Root phenotypic characterization of lesquerella genetic resources

Industrial Crops and Products 62 (2014) 130–139

Contents lists available at ScienceDirect

Industrial Crops and Products journal homepage: www.elsevier.com/locate/indcrop

Root phenotypic characterization of lesquerella genetic resources Von Mark V. Cruz a,b,∗ , Louise H. Comas c , David A. Dierig a,1 a

USDA-ARS National Center for Genetic Resources Preservation, 1111 S. Mason St., Fort Collins, CO 80521, USA Dept. Bioagricultural Sciences and Pest Mgt., Colorado State University, Fort Collins, CO 80523, USA c USDA-ARS Water Management Research Unit, 2150 Centre Avenue, Building D, Suite 320, Fort Collins, CO 80526, USA b

a r t i c l e

i n f o

Article history: Received 18 June 2014 Received in revised form 9 August 2014 Accepted 14 August 2014 Keywords: Bladderpod Phenotyping Genebank Root morphological diversity Arid zone species

a b s t r a c t Root systems are crucial for optimizing plant growth and productivity. There has been a push to better understand root morphological and architectural traits and their plasticity because these traits determine the capacity of plants to effectively acquire available water and soil nutrients in the soil profile. In this study, two sets of germplasm materials were used to investigate the root system of the new oilseed crop Physaria fendleri (syn. Lesquerella fendleri) and gather preliminary information on available variability in root traits of the taxa and determine their response to temperature previously found optimal for above ground biomass development in the field. One experiment consisted of eighteen Physaria accessions grown in germination pouches for 21 days under two temperature treatments (21/13 ◦ C and at 30/21 ◦ C) then screened for nine root system parameters. Substantial variation in root length was found within the taxon. Apical root length was plastic in response to temperature with plants growing longer apical root zones when grown at a higher temperature and no difference in other root variables associated with temperature. The second experiment consisted of three accessions of P. fendleri and two of its sister genus Paysonia grown for 60 days in the greenhouse. Root trait analyses indicated that total root length, root length density, specific surface area and diameter differed between the two genera. Two accessions of P. fendleri, WCL-LO4 and PI 596456, were represented in both laboratory and greenhouse experiments. PI 596456 exhibited greater root:shoot ratio and root mass ratio than WCL-LO4 in both growth environments. This root trait screening in P. fendleri and Paysonia provided initial information in lesquerella as basis for future genetic and/or physiological studies relating to its root system. © 2014 Elsevier B.V. All rights reserved.

1. Introduction Screening for root trait variation has already been conducted on different crop species to assist breeding programs in identifying genes responsible for nutrient uptake, drought tolerance and root architecture. For example germplasm sets in chickpea (Jha et al., 2014; Kashiwagi et al., 2005), pea (McPhee, 2005), radish (Jatoi et al., 2011), barley (Meskine et al., 2006), rice (Gowda et al., 2011) and soybean (Manavalan et al., 2010) have been analyzed for root trait architecture and root growth under different conditions. It is recognized that screening of plant roots in nonstandard growth conditions have inherent limitations (Silberbush, 2013), but valuable information has been obtained in ex situ

∗ Corresponding author at: USDA-ARS National Center for Genetic Resources Preservation, 1111 S. Mason St., Fort Collins, CO 80521, USA. Tel.: +1 9704953260. E-mail address: [email protected] (V.M.V. Cruz). 1 Present address: Bridgestone Americas Inc., 4140W. Harmon Rd. Eloy, AZ 85131, USA. http://dx.doi.org/10.1016/j.indcrop.2014.08.029 0926-6690/© 2014 Elsevier B.V. All rights reserved.

screening. Researchers are also bringing forward new technologies and screening protocols that allow looking at these ‘hidden’ plant organs in different ways, such as utilizing 3D structural tomography, radar and functional imaging technologies (Fiorani and Schurr, 2013; Thompson et al., 2013; Yang et al., 2013). A number of root quantitative trait loci (QTL) have been identified in different crops, with the most reported in rice (Mir et al., 2013; Uga et al., 2013). Knowledge from these root screening studies has enabled breeders to identify materials that may be utilized as source of useful alleles that can be incorporated in advanced lines (Stevanato et al., 2013; Henry, 2012). Several germplasm collections of the U.S. National Plant Germplasm System (NPGS) are also currently being characterized for root traits but phenotyping is still not routinely done, unlike for above ground traits. Investigating the variation in root traits in germplasm materials will enhance the suite of associated information available to stakeholders and germplasm users. Understanding key root traits and their response to environmental stimuli are considered important in helping increase the productivity of plants, especially in being able to develop varieties

V.M.V. Cruz et al. / Industrial Crops and Products 62 (2014) 130–139

that thrive on environments with poor growing conditions and limited water resources (Comas et al., 2013). It has been postulated that by modifying the root morphology and architecture of plants, there could be significant increases in their ability to tolerate abiotic stress or nutrient and water uptake resulting to greater productivity (Liu et al., 2011; Schultz et al., 2010). Positive reports on this specific endeavor exist on the model species Arabidopsis (Iwata et al., 2013), as well as the major cereal crops; rice (Uga et al., 2013; Kato et al., 2006), wheat (Sayar et al., 2007), and maize (Ruta et al., 2010; Giuliani et al., 2005). Lesquerella (Physaria fendleri) is a member of the Brassicaceae and native to the southwestern states of the United States and northern Mexico. It is a new oilseed crop species with domestication and formal breeding research and development activities that started in the 1980s (Cruz and Dierig, 2012; Van Dyne, 1997). Several member species of Physaria and its sister genus Paysonia were identified to contain high percentage of seed oils with unique fatty acid profiles that can easily substitute for imported castor oil as a source of a myriad of industrial products (Thompson, 1985; Princen, 1983). The U.S. Department of Agriculture holds the national collection of lesquerella germplasm which was initially assembled in the 1960s and later expanded through several collecting missions in the U.S. Southwest and in Mexico during the 1990s (Dierig and Ray, 2009; Thompson, 1985). Additional germplasm exploration activities to expand the collection were done in the U.S. Southwest in 2010 (Cruz and Dierig, 2010). Characterization of the lesquerella plant genetic resources collections have mostly focused on the oil content, fatty acid profile, and above-ground parts. There has been no prior investigation into the root morphological variation in lesquerella and any of its Paysonia relatives, nor responses of lesquerella root systems to various environmental conditions. We seek to gather initial information on these traits using an advanced lesquerella breeding line (WCL-LO4) and several unimproved germplasm to get an indication of the available root diversity in the germplasm collection as well as to get insight of root responses to temperature regimens that were previously found to significantly affect yield and seed production in the species. 2. Materials and methods 2.1. Plant materials Seeds were obtained from germplasm collections of the USDAARS National Arid Land Plant Genetic Resources Unit (NALPGRU), Parlier, CA for Physaria accessions and USDA-ARS National Center for Genetic Resources Preservation (NCGRP), Fort Collins, CO for Paysonia (Table 1). The accessions were selected based on available seed quantities in the collection. The Physaria and Paysonia species used in this study were previously all classified as Lesquerella prior to taxonomic revision (Al-Shehbaz and O’Kane, 2002). Germplasm passport data was obtained from the USDA Genetic Resources Information Network (GRIN) database with associated climate data for the germplasm locality source downloaded from the climate normals database of the PRISM Climate Group, Oregon State University (PRISM, 2013) (Table 1). 2.2. Germination pouch experiment for temperature response determination Seeds of 18 P. fendleri accessions were grown in cygTM Seed Germination Pouches (16.5 × 17.5 cm) (Mega Intl., St. Paul, MN) for 21 days. Three pouches per replicate were established with four seeds each to obtain at least eight plants per replicate. Three replicates per treatment of each accession were set up in staggered

