Brassicaceae Germplasm Diversity for Agronomic and Seed Quality Traits

Home , Brassica carinata, Camelina oil

Industrial Crops and Products 47 (2013) 176–185

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Review

Brassicaceae germplasm diversity for agronomic and seed quality

traits under drought stress

a,∗ a,1 a b

Jean-Nicolas Enjalbert , Shusong Zheng , Jerry J. Johnson , Jack L. Mullen ,

a b

Patrick F. Byrne , John K. McKay

Department of Soil & Crop Sciences, Colorado State University, Fort Collins, CO 80523, USA

Department of Bioagricultural Sciences & Pest Management, Colorado State University, Fort Collins, CO 80523, USA

a r t i c l e i n f o a b s t r a c t

Article history: Brassica juncea, Brassica carinata and Camelina sativa have previously shown potential as oilseed crops

Received 18 March 2012

in semi-arid climates. However, there is limited information on variation of agriculturally important

Received in revised form 28 February 2013

traits under water stress. This study screened 94 accessions of B. juncea, 30 accessions of B. carinata and

Accepted 28 February 2013

81 accessions of C. sativa under dryland and fully irrigated conditions in eastern Colorado to evaluate

responses to drought stress within and among species. B. carinata had the greatest phenotypic variabil-

Keywords:

ity. It had the largest average thousand-seed-weight (TSW), though with a 10-day longer life cycle than

Oilseed crops

the other species, it also suffered the most from summer heat stress during seed ﬁlling. Earlier-ﬂowering

Genetic diversity

accessions among the three species were more adapted to dryland conditions. B. carinata and B. juncea

Drought adaptation

were both twice as tall as C. sativa and produced signiﬁcantly higher biomass though they yielded less Fatty acids

−1 −1 −1

under dryland conditions, 711 kg ha , 933 kg ha , and 1383 kg ha , respectively. C. sativa showed bet-

ter adaptation to semi-arid environments, likely due to its shorter stature, higher harvest index, and

resistance to flea beetles. We measured seed-oil fatty acid profiles in response to water stress, finding a

signiﬁcant decrease in linolenic acid content under dryland conditions. C. sativa had the highest levels of

linolenic acid, averaging 30% of seed-oil fatty acid. B. carinata had the highest levels of erucic acid with 42%

on average. B. juncea accessions showed a large range of oil proﬁles, related to their geographical origin.

Oil proﬁle characteristics such as high linolenic acid were correlated with ﬁtness traits such as height and

biomass. Oil proﬁle traits could play an important future role in plant breeding, especially under dryland

conditions. This work highlights traits where breeding efforts can utilize existing germplasm diversity

such as ﬂowering time, yield components, oil quality, and ﬂea beetle susceptibility to improve cultivar

Contents

1. Introduction ...... 177

2. Materials and methods...... 177

2.1. Plant material and environmental conditions ...... 177

2.2. Field experiments ...... 177

2.3. Data analysis...... 178

3. Results ...... 178

3.1. Variation in growth and development among species ...... 178

3.2. Insect damage evaluation ...... 180

3.3. Seed-oil FA proﬁles ...... 180

4. Discussion ...... 183

5. Conclusions ...... 184

Acknowledgements ...... 184

References ...... 184

Abbreviations: DR, desaturation ratio; ER, elongation ratio; LDR, linoleic desaturation ratio; ODR, oleic desaturation ratio; TSW, thousand seed weight.

∗

Corresponding author. Tel.: +33 685539431.

E-mail address: [email protected] (J.-N. Enjalbert).

Present address: Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China.

J.-N. Enjalbert et al. / Industrial Crops and Products 47 (2013) 176–185 177

1. Introduction 2. Materials and methods

Brassicaceae oilseed crops offer the potential of producing 2.1. Plant material and environmental conditions

sustainable biofuels in arid and semi-arid regions. Unlike some

new cellulosic bioenergy grass crops, such as switchgrass (Pan- A total of 30 accessions of B. carinata, 94 accessions of B. juncea,

icum virgatum L.), Brassicaceae oilseeds ﬁt well into semi-arid and 81 accessions of C. sativa were evaluated for plant and seed

rotations, such as the dryland winter wheat (Triticum aestivum quality traits. The C. sativa, B. carinata and B. juncea accessions orig-

L.)-based cropping system. Ideally, new oilseed cultivars will inated from 16, three, and ﬁve countries, respectively. B. carinata

combine positive growth and development characteristics (e.g., and C. sativa accessions were sourced from the Institute of Plant

nutrient efﬁciency, pest tolerance, early maturity and heat- and Genetics and Crop Plant Research (IPK) at Gatersleben, Germany. B.

water-stress tolerance) with diverse fuel, feed and food applica- juncea accessions were received from the USDA-ARS North Central

tions (Gehringer et al., 2006). Genetic information and breeding Regional Plant Introduction Station germplasm collections. Acces-

efforts are needed in order to optimize oilseed crops for sus- sions were a mix of wild and landraces germplasm. Accessions were

tainable oil production in diversiﬁed crop rotations. This study grown at the Colorado State University Agriculture Research Devel-

examined genetic diversity in traits relevant to adaptation to semi- opment and Education Center (ARDEC) in Fort Collins in the 2008

arid environments. Speciﬁcally, we evaluated three crops all in crop season. ARDEC is located at latitude 40.65 N and longitude

the Brassicaceae family – Brassica juncea (L.) Czern, Brassica car- 105.00 W, at an elevation of 1557 m. The average annual precip-

inata A. Braun, and Camelina sativa (L.) Crantz – that could be itation is 356 mm. The climate is considered semi-arid, and the

integrated into the dryland winter wheat rotations dominant in soil type is Nunn clay loam. In 2009 and 2010, three accessions

the High Plains of Colorado, Nebraska, Kansas, Oklahoma, and per species, already tested in 2008, chosen for their yield perfor-

