 479

chamber CO2 concentration of 400 mol mol-1. 480

Following respiration measurements, 2.5 cm of each root segment used for 481

respiration measurements was used for characterization of anatomy. These 482

segments were preserved using a Leica EM CPD300 critical point dryer (Leica 483

Microsystems, Inc., Buffalo Grove, IL, USA). Preserved segments were 484

sectioned with laser ablation tomography (LAT) using an Avia 7000, 355 nm 485

pulsed laser and simultaneously imaged with a camera equipped with a 5x zoom 486

lens. Root cross-section images were analyzed using MIPAR software 487

(MIPAR.beta.8, MIPAR, Columbus, OH). Anatomical features measured include 488

total cross sectional area (TCSA), percent stele area, metaxylem number, and 489

metaxylem area. Theoretical axial metaxylem conductance (Kh) (kg m MPa-1 s-1) 490

was calculated for each cross-sectional image using the modified Hagen-491

Poiseuille law (Eq. 1) where d is the diameter of the vessel in meters, is the 492

fluid density (equal to water at 20° C; 1000 kg m-3), and is the viscosity of the 493

fluid (equal to water at 20°C; 1 x 10-9 MPss) (Tyree & Ewers 1991). The 494

remaining 7.5 cm of root segments used in respiration measurements were dried 495

at 65°C for 7 d, and 2.5 mg subsample of this tissue was analyzed for N, C, and 496

H content using an elemental analyzer (Series II CHNS/O Analyzer 2400; 497

PerkinElmer). 498

𝑘ℎ = (𝜋𝜌

128𝜂)∑(𝑑𝑖

4)

𝑛

𝑖=1

Equation 1. Modified Hagen-Poiseuille law



19

Basal root whorl number, basal root number, and adventitious root number were 499

determined by counting the root whorls and basal roots after washing the root 500

system. One intact, representative basal root that was sectioned into 20 cm 501

segments along its primary axis and each segment was imaged using an EPSON 502

Perfection V700 PHOTO scanner. From the scanned image, total basal root 503

length, including length and diameters of lateral roots, was quantified with 504

WinRhizo software (WinRhizo Pro, Regent Instruments, Quebec City, Quebec, 505

Canada). The scanned basal root was then dried at 65°C and weighed to 506

determine specific root length, calculated by dividing the total root length by the 507

total root dry weight. Root P content was then determined from these dried 508

segments spectrophotometrically after ashing at 500°C for 16 h (Murphy & Riley 509

1962). 510

Field Study 511

This study was conducted at the Russell E. Larson Agricultural Research Farm, 512

at Rock Springs, Pennsylvania, USA (40.709746° N, -77.956965° W) from June 513

through September 2016. A split plot design was utilized with two P levels; two 514

0.05 ha low P fields (10 ppm mean available P by Mehlich-3 (ICP)) split into two, 515

0.025 ha blocks each and two 0.05 ha high P fields (38 ppm mean available P) 516

split into two, 0.025 ha blocks each. Plant genotypes were randomized within 517

each block. Fields were fertilized according to each treatment with soil nutrient 518

levels adjusted to meet P. vulgaris requirements as determined by soil tests at 519

the beginning of each season. Each genotype was planted in a five-row, 3 m long 520

plot with 72 cm row spacing and 10 cm intra-row spacing. During periods of 521

inadequate rainfall, irrigation was supplied through drip tape. The experiment 522

was run until destructive measurements were taken from all genotypes in all 523

treatments at time of flowering (49 DAP). Each genotype had four replications 524

within each P treatment. Average max/min temperature of this site for duration of 525

the experiment were 27°C/17°C, average total rainfall was 18.5 cm, and average 526

light:dark photoperiod was 14.5:9.5. Mid-day photosynthetic active radiation 527



20

(PAR) was approximately 1500-2000 mol photons m-2 s-1. Soil is a Hagerstown 528

silt loam (fine, mixed, semi-active, mesic Typic Hapludalf). 529

To limit the presence of fungal disease, seed were treated with Captan 50W 530

fungicide at a rate of 0.5 ml/ 100 seeds prior to planting. At time of flowering (49 531

DAP), destructive shoot measurements were taken including leaf number, dry 532

shoot biomass, and leaf tissue P content. Dry mass was determined from tissues 533

dried at 65°C. Leaf P content was measured from 10, 2.5 cm leaf discs taken 534

from throughout the canopy in each plot. 535

At flowering (49 DAP), the crown of the root system for 3 representative plants 536

per plot (i.e. per replicate) were extracted, washed, and basal root whorl number, 537

basal root number, adventitious root number, basal root growth angle were 538

measured. A representative plant is a healthy plant that is comparable in shoot 539

size to the majority of plants throughout the plot. Basal root growth angle was 540

visually scored against a protractor. Three soil cores were taken from each plot 541

to a depth of 40 cm, 10 cm from the base of representative plants toward plants 542

from the neighboring row (Giddings Machine Co., Windsor, CO, USA). Soil cores 543

were 5.1 cm in diameter and were divided into 4, 10 cm increments, washed, and 544

extracted roots from each segment were scanned with an EPSON Perfection 545

V700 PHOTO scanner. From these images root length density (length of root per 546

volume of soil) in the top 40 cm of soil was quantified with WinRhizo software 547

