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a Unitat de Fisiologia Vegetal, Facultat de Biologia, Universitat de Barcelona, Diagonal 645, 08028 Barcelona, Spain
b Area de Conreus Extensius, Centre UdL-IRTA, Alcalde Rovira Roure 191, 25198 Lleida, Spain
c Departamento de Biología Vegetal, Facultad de Ciencias, Universidad de Granada, 18071 Granada, Spain
* Corresponding author (josel{at}porthos.bio.ub.es)
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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) and yield was studied for durum wheat (Triticum turgidum L. var. durum) under Mediterranean conditions. A group of 25 genotypes was grown under contrasting water regimes in two regions of Spain during three years. The first objective was to determine the environmental factors responsible for the strong positive relationship previously observed between and yield across trials. Environmental factors tested were total water input (Wi), mean temperature, accumulated reference evapotranspiration (ET0), and the ratio Wi/ET0 during different periods of the crop cycle. Water input during grain filling was the variable most strongly correlated with grain and yield across all the trials, as well as across the subset of trials in northeastern Spain. In southeastern Spain, the most drought prone of the two regions, Wi from sowing to heading explained the most variation in grain and yield. The second objective was to study the effect of environment on the relationship between and yield across genotypes. No significant correlation was found for trials with a mean yield up to about 2000 kg ha-1, but the strength of the relationship increased sharply and attained significance in trials yielding 2500 kg ha-1. When yield above 2500 kg ha-1 the correlation between and yield remained relatively steady and positive, with an r value around 0.5. It is concluded that breeding to raise durum wheat yield in Mediterranean conditions could take advantage of selecting for higher only in relatively wet years or under supplementary irrigation.
Abbreviations: , grain carbon isotope discrimination • CIMMYT, Centro Internacional de Mejoramiento de Maíz y Trigo • DA, days from sowing to anthesis • DH, days from sowing to heading • ET0, accumulated reference evapotranspiration • ICARDA, International Center for Agricultural Research in the Dry Areas • NE-, northeastern • SE-, southeastern • Wi, total water input
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Carbon isotope discrimination (), when measured in plant dry matter, integrates transpiration efficiency, the ratio of net photosynthesis to water transpired, over the period during which the dry matter is assimilated, and transpiration efficiency being negatively related (Farquhar and Richards, 1984; Condon et al., 1990). On dry matter basis, has been proposed as a breeding criterion for increasing yield in temperate cereals and other crops, under either favorable or drought stress conditions. Although water status during growth dramatically affects yield and , a specific environmental variable responsible for the positive relationship usually found between and yield across growing conditions (i.e., trials) has not been unequivocally identified (Farquhar and Richards, 1984; Craufurd et al., 1991; Acevedo, 1993; Stewart et al., 1995; Araus et al., 1999a,b).
For breeding purposes, it is crucial to assess how the growing environment affects the relationship between and yield across genotypes (Acevedo, 1993; Condon and Richards, 1993; Richards, 1996; Araus et al., 1999b). Patterns in this relationship may be masked by phenological differences among genotypes that may affect yield and also , especially in drought-prone environments. For example, under Mediterranean conditions those genotypes with fewer days from sowing to heading or to anthesis show higher values (Craufurd et al., 1991; Richards and Condon, 1993; Richards, 1996; Araus et al., 1998) probably because they attain grain filling with more water in the soil, whereas the evapotranspirative demand is lower. Nevertheless, in bread wheat (Triticum aestivum L., Sayre et al., 1995) and durum wheat (Araus et al., 1998) large genotypic variability in , independent of phenology, has been reported.