131

weeks using a complete block design. The pouches were filled with 15 ml of distilled water and were positioned vertically inside hanging file folders (Pendaflex, Melville, NY) suspended in racks and placed in growth chambers (Percival Scientific Inc., Perry, IA); one set at 21/13 ◦ C and another at 30/21 ◦ C, both with fluorescent light (2738 lux) for 12 h during the high temperature cycle. The two temperature settings were chosen because they were previously shown to affect shoot branching, reproductive development and silique production during field trials of lesquerella conducted previously by Dierig and Crafts-Brandner (2011). The pouches were topped with distilled water when the top of the pouches were dry. Roots from eight selected lesquerella plants per replicate were suspended in shallow water and scanned with a desktop scanner. Estimates of root:shoot ratios were computed based on pooled dry mass of roots and shoots of seedlings per replicate for each treatment because dry mass of individual seedling roots and shoots was insufficient to register on a microbalance. Root mass ratio was estimated using the root dry mass divided by the total plant dry mass. 2.3. Greenhouse experiment to compare Physaria and Paysonia In the greenhouse, seeds of three Physaria and two Paysonia accessions were planted in D40 deepots (6.4 cm dia × 25 cm, 656 ml) filled with 1:1 mixture of fritted clay (Turface MVP, Profile Products LLC, Buffalo Grove, IL) and sand (Pavestone, Denver, CO) placed in D20T support trays (Stuewe & Sons, Tangent, OR). The sand-clay mixture had a total bulk density of 0.97 ± 0.07 g/cm3 equivalent to that observed from soils in the species’ native habitat (Cruz et al., 2013a). The growth media was supplemented with dolomite lime (GrowMore, Gardena, CA) at ¼ tsp per pot since native populations of the species are found in alkaline soils (Dierig and Ray, 2009). The bottom of each pot was plugged with Polyfil® (Fairfield, Danbury, CT) to prevent the clay-sand mixture from passing through the drain holes. The penetration resistance of the sand–clay mixture was tested using a Field Scout SC900 soil compaction meter (Spectrum Tech., Plainfield, IL) and was determined to range between 0.16 ± 0.06 MPa at 2.54 cm and 1.23 ± 0.13 MPa at 7.62 cm. Eight pots were used for each of three replicates for each accession. The greenhouse temperature was set to 21 ◦ C during the day and 13 ◦ C at night. Relative humidity was set to 50%. Metal halide lamps provided 12-h of supplemental light giving a total illuminance of 8207 lux. An automatic drip watering system was used to schedule the watering regimens of the deepots. All pots were kept well watered until the seeds germinated. At 20 days after planting (DAP), the watering schedule was modified to have the drip emitters turned on for 3 min at 1 gph (3.8 lph) once a week. Scotts 15-5-15 Cal-Mag Special fertilizer was applied at 20 and 40 DAP at the rate of 200 ppm using a fertilizer injector (Dosatron, Clearwater, FL) and saturating pots. The plants were harvested at 60 DAP. Whole plants were extracted from the clay:sand mixture, carefully washed with water in sieve trays, and immediately scanned intact. The roots and shoots were placed in paper bags then dried at an oven set at 60 ◦ C for 48 h and the respective weights recorded. 2.4. Image acquisition and root measurement Digital root image capture was done at 600 dpi (236 dpcm) using an Epson V750 PRO scanner (Seiko Epson Corp., Long Beach, CA). The images were processed to remove large non-root debris using Adobe Photoshop (Adobe Systems Inc., San Jose, CA). Root parameters from 21-day old seedlings were measured using EZ-Rhizo software v.1 (Armengaud et al., 2009). Measurements on the following variables were obtained: main (MR) and lateral root lengths (LR length), number of lateral roots (LR), length of the following zones on the main root – the basal zone (length from root origin

132

V.M.V. Cruz et al. / Industrial Crops and Products 62 (2014) 130–139

Table 1 Germplasm passport data for Physaria and Paysonia accessions and climate data of collection sites. Coll. ID

Accession ID

Species

Country

State

County

Lat

Long

Elevation (m)

Tmax (◦ C)

Tmin (◦ C)

PPT (mm)

A. pouches 1809 1840 2297 1933 2277 2278 2281 2282 2286 2290 2291 2292 2299 2301 4006 4007 19233 Gail

W6 20822 W6 20858 W6 20859 PI 596434 PI 596452 PI 596453 PI 596454 PI 596455 PI 596456 PI 596457 PI 596458 PI 596459 PI 596464 PI 596466 PI 641922 PI 641923 PI 293010 WCL-LO4

PF PF PF PF PF PF PF PF PF PF PF PF PF PF PF PF PF PF

USA USA USA USA USA USA USA USA USA USA USA USA USA USA Mexico Mexico USA USA

AZ NM TX AZ TX TX TX TX TX TX TX TX TX TX Coahuila Coahuila TX AZ

Cochise Eddy Presidio Graham Brewster Brewster Crockett Pecos Andrews Winkler Reeves Reeves Presidio Presidio – – Ector –

31.76 32.62 30.28 33.27 29.78 30.20 30.93 30.97 32.32 31.78 31.12 31.02 30.15 30.27 28.88 28.61 31.67 –

−110.06 −104.40 −104.02 −110.32 −103.18 −103.20 −101.87 −101.97 −102.50 −103.27 −103.72 −103.73 −104.08 −103.90 −100.61 −100.50 −102.71 –

