Journal of Experimental Botany, Vol. 52, No. 362, pp. 1857-1864,
September 1, 2001
© 2001 Oxford University Press
Original Papers |
QTL analysis of photosynthesis and water status traits in sunflower (Helianthus annuus L.) under greenhouse conditions
Laboratoire de Biotechnologie et Amélioration des Plantes, INP/ENSAT, Pôle de Biotechnologie Végétale, Chemin de Borde-Rouge, Auzeville, BP107, F-31326 Castanet-Tolosan cedex, France
Received 2 March 2001; Accepted 17 May 2001
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Abstract |
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The identification of QTL for several physiological traits in sunflower is described. Traits related to photosynthesis (leaf chlorophyll concentration, net photosynthesis and internal CO2 concentration) and water status (stomatal conductance, transpiration, predawn leaf water potential, and relative water content) were evaluated in a population of recombinant inbred lines under greenhouse conditions. Narrow-sense heritabilities were low to average. Using an AFLP linkage map, 19 QTL were detected explaining 8.8–62.9% of the phenotypic variance for each trait. Among these, two major QTL for net photosynthesis were identified on linkage group IX. One QTL co-location was found on linkage group VIII for stomatal movements and water status. Coincident locations for QTL regulating photosynthesis, transpiration and leaf water potential were described on linkage group XIV. These results lead to the first description of the organization of genomic regions related to yield in sunflower.
Key words: Helianthus annuus, recombinant inbred lines, gas exchange, water potential, chlorophyll content.
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Introduction |
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Sunflower (Helianthus annuus L.) is an important oil seed crop which can also be a valuable source of protein. The oil production, a yield parameter, is positively correlated with leaf area which determines the photosynthetic capacity of sunflower. During anthesis, the maintenance of active leaf area is a requirement for achieving a high seed yield (Rawson et al., 1980
). Sunflower has a C3 carbon metabolism. However, its photosynthetic potential is high, similar to maize, i.e. 25–32 µmol CO2 fixed m-2 s-1 of leaf (Fock et al., 1979; Potter and Breen, 1980). This capacity is due to the presence of stomates on both leaf surfaces, permeability of tissues for CO2 diffusion and an intense Rubisco activity (Delanay and Walker, 1978; Ranty and Cavalié, 1982). Photosynthesis in sunflower leaves reaches high levels despite important transpiration rates (Rawson and Constable, 1980). The internal water behaviour of sunflower is complex: sunflower has a strong capacity to extract and conduct water, however, water consumption is high and transpiration rates can reach 22 mmol H2O m-2 s-1 when vapour pressure deficit is very severe (Rawson et al., 1980).
In nature, the vast majority of physiological traits are quantitative. Quantitative genetics can describe the characteristics of continuous phenotypic distributions and estimate the number of loci affecting a trait, the average gene action and the degree of interaction between quantitative trait loci (QTL) and environment (Tanksley, 1993). Genetic determinism of photosynthesis has been estimated in wheat (Ecochard et al., 1988; Simon, 1994), maize (Rocher et al., 1989) and pea (Hobbs and Mahon, 1985). A large genetic variability concerning the amount of Rubisco and the carboxylase activity of this enzyme in tetraploid wheat has been demonstrated previously (Nicco et al., 1993). In wheat and pea, photosynthetic activity seems to be controlled predominantly by genes acting additively (Hobbs and Mahon, 1985; Simon, 1994). Chlorophyll content, stomatal resistance and Rubisco activity are also governed by a preponderance of additive effects in pea (Hobbs and Mahon, 1985). The relations between photosynthesis and water traits, in particular during water stress, are well described in sunflower (Conroy et al., 1988; Fredeen et al., 1991; Hirasawa et al., 1995; Guidi and Soldatini, 1997; Pankovic et al., 1999). However, only a few papers reported the genetic determinism of these traits: Virgona et al. showed a significant genotypic variation in transpiration efficiency (ratio of carbon accumulation to transpiration) (Virgona et al., 1990); Jamaux et al. identified specific molecular markers of osmotic adjustment in sunflower (Jamaux et al., 1997).
The basis of QTL detection is to associate variation of the measured phenotype with marker genotypes in a natural or controlled segregating population by statistical methods. Because of their direct interest for plant breeding, QTL for agronomic traits like crop yield are the most frequently studied (Xiao et al., 1996; Quarrie et al., 1997; Foolad and Chen, 1999; Tozlu et al., 1999). In recent years, QTL for a range of physiological traits have been identified: abscisic acid, Na+ and Cl- accumulation (Quarrie et al., 1997); osmotic adjustment (Lilley et al., 1996; Zhang et al., 1999); heat shock proteins synthesis (Ottaviano et al., 1991; Jorgensen and Nguyen, 1995); protein and starch concentration (Goldman et al., 1993); the flavonoid metabolic pathway (Byrne et al., 1996; McMullen et al., 1996), and enzymes activities like vacuole invertase (Pelleschi et al., 1999; Prioul et al., 1999). However until now, QTL of photosynthetic processes and their putative relationships with water status (for example, leaf turgescence) was never reported.