Texas. mance, seed size and oil characteristics, were planted at Iliff, CO

B. juncea, which originated in India, can be more productive than (elevation 1165 m, latitude 40.768 N, longitude 103.045 W) under

B. napus in semi-arid regions with unreliable rainfall while produc- both irrigated and dryland conditions in Randomized Complete

ing similar yields in well-watered conditions (Wright et al., 1995; Block Design. A spring commercial hybrid Brassica napus check from

Oram et al., 2005; Gan et al., 2007). These results suggest the fea- Cargill was included in the trial.

sibility of developing high-yielding cultivars for both dryland and

irrigated conditions. B. carinata, a native of Ethiopia appears better 2.2. Field experiments

adapted and more productive than B. napus in clay and sandy soils

in semi-arid temperate climates (Alemayehu and Becker, 2001; In 2008 at Fort Collins, CO, the experimental design included

Fernandez-Martinez et al., 2001). C. sativa originated in Northern dryland and ﬂood-irrigated treatments, with two replicates for

Europe and Central Asia (Putnam et al., 1993). It is considered a each accession within a treatment. The study area was divided

promising oilseed crop for dryland environments, with low input into two 11 m by 7.3 m blocks. Glyphosate was used to eradicate

requirements (Zubr, 1997) and favorable oil properties (Bernardo alfalfa plants remaining from the previous year, and the seedbed

−1

et al., 2003). C. sativa has shown higher seed yield performance was prepared by disking at 2 l ha . Seeds were sown by hand on

under semi-arid conditions than B. napus (Francis and Campbell, May 12, 2008, in single-row plots of 1-m length with 0.3-m row

−1

2004). spacing between plots. Density of planting was based on 6 kg ha

−1

Variation in the levels of the particular fatty acids (FA) between for C. sativa and 8 kg ha for both Brassica species – rates typically

and within species has been exploited for Brassica breeding, such used in the High Plains. Both blocks were ﬂood-irrigated until full

as for lines with low erucic or linolenic acid levels (Velasco et al., emergence in all accessions. The dryland block was not irrigated

1997; Alonso et al., 1991; Pleines and Friedt, 1988). We have after emergence, while the other continued to be irrigated. The irri-

found that variation in the proﬁles of FA in seed oils can have gated treatment was ﬂood-irrigated four times: at planting, prior

large impacts on fuel quality (J.-N. Enjalbert, J.L. Mullen, A. Lak- to flowering, post-flowering and during the seed-filling period.

shminarayanan, J.J. Johnson, D. Olsen, J.K. McKay, unpublished No fertilizer was applied to the ﬁeld. During the growing season,

data). Thus, even if biofuels derived from these crops have been weeds were controlled manually. Flea beetles (Phyllotreata cru-

shown, on average, to be in line with American Society for Testing ciferae) were controlled as needed from emergence to the ﬂowering

and Materials (ASTM) certiﬁed biodiesel (Alemayehu and Becker, stage with applications of Ortho Max (Ortho Group, Marysville,

2002), genetic variation in FA proﬁles can lead to differences in OH), following manufacturer instructions. Flea beetle infestation

engine performance of the oil extracted from diverse cultivars was scored from one to three (no infestation, 50% infested, 100%

(Nettles-Anderson and Olsen, 2009). In addition, because seed-oil infested). Flowering time was recorded in each plot as the date

composition is correlated with FA proﬁle in leaves (Wang et al., when 50% of the plants had reached ﬂowering. Plant height was

1989; Lemieux et al., 1990; Shaw et al., 1997), genetic variation in determined for ﬁve randomly selected plants per plot by measur-

the FA proﬁles may have a role in plant acclimation under stressful ing the distance from the soil surface to the highest point on the

environments (Mene-Saffrane et al., 2009). Lipids have a number plant at the time of pod maturity. Five pods were taken randomly

of essential roles in plants related to stomatal closure, pathogen from each plot at full maturity to estimate seed number per pod

invasion and water loss (Slabas et al., 2001). Therefore, selection and thousand seed weight (TSW). At the same time, number of

based on seed-oil proﬁles may have a direct impact on drought pods on the primary branch, primary branch length, pod density

tolerance. and number of branches were counted on ﬁve randomly selected

Phenotypic variation in biomass production, ﬂowering period, plants. The stand density was determined by counting the number

seed oil content, and seed oil composition are essential for of plants per row. Five plants per plot were randomly selected and

improvement of these three species through plant breeding. cut with a sickle at soil level, for plant biomass measurement when

◦

The objective of this study was to evaluate phenotypic vari- the plants were fully ripened. These samples were dried at 40 C

ation for these traits within and among the three species for 48 h. Seeds were separated from the vegetative tissue after the

under dryland and irrigated conditions. Select accessions were biomass of the whole plant was measured. Single-row plots were

then evaluated for adaptability to Colorado dryland agricultural harvested at full maturity, between August 1 and August 10, 2008,

production. at Fort Collins, CO.