134 1043 1463 811 853 1311 640 549 808 853 945 1006 1402 1433 305 911 876 –

25.46 25.43 24.31 27.11 27.97 25.45 26.25 26.52 25.36 26.73 26.66 26.43 24.89 23.93 28.3 28.5 25.89 –

8.93 8.21 6.62 10.22 11.39 8.22 11.3 11.1 9.85 9.92 9.57 9.44 7.48 6.18 15.36 15.23 10.43 –

340.22 317.19 375.18 342.18 261.95 358.01 408.20 393.79 367.32 315.46 314.89 334.64 398.15 397.12 523.02 510.63 335.29 –

B. deepots 1889 2246 2286 3011 Gail

PI 596425 W6 20836 PI 596456 W6 20320 WCL-LO4

PF PG PF PA PF

USA USA USA USA USA

NM TX TX OK AZ

Socorro Wilson Andrews Blaine –

33.88 28.85 32.32 35.79 –

−106.40 −98.35 −102.50 −98.42 –

1661 122 808 454 –

22.06 28.47 25.36 21.75 –

4.54 14.91 9.85 8.93 –

286.55 707.26 367.32 804.22 –

Notes: Species: PA = Paysonia auriculata; PF = Physaria fendleri; PG = Paysonia grandiflora; Climate data: Tmax = average maximum temperature, Tmin = average minimum temperature, PPT = average annual precipitation.

to first lateral), branched zone (length from first lateral to last lateral), and apical zone (length from last lateral to root tip), total root size (total root length of sample), lateral root number per length of main root (LR/MR), and number of lateral roots per branched zone length on main root (LR/Brz) (Table 2). For greenhouse plants, image analysis was done using WinRHIZO (Regent Instruments, Quebec, Canada). The parameters obtained using WinRHIZO on the greenhouse plants included total root length, average root diameter, and surface area. Other parameters were derived as follows: (1) root length density (root length per volume of growing media), (2) root mass ratio (root dry weight per whole plant dry weight), (3) specific root length (root length per root dry weight), (4) specific surface area (root surface area per root dry weight), and (5) root tissue density (root mass per root tissue volume). 2.5. Data analysis Root traits were analyzed using JMP (SAS Institute Inc., Cary, NC). Trait data were checked for normality (Shapiro and Wilk, 1965), homogeneity of variance (Levene, 1960), and tested for interaction effects. Tukey’s honest significant difference test and Student’st test (Hsu, 1996) were used in conjunction with an analysis of variance to find means that were significantly different from each other. The derived variables root:shoot ratio and root mass ratio were arcsine transformed prior to analyses (Goodman and Ennon, 1996). Principal components were derived from eigenvalues of the root parameter correlations and visualized using a biplot in JMP. Cluster analysis was performed using the correlation data matrix and the average linkage hierarchical clustering method (Sokal and Michener, 1958). 3. Results and discussion 3.1. Germination pouches, root parameters and temperature effects There was a substantial variation observed in P. fendleri seedlings root traits after 21 days in the germination pouches

(Table 2). The coefficients of variation observed on the root traits ranged from 47 to over 100, which is within the range previously reported in maize and soybean roots (Logsdon and Allmaras, 1991) but greater than values reported in pea (McPhee, 2005). The average total root system length of lesquerella seedlings after 21 days was 7.6 cm. Among the accessions, W6 20858 had the longest root system (12.14 cm) under both growing temperatures, followed by roots of three other accessions with longer than 10 cm: PI 596434 (11.63 cm), PI 596459 (11.26 cm), and W6 20822 (10.83 cm). The shortest root system was observed in PI 596457 (4.11 cm). The advanced breeding line WCL-LO4 ‘Gail’ had below average total root system size among this group of accessions (6.59 cm). In other oilseed species, seedling root length has been shown to be highly predictive of seedling vigor and seed yield (Koscielny and Gulden, 2012; Rauf and Sadaqat, 2008) but this relationship is yet to be studied in lesquerella. The mean total root length of P. fendleri seedlings observed at 30/21 ◦ C was not significantly different than at 21/13 ◦ C (Table 2). The average total root length of 8.48 cm at 30/21 ◦ C and 7.15 cm at 21/13 ◦ C indicated root elongation rates of approximately 3.38–4.04 mm/day among accessions and treatments. PI 596457, PI 596458, and W6 20859 produced longer total root length at 30/21 ◦ C while total root length among the remaining accessions did not appear sensitive to temperature. There was no significant interaction found between temperature and accessions. In other crops such rice (MacMillan et al., 2006) and wheat (Wade and Botwright-Acuna, 2013), plasticity in growth of roots with varied levels of soil nitrogen, light intensity and soil water was documented. This phenomenon presents a significant challenge in quantitative analysis of root system architecture (Topp and Benfey, 2012). In particular, ex situ growth conditions for the morphological variation screening should mimic the typical growing conditions in the field to get an accurate estimate of the plant’s response. In many plant species, exposure to high temperatures results in greater elongation in root growth zones with the maximum growth usually occurring at temperatures above 25 ◦ C (Went, 1953; Nobel, 2002). The observations on the root trait in this study

Table 2 Root trait variability and response of P. fendleri plants in germination pouches to two growth temperature regimens.a Listed are averages among temperature regimens for each accession and among accessions for each temperature regimen. No. lateral roots

Lateral root length (cm)

Lateral root number/Main root length

Basal zone length (cm)

Branched zone Apical zone length (cm) length (cm)

Lateral root number/Branched zone

Total root length (cm)

Root:shoot ratio

Root mass ratio

Accessions

PI 293010 PI 596434 PI 596452 PI 596453 PI 596454 PI 596455 PI 596456 PI 596457 PI 596458 PI 596459 PI 596464 PI 596466 PI 641922 PI 641923 W6 20822 W6 20858 W6 20859 WCL-LO4

3.78b 7.62a 7.00a 6.93a 5.17ab 3.96ab 4.75ab 3.51ab 6.44ab 7.40a 6.13ab 5.19ab 4.41ab 4.73ab 7.46ab 7.48a 4.33ab 4.88ab

6.92b 17.62ab 13.45ab 9.21b 8.30b 7.12ab 10.41ab 7.83ab 12.99ab 11.69ab 7.27b 7.73ab 10.47ab 10.73ab 19.64a 16.34ab 9.26ab 16.32ab

0.06b 0.13ab 0.09b 0.07b 0.06b 0.07ab 0.07b 0.04ab 0.11ab 0.23a 0.14ab 0.12ab 0.10ab 0.12ab 0.18ab 0.19ab 0.14ab 0.07ab

