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Published in Crop Sci. 44:449-455 (2004).
© 2004 Crop Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA

CROP PHYSIOLOGY & METABOLISM

Osmotic Adjustment in Chickpea in Relation to Seed Yield and Yield Parameters

Moinuddin*,a and Renu Khanna-Choprab

a Plant Physiology Laboratory, Potash Research Institute of India, Sector-19, Dundahera, Gurgaon-122016, Haryana, India
b Water Technology Center, Indian Agricultural Research Institute (IARI), New Delhi, India

* Corresponding author (moinuddin202{at}rediffmail.com).


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
To ascertain the role of osmotic adjustment (OA) in drought tolerance of chickpea (Cicer arietinum L.), eight cultivars differing in OA capacity were field grown under a line source sprinkler irrigation system. This imposed a soil moisture gradient on either side of the line source. The cultivars were divided into high and low OA groups and crop performance was assessed group-wise at three growth stages and at the time of harvest. A two-way increase in water stress was observed, along the soil moisture gradient and across the growth stages. As a result, water potential, osmotic potential, and relative water content decreased progressively with increasing soil moisture stress and age of the crop, regardless of OA groups. As compared with low OA cultivars, high OA cultivars generally showed an improved plant water status. High OA cultivars proved significantly superior to low OA ones in seed yield and most of its parameters. The yield benefit was 26 and 48% at moderate and severe moisture stress levels of the line source. This coincided with osmotic adjustment ranging from 0.28 to 0.48 MPa and from 0.37 to 0.71 MPa, respectively, at various phases of reproductive growth.

Abbreviations: HOA, high osmotic adjustment group of chickpea cultivars • LOA, low osmotic adjustment group of chickpea cultivars • OA, osmotic adjustment • OP, absolute osmotic potential • OP100, osmotic potential at full turgor • RWC, relative water content • WP, water potential


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
OSMOTIC ADJUSTMENT involves an active accumulation of solutes within the plant in response to a lowering of the soil water potential, reducing the harmful effects of water deficit (Morgan, 1984). As a consequence of solute accumulation, the osmotic potential of the cell is lowered, which, in turn, attracts water into the cell and, thereby, tends to maintain its turgor. Accumulation of solutes in roots leads to lowering of the osmotic potential of the root, which maintains the driving force for extracting soil water under water deficit conditions. In fact, OA has been reported to be an important drought-adaptation mechanism in many crop plants (Morgan, 1983; Ludlow and Muchow, 1990; Subbarao et al., 1995; Hare et al., 1998). It leads to better extraction of water from the soil, stimulates root growth (Greacen and Oh, 1972; Morgan and Condon, 1986; Wright et al., 1983; Santamaria et al., 1990; Leport et al., 1999) and facilitates a better translocation of preanthesis carbohydrate reserves to the grain during the grain-filling period (Morgan, 1980; Pierce and Raschke, 1980; Subbarao et al., 2000b). Additionally, a positive relationship between OA and grain yield in water-deficit environments has been shown in grain sorghum [Sorghum bicolor (L.) Moench](Ludlow et al., 1990; Santamaria et al., 1990; Tangpremsri et al., 1995), wheat (Triticum aestivum L.) (Morgan et al., 1986; Blum et al., 1999), barley (Hordeum vulgare L.) (Blum, 1989), pea (Pisum sativum L.) (Rodriguez-Maribona et al., 1992) chickpea (Cicer arietinum L.) (Morgan et al., 1991), and pigeonpea (Cajanus cajan L.) (Subbarao et al., 2000a). Significantly greater seed yield in groups of genotypes with high osmotic adjustment (HOA) than in groups with low osmotic adjustment (LOA) has also been reported under water deficit condition in various crops (Boyer, 1982; Morgan, 1983, 1995; Ludlow et al., 1990).

