JXB Advance Access originally published online on November 6, 2006
Journal of Experimental Botany 2007 58(2):187-194; doi:10.1093/jxb/erl192
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RESEARCH PAPER |
Osmotic adjustment in chickpea (Cicer arietinum L.) results in no yield benefit under terminal drought
1Centre for Legumes in Mediterranean Agriculture, M080, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia
2Hebrew University of Jerusalem, PO Box 12, Rehovot 767100, Israel
3CSIRO Plant Industry, Private Bag No. 5, Wembley, WA, 6913, Australia
4Indian Institute for Pulses Research, Kanpur, UP 208 024, India
5Western Australian Department of Agriculture and Food, Dryland Research Institute, PO Box 432, Merredin, WA 6415, Australia
6Institute for Pulse and Oilseeds Research, Gulbarga, Karnataka 585 101, India
7Rajasthan Agricultural University, Durgapura Agricultural Research Station, Jaipur, Rajasthan 302 018, India
8Jawaharlal Nehru Krishi Vishwa Vidyalaya, Sehore, MP 466 001, India
* To whom correspondence should be addressed. E-mail: ncturner{at}clima.uwa.edu.au
Received 4 June 2006; Accepted 7 September 2006
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Abstract |
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 Top Abstract IntroductionMaterials and methodsResultsDiscussionReferences |
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Variation in osmotic adjustment (OA) among chickpea (Cicer arietinum L.) cultivars has been observed when exposed to terminal drought, but some studies suggest that this benefits yield while others suggest it does not benefit yield in water-limited environments. In the present study, parents differing in OA were crossed and a set of advanced breeding lines (ABLs) developed for yield testing. The variation in OA during podding was measured under terminal drought in the F2, F3, F7, and F8 progeny and in the parents by either rehydrating the leaves before sampling for osmotic potential (OP) or by measuring the relative water content (RWC) and OP on adjacent leaves for the calculation of the OP at full turgor. Yields were measured in the F8 progeny under terminal drought in Australia and India. While differences in OA were measured in the chickpea lines and parents, OA varied from year to year and did not consistently benefit yield when measured in the field under terminal drought. In Australia, differences in OA were not associated with any yield benefit in any year, while in India early flowering resulted in higher yields at three of the four sites, and OA had an inconsistent effect on seed yields. A comparison of OP at full turgor measured after rehydration and from measurements of RWC and OP showed that the rehydration technique underestimated OA. The lack of contribution of OA to yield of chickpea is discussed.
Key words: Advanced breeding lines, early flowering, phenology, terminal drought, yield components
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Introduction |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Chickpea (Cicer arietinum L.) is an important cool-season food legume (pulse) that is generally grown under rainfed conditions either on stored soil moisture in subtropical environments with summer-dominant rainfall or on current rainfall in winter-dominant Mediterranean-type environments. In both environments, unirrigated chickpea suffers yield penalties from terminal drought (Siddique et al., 2000; Turner, 2003; Yadav et al., 2006). While the primary adaptive strategy to terminal drought is drought escape through early flowering (Singh et al., 1990; Silim and Saxena, 1993a, b; Berger et al., 2004, 2006), osmotic adjustment (OA) has been suggested as an important trait in postponing dehydration in water-limited environments as it maintains cell turgor and physiological processes as water deficits develop (Turner and Jones, 1980; Morgan, 1984). Variation in OA among chickpea cultivars in response to developing water deficits has been observed in several studies (Singh et al., 1990; Morgan et al., 1991; Lecoeur et al., 1992: Leport et al., 1999; Moinuddin and Khannu-Chopra, 2004). However, the relationship between OA and yield of chickpea under water-limited environments is inconsistent. Morgan et al. (1991) indicated that the degree of OA observed under controlled conditions was positively correlated with the yield of the cultivar under rainfed conditions in the field. Moinuddin and Khanna-Chopra (2004) found that seed yield of chickpea was correlated with the degree of OA when grown under a line-source irrigation system in the field. However, Leport et al. (1999), who observed a range of OA in chickpea from 0 to 1.3 MPa, did not observe any effect on yield, and Singh et al. (1990) observed that OA did not always result in a yield increase, particularly in cultivars that had the greatest degree of OA and partitioned a large fraction of assimilates to the root. Indeed, Serraj and Sinclair (2002) concluded that no yield advantage from OA had been demonstrated in any crop except at very low and uneconomic yields.