(WinRhizo Pro, Regent Instruments, Quebec City, Quebec, Canada). The 548

anatomy of 5 representative basal roots was analyzed from the segment of root 549

2.5 cm from the hypocotyl. Basal root segments were preserved, sectioned, and 550

anatomical features were measured following the same protocol as described 551

above. 552

Mycorrhizal Study 553

This study was conducted under the same growth conditions as described above 554

for the greenhouse trial. Two genotypes contrasting in secondary growth (DG35 555

and DG51) were used. A complete randomized block design was utilized with 556



21

two P levels; P stress and high P, and two vesicular-arbuscular mycorrhizae 557

(VAM) levels; inoculated and mock-inoculated. Each genotype had three 558

replications in each of the VAM levels within each P treatment. 559

Glomus intraradices (now known as Rhizophagus irregularis, Tisserant et al., 560

2013) promotes P acquisition in P. vulgaris (Nielsen et al, 1998) and was used 561

for this study. To facilitate even distribution of spores, the inoculant (Premier 562

Tech Biotechnologies, Rivière-de-Loup, Québec, Canada), consisting of R. 563

irregularis spores, was mixed thoroughly with 1.5 kg of sterilized sand before 564

being mixed into the bulk growth media prior to planting. The final inoculation 565

intensity for mesocosms assigned to the inoculated treatment was 200 spores 566

per liter of growth media. For the mock-inoculated treatment, the same amount of 567

the liquid inoculant was filtered through Whatman filter papers #1 and #42 (Li et 568

al., 2012), mixed with 1.5 kg sterilized sand, and added to the growth media in 569

mock inoculated mesocosms to introduce inoculum factors other than VAM fungi. 570

At 49 DAP, root and shoot measurements were taken as described in the above 571

greenhouse study. VAM colonization was quantified using the magnified 572

intersections method (McGonigle et al. 1990). Two 10 cm segments of root were 573

harvested from the basal, middle, and apical ends of 2 basal roots from each 574

plant. Segments were cleared in 10% KOH, stained in a 5% ink-vinegar solution 575

(Vierheilig et al. 1998). A minimum of 50 intersections per sample were observed 576

and the incidence of hyphae, arbuscules, and vesicles was scored. The 577

percentage incidence of each structure over total intersections was calculated. 578

Statistical Analysis 579

All statistical analyses were performed using RStudio Version 0.99.903 (RStudio, 580

Inc.). Normality and homoscedasticity of the data were determined using the 581

Shapiro-Wilk test and the non-constant error variance test respectively. Where 582

data did not meet these assumptions, a box-cox or log transformation was used 583

to normalize the data. Analysis of variance (ANOVA), Tukey HSD, and 584

regression analysis were performed with significant effects considered at P 585

0.05. Because plants grown under high P were larger than those under P stress, 586



22

allometric relationships between root phenotypes and shoot mass were explored 587

as in Burridge et al. (2017). The relationship between the decadic logarithm of 588

the root phene and shoot biomass were fitted by linear regression. Log 589

transformation of data prior to the regression analysis is necessary to normalize 590

any multiplicative relationships that may exist between the shoot biomass and 591

value of a given metric. The scaling coefficient of = 0.33 is considered to be the 592

threshold where root phenes with ≥ 0.33 have scaled faster than shoot size 593

and are considered hyperallometric, while root phenes where < 0.33 scale at a 594

slower rate than shoot size and are considered hypoallometric. Statistical 595

analysis of SimRoot output was not performed, as modeling output is most suited 596

for qualitative comparisons rather than statistical tests designed for empirical 597

data. Performing statistical tests on modeling output results in artificially high p 598

values, regardless of effect size, as differences in replicates are simply the result 599

of random number generators within the model. Additionally, because the 600

contrasting parameters are programmed into the model, it is known before the 601

model is run that the null hypothesis is false (White et al. 2014). 602

Acknowledgements: We thank James Burridge for his assistance with field 603

research, Bob Snyder for oversight of lab and field activities, Johannes Postma 604

and Harini Rangarajan for support with SimRoot, Airong Li for guidance with 605

mycorrhizal research, and Michael Williams for assistance with elemental 606

analysis. 607



23

Table 1. Allometric analysis comparing shoot biomass to root phenes in the greenhouse at 46 DAP, and in the field at 49 DAP. Root phenes include total cross sectional area (TCSA; mm2), metaxylem vessel area (MXA; mm2), metaxylem vessel number (MXN), axial hydraulic conductance (cond.; kg m MPa-

1 s-1), basal root length measured in the greenhouse (BRL; cm)/ root length density (RLD; cm/cm3), basal root whorl number (BRWN), basal root number (BRN), adventitious root number (ARN), stele cross sectional area (SCSA; mm2),

percent stele area (% Stele), basal respiration rate (Resp.; mol CO2 cm-1 s-1), total root length (Tot. RL; cm), specific root length (SRL; cm/g), and total root dry mass (R Mass; g). Anatomical data were means from the basal segment for each mesocosm/plot. Adjusted coefficient of determination (R2), y intercept (Int.),

scaling coefficient (), and P-value (p) for the regression line are shown.