178 J.-N. Enjalbert et al. / Industrial Crops and Products 47 (2013) 176–185

The Iliff trial, in 2009 and 2010, was a randomized complete where Vg, Ve and Vr represent the respective variance components

block design with three replicates in each of two treatments, well for genotype (g), environment (e) and (r) residual (Falconer and

watered and limited irrigation. The plot size was 1.5 m wide by Mackay, 1996).

4.6 m long, with seven rows, 25 cm apart. The seeding rate was

−1

8 kg ha . In 2009, the two moisture treatments were combined

into a single treatment due to high precipitation. In 2010, the Iliff

trial had two randomly assigned treatments, dryland and limited 3. Results

irrigation. The limited irrigation treatment received 25 mm of water

at the pre-ﬂowering stage and 25 mm during the seed-ﬁlling stage. 3.1. Variation in growth and development among species

Plant height, ﬂowering time and seed yield were recorded as

described above for the Fort Collins trial in 2008. Trials were har- For most measured growth and development traits, in the 2008

vested between July 16 and August 3 in 2009 and between July 20 experiment, signiﬁcant differences were found between irrigation

and August 6 in 2010. treatments and accessions within species (Table 1). The days to

FA profile analyses were determined by gas chromatography– flowering in B. carinata were significantly later (p < 0.0001) than

mass spectrometry (GC–MS) on a 1-g seed sample per plot. Because in the two other species regardless of treatment and years, occur-

FA contents are inter-correlated (Velasco et al., 1997), ratios were ring more than 10 days after B. juncea and C. sativa. Heritability for

calculated to compare FA biosynthetic pathways (Velasco et al., ﬂowering time was high for B. juncea and B. carinata (Table 1), but

1998). The elongation ratio (ER) estimates the relative weight of the lower for C. sativa, perhaps due to soil crusting that retarded emer-

elongation pathway from oleic acid (C18:1) to eicosenoic (C20:1) gence in the lower section of the ﬁeld where C. sativa was grown.

and erucic acid (C22:1). The desaturation ratio (DR) estimates the All three species required more days to ﬂower in the irrigated treat-

relative weight of the desaturation pathway from oleic acid to ment compared to non-irrigated plants, on average by one day

linoleic (C18:2) and linolenic acid (C18:3) within the overall fatty (Table 2). However, within species, ﬂowering time of some acces-

acid biosynthetic system. Within the desaturation pathway, oleic sions decreased from irrigated to dryland treatment (for example,

desaturation ratio (ODR) and linoleic desaturation ratio (LDR) esti- BRA-2464, Ji-019, Cam-143) while for other accessions, the oppo-

mate the efﬁciency of the desaturation from oleic to linolenic (ODR) site effect was observed (BRA-1151, jb-012, Cam-194; Fig. 1). We

and from linoleic to linolenic acid (LDR) (Pleines and Friedt, 1988). followed up with three selected lines per species in 2009 and 2010

These FA content ratios were calculated following Velasco et al. at Iliff, CO. Similar ﬂowering time results were found, with B. juncea

(1998): and C. sativa ﬂowering times not signiﬁcantly different, whereas B.

carinata ﬂowered on average seven days later than the other two

%C20 : 1 + %C22 : 1 species (Table 3). B. carinata also ﬂowered later than the commer-

ER =

%C18 : 1 + %C18 : 2 + %C18 : 3 + %C20 : 1 + %C22 : 1 cial B. napus hybrid check.

In 2008, B. carinata produced the largest seed, TSW of 3.6 g,

%C18 : 2 + %C18 : 3

DR = averaged across both irrigation treatments, while C. sativa had

%C18 : 1 + %C18 : 2 + %C18 : 3 + %C20 : 1 + %C22 : 1

the smallest seed, TSW of 1.0 g (Table 2). B. carinata and C. sativa

%C18 : 2 + %C18 : 3 seed size did not differ signiﬁcantly between irrigation treatments,

ODR =

whereas B. juncea had signiﬁcantly larger seed under irrigation.

%C18 : 1 + %C18 : 2 + %C18 : 3

Within the three species, a wide range of TSW treatment responses

%C18 : 3

were expressed (Fig. 1). In some B. carinata accessions, TSW

LDR =

%C18 : 2 + %C18 : 3

increased from the dry to the irrigated treatment, while in others

it decreased. In all species, seed size was positively correlated with

biomass under dryland conditions (Table 4). Seed size heritability

was high for all three species (Table 1). In the dryland treatment,

2.3. Data analysis

there were accessions of C. sativa (Cam-7, Cam-10, Cam-111) hav-

ing seed as large as some B. juncea accessions.

For each of the three species, accessions were considered as

B. juncea, B. carinata and C. sativa had similar seed number per

samples from a large gene pool representing the range of varia-

pod. While B. juncea showed no effect of irrigation on the number of

tion available to breeders. The population means were estimated

seeds per pod, the number of seeds per pod was signiﬁcantly lower

with this set of materials. Data were analyzed using the statis-

in the dry treatment for B. carinata and C. sativa (Tables 1 and 2). In B.

tical analysis software SAS version 9.2 (SAS Institute, Inc., Cary,

juncea and C. sativa, seeds per pod under irrigation was positively

NC). A mixed model was used with irrigation and species effects

correlated with ﬂowering time but negatively correlated to TSW

as ﬁxed, and accessions as random effects nested within species

(Table 4).

using the PROC MIXED procedure. Pearson correlation coefﬁcients

In 2008, the biomass per plant of C. sativa in the irrigated treat-

among different traits and treatments were generated by the PROC

ment was less than half of the Brassica species biomass. However, C.