2.36ab 2.78+ 2.01ab 1.32b 2.03ab 2.15ab 2.97ab 2.16ab 2.20ab 1.59ab 1.49ab 1.58ab 2.69ab 3.10b 2.54ab 2.77ab 2.40ab 3.56ab

0.28 0.28 0.30 0.45 0.14 0.29 0.13 0.29 0.29 0.36 0.55 0.46 0.25 0.13 0.28 0.38 0.55 0.23

1.73c 6.11a 4.50abc 4.26abc 2.94abc 2.49abc 2.97abc 1.88ab 4.63abc 4.70abc 2.85abc 2.31abc 2.97abc 3.01abc 5.07abc 6.33a 2.29bc 3.61abc

1.77 1.23 2.20 2.22 2.09 1.19 1.65 1.35 1.52 2.33 2.72 2.42 1.19 1.59 2.12 0.76 1.49 1.04

7.04 3.65 3.77 2.85 2.15 4.87 5.80 4.91 4.41 2.36 3.85 4.83 4.89 4.87 4.06 3.78 3.84 5.28

4.28c 11.63ab 8.90abc 7.88abc 5.90bc 4.85abc 5.78abc 4.11abc 8.82abc 11.26ab 7.96abc 6.44abc 5.85abc 6.50abc 10.83ab 12.14a 6.08abc 6.59abc

0.20b−e 0.13cde 0.16b−e 0.07e 0.33ab 0.15b−e 0.35ab 0.19b−e 0.30a−d 0.16b−e 0.12cde 0.10de 0.30abc 0.11cde 0.10de 0.24a−e 0.42a 0.12cde

0.16a−g 0.11d−g 0.14b−g 0.06g 0.25abc 0.13c−g 0.26ab 0.15a−g 0.22a−e 0.13c−g 0.11efg 0.09fg 0.23a−d 0.10fg 0.09fg 0.19a−f 0.27a 0.10efg

Temperature

21/13 ◦ C 30/21 ◦ C

5.37 6.28

10.73 12.11

0.11 0.12

2.27 2.33

0.31 0.32

3.53 3.81

1.53a 2.14b

5.04 4.59

7.15 8.48

0.17 0.22

0.14 0.17

*

*

*

*

NS

*

*

NS NS

NS NS

NS

*

*

NS

NS NS NS

*

NS

NS NS NS

*

NS NS

NS NS

NS NS

NS NS

ANOVA Acc. (A) Temp. (T) AXT a *

*

V.M.V. Cruz et al. / Industrial Crops and Products 62 (2014) 130–139

Main root length (cm)

Values shown are means; different superscript letters in the column within the same factor are significantly different according to Tukey HSD test (˛ = 0.05). Denotes significant difference (p < 0.05).

133

134

V.M.V. Cruz et al. / Industrial Crops and Products 62 (2014) 130–139

A 0

MR length (cm)

2

4 6 8 10 12 basal

branched

apical

basal

branched

apical

B 0

MR length (cm)

2

4 6 8 10 12

Fig. 1. Variation in P. fendleri main root (MR) length within basal, branched and apical zones when grown in pouches at two temperature regimens (A = 21/13 ◦ C, B = 30/21 ◦ C). Accessions are ordered by MR length at 21/13 ◦ C.

supplement those reported by Dierig and Crafts-Brandner (2011) on above-ground parts – that warmer temperatures enhanced the development of above ground traits in an advanced P. fendleri breeding line WCL-LO3, resulting in higher bud, flower and silique counts than when plants were grown at other temperature conditions. The average number of laterals per main root in the P. fendleri seedlings was determined to range from 6.92 (PI 293010) to 19.64 (W6 20822). The average length of lateral roots range from 0.06 cm (PI596454) to 0.23 cm (PI 596459), while the proportion of lateral root length to main root length range from 1.32 (PI596453) to 3.10 (PI641923). Root length density is highly correlated with belowground competitive ability for soil resources (Casper and Jackson, 1997). In water limited habitats, the competition for resources is very high and root length density and its distribution plays a crucial role for stand establishment (Garay and Wilhelm, 1983; Cannon, 1911). Nine accessions had more lateral roots at 21/13 ◦ C, while the remaining accessions had more at 30/21 ◦ C. The initiation of lateral

root branching in pea and Arabidopsis is highly regulated by temperature and other environmental signals (Moriwaki et al., 2011; Malamy and Ryan, 2001; Gladish and Rost, 1993). However, we did not find an overall effect of temperature in lesquerella on this study (p = 0.84, see Table 2). Only four accessions (W6 20822, PI 596434, W6 20858, and WCL-LO4) were observed to have more than 15 lateral roots. Overall, the average number of lateral roots in 21 d plants was 11. Lesquerella main root length at 30/21 ◦ C was not significantly different at 21/13 ◦ C (p = 0.14). Among the three designated root zones, there was only significant difference at the root apical length between the two temperature treatments. The root apical zones of seedlings grown at 30/21 ◦ C were greater in length than those established at the cooler temperature by an average of 0.6 cm (Table 2 and Fig. 1). Slower root growth and smaller root diameter have been previously observed on plants cultivated at lower temperatures than warm temperatures and these were hypothesized as resulting from reduced cell extension rate or differential metabolite partitioning (Barber et al., 1998; Drennan and Nobel,

V.M.V. Cruz et al. / Industrial Crops and Products 62 (2014) 130–139

135

Table 3 Correlation among root variables of P. fendleri accessions in germination pouches. Parametera

No. lateral roots

0.667 0.649

Main root length No. lateral roots Lateral root length Lateral root number/Main root length Basal zone length Branched zone length Apical zone length Lateral root number/Branched zone a

Lateral root length 0.464

Lateral root number/ Main root length

Basal zone Branched Apical zone length zone length length

Lateral root number/ Branched zone

Total root length

−0.213 0.510 −0.091

0.216 −0.197 0.385 −0.592

−0.441 −0.309 −0.504 0.133 −0.531 −0.405 −0.003

0.954 0.754 0.787 −0.038 0.197 0.941 0.063 −0.491

0.909 0.829 0.580 0.127 −0.001

0.261 −0.311 0.136 −0.739 0.336 −0.157

Bold values are significant at ˛ = 0.05.