24

Fie

ld

Hig

h P

p

0.4

4

0.3

5

0.7

9

0.2

5

0.9

5

0.0

6

0.0

9

0.3

6

()

0.0

8

0.0

7

0.0

3

0.0

6

-0.0

1

0.6

6

0.3

0

0.1

9

Int.

1.2

2

1.2

8

1.1

6

1.6

7

1.2

2

1.0

2

1.0

1

1.0

3

R2

-0.0

1

-0.0

04

-0.0

3

0.0

1

-0

.03

0.1

0

0.0

8

-0.0

05

P S

tre

ss

p

0.0

6

0.1

3

0.3

9

0.0

4

0.0

1

0.6

1

0.2

5

0.5

7

()

-0.2

6

-0.1

9

-0.1

4

-0.1

8

0.7

1

0.4

5

0.4

8

-0.2

1

Int.

0.9

9

0.8

1

1.2

4

-0.4

0

1.2

3

0.8

6

0.6

3

1.2

4

R2

0.0

9

0.0

4

-0.0

08

0.1

0

0.2

0

-0.0

2

0.0

1

-0.0

2

G

ree

nh

ou

se

Hig

h P

p

0.9

8

0.8

1

0.5

1

0.9

9

0.3

0

0.2

0

0.0

2

0.4

8

0.9

7

0.6

9

0.2

3

0.0

4

0.9

8

<0.0

1

()

0.0

03

0.0

2

0.0

8

0.0

01

-0.1

8

0.2

6

0.5

7

-0.0

5

0.0

04

0.2

8

0.1

0

0.1

8

0.0

04

0.5

0

Int.

1.5

9

1.6

0

1.4

3

1.5

9

1.9

2

1.4

9

1.0

6

1.6

3

1.5

8

1.0

2

1.9

2

0.9

6

1.5

7

1.1

0

R2

-0.0

3

-0.0

3

-0.0

2

-0.0

3

0.0

03

0.0

2

0.1

4

-0.0

2

-0.0

3

-0.0

3

0.0

2

0.1

0

-0.0

3

0.6

0

P S

tre

ss

p

0.2

0

0.7

9

0.7

3

0.6

4

<0.0

1

0.1

6

0.0

5

0.0

8

0.4

1

0.8

3

<0.0

1

0.0

1

<0.0

1

<0.0

1

()

-0.2

7

-0.4

-0.0

6

0.0

5

1.9

0

0.6

2

0.9

0

-0.4

8

-0.1

0

-0.0

5

-0.3

2

0.3

5

0.6

8

0.6

7

Int.

0.5

0

0.5

1

0.6

6

0.9

6

-2.8

7

0.3

6

-0.2

8

1.0

7

0.5

2

0.6

6

-0.8

7

-0.4

7

-2.3

2

0.5

2

R2

0.0

2

-0.0

3

-0.0

3

-0.0

3

0.5

2

0.0

3

0.0

9

0.0

7

-0.0

1

-0.0

3

0.2

3

0.1

6

0.1

9

0.6

9

TCSA

MX

A

MX

N

Co

nd

.

BR

L/R

LD

BR

WN

BR

N

AR

N

SCSA

% S

tele

Re

sp.

Tot.

RL

SRL

R M

ass



25

Figure Legends

Figure 1. SimRoot results showing meanSE root respiration rate (g C/g root-1 day-1) (A), total root length (m) (B), total P uptake (mmol) (C), and shoot biomass (g) (D) in roots systems with three levels of secondary growth (advanced,

intermediate, reduced) under P stress (4 m P) and high P (30 m P) at 40 days of growth.

Figure 2. MeanSE shoot mass (g) (A), leaf number (B), and leaf area (cm2) (C) at 18, 32, and 46 DAP under P stress in the greenhouse. Comparisons are made across all timepoints.

Figure 3. MeanSE specific root length (m/g) (A), axial basal root length (cm) (B), and total shoot P (mg) (C) at 18, 32, and 46 DAP under P stress in the greenhouse. Comparisons are made across all timepoints.

Figure 4. Field data comparing basal TCSA (mm2) (A), root length density (RLD) (cm/cm3) (B), and total shoot P (mg) (C) between advanced and reduced phenotypes under P stress. Comparisons for each variable were made across phenotypic groups and P treatments.