The present study was initiated to determine the association between the degree of OA and grain yield of advanced breeding lines (ABLs) of chickpea developed from crosses between cultivars with high and low OA. The association was assessed under rainfed conditions in the field in Australia and India in F8 progeny which were assumed to be stable for the OA trait. By measuring OA in the parents and the progeny of the crosses during the development of the ABLs, the stability of OA could also be evaluated.
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Materials and methods |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Random single plant selections from the chickpea (C. arietinum L.) cultivars Kaniva (a large-seeded kabuli type), Tyson (a small-seeded desi type), and CTS60543 (a small-seeded desi type), identified by Leport et al. (1999) as having low (0.0 MPa), medium (0.7 MPa), and high (1.3 MPa) OA, respectively, were used for crossing. Crosses were performed in Rehovot, Israel, using the technique of Retig (1971) with the white-flowered Kaniva as the female parent and the pink-flowered Tyson and CTS60543 as the pollen donors. Several F1 seeds were obtained from the two crosses and grown under quarantine conditions in Perth, Western Australia. Their hybrid nature was confirmed by the dominant pink corolla trait, typical of the two pollen donors. In order to generate a representative range of OA with all the available genetic variation, the F2 seeds harvested from the individual F1 plants were bulked to give a mixed F2 population (similar to a three-way cross). On 17 July 2000, 120 randomly selected F2 plants and the three parents were grown in free-draining pots, 0.15 m diameter and 0.4 m deep, in the greenhouse at CSIRO, Perth, Australia (31°57'S; 115°47'E) in a red brown earth (Calcic Haploxeralf) soil sourced from a field at the Merredin Research Station, Western Australia (Thomson et al., 1997). The benches were rotated twice weekly and the pots kept well watered until 3 October when water was withheld from the onset of podding. On 24–26 May 2000, a second random sample of the bulked F2 population was hand sown as spaced plants (0.1 m interplant distance, 1 m row length and width) in the field at the Merredin Research Station (31°30'S; 118°12'E), Western Australia. In 2000, the rainfall at Merredin during the growing season was 123 mm, with only 1 mm after flowering (Berger et al., 2004; Palta et al., 2004).
A random set of F3 families was selected from the field-grown F2 plants. On 23 May 2001, 25 families and the three parents were hand sown at the Merredin Research Station in a block adjacent to that in 2000 and irrigated to ensure full and uniform emergence. A randomized block design with three replicates was used, with each family and parental lines represented by a row of 3–5 plants in each block. The mean of the 9–15 samples is considered sufficient to give an estimate of the phenotypic variation among the families but, due to poor growth in some lines, only 14 families and the three parents were used to measure OA. The rainfall in the 2001 growing season was 197 mm.
From 2002 to early 2003, the 25 families were progressed from the F4 to the F6 as separate families by single seed descent and then bulked up in the F6, growing two generations per year in the greenhouse at CSIRO Floreat in a standard potting mix and kept well watered. In 2003 and 2004, the F7 and F8 progeny were grown in the field at the Merredin Research Station under a rainout shelter. In 2003, small plots were hand sown on 22 May at standard field densities in double rows 2.5 m long separated by 0.2 m (0.1 m interplant distance) and replicated four times in a randomized block design. The outside borders of the plot were planted with narrow-leafed lupin (Lupinus angustifolius L.) to prevent edge effects and to facilitate plot identification. The rainfall from sowing to the time that the rainout shelter covered the plots (25 September) was 164 mm. In 2004, six of the 25 ABLs measured in 2003 were selected on the basis of differences in times to flower and OA [early flowering (111 days after seeding; DAS), M55, M76, and M12; late flowering (116 DAS), M129, M89, and M45; low OA (0.60 MPa), M55, and M129; intermediate OA (0.72 MPa), M76, and M89; high OA (1.02 MPa), M12, and M45] to form six combinations of early and late flowering, and low medium and high OA. This material was bulked over the summer in the greenhouse. To ensure the accuracy and precision of yield measurements, the seeds were hand sown in the rainout shelter on 9–10 June 2004 together with the parents in plots (2.5 m long by four rows separated by 0.2 m) at standard field density and replicated six times in a randomized complete block design. Edge effects were minimized between plots by sowing a row of lentil (Lens culinaris Medikus cv. Cassab) and on the outside of the plots by several rows of lentil. The rainfall from sowing to the time that the rainout shelter covered the plots (14 September) was 102 mm.