1998; Lahti et al., 2005). Exposure to varying temperature also affects the distribution of gibberellins (GAs) in the root elongation zone and this was postulated to influence root growth (Shani et al., 2013). We have yet to investigate lesquerella plants that have reached later maturity stages or completed their reproductive stage for root characters, but the available data gathered in the current study suggested that root response of young P. fendleri plants to temperature is highly dependent on its genotype, as was also reported in maize roots and environmental gradients (Rahnama et al., 2011). Exploring correlations among root traits provide opportunities to quickly screen for desired phenotypes enabling higher throughput phenotypic evaluations of germplasm materials (Wasson et al., 2012). On the lesquerella seedlings, longer total root system length was associated with longer main root length, number of lateral roots, lateral root length, and branched zone length (Table 3). The number of lateral root per main root length, and lateral root number in the branched zone have negative correlation to main root length, basal zone length, lateral root length, and total root length

(Table 3). The significant contribution of the length of branched zone to the total root length is consistent with previous reports in other members of the Brassicaceae such as Brassica napus where the length of lateral roots significantly affected the total length, especially the length of the branched zone (Larcher et al., 2003). The biplot shown in Fig. 2 summarizes the trait correlations and relationships among the root parameters and germplasm samples with high total root length values (W6 20858, PI 593434, W6 20822). A subsequent hierarchical cluster analysis using the root data (dendrogram not shown) showed that the germplasm set tested can be grouped into three major clusters: cluster 1) PI 293010, PI 596454, PI 596455, PI 596456, PI 596457, PI 641922, PI 641923, and W6 20859; cluster 2) PI 596434, PI 596452, PI 596453, PI 596458, PI 596459, PI 596464, PI 596466, W6 20822, and W6 20858; cluster 3) WCL-LO4. We speculate that the separate grouping of the breeding line WCL-LO4 may have been influenced by selection activities during line development and breeding. WCL-LO4 has the highest LR densityMR among the accessions. The summary of mean values for these three groups is shown on Table 4. Accessions in cluster 1 have an overall lower number of laterals per

Fig. 2. Biplot summarizing relationships among root variables and lesquerella accessions.

136

V.M.V. Cruz et al. / Industrial Crops and Products 62 (2014) 130–139

Table 4 Root trait mean values of P. fendleri cluster groups. Cluster No. ID accessions

Main root length (cm)

No. lateral roots

Lateral root length (cm)

Lateral root number/ Main root length

Basal zone length (cm)

Branched zone length (cm)

Apical zone length (cm)

Lateral root number/ Branched zone

Total root length (cm)

1 2 3

4.330 6.849 4.877

8.882 12.882 16.325

0.083 0.140 0.073

2.481 2.031 3.565

0.257 0.372 0.228

2.534 4.529 3.613

1.539 1.948 1.037

6.045 3.728 5.276

5.418 9.539 6.595

8 9 1

Fig. 3. Relative root sizes of Physaria and Paysonia seedlings (A = Physaria at 21 days, B = Physaria at 60 days, C = Paysonia at 60 days) (bar = 1 cm).

main root (LR), length of branched zone, and total root size, but very high lateral root number in the branched zone. In cluster 2, PI 596434 grouped with eight other accessions with more than 5 cm mean total root length. This group of accessions also exhibit higher branched zone lengths and LR than cluster 1 (Fig. 2 and Table 4). After exploring for possible correlations among root traits and climate data from the germplasm collection sites, we observed that that the length of root basal zone positively vary (r = 0.70, p < 0.01) with elevation. This might relate to previous observations by Kiirner and Renhardt (1987) on several herbaceous perennial plant species, indicating altitudinal differences in root lengths and biomass allocation with samples from higher elevations showing two times of total dry matter allocated to fine roots and with four to five times higher root length per unit leaf area. 3.2. Greenhouse study At 60 days after planting in the deepots, the lesquerella roots grew to an average total length of 22.52 cm, reaching about three times the size of those from 21 day old seedlings grown in the pouches (Fig. 3). Based on the length of the growing period, the roots were estimated to have an average elongation rate of 3.75 mm/day and this value is consistent with previous estimates on seedlings grown in the pouches. The elongation rate observed in the lesquerella studied is very low compared to other crops. The rate is comparable to those of oilseed rape when plants were grown in nutrient deficient media (1–4 mm/day) and less than the values observed when rape plants were grown in media with adequate nutrients (10–19 mm/day) (Stangoulis et al., 2000). Other crops with greater root elongation rates include inbred

maize lines, 50–82 mm/day (Leach et al., 2011) and soybeans, 31–72 mm/day (Yamaguchi et al., 2010). In comparison with maize, soybean and rape, lesquerella is a small statured plant. Root elongation is important in securing diminishing soil moisture and resources. However lesquerella could be among species that normally exhibit slow growth rates, typical of desert plants (Nicotra et al., 2002; Nobel, 2002). Arid plant species show two possible modes of adaptation to cope with limited water in their environment. Some species can grow roots to very deep soil layers to access water if it is available. Others produce shallow root systems to quickly exploit brief and episodic precipitation (Lynch, 1995). There were two accessions of P. fendleri, WCL-LO4 and PI 596456 that were used in both the laboratory and greenhouse studies. The root:shoot ratio and root mass ratio of PI 596456 were greater than WCL-LO4 in both environments but not significantly different, similar to results on other root parameters. Follow up studies are being planned to determine if rank positions among accessions with contrasting root allocation are consistent between germination pouches and pot studies or highly dynamic across this tiered-screening process. Between the two genera, Paysonia were bigger plants with greater average shoot weight and total plant weight than Physaria (Table 5). This supports previous morphological plant descriptions by Rollins and Shaw (1973). Analogous to the observation on the above ground plant part, Paysonia roots also were longer (by a factor of 2.2) than those of Physaria with an average total length of 50.03 cm and had significantly higher values on the following parameters: root diameter, root length density, and specific surface area. Root:shoot ratio did not differ significantly among genera indicating that overall root allocation patterns were similar but the list of accessions should be expanded (Table 5). Intra and interspecific differences in root morphological properties have been reported previously in other plants but reports about the consequences of this variation are lacking in the literature (Monneveux and Belhassen, 1996). The Paysonia species included in this study have habitat distributions that are limited to regions of Oklahoma (P. auriculata) and south central to southern Texas (P. grandiflora) (Rollins and Shaw, 1973). These regions normally receive more rainfall than most areas where P. fendleri is found (NWS, 2013; Table 1). The two Paysonia species have very high genetic similarity with P. fendleri (Cruz et al., 2013b) and the native habitat difference may partly account for the observed differences in plant morphology. In cacti species, it was determined that the primary root growth matches their environment, with determinate growth in species that inhabit arid and semi-arid regions, while indeterminate growth is exhibited by those from mesic habitat (Shishkova et al., 2013). The same case has been reported in several Australian species with species found at lower rainfall environments having roots that showed slower root system elongation rates or total root production rates (Nicotra et al., 2002). We intend to expand the number of representative Physaria and Paysonia species to further examine this on both genera and likewise verify if the same pattern between genera occurs in the field, as well as the results from screening the seedling root traits in pouches and how they correlate to productivity values.