CORR procedure based on the least squares means. Oil traits were

sativa was less sensitive to changes in water availability, such that in

ln-transformed to improve normality. In order to assess varia-

the dryland treatment it had similar biomass to B. juncea (Table 2).

tion in overall seed oil proﬁles, a principal components analysis

In all three species, accessions producing higher biomass under

(PCA) was performed using proportions of individual FA compo-

irrigation tended to have low biomass production under dryland

nents, and the sum of the saturated FAs. Principal component

conditions (Fig. 1). In 2008, plant height and main branch length of

analysis was performed on the FA proﬁle using the PROC PRIN-

the two Brassica species were greater than those of C. sativa under

COMP procedure. Broad-sense heritability for mean values over

both treatments (Table 2). The same trend was observed in the 2009

environments was calculated from components of variance with

and 2010 trials at Iliff. Despite the difference in size, C. sativa had

REML iteration in SAS using PROC VARCOMP, according to the

higher yields (Table 3). The two-year seed yield average of C. sativa

formula: −1 −1 −1

was 1383 kg ha compared to 711 kg ha and 933 kg ha for B.

carinata and B. juncea, respectively. C. sativa yielded at least 30%

h2 = more than the two Brassica species in 2009 and 2010, but were

Vg + Ve + Vr

only half their size, giving C. sativa a higher harvest index than the

J.-N. Enjalbert et al. / Industrial Crops and Products 47 (2013) 176–185 179

Table 1

ANOVA table of multiple traits of three oilseed species grown in Fort Collins, CO, in 2008.

a a

Species Effect Days to Biomass Main Plant Pod Yield per Seed per Seed Sats PUFA ER DR ODR LDR

ﬂower per plant branch height density plant pod size

length

*** *** *** *** *** *** *** *** ** *** *** *** ***

C. sativa (n = 81) Treatment ns

Genotype § ns *** ns *** ns *** *** *** *** *** *** *** ***

r 0.45 0.31 0.64 0.72 0.59 0.35 0.47 0.72 0.73 0.41 0.61 0.66 0.61 0.74

Heritability 0.06 0.03 0.23 0.01 0.20 0.03 0.25 0.62 0.52 0.13 0.41 0.47 0.43 0.59

*** *** *** *** *** *** *** *** *** § *** *** ***

B. juncea (n = 94) Treatment ns

Genotype *** *** *** *** *** *** *** *** *** *** *** *** *** ***

r 0.85 0.58 0.68 0.80 0.56 0.58 0.55 0.81 0.75 0.83 0.88 0.82 0.85 0.82

Heritability 0.74 0.06 0.12 0.31 0.44 0.06 0.27 0.65 0.30 0.66 0.83 0.66 0.54 0.54

*** *** *** § *** * *** *** *** ***

B. carinata (n = 30) Treatment ns ns ns ns

*** *** *** *** ** *** *** §

Genotype ns ns ns ns ns ns

r 0.82 0.75 0.67 0.88 0.25 0.75 0.43 0.58 0.31 0.51 0.56 0.48 0.30 0.35

Heritability 0.77 0.25 0.14 0.22 0.00 0.03 0.06 0.36 0.00 0.06 0.09 0.06 0.00 0.05

“ns”, non signiﬁcant.

Signiﬁcant at the 0.10 probability level.

Signiﬁcant at the 0.05 probability level.

Signiﬁcant at the 0.01 probability level.

***

Signiﬁcant at the 0.001 probability level.

Sats, saturated FAs; PUFA, polyunsaturated FAs.

Fig. 1. Flowering time, biomass, TSW and LDR reaction norms between irrigated and dryland treatments of three oilseed species at Fort Collins, CO, 2008.

180 J.-N. Enjalbert et al. / Industrial Crops and Products 47 (2013) 176–185

Table 2

Summary of yield components and oil quality trait under irrigation and dryland conditions for three oilseed species at Fort Collins, CO, 2008.