Many reports regard OA to be a causal mechanism favoring crop productivity under water-deficit environments. However, there are also conflicting reports indicating a negative relationship between OA and seed yield under drought (Grumet et al., 1987; Kirkham, 1988; Subbarao et al., 2000a). Other reports indicate no relationship between OA and growth and/or seed yield in field conditions under drought (Shackel and Hall, 1983; Munns, 1988; Flower and Ludlow, 1986; Tangpremsri et al., 1995). Thus, OA as an adaptation mechanism for drought resistance is somewhat debatable (Munns, 1988) and requires further analysis. The present investigation was conducted on chickpea cultivars differing in OA capacity. The objective was to evaluate whether an OA-based mechanism is responsible for sustained crop productivity under water deficit. Little work on chickpea has been conducted on this topic (Morgan et al., 1991; Leport et al., 1998, 1999), although chickpea is an important crop with a higher OA capacity than several other legume crops (Leport et al., 1999). It needs to be determined whether OA can be used as a selection criterion for screening drought resistant cultivars for rain-fed areas, which cover approximately 70% of the total agricultural land of India.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Plant Material and Field Culture
The field experiment was conducted in the winter season of 1992-1993 at the research farm of Water Technology Center (WTC) of the Indian Agricultural Research Institute (IARI), New Delhi, India. Eight chickpea cultivars, namely, BG-329, BG-365, BG-372, BG-380, BG-384, BG-1001, PUSA-256, and PUSA-267 were included in the study to investigate their performance in varying drought environments imposed by a line source sprinkler irrigation system. The experimental field comprised of 12-m-long and 1.5-m-wide beds laid out on either side of the line source. These beds were further divided length-wise into four moisture treatments, T1, T2, T3, and T4, which were 3 by 1.5 m (4.5 m2) in size each. The results reported in this paper are from the T1, T3, and T4 moisture levels only, because in most cases there was no difference in plant water relations parameters at the T1 and T2 moisture levels, which were nearest to the line source. In each treatment bed, seeds were sown at 80 kg ha–1 in six rows. Row-to-row distance was 0.25 m. There were four replications. The line source imposed the water stress, so the treatment plot nearest to the line source (T1) received maximum water, and the water deficit increased progressively with the distance from the line source. Nitrogen, phosphorus (P2O5), and potassium (K2O) were supplied as urea, single superphosphate, and muriate of potash at the rate of 20: 60: 60 kg ha–1 at the time of sowing. The soil of the experimental field was sandy loam with a mean depth of 3 m and bulk density of 1.55 Mg m–3. The available surface (0- to 180-cm soil depth) soil water content measured gravimetrically at the time of sowing was 233 mm. Subsequently, three irrigations were given at 30, 50, and 80 d after sowing (DAS) with the line source sprinkler irrigation system. Total rainfall during the crop season was 51.3 mm. The line source irrigation cumulatively supplied 92.7, 51.7, and 2.8 mm water, with the total water available to the crop being 377, 336, and 287 mm in the T1, T3, and T4 moisture levels. The weekly averages of maximum and minimum temperature and rainfall events during the season are shown in Fig. 1 .



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  		Fig. 1. Pattern of weekly averages of maximum and minimum temperature and total rainfall recorded during the crop season.

 
Standard agricultural practices were maintained throughout the crop cycle. The line source irrigation applications were always made when the wind speed was low (<1 m s–1). All the chickpea cultivars flowered within 5 d and matured almost at the same time. At harvest, four 2-m rows of plants were hand harvested (total harvest area 2 by 1 m = 2 m2) from each of the four plots in each moisture treatment. Seed yield and the yield parameters viz., biomass, 500 seed weight, number of seeds per square meter and harvest index, were recorded for each plot at harvest to assess the yield performance of the two OA groups of chickpea.

Leaf Water Relations Parameters
Quantification of crop water status was made by measuring the leaf water relations parameters water potential (WP), osmotic potential (OP), and relative water content (RWC) during the crop reproductive phase at early flowering (104 DAS), late flowering (114 DAS), and early fruiting (130 DAS) stages, using leaves having flowers in their exils. Leaf WP was measured between 1000 and 1100 h on each sampling date in four replicates with a pressure chamber (Soil Moisture Equipments Corp., Santa Barbara, CA). The same leaves were then frozen in sealed polyethylene vials in a freezer at –20°C. After thawing at room temperature (about 15 min), cell sap was expressed with a hand press, and the OP of the cell sap was measured with a vapor pressure osmometer (model 5500, Wescor, Inc., Logan, UT). The osmometer was calibrated with known concentrations (mmol kg–1) of NaCl solutions. These values were converted to pressure unit according to the following equation:

where R is the gas constant (0.008314) and T is the temperature measured in the Kelvin scale (298 K in these measurements). The OP was corrected (OP + 0.1 OP) for the dilution of symplastic sap by apoplastic water, assuming 10% apoplastic water (Kramer, 1983). The osmotic potential at full turgor (OP100) was calculated according to Wilson et al. (1979) by the following equation:

Relative water content (RWC) was determined by the method of Barrs and Weatherley (1962) according to the following equation:

where FW is fresh weight, DW is dry weight and TW is turgid weight of the leaf samples (4-mm diameter leaf discs). The turgid weight was determined after floating the leaf discs on distilled water for 24 h at room temperature (about 20°C) under dim light, whereas, dry weight was measured after oven-drying the samples at 80°C for 48 h.