NS NS *

a

The values shown are means; different superscript letters in the column within the same factor are significant different according to Tukey HSD and Student’s-t tests (˛ = 0.05). Denotes significant difference (p < 0.05).

*

NS

NS NS *

NS

* * *

ANOVA Acc within Genus (A[G]) Genus (G)

*

NS NS

*

NS

0.17 0.16 0.21a 0.20b 2.62a 1.41b Paysonia Physaria Genus

0.39 0.23

2.83a 1.63b

50.03a 22.52b

*

NS

NS NS

NS NS

0.03 0.04 15.19a 9.57b 0.08a 0.03b 0.14 0.13

233.90 414.62

0.02 0.02 0.05 0.04 0.05 13.17 18.20 8.54 11.58 8.98 975.06 291.14 142.25 164.88 143.58 0.03 0.08 0.04 0.07 0.03 0.09 0.10 0.15 0.20 0.14 0.20 0.20 0.19 0.22 0.20 17.75 53.46 29.31 45.82 20.09 0.96c 2.70a 1.78bc 2.52ab 1.48c PI 596425 W6 20836 PI 596456 W6 20320 WCL-LO4 Accessions

0.10 0.24 0.35 0.56 0.23

1.04c 2.77a 2.13ab 2.90a 1.71bc

0.11 0.10 0.20 0.25 0.17

Root length density (cm/cm3 ) Root:shoot ratio Avg. root diameter (mm) Total root length (cm) Total plant weight (mg) Root weight (mg) Shoot weight (mg) Levels Factors

Table 5 Trait observations in Physaria and Paysonia plants at 60 DAP.a

137

4. Conclusions

Root mass ratio

Specific root length (cm/mg)

Specific surface area (cm2 /mg)

Root tissue density (mg/cm3 )

V.M.V. Cruz et al. / Industrial Crops and Products 62 (2014) 130–139

We have gathered preliminary information about root trait variability and root development in seedlings of the new oilseed crop lesquerella at 21 and 60 days after planting and recorded phenotypic differences under varying growth conditions. The amount of variation in the various root zones, main and lateral roots of young plants on the limited number of accessions used in this study was observed to be within the parameter range as observed on other crop species. Among the root parameters considered in seedlings grown in pouches, only the root apical length was found highly influenced by temperature. The differential response of lesquerella accessions to the temperature regimens presents a challenge to screening germplasm for root traits in the laboratory and extrapolating the results to actual field response where conditions are often dynamic. This study also documented that Paysonia do not show a significant change in allocating growth to roots than Physaria. The larger plant size of Physaria merely led to a larger root system. Analyzing additional accessions and representative species from different localities may be needed to validate similarities in allocation between these genera. We plan to further test if these observations are consistent when plants are established under field conditions and generate additional information about the root biology and diversity of lesquerella species using collected germplasm for possible utility in crop improvement. Disclaimer and EEO/Non-discrimination Statement Mention of companies or commercial products does not imply recommendation or endorsement by the U.S. Department of Agriculture (USDA). USDA neither guarantees nor warrants the standard of any product mentioned. Product names are mentioned solely to report factually on available data and to provide specific information. USDA is an equal opportunity provider and employer. Acknowledgements We would like to thank Tammy Brenner and Josephine Bunker for the valuable assistance during this study. References Al-Shehbaz, I.A., O’Kane Jr., S.L., 2002. Lesquerella is united with Physaria (Brassicaceae). Novon 12, 319–329. Armengaud, P., Zambaux, K., Hills, A., Sulpice, R., Pattison, R.J., Blatt, M.R., Amtmann, A., 2009. EZ-Rhizo: integrated software for the fast and accurate measurement of root system architecture. Plant J. 57, 945–956. Barber, S.A., MacKay, A.D., Kuchenbuch, R.O., Barraclough, P.B., 1998. Effects of soil temperature and water on maize root growth. Plant Soil 111, 267–269. Cannon, W.A., 1911. The Root Habits of Desert Plants. Carnegie Institution of Washington Publ. 131. Gibson Bros., Washington, DC. Casper, B.B., Jackson, R.B., 1997. Plant competition underground. Annu. Rev. Ecol. Syst. 28, 545–570. Comas, L.H., Becker, S., Cruz, V.M.V., Byrne, P., Dierig, D.A., 2013. Root traits and responses contributing to plant productivity under drought. Front. Plant Sci. 4, 442, http://dx.doi.org/10.3389/fpls.2013.00442. Cruz, V.M.V., Dierig, D.A., 2010. Collecting lesquerella for conservation and research on comparative seed dormancy among wild populations. In: Proc. AAIC Annual Mtg, Sept. 18–20, 2010. Fort Collins, CO, http://www.aaic. org/10program.htm#POSTER PRESENTATIONS (Oilseeds) (accessed 18.12.13). Cruz, V.M.V., Dierig, D.A., 2012. Trends in literature on new oilseed crops and related species: seeking evidence of increasing or waning interest. Ind. Crops Prod. 37, 141–148. Cruz, V.M.V., Walters, C.T., Dierig, D.A., 2013a. Dormancy and after-ripening response of seeds from natural populations and conserved Physaria (syn Lesquerella) germplasm and their association with environmental and plant parameters. Ind. Crops Prod. 45, 191–199. Cruz, V.M.V., Kilian, A., Dierig, D.A., 2013b. Development of DArT marker platforms and genetic diversity assessment of the U.S. collection of the new