Environment Dryland Irrigated

Trait Variables B. carinata C. sativa B. juncea B. carinata C. sativa B. juncea

Flowering (days) Mean 59.88 49.69 50.56 60.13 50.67 52.24

Min. 53.00 47.00 40.24 54.00 48.00 31.00

Max. 67.50 50.24 62.50 66.00 51.00 64.23

SD 4.04 2.90 7.90 3.85 3.20 7.14

Biomass (g) Mean 2.68 2.09 1.89 5.43 2.82 5.48

Min. 0.60 0.96 0.50 2.40 0.90 0.34

Max. 5.40 3.95 5.99 13.20 14.11 21.03

SD 1.22 0.60 0.80 2.58 1.71 2.48

Main branch (cm) Mean 19.41 8.94 28.17 32.14 13.59 41.09

Min. 12.20 5.72 15.17 15.20 8.84 19.17

Max. 26.70 13.34 41.51 51.20 23.31 61.50

SD 3.98 1.78 5.4 8.44 2.75 8.20

Height (cm) Mean 53.23 38.04 65.54 101.26 55.19 92.39

Min. 38.50 27.80 32.70 75.80 41.40 35.40

Max. 72.00 46.60 90.30 125.50 69.90 142.80

SD 1.19 0.39 0.93 1.81 0.62 1.74

−1

Pod density (no. cm ) Mean 2.46 2.00 0.59 2.64 1.61 0.55

Min. 1.70 1.14 0.33 2.10 1.12 0.31

Max. 3.80 2.66 0.91 3.30 2.05 0.88

SD 0.44 0.28 0.14 0.34 0.20 0.31

TSW (g) Mean 3.76 0.98 2.08 3.45 0.99 2.85

Min. 2.70 0.59 1.09 2.40 0.69 1.47

Max. 5.00 1.38 3.20 5.60 1.36 4.22

SD 0.74 0.15 0.04 0.71 0.14 0.04

Seed per pod Mean 13.90 11.24 13.74 15.06 12.20 14.07

Min. 8.40 6.40 9.30 11.10 8.40 8.10

Max. 18.60 16.75 19.90 20.00 15.90 19.55

SD 0.87 0.21 0.16 1.07 0.16 0.17

ER Mean 0.52 0.20 0.49 0.58 0.19 0.49

Min. 0.50 0.17 0.03 0.50 0.17 0.06

Max. 0.60 0.22 0.60 0.60 0.21 0.60

SD 0.03 0.01 0.09 0.02 0.01 0.09

DR Mean 0.38 0.59 0.30 0.32 0.60 0.32

Min. 0.30 0.52 0.26 0.30 0.54 0.27

Max. 0.40 0.63 0.50 0.40 0.64 0.44

SD 0.02 0.02 0.04 0.01 0.02 0.03

ODR Mean 0.78 0.73 0.59 0.79 0.74 0.64

Min. 0.70 0.65 0.45 0.70 0.68 0.46

Max. 0.80 0.80 0.69 0.80 0.79 0.72

SD 0.02 0.02 0.04 0.02 0.02 0.05

LDR Mean 0.49 0.58 0.33 0.48 0.60 0.37

Min. 0.40 0.49 0.23 0.40 0.52 0.26

Max. 0.60 0.66 0.42 0.50 0.65 0.46

SD 0.03 0.03 0.04 0.03 0.03 0.04

Brassica species. C. sativa also had higher yields than the commercial we were able to examine whether there was a geographic corre-

B. napus hybrid check (Table 3). lation with oil proﬁle for that species. We did ﬁnd a geographic

pattern, with accessions from Bangladesh, India, and Pakistan clus-

3.2. Insect damage evaluation tering together, while accessions from China and Russia were

clustered separately and showed larger variation in fatty acid pro-

No flea beetle damage was observed on C. sativa under either files (Fig. 2B). The first component, PC1, was most highly correlated

irrigation treatment in any year (mean infestation index, 1.0). In with erucic acid content. The second component (PC2) was primar-

contrast, B. carinata (mean index, 1.7) and B. juncea accessions ily related to oleic acid and linolenic acid content. The accessions

(mean index, 2.4) showed much higher susceptibility to ﬂea beetle from Bangladesh, India, and Pakistan tended to have higher lev-

damage and required insecticide treatments. els of erucic acid, whereas the Chinese and Russian accessions had

higher levels of oleic and linoleic acid.

3.3. Seed-oil FA proﬁles Considering the FA components contributing the most to the

ﬁrst two principal components, it appeared that much of the

In order to assess variation in overall seed-oil proﬁles, we per- observed variation was related to speciﬁc FA biochemical path-

formed a principal components analysis. Despite the large variation ways. The three species showed signiﬁcant differences in the

in oil composition within species, each species had a character- efﬁciency of FA pathways (Fig. 3), as represented by ER and DRs

istic oil proﬁle (Fig. 2A). For B. juncea, we had ﬁve countries of (Velasco et al., 1997, 1998). B. carinata and most B. juncea acces-

origin well-represented in our sample of accessions. Therefore, sions had high ERs compared to C. sativa. However, a few B. juncea

J.-N. Enjalbert et al. / Industrial Crops and Products 47 (2013) 176–185 181 ) 1 − 0.56 ha

24.2 850 711 572 854 869 481 1076 1325 1348 1477 1119 Yield (kg

average

0.85 3.4 4.75 68 67 67 57 59 59 58 58 58 62 Flowering (d)

0.87 61 57 58 18.2 14.6 120 120 3-Environment 111 137 132 148 111 Height (cm) )

−

0.72 ha

23.5 801 850 890 857 593 1002 1021 1067 1314 1366 1535 Yield (kg

0.98 2.7 1.84 60 60 60 72 72 72 57 59 59 67 Flowering (d)

0.91 60 64 53 38 15.4 140 Height (cm) Irrigated 122 112 151 117 142 111 )

−

0.96 ha

15.7 298 114 339 834 546 772 912 267 1190 1175 1245 Yield (kg

0.87 6.9 4.6 72 72 72 66 62 63 61 59 59 67 Flowering (d)

0.96 9 2010.

61 52 62 21.6 104 106 111 122 138 136 151 2010 Dryland Height (cm) and

2009

) in

−

CO,

0.78 24.3 708 528 473 Yield (kg Iliff,

1390 1395 1218 1172 1485 1486 1652 1443 in

growing

0.83 2.79 2.92 60 58 56 51 57 53 53 55 55 56 Flowering (d)

species

0.98 6.4 88 61 55 61 11.51 2009 Dryland Height (cm) 125 116 134 142 152 112 oilseed

three

Line BC-1029 BC-1151 BC-2135 DZJ Jc-015 Jr-006 IPK33 IPK739 IPK851 Cargill trials