This study was performed on a large collection of durum wheat genotypes cultivated in a wide range of Spain that differ in drought severity. The objective was to determine whether there is a common specific environmental variable which simultaneously affects the of mature kernels and yield. That information may indicate the basis of the widely reported strong positive relationship between yield and across trials. An additional objective was to assess how growing conditions affect the strength and sign (positive or negative) of the relationship between and yield across genotypes.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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, these genotypes were selected with a relatively narrow range of variability in the number of days from planting to heading, days to anthesis, and days to physiological maturity (a mean range of 7 and 6 d for heading and anthesis dates, respectively). The times from sowing to heading (DH) and anthesis (DA) were recorded when more than half the plants in a plot reached the stages 55 and 65 of Zadoks' scale (Zadoks et al., 1974), respectively. Thermal time was calculated in growing degree-days (GDD) by summing the daily values of mean temperature, with a base temperature of 0°C (Gallagher, 1979). Physiological maturity was recorded when most of the plants had reached Zadoks' stage 87, representing kernels in hard dough stage. Plots were harvested mechanically when the grain was ripe, yield (kg ha-1) expressed at a 100 g kg-1 moisture content (Table 2).
Environmental Parameters
For each trial, Wi was calculated as the sum of rainfall and irrigation (when applicable) for the following periods: sowing to heading, sowing to anthesis, sowing to maturity, heading to anthesis, heading to one week after anthesis, heading to maturity, anthesis to maturity (grain filling), and from one week after anthesis to maturity. Mean temperature and reference ET0 for the same periods were also assessed. ET0 was calculated from the mean maximal and minimal average temperatures of each period using the PC-program ETO (Sub-zero Evapotranspiration) (Snyder and Pruitt, 1991) version 1.04 (revised in February, 1994).
Carbon Isotope Discrimination
For each plot, a sample of about 2 g of mature kernels was oven dried and finely ground (mesh diameter of 0.5 mm). The 13C/12C ratio of samples was subsequently determined by mass spectrometry at the Serveis Científico-Tècnics de la Universitat de Barcelona, Spain. Samples of 0.7 to 0.9 mg were combusted in an elemental analyzer (EA1108, Series 1, Carlo Erba Instrumentazione, Milan, Italy) and the 13C/12C ratio was measured with an isotope ratio mass spectrometer (Delta C, Finnigan Mat, Bremen, Germany) operated in continuous flow mode. A system check for elemental analyses was achieved with an interspersed working standard of atropine. Stable carbon isotope composition was expressed as 
13C values (Farquhar et al., 1989), where 13C(
) = [(R sample/R standard)-1] x 1000, and R is the 13C/12C ratio. Secondary standards of graphite, sucrose, and polyethylene foil (IAEA, Vienna, Austria) calibrated against Peedee belemnite (PDB) carbonate were used for comparison. The accuracy of the 13C measurements was ±0.1. Following Farquhar et al. (1989), was further calculated from 13C as = (a - p)/(1 + p), where a and p refer to air and plant, respectively. On the PDB scale, free atmospheric CO2, a, has a current composition of approximately -8 (Farquhar et al., 1989).
Statistical Analysis
Analyses were done with the SAS-STAT package (SAS Institute Inc., 1996). An analysis of variance was performed for grain yield and , considering days from sowing to heading or from sowing to anthesis as the covariant. Means of trials for yield and were compared by the LSD test at P = 0.05. Stepwise discriminant analysis was used to ascertain the relationship between either or grain yield as the dependent variable and three different periods of the crop cycle (sowing to heading, heading to anthesis and anthesis to maturity) for each environmental parameter as the independent variables. The relationship between Pearson's correlation coefficients of individual trials and mean grain yield was fitted by Table Curve (Jandel Co., 1994).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The effect of environment, understood as the combination of region and water regime, on grain yield and of grain was much higher than that of genotypic variability (Table 3). Also, DH had a strong effect on yield. Although variation in phenology was limited within trials, DH probably also reflects an environmental effect as the trials differed dramatically in DH (Table 2). Therefore, environmental conditions were responsible by far for most of the variability observed in yield and . The main environmental factor affecting yield and was water regime, rainfed or irrigated, but the interaction between year and region also had a strong affect on . Grain yield was doubled and was 2.5 higher in irrigated than in rainfed trials in NE Spain and 64% and 1.6 higher, respectively, in SE-Spain trials (Table 2).