138

V.M.V. Cruz et al. / Industrial Crops and Products 62 (2014) 130–139

oilseed crop lesquerella and related species. PLOS ONE 8 (5), e64062, http://dx.doi.org/10.1371/journal.pone.0064062. Dierig, D.A., Crafts-Brandner, S.J., 2011. The relationship of temperature to plant morphology of lesquerella. Crop Sci. 51, 2165–2173. Dierig, D.A., Ray, D.T., 2009. New crops breeding: Lesquerella. In: Vollman, J., Rajcan, I. (Eds.), Oil Crops, Handbook of Plant Breeding, 4. Springer, New York, pp. 507–516. Drennan, P.M., Nobel, P.S., 1998. Root growth dependence on soil temperature for Opuntia ficus-indica; influences of air temperature and a doubled CO2 concentration. Funct. Ecol. 12, 959–964. Fiorani, F., Schurr, U., 2013. Future scenarios for plant phenotyping. Annu. Rev. Plant Biol. 64, 267–291. Garay, A.F., Wilhelm, W.W., 1983. Root system characteristics of two soybean isolines undergoing water stress conditions. Agron. J. 75, 973–977. Giuliani, S., Sanguineti, M.C., Tuberosa, R., Bellotti, M., Salvi, S., Landi, P., 2005. RootAba1, a major constitutive QTL, affects maize root architecture and leaf ABA concentration at different water regimes. J. Exp. Bot. 56, 3061–3070. Gladish, D.K., Rost, T.L., 1993. The effects of temperature on primary root growth dynamics and lateral root distribution in garden pea (Pisum sativum L., cv “Alaska”). Environ. Exp. Bot. 33, 243–258. Goodman, A.M., Ennon, A.R., 1996. A comparative study of the response of the roots and shoots of sunflower and maize to mechanical stimulation. J. Exp. Bot. 303, 1499–1507. Gowda, V.R.P., Henry, A., Yamauchic, A., Shashidhar, H.E., Serraj, R., 2011. Root biology and genetic improvement for drought avoidance in rice. Field Crops Res. 122, 1–13. Henry, A., 2012. IRRI’s drought stress research in rice with emphasis on roots: accomplishments over the last 50 years. Plant Root 7, 5–19. Hsu, J.C., 1996. Multiple Comparisons: Theory and Methods. Chapman & Hall/CRC, Boca Raton, FL. Iwata, S., Miyazawa, Y., Fujii, N., Takahashi, H., 2013. MIZ1-regulated hydrotropism functions in the growth and survival of Arabidopsis thaliana under natural conditions. Ann. Bot. 112, 103–114. Jatoi, S.A., Javaid, A., Iqbal, M., Ullah, O., 2011. Genetic diversity in radish germplasm for morphological traits and seed storage proteins. Pak. J. Bot. 43, 2507–2512. Jha, U.C., Chaturvedi, S.K., Bohra, A., Basu, P.S., Khan, M.S., Bar, D., 2014. Abiotic stresses, constraints and improvement strategies in chickpea. Plant Breed. 133, 163–178. Kashiwagi, J., Krishnamurthy, L., Upadhyaya, H.D., Krishna, H., Chandra, S., Vadez, V., Serraj, R., 2005. Genetic variability of drought-avoidance root traits in the mini-core germplasm collection of chickpea (Cicer arietinum L.). Euphytica 146, 213–222. Kato, Y., Abe, J., Kamoshita, A., Yamagishi, J., 2006. Genotypic variation in root growth angle in rice (Oryza sativa L.) and its association with deep root development in upland fields with different water regimes. Plant Soil 287, 117–129. Kiirner, C., Renhardt, U., 1987. Dry matter partitioning and root length/leaf area ratios in herbaceous perennial plants with diverse altitudinal distribution. Oecologia 74, 411–418. Koscielny, C.B., Gulden, R.H., 2012. Seedling root length in Brassica napus L. is indicative of seed yield. Can. J. Plant Sci. 92, 1229–1237. Lahti, M., Aphalo, P.J., Finér, L., Ryyppö, A., Lehto, T., Mannerkoski, H., 2005. Effects of soil temperature on shoot and root growth and nutrient uptake of 5-year-old Norway spruce seedlings. Tree Physiol. 25, 115–122. Larcher, M., Muller, B., Mantelin, S., Rapior, S., Cleyet-Marel, J.C., 2003. Early modifications of Brassica napus root system architecture induced by a plant growth-promoting Phyllobacterium strain. New Phytol. 160, 119–125. Leach, K.A., Hejlek, L.G., Hearne, L.B., Nguyen, H.T., Sharp, R.E., Davis, G.L., 2011. Primary root elongation rate and abscisic acid levels of maize in response to water stress. Crop Sci. 51, 157–172. Levene, H., 1960. Robust tests for equality of variances. In: Olkin, I., Ghurye, S.G., Hoeffding, W., Madow, W.G., Mann, H.B. (Eds.), Contributions to Probability and Statistics: Essays Honor of Harold Hotelling. Stanford University Press, Menlo Park, CA, pp. 278–292. Liu, L., Gan, Y., Bueckert, R., van Rees, K., 2011. Rooting systems of oilseed and pulse crops II. Vertical distribution patterns across the soil profile. Field Crops Res. 122, 248–255. Logsdon, S.D., Allmaras, R.R., 1991. Maize and soybean root clustering as indicated by root mapping. Plant Soil 131, 169–176. Lynch, J., 1995. Root architecture and plant productivity. Plant Physiol. 109, 3, 7-1. MacMillan, K., Emrich, K., Piepho, H.P., Mullins, C.E., Price, A.H., 2006. Assessing the importance of genotype × environment interaction for root traits in rice using a mapping population I: a soil-filled box screen. Theor. Appl. Genet. 113, 977–986. Malamy, J.E., Ryan, K.S., 2001. Environmental regulation of lateral root initiation in Arabidopsis. Plant Physiol. 127, 899–909. Manavalan, L.P., Guttikonda, S.K., Nguyen, V.T., Shannon, J.G., Nguyen, H.T., 2010. Evaluation of diverse soybean germplasm for root growth and architecture. Plant Soil 330, 503–514. McPhee, K., 2005. Variation for seedling root architecture in the core collection of pea germplasm. Crop Sci. 45, 1758–1763. Meskine, S., Romagosa, I., Comadran, J., Russell, J.R., Hackett, C., van Eeuwijk, F., Thomas, W.T.B., 2006. Primary root architecture in a diverse set of barley germplasm. In: Meeting of the Eucarpia Cereal Section Cereal Science and Technology for Feeding Ten Billion People: Genomics Era and Beyond, Lleida, Spain, 13–17 November, p. 2006.