Poland Zambia Russia Origin Canada Germany Italy Ethiopia Ethiopia China Russia performance

dryland

and

0.05

3 %

sativa carinata juncea napus

2 Species B. C. B. LSD, R B. CV, Irrigated Table

182 J.-N. Enjalbert et al. / Industrial Crops and Products 47 (2013) 176–185 ** • *** * * • * • *** *** * • 0.13 0.13 0.06 0.15 0.35 0.20 0.19 0.12 0.41 0.09 0.27 0.21 0.13 − 0.20 0.37 0.13 0.13 0.33 0.08 0.06 − 0.01 LDR − 0.03 − − − − − 0.52 − 0.65 LDR − − 0.24 0.05 0.07 − − 0.15 0.11 0.18 LDR • ** *** *** • * *** * * **

• • • • *** *** *** * ***

0.10 0.08 0.02 0.19 0.08 0.34 0.62 0.49 0.18 0.27 0.56 0.27 0.08 0.22 0.32 0.02 0.04 0.38 0.33 0.04 0.31 − − − 0.25 0.34 ODR 0.68 − − − − − − − 0.77 − ODR 0.64 0.09 − − − − 0.24 − 0.08 0.95 ODR − *** *** * *

• *** ** • ** ** * ** *** ***

0.21 0.30 0.80 0.07 0.77 0.45 0.40 0.26 0.06 0.20 0.30 0.13 0.25 0.04 0.20 0.25 − 0.12 0.03 − − DR 0.57 0.35 0.12 − 0.08 0.31 0.42 0.03 0.05 − DR − − 0.05 − − − − 0.15 − − DR 0.94 − *** * *** *** * ***

*** *** *

2008.

0.09 0.100.09 0.85 0.03 0.08 0.05 0.15 0.21 0.48 0.48 0.10 0.17 0.80 0.02 0.04 0.01 0.22 0.08 − 0.06 − − 0.25 ER − − − − 0.01 − − − − − ER − 0.62 0.47 0.11 − − 0.01 − 0.25 0.12 ER − 0.11 0.02 in

Collins

Fort

at * * *

** * **

* 81)

0.24 0.20 0.44 0.21 0.45 0.21 0.10 0.17 0.07 0.01 0.04 0.13 0.08 0.09 0.02 0.25 0.08 0.07 0.08 0.09 =

− − − − 0.12 − 0.21 − 0.13 − 0.20 0.12 0.17 0.31 0.26 − Seedpods − − − − 0.32 − − 0.08 0.17 − Seedpods − − − − n (

sativa

* ** ** * *** • *** •

and • * **

0.09 0.21 Seedpods 0.26 0.37 0.17 0.20 0.11 0.06 0.39 0.29 0.48 0.19 0.42 96), − 0.10 0.32 0.03 0.10 TSW − 0.06 0.07 0.18 0.26 0.05 0.09 0.09 0.15 − TSW − − 0.12 − − − − − − TSW − 0.17 0.32 0.36 −

n (

juncea

• ** * *

** 30),

* *** • *** *** * •

n 0.12 0.32 0.15 0.10 0.28 0.11 0.38 0.24 0.28 0.12 0.080.40 0.07 0.03 0.11 (

− − − 0.00 − − Poddensity 0.38 0.23 − 0.17 0.27 0.37 0.12 0.19 0.53 Poddensity 0.00 0.00 − 0.39 − − − − 0.02 0.05 Poddensity − 0.21 − − 0.18 carinata

*** *** * *

*** * * ** ** *** • * *** *** *** *** • 0.06 0.05 0.44 0.41 0.29 0.24 0.06 − 0.21 0.41 Height 0.19 − 0.07 0.05 0.27 0.60 0.35 0.70 Height 0.35 0.42 0.15 − 0.40 − − 0.12 0.26 0.47 Height 0.17 − 0.20 0.07 − 0.06 dryland

and

irrigation

** ***

* ** *** • *** * *** 0.110.03 0.080.15 0.67 0.06 0.040.02 0.46 0.24 0.29 0.04 0.13 0.45 0.07 0.09 0.09 under

− − Mainbranch 0.49 − − 0.11 − 0.03 − − 0.50 0.34 Mainbranch 0.39 − 0.12 0.10 0.06 − 0.08 0.18 − 0.17 Mainbranch 0.52 0.07 − 0.07 − − − 0.25 traits

•

level. * • ** *** *** ** * • * * • •

measured level. level.

level.

0.18 0.14 0.07 0.00 0.16 the − 0.27 Biomass 0.27 0.28 0.09 0.46 0.08 0.13 0.30 0.32 0.32 Biomass 0.44 0.44 0.09 0.37 − 0.26 0.11 − Biomass 0.01 0.23 − 0.22 0.04 0.01 0.20 0.18 −

probability

probability probability

probability

0.1 0.05 0.01 0.001

coefﬁcients

* *** * • the the the the • * • • ** ** *** *

at at at at 0.27 0.02 0.16 0.070.49 0.19 0.26 0.21 0.02 0.18 0.22

Flowering Flowering Flowering 0.04 0.46 − 0.44 0.11 − 0.23 − − − − 0.08 0.31 0.24 0.25 0.35 − 0.31 0.10 − 0.12 0.08 0.04 0.11 0.03 0.33 0.34 − 0.14 0.07 irrigated

irrigated

correlation

sativa carinata juncea Significant Significant Significant Significant

* • Dryland B. Dryland Dryland B. C. ** *** Table Pearson

J.-N. Enjalbert et al. / Industrial Crops and Products 47 (2013) 176–185 183

Fig. 2. Principal components analysis of seed-oil fatty acid proﬁles. (A) Oil proﬁles Fig. 3. Correlations between (A) ER and DR and (B) ODR and LDR among accessions

for B. carinata (green), B.juncea (blue), and C. sativa (black). Circles, irrigated treat- of B. carinata, B. juncea, and C. sativa. Solid circles, irrigated treatment; open circles,

ment; squares, dryland treatment. (B) Oil proﬁles for accessions of B. juncea based dryland treatment.

upon country of origin (mean ± SD). (For interpretation of the references to color in

this ﬁgure legend, the reader is referred to the web version of the article.)