Additionally, two ABLs with low (0.60 MPa) OA (M55 and M129), three with intermediate (0.85 MPa) OA (M39, M51, and M75), and three with high (1.05 MPa) OA (M86, M93, and M110) when measured in the field in Merredin in 2003 were selected and transferred to India. These genotypes were multiplied through two generations, the first at the Indian Institute of Pulses Research, Kanpur, UP (20°27'N; 80°14'E), and the second at the University of Agricultural Sciences, Dharwad, Karnataka (15°30'N; 75°04'E), India, respectively. The eight ABLs and the three parents were grown under rainfed conditions at four locations in India: (i) at the research farm of the Indian Institute of Pulses Research, Kanpur, UP; (ii) Karnataka University of Agricultural Sciences, Oilseed and Pulses Research Station, Gulbarga, Karnataka (17°24'N; 76°54'E); (iii) Jawaharlal Nehru Krishi Vishwa Vidyalaya, Sehore, MP (23°12'N; 77°06'E); and (iv) Rajasthan Agricultural University, Durgapura Agricultural Research Station, Jaipur, Rajasthan (26°48'N; 75°48'E). The trials were sown between 15 October in Gulbarga to 10 November 2004 in Sehore. No pre-sowing irrigation was applied before hand planting; the crops were grown in the winter (dry) season on stored soil moisture and no irrigation was applied during the growing season. The rainfall during the growing season was <30 mm at all sites. The plots were 3–4 m long by 1.5 m wide and the 11 genotypes were sown in rows 0.3 m apart and 0.1 m between plants in a randomized block design with three replications. In both Australia and India, seeds were pretreated with Bavistin® to minimize the probability of seed- and soil-borne diseases such as Asochchyta blight (Ascochyta rabiei), Botrytis grey mould (Botrytis cinerea), Fusarium wilt (Fusarium oxysporum), and root rot (Rhizoctonia bataticola), and inoculated with group N rhizobia immediately prior to sowing.
Osmotic adjustment
OA was assessed in two ways as described by Turner (2004). In the greenhouse in 2000 and in the field in 2003 and 2004 in Australia, the plants were sampled for the measurement of relative water content (RWC) and osmotic potential (OP) at 09.00 h. Leaf samples for OP were cut and placed in aluminium foil and quickly frozen in liquid nitrogen, transferred to the laboratory and kept at –18 °C. After thawing, the sap was extracted with a syringe or press and the OP of the sap measured by vapour pressure osmometry with a Wescor C52 chamber (Wescor Inc., Logan, UT, USA) attached to a Wescor HR33T microvoltmeter. Adjacent leaves were sampled for RWC. The leaves were placed in a vial, transferred to the laboratory, weighed, and then floated on freshly distilled water for 8 h in low light and the turgid weight determined. The sample was then oven-dried at 70 °C for 24 h and weighed. The RWC is then:
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The OP at full turgor (OP100) was then estimated from the measured OP and RWC by:
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Samples were taken at four or five times, from just prior to flowering until senescence of leaves became severe, and OA was calculated as the difference between OP100 at the beginning of the drying cycle when the RWC was 
80% and OP100 when the RWC in all genotypes was 60% and before senescence of the leaves.