Mir, R.R., Thudi, M., Chamarthi, S.K., Krishnamurthy, L., Gaur, P.M., Varshney, R.K., 2013. Translational root genomics for crop improvement. In: Crespi, M. (Ed.), Root Genomics Soil Interactions. , 1st ed. John Wiley & Sons, Inc., Vivar Printing, Malaysia. Monneveux, P., Belhassen, E., 1996. The diversity of drought adaptation in the wide. Plant Growth Regul. 20, 85–92. Moriwaki, T., Miyazawa, Y., Kobayashi, A., Uchida, M., Watanabe, C., Fujii, N., Takahashi, H., 2011. Hormonal regulation of lateral root development in Arabidopsis modulated by MIZ1 and requirement of GNOM activity for MIZ1 function. Plant Physiol. 157, 1209–1220. Nicotra, A., Babicka, N., Westoby, M., 2002. Seedling root anatomy and morphology: an examination of ecological differentiation with rainfall using phylogenetically independent contrasts. Oecologia 130, 136–145. Nobel, P., 2002. Ecophysiology of roots of desert plants, with special emphasis on agaves and cacti. In: Kafkafi, U., Waisel, Y., Eshel, A. (Eds.), Plant Roots: The Hidden Half. , 3rd ed. Marcel Dekker Inc., NY, pp. 961–973. NWS, 2013. 30-year PRISM Normals. Advanced Hydrologic Prediction Service, National Weather Service (NWS). National Oceanic and Atmospheric Administration (NOAA), Silver Spring, MD. Princen, L.H., 1983. New oilseed crops in the horizon. Econ. Bot. 37, 478–492. PRISM, 2013. PRISM Climate Group. Oregon State University http://prism. oregonstate.edu Ruta, N., Stamp, P., Liedgens, M., Fracheboud, Y., Hund, A., 2010. Collocations of QTLs for seedling traits and yield components of tropical maize under water stress conditions. Crop Sci. 50, 1385–1392. Rahnama, A., Munns, R., Poustini, K., Watt, M., 2011. A screening method to identify genetic variation in root growth response to a salinity gradient. J. Exp. Bot. 62, 69–77. Rauf, S., Sadaqat, H.A., 2008. Effect of osmotic adjustment on root length and dry matter partitioning in sunflower (Helianthhus annuus L.) under drought stress. Acta Agric. Scand. B 58, 252–260. Rollins, R.C., Shaw, E.A., 1973. The Genus Lesquerella (Cruciferae) in North America. Harvard Univ. Press, Cambridge, MA. Sayar, R., Khemira, H., Kharrat, M., 2007. Inheritance of deeper root length and grain yield in half-diallel durum wheat (Triticum durum) crosses. Ann. Appl. Biol. 151, 213–220. Schultz, C.J., Kochian, L.V., Harrison, M.J., 2010. Genetic variation for root architecture, nutrient uptake and mycorrhizal colonisation in Medicago truncatula accessions. Plant Soil 336, 113–128. Shani, E., Weinstain, R., Zhang, Y., Castillejo, C., Kaiserli, E., Chory, J., Estelle, M., 2013. Gibberellins accumulate in the elongating endodermal cells of Arabidopsis root. Proc. Natl. Acad. Sci. U. S. A. 110, 4834–4839. Shapiro, S.S., Wilk, M.B., 1965. An analysis of variance test for normality (complete samples). Biometrika 52, 591–611. ˜ Shishkova, S., Las Penas, M.L., Napsucialy-Mendivil, S., Matvienko, M., Kozik, A., Montiel, J., Patina, A., Dubrovsky, J.G., 2013. Determinate primary root growth as an adaptation to aridity in Cactaceae: towards an understanding of the evolution and genetic control of the trait. Ann. Bot. 112, 239–252. Silberbush, M., 2013. Root study: why is it behind other plant studies? Am. J. Plant Sci. 4, 198–203. Sokal, R., Michener, C., 1958. A statistical method for evaluating systematic relationships. Univ. Kansas Sci. Bull. 38, 1409–1438. Stangoulis, J.C., Webb, M.J., Graham, R.D., 2000. Boron efficiency in oilseed rape: II. Development of a rapid lab-based screening technique. Plant Soil 225, 253–261. Stevanato, P., Trebbi, D., Biancardi, E., Cacco, G., McGrath, J.M., Saccomani, M., 2013. Evaluation of genetic diversity and root traits of sea beet accessions of the Adriatic Sea coast. Euphytica 189, 135–146. Thompson, A.E., 1985. New native crops for the arid Southwest. Econ. Bot. 39, 436–453. Thompson, S.M., Cossani, C.M., Ibrahim, A.M.H., Reynolds, M.P., Goodman, D., Hays, D.B., 2013. Estimating wheat root biomass using ground penetrating radar. In: Proc. ASA, CSSA, SSSA International Annual Mtgs, Nov. 3–6, 2013, Tampa, https://scisoc.confex.com/crops/2013am/webprogram/Paper78536.html FL, (accessed 18.12.13). Topp, C.N., Benfey, P.N., 2012. Growth control of root architecture. In: Altman, A., Hasegawa, P.M. (Eds.), Plant Biotechnology Agriculture: Prospects for the 21th Century. Elsevier, Inc., San Diego, CA, pp. 373–382. Uga, Y., Sugimoto, K., Ogawa, S., Rane, J., Ishitani, M., Hara, N., Kitomi, Y., Inukai, Y., Ono, K., Kanno, N., Inoue, H., Takehisa, H., Motoyama, R., Nagamura, Y., Wu, J., Matsumoto, T., Takai, T., Okuno, K., Yano, M., 2013. Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nat. Genet. 45, 1097–1102. Van Dyne, D.L., 1997. Comparative economics of producing lesquerella in various areas of the Southwestern United States. In: Industrial Uses of Agricultural Materials. USDA Economic Research Service IUS-7, pp. 32–35. Wade, L.J., Botwright-Acuna, T.L., 2013. Genotype by environment (GxE) interactions for root depth of wheat: associations and implications, “Capturing Opportunities and Overcoming Obstacles in Australian Agronomy”. In: Proceedings of the 16th Australian Agronomy Conference, 14–18 October 2012, University of New England Armidale, NSW, pp. 1–5. Wasson, A.P., Richards, R.A., Chatrath, R., Misra, S.C., Sai Prasad, S.V., Rebetzke, G.J., Kirkegaard, J.A., Christopher, J., Watt, M., 2012. Traits and selection strategies to improve root systems and water uptake in water-limited wheat crops. J. Exp. Bot. 63, 3485–3498.

V.M.V. Cruz et al. / Industrial Crops and Products 62 (2014) 130–139 Went, F.W., 1953. The effect of temperature on plant growth. Ann. Rev. Plant Physiol. 4, 347–362. Yamaguchi, M., Valliyodan, B., Zhang, J., Lenoble, M.E., Yu, O., Rogers, E.E., Nguyen, H.T., Sharp, R.E., 2010. Regulation of growth response to water stress in the soybean primary root. I. Proteomic analysis reveals region-specific regulation

139

of phenylpropanoid metabolism and control of free iron in the elongation zone. Plant Cell Environ. 33, 223–243. Yang, W., Duan, L., Chen, G., Xiong, L., Liu, Q., 2013. Plant phenomics and high-throughput phenotyping: accelerating rice functional genomics using multidisciplinary technologies. Curr. Opin. Plant Biol. 16, 180–187.