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and Yield across Trials values of mature kernels and grain yield were strongly (P < 0.001) and positively correlated across all the trials (Fig. 1). Correlations between these traits in trials across either NE or SE Spain were similar in slope. To ascertain the basis of these relationships, Pearson's correlation coefficients were calculated across the 12 trials between these traits and several environmental parameters evaluated during the crop cycle (Table 4) plus DH and DA, these last being nonsignificant at the P = 0.05 level (DH, r = 0.51 and r = 0.14; DA, r = 0.49 and r = 0.11 for yield and , respectively). The strongest relationships observed with either yield or were those that involved Wi, for the whole crop cycle or just from the last part of the cycle. The Wi/ET0 ratio for the complete crop cycle, between heading and maturity, or only during grain filling, was also significantly correlated with yield and . For the interval from sowing to heading, Wi and Wi/ET0 showed much weaker relationships with yield and . In general, mean temperature and accumulated evapotranspiration correlated less strongly with yield and regardless of the stage of the crop cycle. Significant relationships of either Wi or Wi/ET0 with yield and were linear (Fig. 2 and Fig. 3).
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. The combination of Wi or Wi/ET0 for the three crop cycle periods explained about 70% of the total variability in yield and across the 12 trials and about 90% across the six trials in NE and SE Spain separately (Table 5). Water input or Wi/ET0 from anthesis to maturity were the independent variables selected first in the stepwise analysis for the whole set of trials and the subset of NE Spain. In the case of SE Spain, however, Wi or Wi/ET0 from sowing to heading were the first choices in the analysis (Table 5), and were also linearly related with yield and (Fig. 3). Moreover, Wi and Wi/ET0, either from heading to maturity (Fig. 3), or anthesis to maturity, were correlated with yield and only for NE Spain. The slope of all these relationships tended to be steeper in NE than in SE Spain.
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and Yield within Trials and yield, the set of genotypes chosen in this study had a relatively small variability in DH and DA within each trial. Analysis of variance for and yield using DH or DA as covariables confirmed that the effect of genotype on these traits remained highly significant after subtracting the effect of phenology expressed as DH or DA (Table 3). Genotype effects, although only accounted for about 2% of total variability in both yield and , were highly significant. On the other hand, these phenological traits also had a highly significant effect, particularly on yield (Table 3). However, the effect of phenology in the analysis of variance may have incorporated an environmental bias. Moreover, no significant correlation across genotypes was observed between DH or DA and either or grain yield in any of the trials.
For the 12 trials, mean trial yield was plotted against the Pearson's correlation coefficient of the phenotypic relationship between and yield within the same trial (Fig. 4a). This coefficient was positive in all the trials. The relationship fitted an asymptotic function (P < 0.01). Thus, trials yielding around 2000 kg ha-1 showed no significant (P < 0.05) relationships, but coefficients of correlation increased sharply to attain significance for trials yielding about 2500 kg ha-1. Above this yield, they remained steady at around 0.5, except for a trial under irrigation in SE Spain with r = 0.69. Many of these relationships remained almost unchanged after subtracting the effect of DH (Fig. 4b), although the correlation coefficient in the highest yielding trial was greatly decreased when the effect of DH was removed. The slope of the linear regression between yield and showed the same pattern of changes as the growing conditions of the trials improved. It increased from values near zero in the lowest yielding trial (SE Spain rainfed 1997) (Table 2) to around 1000 kg ha-1 per 1 increase in , for trials that yielded about 2500 kg ha-1. Above these yields, slope values remained steady (Fig. 5a). Moreover, the slopes of these relationships were unaffected when the effect of DH was subtracted (Fig. 5b). From the set of 25 genotypes two groups of five genotypes each, having the extreme values of at the two most productive trials were selected. Further, for each trial the percentage in yield as a result of picking based on these two groups was calculated as [mean yield high group – mean yield low group/mean yield low group] x 100. The average yield differential showed a similar pattern to that on Fig. 4 (but P < 0.10). Thus, the high group consistently showed a higher yield (about 10%) for trials yielding about 2500 kg ha-1 and above.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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and Yield across Trials across trials. The lack of a stronger correlation between crop phenology and yield and its absence for could be due to the dependence of DH and DA on temperature (Hay, 1999 and references herein). Indeed, mean temperature from sowing to heading and from sowing to anthesis was negatively correlated (P < 0.05) with yield but not with . In our study, differences in DH and DA between trials were mainly caused by regional differences in temperature. Thus, the higher temperatures in the trials in SE Spain caused an accelerated accumulation of growing-degree days and therefore a shorter DH and DA than in those in NE Spain.