Where there were many samples for measurement, it was not feasible to measure both the OP and RWC. Therefore, the leaves were sampled into vials containing freshly distilled water and taken to the laboratory where they were allowed to rehydrate for 8 h in low light at 20 °C. After 8 h, the leaves were placed in aluminium foil, quickly frozen in liquid nitrogen, and the OP at full rehydration (equivalent to OP100) measured as above. This method was used for the 2001 sampling. In 2004, both methods were used on the nine genotypes sampled for OA to compare the degree of OA by the two methods. The plants were sampled four or five times over a 5-week period as the soil under the rainout shelter dried and OA determined by the two methods as detailed above.
Phenology, yield, and yield components
In 2003, the time to 50% flowering for each plot was noted by twice weekly visits to the site. In 2004, the percentage of plants that were flowering on 23 September (106 DAS) was recorded.
In 2004, all the plants in the plots under the rainout shelter were harvested at ground level, the number of plants counted and brought back to the laboratory, oven-dried at 70 °C for a minimum of 24 h, and the total biomass obtained. The pods were removed, threshed, and the number of seeds, total seed weight, and mean 100-seed weight determined.
Statistical analysis
The data were analysed by analysis of variance (ANOVA) using Genstat Version 8, fitting replicates as blocks, and genotypes as the main effect. Within the main effect of genotype, two orthogonal contrasts were made: (i) parents were compared with ABLs; and (ii) within the parental group, CTS60543 was contrasted with Kaniva to test whether the original rank order established by Leport et al. (1999) was maintained. Residual plots were graphed to identify outliers and check that the errors were normally and independently distributed. The variance components between and within F3 families were used to calculate heritability (h2) using the method of Cahaner and Hillel (1980).
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Results |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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In the greenhouse in 2000, the range of OA in the mixed F2 population derived from the two crosses (KanivaxTyson and KanivaxCTS60543) varied from 0 to 1.9 MPa and exceeded that of the parents (0.39–0.55 MPa) (Fig. 1). In 2001 (Fig. 2a), the range of OA in the selected F3 families was much smaller (0.08–0.45 MPa), but still greater than among the parents (0.11–0.35 MPa). In 2003, the 25 families ranged in OA from 0.51 to 1.23 MPa while the parents ranged from 0.44 to 0.70 MPa (Fig. 2b). In 2004, the six ABLs varied in OA from 0.67 to 1.06 MPa, compared with from 0.68 to 1.30 MPa for the parents (Fig. 2c; Table 1). In 2001, the F3 between-family variance was low (13.6% of the total mean square), giving a narrow sense heritability value (Cahaner and Hillel, 1980) of h2=0.20±0.13 (Abbo et al., 2002).
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While there was measurable and significantly different OA in all years, the ranking of the parents and the progeny differed in each year (Table 1).
Indeed, the original rank order of low, medium, and high OA from Kaniva to Tyson to CTS60543 observed by Leport et al. (1999) could not be repeated in any of the subsequent years. Similarly, ABLs selected on the basis of OA in 2003 performed completely differently in 2004, when there were no significant differences between the low, medium, and highly adjusting categories (P=0.957). However, in 2004, there were highly significant differences between the early and late flowering ABLs (P=0.002), with late flowering varieties adjusting more than early ones (Table 1).
In Australia, the yield of the genotypes when grown under a rainout shelter in the field in 2004 to induce terminal drought varied from 83 to 122 g m–2, but these differences were not statistically different (P=0.226). Indeed, yield was not associated with OA in 2004 (Fig. 3). OA was not associated with biomass or harvest index (P=0.09, 0.06), both of which varied significantly among genotypes (P <0.05) (Table 2). While there were significant differences in flowering time in 2004 (Table 2), earliness did not influence the yield in these ABLs and parents (Table 2).