Osmotic Adjustment Groups
Osmotic adjustment was expressed as the difference between leaf OP100 of irrigated (at T1 moisture level) and stressed (at T3 and T4 moisture levels) plants. Based on OA capacity, the eight chickpea cultivars were separated into two OA groups, namely LOA (with low osmotic adjustment), having an OA value up to 0.35 MPa and HOA (with high osmotic adjustment), having an OA value greater than 0.35 MPa at the T4 stress level. The HOA group comprised of three chickpea cultivars (BG-329, BG-365 and BG-372), whereas the LOA group consisted of five chickpea cultivars (BG-384, BG-386, BG-1001, PUSA-256 and PUSA-267). The performance of the two groups of chickpea cultivars was assessed group-wise for all the parameters studied.

Statistical Analysis
Statistical analyses were performed assuming that the experiment was a split block design with irrigation levels arranged systematically in each replicate along the gradient of applied water and genotypes randomized in each replicate. All the parameters were subjected to analysis of variance (ANOVA). Means and standard errors were calculated according to standard statistical procedures, and Fischer's least significant difference (LSD) was used to test for the significance of the differences between means of varietal groups and moisture levels at P < 0.05 according to Gomez and Gomez (1984).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Leaf Water Relations Parameters
Progressively increasing water stress, as imposed by the line source, affected all leaf water relations parameters significantly (Table 1). Cultivars with high osmotic adjustment generally showed significantly distinct values of leaf water relation parameters. The LOA group failed to show significant differences between T1 and T3 moisture levels for OP at the early flowering stage and for OP100 at all stages. It also exhibited no significant differences between T3 and T4 stress levels for OP, OP100, and RWC at the early fruiting stage. However, differences between HOA and LOA cultivars were generally significant. Both WP and OP decreased (became more negative) progressively with increasing moisture stress and crop age and, therefore, the values were the lowest at the T4 moisture level at the early fruiting stage regardless of OA groups. Likewise, RWC decreased with increasing water stress and crop age, irrespective of OA groups. However, HOA cultivars invariably achieved significantly higher RWC values than LOA cultivars.


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  		Table 1. Effect of line source moisture levels and osmotic adjustment on leaf water relations parameters of two groups of chickpea cultivars differing in osmotic adjustment capacity.

 
The effect of moisture stress induced by decreasing WP on OP100 and RWC is shown in Fig. 2 . Both HOA and LOA cultivars showed progressive decrease in OP100 with decreasing WP. However, the HOA group showed significantly lower OP100 than the LOA group regardless of moisture levels and growth stages (Table 1). Further, OP100 as well as RWC was higher in HOA than LOA cultivars through the range of water potentials (Fig. 2). Figure 3 shows that RWC in LOA cultivars did not change with the decreasing OP100 as soil moisture stress progressed. However, HOA cultivars showed a gradual decrease in RWC with decreasing OP100, approaching almost a constant value of about 69% RWC at approximately –1.7 MPa OP100. There was maintained a more negative OP100 in HOA than LOA cultivars at comparable RWC levels (Table 1; Fig. 3).



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  		Fig. 2. Relationship of water potential with (A) osmotic potential at full turgor and (B) relative water content of low and high osmotic adjustment (OA) groups of chickpea cultivars. All data points in the figure represent mean values recorded at various growth stages.

 


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  		Fig. 3. Relationship of osmotic potential at full turgor with relative water content of low and high osmotic adjustment (OA) groups of chickpea cultivars. All data points in the figure represent mean values recorded at various growth stages. NS, nonsignificant (P < 0.05).

 
Osmotic Adjustment Capacity
Osmotic adjustment capacity of the chickpea cultivars increased with decreasing WP regardless of stress levels and growth stages. The HOA group showed a higher degree of OA accompanied with a greater decrease in WP at the T4 level compared with the T3 level at each growth stage. However, the magnitude of OA increased as the water deficit intensified as a result of decreasing WP with stage-wise advancing age of the crop. At the late flowering stage, values of WP and OA were not much different from those at the early flowering stage under the T3 or T4 stress level. On the other hand, at the early fruiting stage, the plants experienced the highest water stress, resulting in maximum OA (0.48 and 0.71 MPa) of HOA cultivars in the T3 and T4 levels at WP levels of –1.89 and –2.17 MPa ({Delta}WP = 15%), respectively (Table 2). LOA cultivars showed no difference in OA capacity at the T3 and T4 levels in spite of a {Delta}WP of 19%.


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  		Table 2. Effect of line source moisture levels and osmotic adjustment with reference to water potential of two groups of chickpea cultivars differing in osmotic adjustment capacity.