Figure 5. Correlation between mean basal TCSA (mm2) and mean root length density (RLD) (cm/cm3) (A, B), as well as mean root length density (RLD) (cm/cm3) and total shoot P (mg) (C, D) for each plot under P stress and high P treatments in the field. Red lines indicate a significant correlation at a confidence

levels of p 0.05 using Pearson’s product-moment correlation analysis. n = 32

Figure 6. MeanSE TCSA (mm2) of basal root at three locations along the root axis taken at 18 DAP (A), 32 DAP (B), and 46 DAP (C) under P stress in the greenhouse. Comparisons are made within each timepoint.

Figure 7. Comparison of basal root anatomy between reduced and advanced groups under high P and P stress in greenhouse conditions at 46 DAP. All cross

sections are at the same scale (bar is 100 m).

Figure 8. MeanSE basal root TCSA (mm2) (A), metaxylem number (B), total metaxylem area (mm2) (C), and axial hydraulic conductance (kg m MPa-1 s-1) (D) at 49 DAP in the field. Comparisons for each variable were made across phenotypic groups and P treatments.

Figure 9. Correlation between basal TCSA (mm2) and basal respiration rate (μmol CO2 cm-1 s-1) (A), total basal root length (cm) (B), and total shoot P (mg) (C) under P stress and high P treatments at 46 DAP in the greenhouse. Red

lines indicate a significant correlation at a confidence levels of p 0.05 using Pearson’s product-moment correlation analysis. n = 32



26

Figure 10. MeanSE respiration rate (mol CO2 cm-1 s-1) of the basal (A), middle (B), and apical (C) positions at 18, 32, and 46 DAP under P stress in the greenhouse. Comparisons are made within each timepoint.

Figure 11. Cortical tissue containing fungal hyphae being shed during secondary growth (A). Cross section of basal root axis at 46 DAP in the greenhouse showing difference in cortical tissue abundance under high P and P stress (B).

MeanSE percent colonization of basal root axis at three positions of the root under high P and P stress (C). Relationship between mean cortical tissue abundance in cross section and mean percentage colonization for roots grown under high P and P stress (n = 36) (D).

Supplemental Data

Supplemental Figure S1. Transverse section of basal root at different developmental stages to highlight changes in tissue as secondary growth progresses.

Supplemental Figure S2. SimRoot results for three P. vulgaris root systems with three levels of secondary growth.

Supplemental Figure S3. Model of P. vulgaris root systems with two levels of secondary growth.

Supplemental Figure S4. SimRoot results showing meanSE total P uptake, and shoot biomass in roots systems with no secondary growth.

Supplemental Figure S5. MeanSE root mass of genotypes with advanced and reduced secondary growth in the greenhouse at 46 DAP.

Supplemental Figure S6. MeanSE net length of lateral roots per basal root.

Supplemental Figure S7. MeanSE percent stele area of cross section of basal, middle, and apical positions.

Supplemental Figure S8. MeanSE metaxylem vessel number of basal, middle, and apical positions.

Supplemental Figure S9. MeanSE net metaxylem vessel area (mm2) of basal, middle, and apical positions.

Supplemental Figure S10. MeanSE theoretical axial hydraulic conductance (kg m MPa-1 s-1) of basal, middle, and apical positions.

Supplemental Figure S11. Root crowns of genotypes with advanced and reduced secondary growth excavated at 49 DAP from the field under P stress.



27

Supplemental Figure S12. MeanSE basal TCSA:root length (mm2/m) of eight genotypes in the greenhouse at 32 and 46 DAP under P stress.

Supplemental Figure S13. Correlation between total basal root length (cm) and respiration rate (μmol CO2 cm-1 s-1) of the apical, middle, and basal segments under P stress and high P treatments.

Supplemental Figure S14. Correlation between dry shoot weight (g) and respiration rate (μmol CO2 cm-1 s-1) of the apical, middle, and basal segments under P stress and high P treatments at 46 DAP in the greenhouse.

Supplemental Figure S15. MeanSE TCSA (mm2) (A), N concentration (%), and P concentration (mg P/g tissue) of the basal segment in each phenotypic group.

Supplemental Figure S16. MeanSE TCSA (mm2), percent stele area (%), cortex area (mm2), and theoretical hydraulic conductance

Supplemental Figure S17. Diagram of basal root segment locations for anatomy, respiration, and elemental analysis.

Supplemental Data. Summarized hierarchical input file showing context of SimRoot parameters.

Supplemental Figure S1. Transverse section of basal root at different developmental stages to highlight changes in tissue as secondary growth progresses. Bars are 0.5 mm; images are all to the same scale.

Supplemental Figure S2. SimRoot results for three P. vulgaris root systems with three levels of secondary growth (advanced, intermediate, and reduced) grown

over 40 days under 4m available P where reducing secondary growth of roots results in reduced metabolic cost (A), greater total root length (B), greater P uptake (C), and greater shoot biomass (D).