4. Discussion

accessions had very low ER (Jr-00, Jc-024, and Jr-013). Despite

Though these three Brassicaceae species appear promising as

the low ER in C. sativa, its long-chain FAs eicosenoic acid (C20:1)

crops for the northern High Plains (Pavlista et al., 2012), the rel-

and erucic acid (C22:1) showed a signiﬁcant positive correlation

ative performance of these species for agronomic and seed oil

(p < 0.01), whereas in B. carinata and B. juncea they were nega-

traits under water stress conditions has not been extensively doc-

tively correlated, leading to differences in the levels of these FAs.

umented. Under irrigated conditions, Pavlista et al. (2012) did not

ER was negatively correlated with DR for B. juncea and B. carinata

ﬁnd a difference in yield between Brassica spp. and C. sativa. In this

(Fig. 3). Thus, accessions favoring long-chain FA synthesis had lower

study we observed a wide range of phenotypic responses, or plastic-

polyunsaturated FA levels.

ity, between dryland and irrigated treatments, a condition offering

DR decreased slightly from the irrigated to dryland treat-

breeding opportunities for semi-arid environments. Plasticity is of

ment for B. juncea and C. sativa, while it increased for B. carinata

interest to breeding programs attempting to develop varieties bet-

(Fig. 3A). Both Brassica species showed signiﬁcant positive correla-

ter adapted to speciﬁc environments (Bradshaw, 2006; Chapman,

tions between LDR and ODR (Table 4 and Fig. 3B). C. sativa did not

2008; Forde, 2009; Sadras et al., 2009). Emergence, biomass, ﬂow-

show a signiﬁcant correlation between the two ratios perhaps due

ering time, oil proﬁle, and yield were characteristics of interest and

to a strong negative correlation between C18:2 and C18:3, which

showed signiﬁcant differences in this study, with C. sativa most

was not signiﬁcant for the other species. C. sativa had the highest promising.

LDR at 0.59, compared to 0.35 and 0.48, respectively, for B. juncea

In semi-arid climates, emergence remains a major issue

and B. carinata (Fig. 3B). Hence, C. sativa had a very active path-

(Richards et al., 2010) for small-seeded species due to wind, plant

way converting C18:2 to C18:3 by the enzyme linoleate desaturase.

residue and soil crusting impediments. The earlier the seed germi-

Because of this, C. sativa had the highest levels of linolenic acid in

nates, the faster the seedlings can reach deeper stored moisture.

both treatments (Fig. 3B), and its linolenic acid levels were also the

Earlier seedling establishment means that the crop ﬂowers earlier,

least sensitive to water availability.

avoiding higher temperatures later in the season that negatively

B. juncea’s DR was highly and positively correlated to ﬂow-

impact pollination. Seed size, known to be positively correlated to

ering time, biomass, plant height and pod density under both

faster emergence, showed large differences in the three species

irrigation treatments (Table 4). In B. carinata, LDR was positively

and accessions within species. B. carinata had the largest seed

correlated to biomass and ﬂowering time under dryland conditions.

and C. sativa the smallest. B. carinata demonstrated very good

Interestingly, in C. sativa, DR was positively correlated to biomass

emergence under both moisture treatments. Seed size heritability

under dryland conditions while it was negatively correlated under

was high among all three species, indicating potential to improve

irrigation.

seed weight in all three species. However, TSW was negatively

184 J.-N. Enjalbert et al. / Industrial Crops and Products 47 (2013) 176–185

correlated to other yield components such as pod density in C. pathway have been discovered in all three species, providing infor-

sativa, complicating breeding for improvement of seed weight. mation for improved selection (Jourdren et al., 1996; Tanhuanpaa

In addition to seed size, fatty acid proﬁles could be related to et al., 1998; Lionneton et al., 2002; Sharma et al., 2002; Gehringer

better emergence under cold soil temperatures. Oilseed species et al., 2006; Qiu et al., 2006).

that perform well in colder environments, such as ﬂax (Linum Water stress affected FA composition, such that linolenic acid

usitatissimum) and some Brassica species, have higher levels of content decreased from the irrigated to the dryland treatment in

polyunsaturated fatty acids (and higher DRs) than oilseed species B. juncea and C. sativa (Fig. 1). Water deﬁcit has been shown to

that perform well in warmer environments (Linder, 2000). Indeed, impact oil composition, reducing linolenic acid content in coconut

we found higher linoleic acid content in B. juncea accessions from and rapeseed leaves (Canvin, 1965; Williams et al., 1992).

colder climates (Fig. 2B). Higher levels of poly-unsaturated FAs C. sativa appears to be the most drought-tolerant among the

increase cell membrane ﬂuidity, improve seedling establishment, three species, in terms of the least reduction in biomass production

and result in higher shoot vigor under cold temperatures (Linder, under dry conditions and the highest seed yield. One key difference

2000). We have found faster emergence of C. sativa compared to B. between C. sativa and the Brassica species was the high linolenic

napus and B. juncea at low temperatures, allowing earlier planting acid content in C. sativa seeds, around 30% compared to approxi-