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In India, yields were below those in Australia (38 g m–2 at Sehore, 49 g m–2 at Gulbarga, 69 g m–2 at Durgapura to 95 g m–2 at Kanpur) (Table 3). There were significant differences (P <0.001) among the sites in seed yield, but no difference between the parents and ABLs as a whole except at Kanpur where the ABLs were much higher yielding than the parents (P <0.001). In contrast to Australia, in India yield was strongly influenced by phenology. Early-flowering ABLs had significantly higher yields than the late-flowering ABLs (P <0.001 to <0.025) at all sites except Sehore (P=0.53). There were consistent yield differences between all OA categories (P=0.007) where genotypes with intermediate levels of OA had low yields at all sites, whereas the low and highly adjusting ABLs were higher yielding (Table 3). This is likely to be a consequence of the confounding effect of phenology. The medium OA ABL category comprised later flowering germplasm compared with the low and high OA categories, and was therefore subject to greater terminal drought stress.
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When the OP100 was obtained by rehydrating the leaf, the values were higher (less negative) than the OP100 calculated from the OP and RWC measured at the same time, but were correlated (r2=0.66) before the soil began to dry (Fig. 4). However, there was no correlation (r2=0.004) between OP100 measured/estimated by the two methods when the soil had dried and the leaves had osmotically adjusted (Fig. 4). This suggests that rehydrating the leaves for 8 h induced loss or metabolism of the solutes that accumulated with OA.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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This study has shown that OA does occur in chickpea, but that the expression of OA in the measured phenotype is not stable and does not consistently increase yields under terminal drought. The values of OA obtained in this study were similar to those obtained previously (Morgan et al., 1991; Lecoeur et al., 1992; Leport et al., 1999; Moinuddin and Khannu-Chopra, 2004), but previous studies have not attempted to compare the performance of cultivars through several years or tried to establish the stability of OA in chickpea. While OA was significantly different among the genotypes in each year of measurement, the narrow sense heritability measured in the F3 families was low and the ranking of the genotypes varied from year to year. This was clearly evident in the parents that were not consistently ranked in the order measured by Leport et al. (1999) in any of the years in this study and also among the ABLs that were selected for differences in OA in 2003. This suggests that the phenotypic expression of OA is not stable in chickpea, but varies with level of plant water deficit, location, and physiological stage of the plant, a conclusion reached in a study in India with a different set of ABLs (Basu et al., 2006).
In relation to the influence of OA on yield, previous research had shown mixed results, with some authors concluding that OA increased yields in water-limited environments (Morgan et al., 1991; Moinuddin and Khannu-Chopra, 2004), others that there was no effect on yield (Leport et al., 1999), while others found that it increased yields in some cultivars and decreased yields in others (Singh et al., 1990). The previous research was conducted with cultivars that vary in a number of traits that could prove beneficial in water-limited environments, such as early flowering, phenological plasticity, deep roots, and small leaves (Silim and Saxena, 1993a, b; Saxena, 2003; Berger et al., 2004, 2006). In this study, ABLs were developed which had significantly different degrees of OA in each year of measurement, but yields that were not associated with OA when grown under rainout shelter conditions in the field in Australia in sufficiently large plots to provide reliable yield estimates. The ABLs did vary in time to 50% flowering so that it was necessary to select ABLs with high and low OA and both early and late flowering. However, neither early flowering nor OA benefited yields when the F8 progeny were exposed to terminal drought in Australia. However, early flowering did increase yields at three of the four sites in India, and OA did significantly affect yields in India. This was because the intermediate OA ABLs had consistently low yields, whereas the high OA lines did not consistently increase yields in the water-limited environments.
This confirms the conclusions of Serraj and Sinclair (2002) who argued that there were few examples in any crop of yield benefits from OA except in extremely low-yielding environments. However, they did conclude that some benefits may be observed if OA increased the extraction of soil water from deeper in the soil profile. The major yield advantage from OA has been observed in wheat (Serraj and Sinclair, 2002; Richards, 2006) that has been shown to extract more soil water in high OA genotypes than in low OA genotypes (Morgan and Condon, 1986). Turner et al. (1987) showed that roots of lupins (L. angustifolius) adjusted more than leaves, and Singh et al. (1990) showed that those chickpeas that osmotically adjusted to a greater extent in their leaves extracted more water from the deep soil profile than those that osmotically adjusted less. Thus it was expected that chickpea might yield better under drought if it exhibited the OA trait, especially in India where the crop is grown on stored soil moisture. However, the high OA lines only increased yields at one site in India, the wettest and longest season site (Berger et al., 2006).