Role of Environmental Variables in the Relationships between and Yield across Trials
Our results show that Wi for the whole crop cycle and specifically that comprising the part from heading onwards was the main environmental variable affecting grain yield and . Sharing a common environmental variable would explain the strong positive relationship between grain yield and across trials (Fig. 1). Similar results have been reported in durum wheat (Araus et al., 1999b) and other cereals (Condon et al., 1987; Romagosa and Araus, 1991; Acevedo, 1993).
Previous reports on barley (Hordeum vulgare L.) and durum wheat under Mediterranean conditions have found a strong dependence of grain on Wi during the later stages (from heading and anthesis to maturity) of the crop cycle (Araus et al., 1999a). In the present study, Wi explained the differences in across growing environments better than ET0 or even the ratio Wi/ET0 (Table 4) as well as other related variables such as ET0–Wi (data not shown). The strength of the relationships of Wi/ET0 with yield and was almost comparable to that obtained with Wi. However, because ET0 alone related poorly to yield and , the good performance of Wi/ET0 seemed to be due only to the weight of Wi in this ratio. In fact, the range of variability in accumulated ET0 across environments was smaller than that for Wi. Stewart et al. (1995), working with wild plant communities along a natural rainfall gradient, also concluded that Wi was the environmental variable best related to carbon isotope composition. Most of the studies on this topic, however, deal with tree species and not annual plants (see references below). In general, these studies are not conclusive in terms of agreement on a common, single environmental variable. They relate to rainfall amounts, evapotranspiration, the Wi/ET0 ratio, soil water status, or different drought stress indices either at the seasonal level or during a particular period of the growing season (Francey and Farquhar, 1982; Freyer and Belacy, 1983; Leavitt and Long, 1989; Dupouey et al., 1993; Guehl et al., 1995; Korol et al., 1999; Moore-Darrin et al., 1999). Water input during grain filling was not only the variable best correlated with yield and for the whole set of trials (Table 4), but also for the subset of NE Spain (Fig. 3). However, whereas no significant correlations were attained, in SE Spain, Wi from the first part of the crop cycle (sowing to heading) tended to be the variable best related to yield and (Fig. 3). On the other hand, no significant correlation was attained between Wi from sowing to heading and yield or in NE-Spain trials (Fig. 3). These differences between regions may have an environmental basis. The Mediterranean environment of SE Spain is characterized by more severe drought stress during the last part of the crop cycle than is that of NE Spain (Table 6). The presence of a higher level of drought stress during grain filling in SE-Spain trials is further supported by the generally lower 1000-kernel weight in SE than in NE Spain (Table 2). Under the growing conditions of SE Spain, grain yield and are defined earlier in the crop cycle because photoassimilates produced before anthesis may play a major role not only in defining the total number of grains per unit land, but also in the filling of these grains (Slafer and Araus, 1998; Royo et al., 1999). Interestingly, for two of the three years studied, the for the rainfed site in SE Spain was higher than in that in the north in spite of the lower yield and greater drought in the former location (Table 2).
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suggest that for the same amount of water input, a higher grain yield and were attained in NE Spain. These regional differences could initially be explained in terms of a higher ET0 or vapor-pressure deficit in the trials done in the south (Table 6) or by differences in soil water-holding capacity and distinct seasonal patterns of rainfall. Canopy temperature depression at anthesis measured by infrared thermometry was about 5°C higher in SE than in NE Spain regardless of the water regime assayed (Royo et al., 2002). This observation suggests higher transpiration rates in the southern trials, irrespective of whether stomatal conductance was lower than in the northern trials as can be inferred from the lower values of SE Spain (Table 2). Thus, Condon et al. (1992) reported a decrease in in wheat which was attributed to stomatal closure in response to increasing VPD. However, complementary explanations may be sought because the relationships between the Wi/ET0 ratio and grain yield or in NE and SE Spain showed the same pattern as those with Wi illustrated in Fig. 3. A possible explanation could be a lower water holding capacity of the sandy soils in SE Spain (Table 1). Decreased soil water availability results in lower values of in cereals (Farquhar and Richards, 1984; Hubick and Farquhar, 1989; Condon et al., 1992) primarily because of the decrease in stomatal conductance. Other soil characteristics, such as soil compaction, may also affect in wheat (Masle and Farquhar, 1988).