Supplemental Figure S3. Model of P. vulgaris root systems with two levels of

secondary growth (reduced and advanced) at 40 DAP under 4 m available P where reducing secondary growth of roots results in greater allocation of resources to increase root length. The reduced phenotype has 14% greater root length than advanced phenotype at this P availability.



28

Supplemental Figure S4. SimRoot results showing meanSE total P uptake (A), and shoot biomass (B) in roots systems with no secondary growth under three levels of P stratification at 40 days of growth. Simulation with no stratification had

4 m P homogenously distributed throughout soil profile. Simulation with weak

stratification had 4 m P in top 15 cm, 1.33 m P from 16 to 29 cm, and 0.27 m

P from 30 cm and below. Simulation with strong stratification had 4 m P in top 5

cm, 1.33 m P from 6 to 10 cm, and 0.27 m P from 11 to 29 cm and 0.24 m P from 30 cm and below.

Supplemental Figure S5. MeanSE root mass (g) of genotypes with advanced

and reduced secondary growth in the greenhouse at 46 DAP (A). MeanSE root mass : shoot mass ratio (g/g) of genotypes with advanced and reduced secondary growth at 46 DAP in the greenhouse (B).

Supplemental Figure S6. MeanSE net length of lateral roots per basal root (cm) (A), percentage of the total basal root length comprised of lateral roots (%) (B), and percentage of lateral roots <0.5mmin diameter (%) (C) in genotypes with advanced and reduced secondary growth under high P and P stress in the greenhouse at 46 DAP.

Supplemental Figure S7. MeanSE percent stele area of cross section of basal, middle, and apical positions at 18 (A), 32 (B), and 46 DAP (C) under P stress in the greenhouse. Comparisons are made within each timepoint.

Supplemental Figure S8. MeanSE metaxylem vessel number of basal, middle, and apical positions at 18 (A), 32 (B), and 46 DAP (C) under P stress in the greenhouse. Comparisons are made within each timepoint.

Supplemental Figure S9. MeanSE net metaxylem vessel area (mm2) of basal, middle, and apical positions at 18 (A), 32 (B), and 46 DAP (C) under P stress in the greenhouse. Comparisons are made within each timepoint.

Supplemental Figure S10. MeanSE theoretical axial hydraulic conductance (kg m MPa-1 s-1) of basal, middle, and apical positions at 18 (A), 32 (B), and 46 DAP (C) under P stress in the greenhouse. Comparisons are made within each timepoint.

Supplemental Figure S11. Root crowns of genotypes with advanced and reduced secondary growth excavated at 49 DAP from the field under P stress. Cross sections are representative of the mean TCSA of the basal segment of each genotype under P stress.

Supplemental Figure S12. MeanSE basal TCSA:root length (mm2/m) of eight genotypes in the greenhouse at 32 and 46 DAP under P stress (A). Mean basal TCSA (mm2) plotted against mean total basal root length (m) in greenhouse at 32 and 46 DAP under P stress (B). Genotypes in the advanced group had mean TCSA:RL > 0.1 while genotypes in the reduced group had a mean TCSA:RL of <



29

0.1. The dotted line denotes the threshold of 0.1 that separates the phenotypic groups.

Supplemental Figure S13. Correlation between total basal root length (cm) and respiration rate (μmol CO2 cm-1 s-1) of the apical, middle, and basal segments under P stress and high P treatments at 18 (A, B), 32 (C, D), and 46 DAP (E, F) in the greenhouse. Red lines indicate a significant correlation at a confidence levels of p ≤ 0.05 using Pearson’s product-moment correlation analysis. n = 96

Supplemental Figure S14. Correlation between dry shoot weight (g) and respiration rate (μmol CO2 cm-1 s-1) of the apical (A, B), middle (C, D), and basal segments (E, F) under P stress and high P treatments at 46 DAP in the greenhouse. Red lines indicate a significant correlation at a confidence levels of p ≤ 0.05 using Pearson’s product-moment correlation analysis. n = 32

Supplemental Figure S15. MeanSE TCSA (mm2) (A), N concentration (%) (B), and P concentration (mg P/g tissue) (C) of the basal segment in each phenotypic group under P stress (L) and high P (H) treatments at 18, 32 and 46 DAP.

Supplemental Figure S16. MeanSE TCSA (mm2) (A), percent stele area (%) (B), cortex area (mm2) (C), and theoretical hydraulic conductance (kg m MPa-1 s-

1) of the apical segment under P stress and high P at 46 DAP.

Supplemental Figure S17. Diagram of basal root segment locations for anatomy, respiration, and elemental analysis.

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Beebe SE, Rojas-Pierce M, Yan XL, Blair MW, Pedraza F, Munoz F, Tohme J, Lynch JP (2006) Quantitative trait loci for root architecture traits correlated with phosphorus acquisition in common bean. Crop Science 46: 413-423

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A

B

C

D

Figure 1. SimRoot results showing mean±SE root respiration rate (g C/g root-1 day-1) (A), total root length (m) (B), total P uptake (mmol) (C), and shoot biomass (g) (D) in roots systems with three levels of secondarygrowth (advanced, intermediate, reduced) under P stress (4μm P) and high P(30μm P) at 40 days of growth.