If there is no yield benefit and OA has low (if any) heritability in chickpea, the question arises as to why the plants accumulate osmotically active solutes in the leaves. Basu et al. (2006) showed that chickpeas accumulated hexose sugars and sucrose in the leaves when water stress occurred and starch was broken down. Lecoeur et al. (1992) also showed that sucrose accumulated during OA of chickpea, but this was a minor component of the solutes contributing to OA, with malic acid and malonic acid contributing to 75% of the change in osmotic potential under water-limited conditions. It therefore is possible that the accumulation of solutes is a passive consequence of assimilates accumulating faster than they are required during early seed growth and that these solutes are remobilized during late seed filling when OA has been observed to decrease (Leport et al., 1999). To determine whether OA arises from solute accumulation that occurs because of imbalances among these processes would require the careful study of the rates of assimilation, leaf, stem, and root carbohydrate concentrations, and the rate of seed filling after pod set. Certainly, there was no association between OA and harvest index, a potential measure of source–sink capacity.
Several methods have been used to measure the degree of OA (Turner, 2004). Morgan (1983) and Singh et al. (1990) used the slope of the relationship between OP and RWC to determine the degree of OA in chickpea, whereas Jones and Turner (1980) used the difference in the OP of water-stressed and irrigated plants at the same water content, usually at full hydration (100% RWC), to calculate the degree of OA in sunflower. The measurement of RWC and the measurement of both irrigated and stressed plants results in it being difficult to measure many replicates or genotypes, and hence OA has not been widely screened in breeding populations. The measurement of OP of rehydrated samples at different times as the soil dried and the degree of OA calculated as the difference in OP after a period of soil drying minus that when the soil was fully saturated has been suggested as a means of measuring the OA in a large number of samples (Turner, 2004). It was always recognized that this would not take into account the changes in OP with time or stage of plant development, but was considered a useful comparative method among genotypes with similar phenological development. However, this comparative study with chickpea showed that rehydration for 8 h resulted in an increase in the OP, presumably because of solute leakage or metabolism. This was worse when solutes had accumulated in OA, so that there was no correlation between values measured after rehydration and those estimated from the RWC and OP, and presumably the reason for the small range in OA in 2001. It has long been known that solutes can be quickly metabolized during rehydration or thawing (Brown and Tanner, 1983), but the correlation between the two methods before the solutes accumulated in OA proved deceptive.
While this study has confirmed that OA varies in chickpea, it has also demonstrated that the phenotypic expression of OA is not stable, but appears to vary from year to year in each genotype, suggesting that it may be the passive consequence of differences in rates of accumulation and utilization of solutes rather than an active accumulation of solutes in response to a water deficit. The study has also demonstrated that where there are differences in OA, this has no effect on the yield under terminal drought when grown on current rainfall in Mediterranean-type climates and when grown on stored soil moisture in subtropical climates in India. Thus, OA cannot be considered a selectable drought resistance trait in chickpea breeding programmes.
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Acknowledgements |
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This paper reports research supported financially by CSIRO, the Grains Research and Development Corporation (GRDC) of Australia, the Australian Center for International Agricultural Research (ACIAR), the Centre for Legumes in Mediterranean Agriculture (CLIMA), and the Indian Council of Agricultural Research (ICAR). SA thanks the GRDC for a Visiting Fellowship to work in Australia. Renee Buck is thanked for technical support.
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Abbreviations |
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ABL, advance breeding line; DAS, days after seeding; OA, osmotic adjustment; OP, osmotic potential; RWC, relative water content.
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References |
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  L. P. Manavalan, S. K. Guttikonda, L.-S. Phan Tran, and H. T. Nguyen Physiological and Molecular Approaches to Improve Drought Resistance in Soybean Plant Cell Physiol., July 1, 2009; 50(7): 1260 - 1276. [Abstract] [Full Text] [PDF]
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