Role of Environment on the Relationships between and Yield within Trials
For all the trials, the slope of the regression between and grain yield remained positive. In fact, for wheat and other cereals, is frequently positively correlated with grain yield and/or total biomass not only under well-irrigated but also under rainfed conditions (Condon et al., 1987; Romagosa and Araus, 1991; Kirda et al., 1992; Araus et al., 1993, 1998; Merah et al., 2002; Morgan et al., 1993; Sayre et al., 1995). Most of these (and other studies reporting positive relationships) were conducted in Mediterranean or similar environments where there is strong reliance on "within-season" rainfall (Condon et al., 2002). However, unlike the results of Araus et al. (1998) in durum wheat, in the poor-yielding environments of our study (about 2000 kg ha-1), the correlation between grain and yield across genotypes was not significant, with correlation coefficients for two rainfed trials from SE Spain close to zero. Such a relationship attained significance in trials when yield was about 2500 kg ha-1 and greater. In addition, the slope of the regression, which represents the responsiveness of yield across genotypes to changes in within a particular environment, increased to a maximum in trials yielding about 2500 kg ha-1, above which it remained steady with values comparable to those reported before in durum wheat (Araus et al., 1997b). An increase in the strength of this positive relationship as the growing conditions improve has also been reported for barley (Voltas et al., 1999) under Mediterranean conditions.
Carbon isotope discrimination has largely been recommended as a selection criterion for transpiration efficiency (Farquhar and Richards, 1984), which holds true when the amount of captured water is the same for all genotypes. A negative relationship between and either biomass or yield can then be expected (Slafer and Araus, 1998; Araus et al., 2002). This is frequently the case in pot studies where all the water provided is being used by genotypes (Richards, 1996; Slafer and Araus, 1998) or for Mediterranean field trials with very low water input, as is sometimes reported in barley (Romagosa and Araus, 1991; Voltas et al., 1999). It is also the case for wheat and other cereals in water limited environments where crop growth is most dependent on soil moisture stored from rain that falls outside the main crop growth phase, such as in the northern Australian wheat belt (Condon et al., 2002; Richards et al., 2002). Reports of a negative relationship in stressed Mediterranean environments between and yield are less frequent in wheat than in barley. This is perhaps associated with the agronomical observation that the crossover for the genotype x environment interaction seems to be at higher yields (i.e., better environments) for barley (2000–2500 kg ha-1) (Ceccarelli and Grando, 1991) than for wheat (1000–1500 kg ha-1) (Laing and Fischer, 1977; Fischer, 1993). Barley is reported to have a more extensive root system than durum wheat and, consequently a higher capacity of water extraction from the soil (López-Castañeda and Richards, 1994). Therefore, in arid environments, a higher yield in barley would be associated with higher transpiration efficiency, and thus a lower , because all the available water is extracted by the crop.
For trials with moderate stress, when genotypes may show their distinct ability to capture water, the positive effect of a higher transpiration efficiency is probably overridden by greater transpiration rate and water use. Genotypes that use more water keep their stomata more open and therefore discriminate more against 13C than those that use less water (Condon et al., 1987; Richards and Condon, 1993; Turner, 1993; Richards, 1996) while showing higher photosynthesis and yield. In other words, as the growing conditions of trials improve, positive relationships between and grain yield are attained because indirectly reflects differences in water use in addition to those in transpiration efficiency. In fact, water use and transpiration efficiency, the two variables determining crop biomass in Passioura's equation (Passioura, 1977), would not behave as independent traits.