(Enjalbert et al., unpublished data). Shorter germination time can mately 5% for B. juncea and B. carinata. High linolenic acid in the

lead to earlier ﬂowering, a desirable characteristic under dryland seed has been reported to be correlated to high levels of this acid

conditions. in the leaf (Lemieux et al., 1990; Miquel and Browse, 1994). We

Late-ﬂowering accessions of B. juncea and B. carinata produced did not measure FA levels in the leaf, but numerous studies in Ara-

more biomass than early-ﬂowering accessions under both moisture bidopsis (McConn et al., 1994; Matsuda et al., 2005; Mene-Saffrane

treatments. Earlier-ﬂowering C. sativa accessions showed increased et al., 2009), canola (Merrien et al., 2007; Triboi-Blondel and Renard,

pod density and plant height under dryland conditions. These 1999), sunﬂower (Izquierdo et al., 2002), tobacco (Kodama et al.,

accessions escaped some heat and drought, resulting in higher seed 1994; Murakami et al., 2000), and coconut (Repellin et al., 1997)

yield. Both Brassica species produced large amounts of biomass show that an increase in leaf trienoic fatty acids, such as linolenic

early in the season, which impacted them negatively later when acid, improved cold and drought tolerance. Our studies suggest that

water became scarce under dryland conditions. Earlier ﬂowering linolenic acid levels are likely to contribute to superior drought-

time has been shown to increase yield under dry conditions and by tolerance performance of C. sativa.

escaping drought, plants can increase seed production (Siddique

et al., 1990). The two-year average seed yield of C. sativa was

5. Conclusions

signiﬁcantly higher than that of the two Brassica species, as well

as the commercial B. napus hybrid check. However, to evaluate

This research examined three cruciferous species side by side

drought tolerance more precisely within species, it would have

under dryland and irrigated conditions in semi-arid climates. The

been more appropriate to adjust for ﬂowering time when plant-

results indicated that large variations exist for morphological and

ing so the drought event would occur when all plants are at the

oil proﬁle traits both within and among the three species. We com-

same developmental stage. Yue et al. (2006) mentioned that the

pared traits related to adaptive advantages of the three species.

ﬂowering time variation could make the phenotyping of drought

B. carinata had large seed size, but was susceptible to ﬂea bee-

tolerance less accurate because drought at the reproductive stage

tles, ﬂowered later, and yielded poorly under dryland conditions. B.

drastically impacts ﬁtness.

juncea ﬂowered early and had wide variation for seed size, biomass

Major differences in fatty acid proﬁles were found among the

production, and FAs, but was susceptible to ﬂea beetles, and pro-

three species. C. sativa had a distinct proﬁle with a high DR and

duced low seed yield under dryland conditions. C. sativa yielded

low ER, whereas B. carinata and B. juncea had very high ER. Thus,

more than B. juncea and B. carinata in 2009 and 2010 under both

the two Brassica species had more efﬁcient ER pathways, involv-

dry and irrigated conditions. C. sativa had a shorter stature, higher

ing two FA elongases, FAE (e1) elongating C18:1 to C20:1 and FAE

harvest index, more efﬁcient desaturation pathway and showed

(e2) elongating C20:1 to C22:1 (Barker et al., 2007). FAE (e2) was

resistance to ﬂea beetles but it has the smallest seed size. C. sativa

very active within B. carinata and B. juncea, creating high erucic

ﬂowered as early as B. juncea and had low erucic and high linolenic

acid levels, whereas in C. sativa, FAE (e1) was predominant within

acid, two traits that are valuable for use of oilseed meal and for fuel

the elongation pathway resulting in higher levels of eicosenoic acid

and food quality. Oil proﬁle characteristics, such as high linolenic

than erucic acid. B. carinata accession BRA-1154 had an erucic acid

acid, could play an important role in plant adaption especially under

content of 48% and BRA-2135 had 31% erucic acid content, implying

stressful environments. Further work is needed for each species,

wide genetic diversity. Alemayehu and Becker (2001) found even

controlling more precisely the timing of drought relative to ﬂow-

greater diversity for erucic acid content in B. carinata germplasm.

ering time, and measuring more speciﬁc drought-tolerance traits.

However, its erucic content remains high compared to Environ-

mental Protection Agency limits of 2%, based on potential negative

Acknowledgements

impact in feed (McCutcheon et al., 1976).

The C. sativa oil proﬁles had high levels of desaturation. The

We are grateful to Gus Foster for agronomic advice; David John-

two major enzymes involved, fatty acid desaturases two (FAD2)

son, Blake Robinson, Gaelle Berges, and Tom Fitzgerald for help with

and three (FAD3), desaturate C18:1 to C18:2 and C18:2 to C18:3,

ﬁeld data collection and Cargill Specialty Canola Oils for funding S.

respectively. FAD3 was more efﬁcient in C. sativa than in the Bras-

Zheng’s post-doctoral research and conducting seed chemical anal-

sica species, resulting in high levels of linolenic acid (C18:3) in C.

ysis. This work also received funding from the Colorado Ofﬁce of

sativa. B. juncea and B. carinata showed larger genetic variation

Economic Development and International Trade and the Colorado

in oil proﬁles than C. sativa, so oil proﬁle selection for the two

Water Institute.

Brassica species can be partially achieved by choosing the appro-

priate combinations of alleles present in the germplasm. C. sativa

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