 
Seed Yield and Yield Parameters
Seed yield as well as yield parameters, viz. biomass, 500 seed weight, number of seeds per square meter and harvest index, were significantly affected by osmotic adjustment. With the exception of 500 seed weight and harvest index, all yield parameters and the seed yield was also significantly influenced by the water deficit that developed across the line source soil moisture gradient. Seed yield and biomass of HOA cultivars did not differ at the T3 and T4 moisture levels, while there was a significant decrease both in seed yield and biomass as stress increased from T3 to T4 levels in case of LOA cultivars. HOA cultivars performed better than LOA cultivars for seed yield as well as biomass at all stress levels, except at the T1 level at which both HOA and LOA groups gave statistically similar biomass. The HOA cultivars surpassed the LOA cultivars by 26 and 48% in seed yield and by 13 and 32% in biomass at the T3 and T4 stress levels, respectively. As to the number of seeds per square meter, values decreased significantly by increasing water deficit regardless of OA groups, with HOA cultivars giving 27, 47, and 51% higher values than those given by LOA cultivars at the T1, T3, and T4 moisture levels, respectively. In case of 500 seed weight and harvest index, there was no significant effect of moisture levels. However, HOA cultivars proved invariably superior to LOA ones in case of harvest index, whereas 500 seed weight was higher in LOA than HOA cultivars at all soil moisture levels (Table 3).


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  		Table 3. Effect of line source moisture levels and osmotic adjustment on yield parameters of two groups of chickpea cultivars differing in osmotic adjustment (OA) capacity.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Leaf Water Relations Parameters
At the late flowering stage, specifically at the T1 and T3 levels, values of WP, OP, and OP100 generally became less negative. This was due to a rainfall of 9.0 mm, which occurred just a few days before the sampling date at the late flowering stage during the ninth standard week of the season (Fig. 1). However, this rainfall did not ameliorate the stage-wise decrease in RWC in both OA groups (Table 1). Nevertheless, HOA cultivars maintained greater RWC as well as OP100 than LOA cultivars all through the range of water potentials (Fig. 2). In response to a decrease in OP100 due to increasing water deficit, WP decreased in both OA groups, but the decrease in LOA cultivars was much greater than in HOA cultivars. The LOA cultivars reached the lowest WP value (–2.10 MPa) at an OP100 of –1.03 MPa, whereas HOA cultivars reached the lowest water potential (–2.17 MPa) at an OP100 of –1.86 MPa (Table 1), indicating greater accumulation of solutes in HOA cultivars as compared to that in LOA ones at the respective (and more or less comparable) lowest water potentials. Moreover, the HOA cultivars maintained higher RWC than LOA cultivars with decreasing OP100, indicating that the greater accumulation of solutes (osmotic adjustment) in HOA cultivars under water deficit also accompanied the greater retention of RWC (Fig. 3). Morgan (1995) obtained similar results with wheat lines differing in osmoregulative capacity.

Osmotic Adjustment Capacity
As WP decreased progressively across the soil moisture gradient of the line source and growth stages, OA capacity of the two groups of chickpea cultivars, particularly that of HOA cultivars, increased with the increase in moisture stress. In fact, OA increases with the increase in stress, because it is a stress induced plant adaptation through accumulation of solutes (Turner and Jones, 1980; Morgan, 1984; Ludlow and Muchow, 1988). However, enhancement of OA capacity under water deficit, particularly with increasing crop age might, partly, be ascribed to the passive accumulation of solutes (Kikuta and Richter, 1986; Jensen et al., 1992). At the late flowering stage, OA as well as WP values were not different from those recorded at the early flowering stage, obviously, due to amelioration of the stress by a rainfall of 9 mm during the ninth week of the season, a few days before the sampling at the late flowering stage (Fig. 1). However, at the early fruiting stage, the water stress was intensified as shown by the decreasing WP, which resulted in the highest degree of OA in HOA cultivars both at T3 (0.48 MPa) and T4 (0.71 MPa) stress levels. Contrarily, the LOA cultivars, at stress levels T3 and T4, showed almost the same degree of OA, indicating a weak OA capacity of LOA cultivars (Table 2).