4 μmol P 30 μmol P

Sh

oot

Mass

(g)

Tota

l P U

pta

ke(m

mol)

Tota

l R

oot

Length

(m

pla

nt-1

)R

oot

Resp

irati

on

(g C

/g r

oot-1

day

-1)

Advanced Intermediate Reduced



**

*

*

*

**

*A

B

C

Figure 2. Mean±SE shoot mass (g) (A), leaf number (B), and leaf area (cm2) (C) at 18, 32, and 46 DAP under P stress in the greenhouse. Comparisons are made across all timepoints.

18 32 46DAP

1

3

5

7

14

10

6

2

1550

950

350

Leaf

Are

a (

cm2)

Leaf

Num

ber

Sh

oot

Mass

(g)

e

e

a

bc

dfa

bc

de

a

bc

df



*

*

* *

**

*

Shoot

PB

asa

l R

oot

Leng

thSpeci

fic

Root

Length

(mg)

(cm

)A

B

C

100

150

200

250

300(m

/g)

70

55

40

12

9

6

3

0

Figure 3. Mean±SE specific root length (m/g) (A), axial basal root length (cm) (B), and total shoot P (mg) (C) at 18, 32, and 46 DAP under P stress in the greenhouse. Comparisons are made across all timepoints.

18 32 46

a

ab

a a

bcbc

c

b

cd

a

a

ab

bc

cdd



A

B

C

Tota

l S

hoot

P (

mg

)R

LD

(cm

/cm

3)

Basal TC

SA

(m

m2)

Advanced Reduced

bab

a

c

High P

P Stress

aba

ab b

a

b

a

c

Figure 4. Field data comparing basal TCSA (mm2) (A), RLD (cm/cm3) (B), and total shoot P (mg) (C) between ASG and RSG phenotypes under P stress. Comparisons for each variable were made across phenotypic groups and P treatments.

c

a a

b

aab

bab

aab b

c



P Stress High PP Stress High PA B

C D

Figure 5. Correlation between mean basal TCSA (mm2) and mean RLD (cm/cm3) (A, B), as well as mean RLD (cm/cm3) and total shoot P (mg) (C, D) for each plot under P stress and high P treatments in the field. Red lines indicate a significant correlation at a confidence levels of P ≤ 0.05 using Pearson’s product-moment correlation analysis. n= 32



**

*

* **

**

*

A

B

C

Roo

t TC

SA

(m

m2)

Figure 6. Mean±SE TCSA (mm2) of basal root at three locations along the root axis taken at 18 (A), 32 (B), and 46 DAP (C) under P stress in the greenhouse. Comparisons are made within each timepoint.

Basal Middle Apical

0.6

0.5

0.4

0.3

0.6

0.4

0.2

0.8

0.6

0.4

0.2

0

TCS

A (

mm

2)

b

a

c

b

d

a

b

a

b

a

c

a

b

a

b

a

b

a



Adv

ance

d R

educ

ed

P stress

Apical Middle Basal

P stress P stress High P High P High P

Figure 7. Comparison of basal root anatomy between reduced and advanced groups under high P and P stress in greenhouse conditions at 46 DAP. Roots under P stress have smaller TCSA, smaller percent stele area, fewer xylem vessels, less vessel area, and reduced hydraulic conductance compared to roots grown under high P. All cross sections are at the same scale (bar is 100μm).



TCS

AM

eta

xyle

m N

um

ber

Meta

xyle

m A

rea

Conduct

ance

kg m

MPa

-1 s

-1m

m2

mm

2a

b

ca

a

b

a

c

aa

b

c

a

c

a

b

A

B

C

D

Figure 8. Mean±SE basal root TCSA (mm2) (A), metaxylem number (B), totalmetaxylem area (mm2) (C), and axial hydraulic conductance (kg m MPa-1 s-1)(D) at 49 DAP in the field. Comparisons for each variable were made acrossphenotypic groups and P treatments.

Advanced Reduced

TCS

A(m

m2)

Meta

xyle

m N

um

ber

Meta

xyle

m A

rea

(mm

2)

Cond

uct

ance

(kg

m M

Pa-1 s

-1)

High PP Stress

cccccccccccccccccccccccccccccccc

cccccccccccccccccccccccccc

a

bb

c

c

ab

a

a

bb

c

c

bb

a



Figure 9. Correlation between basal TCSA (mm2) and basal respiration rate (μmol CO2 cm-1 s-1) (A), total basal root length (cm) (B), and total shoot P (mg) (C) under P stress and high P treatments at 46 DAP in the greenhouse. Red lines indicate a significant correlation at a confidence levels of P ≤ 0.05 using Pearson’s product-moment correlation analysis. n=32

Basal Respiration (μmol CO2 cm-1 s-1)

A B

C D

E F



Resp

irati

on (μ

mol C

O2

cm

-1 s

-1)

Figure 10. Mean±SE respiration rate (μmol CO2 cm-1 s-1) of the basal, middle, and apical positions at 18 (A), 32 (B), and 46 DAP (C) under P stress in the greenhouse. Comparisons are made within each timepoint.