Under favorable growing conditions, positive associations between yield and have also been reported for several cereals (Condon et al., 1987; Romagosa and Araus, 1991; Richards, 1996; Araus et al., 1998; Voltas et al., 1999). This arises when the highest yielding genotypes have a lower assimilation capacity per unit area than the lowest yielding lines (Araus et al., 1997a, 1997b) or when lines with a higher stomatal conductance have the highest yields, which seems to be the most frequent situation (Richards, 2000). For an historic set of bread wheats, released through several decades and bred at CIMMYT, progress in potential yield was associated with changes in gas exchange characteristics of photosynthesis and transpiration (Fischer et al., 1998). Among these characteristics, correlation with leaf conductance was strongest and was also positively associated with yield progress. Similar results were reported by Richards (2000) and Barbour et al. (2000). Several explanations have been proposed for the positive relationship between stomatal conductance and yield in this CIMMYT set: decreased stomatal sensitivity to vapor-pressure deficit or to subtle water stress, extra cooling particularly at warmer temperatures, or increased sink strength (Fischer et al., 1998, Richards, 2000). Whatever the reason, higher stomatal conductance leads to more photosynthesis and assimilation.
There are, however, reports in barley of a strong positive relationship between grain and yield in the very dry rainfed conditions of northern Syria, whereas negative, although weaker, relationships were recorded in the very productive environments of Cambridge, England (Austin et al., 1990; Acevedo, 1993). Differences in phenology may also explain the positive relationships between grain and yield within Mediterranean rainfed environments (Richards, 1996; Araus et al., 1998; Condon et al., 2002). However, this factor was limited in our study. Thus, the relationship between and yield were positive and still significant for most of the trials after subtracting the effect of DH (Fig. 4).
Implications for Breeding in Mediterranean Conditions
It has been suggested that positive relationships between and yield are attained when the differential ability of the genotypes for taking up available water is the main determinant of differential yields (Richards, 1996; Slafer et al., 1999) even when another factors discussed above and elsewhere (Condon et al., 2002) could also account. The relationship is expected to be negative when the main factor determining genotypic differences in yield is transpiration efficiency and thus its translation into agronomic terms, water use efficiency, the ratio of biomass accumulated to water transpired. Therefore, in the Mediterranean environments of this study, the rainfed conditions may have resulted in the expression of both abilities simultaneously. Thus, some cultivars give improved yields because of their higher water use efficiency while others perform better because of their differential ability to use more water (beyond differences in crop phenology), and therefore the relationship between and yield across genotypes was weak, regardless of whether it was positive or negative. Additionally, a large contribution of preanthesis reserves to the filling of grains (Blum, 1988; Loss and Siddique, 1994), thereby affecting the isotope signature of mature kernels, may also explain the weakness of this relationship in more stressed environments.
Breeding to raise yield could take advantage of selecting for higher only in relatively wet years (or under supplementary irrigation), but selection for this trait should not take place in the drier years under rainfed conditions, particularly in SE Spain.
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ACKNOWLEDGMENTS |
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Received for publication February 5, 2002.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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13C record as derived from 56 pinyon trees at 14 sites in the southwestern United States. Radiocarbon 31:469–474.This article has been cited by other articles:
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  R. C. Johnson, A. A. Hopkins, and M. A. Evans Carbon Isotope Discrimination, Selection Response, and Forage Production of Tall Fescue in Contrasting Environments Crop Sci., May 1, 2008; 48(3): 1048 - 1054. [Abstract] [Full Text] [PDF]
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 C. Royo, V. Martos, A. Ramdani, D. Villegas, Y. Rharrabti, and L. F. Garcia del Moral Changes in Yield and Carbon Isotope Discrimination of Italian and Spanish Durum Wheat during the 20th Century Agron. J., February 26, 2008; 100(2): 352 - 360. [Abstract] [Full Text] [PDF]
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Ma. R. Laza, M. Kondo, O. Ideta, E. Barlaan, and T. Imbe Identification of Quantitative Trait Loci for {delta}13C and Productivity in Irrigated Lowland Rice Crop Sci., February 24, 2006; 46(2): 763 - 773. [Abstract] [Full Text] [PDF]
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A. G. Condon, R. A. Richards, G. J. Rebetzke, and G. D. Farquhar Breeding for high water-use efficiency J. Exp. Bot., November 1, 2004; 55(407): 2447 - 2460. [Abstract] [Full Text] [PDF]
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