Seed Yield and Yield Parameters
Maximum seed yield (yield potential) in the present study was obtained in the T1 moisture level, which was considered as control because of its location nearest to the line source. Owing to the increasing water deficit, moisture levels T3 and T4 gave significantly lower seed yield than the T1 level regardless of OA groups. The HOA cultivars outyielded the LOA cultivars by 26 and 48% at the T3 and T4 moisture levels, respectively (Tables 2 and 3). These results agree with those obtained by Ludlow et al. (1990) and Santamaria et al. (1990) for grain sorghum, which showed 20 to 40% increases in grain yield due to OA as a result of simulated pre- and postanthesis drought. In the case of chickpea, Morgan et al. (1991) reported a positive association of seed yield with OA under water stress, showing a yield benefit of about 20% due to OA. A similar yield benefit due to OA has been reported in wheat (Morgan, 1995; Morgan and Condon, 1986; Chandrababu et al., 1999), pea (Rodriguez-Maribona et al., 1992), and pigeonpea (Subbarao et al., 2000a).

In the present study, the HOA cultivars outyielded the LOA cultivars by 18, 26, and 48% at the T1, T3, and T4 moisture levels, respectively (Table 3). That is, the greater the water stress, the greater was the yield benefit due to OA. Moreover, as compared with the control (T1), HOA and LOA cultivars showed a yield reduction of 20 and 26% at T3 and 24 and 41% at the T4 moisture levels, respectively, indicating that OA maintained higher yields in the water deficit environments. Similar conclusions have been drawn by Santamaria et al. (1990) and Ludlow et al. (1990) for grain sorghum lines differing in OA capacity.

As to the yield parameters, the number of seeds per square meter of HOA cultivars compared with LOA cultivars increased with increasing water stress, indicating the beneficial effect of OA on maintenance of seed number under water deficit. Similar results for chickpea have been published by Leport et al. (1999), who showed that seed yield reduction of 50 to 80% under water deficit occurred because of reduction in seed number and size, and suggested that OA might be important for a high harvest index and seed yield in chickpea. Our study also revealed that biomass and harvest index was significantly enhanced in HOA cultivars compared with LOA cultivars. However, 500 seed weight (a measure of grain size in terms of weight per grain) was significantly higher in LOA than in HOA cultivars. This could, presumably, be attributed to the substantial increase in seed number (21–34%) in HOA compared with LOA cultivars. Thus, in spite of the added advantage of better translocation of dry matter to the developing seeds (Ludlow et al., 1990), as evident by the harvest index (Table 3), HOA cultivars failed to provide heavier (larger) seeds because of OA induced substantially larger sink size (seed number). On the other hand, in LOA chickpea cultivars, where grain number was drastically decreased because of diminished OA capacity (Table 3), grain size (estimated as 500 grain weight) was significantly increased as compared with that in HOA cultivars. These results contrast with those obtained by Santamaria et al. (1990) and Ludlow et al. (1990) in the case of sorghum; they found that, in addition to grain number, grain size (weight per grain) was also significantly higher in HOA than LOA lines.

Such a favorable effect of OA on yield and its components could presumably be attributed to the well-established role of OA in maintaining turgor and plant growth under water deficit as observed in various crops (Jones and Turner, 1980; Wright and Smith, 1983; Morgan and Condon, 1986; Blum, 1989; Morgan, 1995; Grammatikopoulos, 1999). Flower and Ludlow (1987) have shown maintenance of leaf longevity in pigeonpea by preventing RWC from falling below a critical limit of about 32%. Recently, Subbarao et al. (2000b) have recorded a significant positive relationship between OA and RWC under water deficit that led to a significantly positive association between OA and leaf area duration, indicating maintenance of crop growth by OA under moisture deficit. That is, genotypes that adjusted osmotically, could maintain high photosynthetic rate because of more favorable leaf water status, which could, in turn, lead to higher crop growth rate and dry matter production, maintaining, ultimately, a higher productivity under drought. Thus, it could be inferred that maintenance of higher RWC because of OA at lowered water potentials in this study (Table 1) could maintain growth and metabolic activities in plants, including, photosynthesis and other physiological processes (Rawson, 1979; Ackerson et al., 1980; Ludlow et al., 1990; Subbarao et al., 2000b). Additionally, HOA cultivars could, presumably, translocate the preanthesis carbohydrate reserves to developing seeds more efficiently than LOA cultivars (Morgan and Condon, 1986; Santamaria et al., 1990) as is evident by their higher harvest index observed in this study (Table 3).

Finally, OA could play a role in maintenance of turgor and better water content of leaves, which might help the plant, under water deficit, to survive and maintain growth and metabolic activities so as to result, ultimately, in improved crop productivity.


   ACKNOWLEDGMENTS
 
The author is thankful to late Dr. S.K Sinha (Ex-director, IARI, New Delhi) for his valuable suggestions during the experimentation. Thanks are also due to the World Bank for the funding of the research project reported here.

Received for publication July 15, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 




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