A

B

C

a a

a

a

bc

ab

c

d d

a

a

b

bcc c



High P P Stress

A C

DB

Colonization (%)

Co

rtic

al T

issu

e (m

m2 )Cortical Tissue

Cortical Tissue Hyphae Secondary Tissue

Colo

niz

ati

on

(%

)

Basal Middle Apical

High PP Stress

Colo

niz

ati

on

(%

)

bc bc

aba

c cc

Colonization (%)

Cort

ical Tis

su

e (

mm

2)

Figure 11. Cortical tissue containing fungal hyphae being shed during secondary growth (A). Cross section of basal root axis at 46 DAP in the greenhouse showing difference in cortical tissue abundance under high P and P stress (B). Mean±SE percent colonization of basal root axis at three positions of the root under high P and P stress (C). Relationship between mean cortical tissue abundance in cross section and mean percentage colonization for roots grown under high P and P stress (n = 36) (D).

DHigh PP Stress



Parsed CitationsBarber S, Cushman J (1981) Nitrogen uptake model for agronomic crops. In: Iskandar I. ed. Modeling waste water renovation: landtreatment. New York: Wiley Interscience, 382–409.

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

Beebe S, Toro O, Gonzalez AV, Chacon MI, Debouck DG (1997) Wild-weed-crop complexes of common bean (Phaseolus vulgaris L,Fabaceae) in the Andes of Peru and Colombia, and their implications for conservation and breeding. Genetic Resources and CropEvolution 44: 73-91


Beebe SE, Rojas-Pierce M, Yan XL, Blair MW, Pedraza F, Munoz F, Tohme J, Lynch JP (2006) Quantitative trait loci for rootarchitecture traits correlated with phosphorus acquisition in common bean. Crop Science 46: 413-423


Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Annual Review of Plant Physiology and PlantMolecular Biology 24: 225-252


Bonser AM, Lynch J, Snapp S (1996) Effect of phosphorus deficiency on growth angle of basal roots in Phaseolus vulgaris. NewPhytologist 132: 281-288


Borch K, Bouma TJ, Lynch JP, Brown KM (1999) Ethylene: a regulator of root architectural responses to soil phosphorus availability.Plant Cell and Environment 22: 425-431


Brundrett MC (2002) Coevolution of roots and mycorrhizas of land plants. New Phytologist 154: 275-304Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Burridge JD, Schneider HM, Huynh BL, Roberts PA, Bucksch A, Lynch JP (2017) Genome-wide association mapping and agronomicimpact of cowpea root architecture. Theoretical and Applied Genetics 130: 419-431


Chimungu JG, Brown KM, Lynch JP (2014a) Reduced root cortical cell file number improves drought tolerance in maize. PlantPhysiology 166: 1943-1955


Chimungu JG, Brown KM, Lynch JP (2014b) Large root cortical cell size improves drought tolerance in maize (Zea mays L.). PlantPhysiology 166: 2166-2178


Chimungu JG, Maliro MFA, Nalivata PC, Kanyama-Phiri G, Brown KM, Lynch JP (2015) Utility of root cortical aerenchyma under waterlimited conditions in tropical maize (Zea mays L.). Field Crops Research, 171: 86-98


CIAT (1996) Bean program annual report. CIAT, Cali, Columbia.Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

De la Riva LM, Lynch JP (2010) Root etiolation as a strategy for phosphorus acquisition in common bean (Masters dissertation). Thehttps://plantphysiol.orgDownloaded on November 13, 2020. - Published by

Copyright (c) 2020 American Society of Plant Biologists. All rights reserved.

http://www.ncbi.nlm.nih.gov/pubmed?term=Barber S%2C Cushman J %281981%29 Nitrogen uptake model for agronomic crops%2E In%3A Iskandar I%2E ed%2E Modeling waste water renovation%3A land treatment%2E New York%3A Wiley Interscience%2C 382�??409%2E&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Barber S, Cushman J (1981) Nitrogen uptake model for agronomic crops. In: Iskandar I. ed. Modeling waste water renovation: land treatment. New York: Wiley Interscience, 382?409.

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

http://scholar.google.com/scholar?as_q=Nitrogen uptake model for agronomic crops.&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=Nitrogen uptake model for agronomic crops.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Barber&as_ylo=1981&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Beebe S%2C Toro O%2C Gonzalez AV%2C Chacon MI%2C Debouck DG %281997%29 Wild%2Dweed%2Dcrop complexes of common bean %28Phaseolus vulgaris L%2C Fabaceae%29 in the Andes of Peru and Colombia%2C and their implications for conservation and breeding%2E Genetic Resources and Crop Evolution 44%3A 73%2D91&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Beebe S, Toro O, Gonzalez AV, Chacon MI, Debouck DG (1997) Wild-weed-crop complexes of common bean (Phaseolus vulgaris L, Fabaceae) in the Andes of Peru and Colombia, and their implications for conservation and breeding. Genetic Resources and Crop Evolution 44: 73-91

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

http://scholar.google.com/scholar?as_q=Wild-weed-crop complexes of common bean (Phaseolus vulgaris L, Fabaceae) in the Andes of Peru and Colombia, and their implications for conservation and breeding&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=Wild-weed-crop complexes of common bean (Phaseolus vulgaris L, Fabaceae) in the Andes of Peru and Colombia, and their implications for conservation and breeding&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Beebe&as_ylo=1997&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Beebe SE%2C Rojas%2DPierce M%2C Yan XL%2C Blair MW%2C Pedraza F%2C Munoz F%2C Tohme J%2C Lynch JP %282006%29 Quantitative trait loci for root architecture traits correlated with phosphorus acquisition in common bean%2E Crop Science 46%3A 413%2D423&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Beebe SE, Rojas-Pierce M, Yan XL, Blair MW, Pedraza F, Munoz F, Tohme J, Lynch JP (2006) Quantitative trait loci for root architecture traits correlated with phosphorus acquisition in common bean. Crop Science 46: 413-423

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

http://scholar.google.com/scholar?as_q=Quantitative trait loci for root architecture traits correlated with phosphorus acquisition in common bean&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=Quantitative trait loci for root architecture traits correlated with phosphorus acquisition in common bean&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Beebe&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Bieleski RL %281973%29 Phosphate pools%2C phosphate transport%2C and phosphate availability%2E Annual Review of Plant Physiology and Plant Molecular Biology 24%3A 225%2D252&dopt=abstract

http://search.crossref.org/?page=1&rows=2&q=Bieleski RL (1973) Phosphate pools, phosphate transport, and phosphate availability. Annual Review of Plant Physiology and Plant Molecular Biology 24: 225-252

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

http://scholar.google.com/scholar?as_q=Phosphate pools, phosphate transport, and phosphate availability&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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Li H, Xiang D, Wang C, Li XL, Lou Y (2012) Effects of epigeic earthworm (Eisenia fetida) and arbuscular mycorrhizal fungus (Glomusintraradices) on enzyme activities of a sterilized soil-sand mixture and nutrient uptake by maize. Biology and Fertility of Soils 48: 879-887


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Liao H, Yan XL, Rubio G, Beebe SE, Blair MW, Lynch JP (2004) Genetic mapping of basal root gravitropism and phosphorus acquisitionefficiency in common bean. Functional Plant Biology 31: 959-970


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Ma Z, Baskin TI, Brown KM, Lynch JP (2003) Regulation of root elongation under phosphorus stress involves changes in ethyleneresponsiveness. Plant Physiology 131: 1381-1390


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http://www.ncbi.nlm.nih.gov/pubmed?term=Schneider HM%2C Postma JA%2C Wojciechowski T%2C Kuppe C%2C Lynch JP %282017%29 Root cortical senescence improves barley growth under suboptimal availability of N%2C P%2C and K%2E Plant Physiology%2C 174%3A 2333�??2347&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Tisserant E%2C Malbreil M%2C Kuo A%2C Kohler A%2C Symeonidi A%2C Balestrini R%2C Charron P%2C Duensing N%2C Frey NFD%2C Gianinazzi%2DPearson V%2C Gilbert LB%2C Handa Y%2C Herr JR%2C Hijri M%2C Koul R%2C Kawaguchi M%2C Krajinski F%2C Lammers PJ%2C Masclauxm FG%2C Murat C%2C Morin E%2C Ndikumana S%2C Pagni M%2C Petitpierre D%2C Requena N%2C Rosikiewicz P%2C Riley R%2C Saito K%2C Clemente HS%2C Shapiro H%2C Van Tuinen D%2C Becard G%2C Bonfante P%2C Paszkowski U%2C Shachar%2DHill YY%2C Tuskan GA%2C Young PW%2C Sanders IR%2C Henrissat B%2C Rensing SA%2C Grigoriev IV%2C Corradi N%2C Roux C%2C Martin F %282013%29 Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis%2E Proceedings of the National Academy of Sciences of the United States of America 110%3A 20117%2D20122&dopt=abstract

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http://www.ncbi.nlm.nih.gov/pubmed?term=Valenzuela%2DEstrada LR%2C Vera%2DCaraballo V%2C Ruth LE%2C Eissenstat DM %282008%29 Root anatomy%2C morphology%2C and longevity among root orders in Vaccinium corymbosum%28ericaceae%29%2E American Journal of Botany 95%3A 1506%2D1514&dopt=abstract

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Short Title: Root Secondary Growth and Phosphorus ......2017/11/08 · Jonathan P. Lynch, Email:...

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