The aim of the present study was to evaluate the inheritance of photosynthesis and water status traits and to identify markers linked to loci controlling those traits in recombinant inbred lines under non-stress greenhouse conditions. These RIL are particularly well suited for physiological studies as they can be replicated in a variety of environments and conditions (Potter and Breen, 1980; Wiebold et al., 1981; Tanksley, 1993; Causse et al., 1995; Lilley et al., 1996) and they were used to map AFLP (Flores Berrios et al., 2000).
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Materials and methods |
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Plant material and experimental conditions
During the winter of 1999, a population of 99 RIL of sunflower and their parents (PAC2 and RHA266) were grown in the greenhouse under controlled conditions. Three plants per genotype were cultivated and randomly allocated at the beginning of the experiment. Plants were individually grown in 3.0 l pots containing a mixture of clay (8%) and compost. Temperature was set at a minimum of 20 °C for the 16 h light period and 14 °C for the 8 h dark period. The maximum air temperature was maintained under 30 °C by opening panels. Relative humidity (humidors) and irradiance (natural light and fluorescent lamps) were maintained to a minimum of respectively 40% and 250 µmol m-2 s-1. Plants were watered daily after measurements with excess solution to maintain soil water content near field capacity in each pot. Nutrients were supplied using Soluplant 2 g l-1 (N-P-K:18-18-18 and oligoelements) once a day. In accordance with flowering time, the experiment was conducted from 17 February until 3 March 1999 and 40–60 plants were studied for all traits each day for 6 d when the inflorescence began to open (stage R4; Scheiter and Miller, 1981
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Physiological traits
Net CO2 fixation was measured on the last two fully expanded leaves of three plants per genotype with a closed gas exchange system (Li-Cor 6200, Li-Cor Inc, Lincoln, NE, USA) by infrared analyser. About 100 cm2 of leaf area was clamped in a 4.0 l chamber and placed under a fluorescent lamp (OSRAM, 1000 W) to obtain near to 500 µmol m-2 s-1 photosynthetic photon flux in the chamber. The relative humidity of chamber was 70%. Leaf temperature varied between 18–22 °C. Measurements were done between 11 h and 13 h with an initial CO2 concentration about 350 µmol mol-1. The measured parameters were: net photosynthetic rate (Pho, µmol m-2s-1), transpiration rate (Tr, mmol m-2s-1), stomatal conductance (sco, mol H2O m-2s-1) and intercellular CO2 concentration (ic, µmol mol-1).
Leaf chlorophyll content (Chl, g cm-2) was evaluated by light absorbance in the red and infrared with a chlorophyll meter (SPAD-502, Minolta France SA, Carrières-sur-Seine, France; Wood et al., 1993). Measurements were performed on the two leaves per plant which had previously been used for gas exchange evaluation (Li-Cor 6200). A minimum of six measurements were done per leaf, about 3 cm away from the leaf side.
The predawn leaf water potential (Pot, MPa) was measured 2 h before sunrise, on plants that were used for gas exchange evaluation the previous day. During the night, water status in plants is equilibrated: before sunrise, all the leaves show a similar leaf water potential. POT was monitored on one leaf per plant with a pressure chamber (Model 3000, Soil Moisture Equipment Corp., Santa Barbara, CA, USA; Scholander et al., 1964).
Relative water content (RWC, %) was calculated using RWC=100x(Wf-Wd)/(Wt-Wd). Fresh weight (Wf) was determined between 15 h and 17 h from one leaf of the last fully expanded leaves used for gas exchange and chlorophyll measurements. Turgescent weight (Wt) was determined from the same leaf incubated for 4 h at 4 °C in a water bath in a saturated humidity atmosphere (Turner, 1988). Dry weight (Wd) was measured after dehydration of the leaves for 24 h at 80 °C. Relative water content was calculated on one leaf per plant.
Mapping population and QTL detection
Because of the polymorphism of the parents, the PAC2 xRHA266 recombinant inbred lines are a core population of sunflower. A previously described linkage map for these recombinant inbred lines (Flores Berrios et al., 2000) was used to conduct the analysis. Briefly, a total of 99 RIL were mapped with 333 AFLP markers. Among those, 92 RIL were used for QTL detection. The experiment was designed as a randomized complete block with three replicates (3 plants per genotype). Data show non-normality distribution and transformations were as follows: square root (CHl and PHO), natural logarithm (TR and POT) or arcsin (RWC). Analysis of variance and Pearson correlation were conducted using SPSS 10.0. Genetic and environmental effects were tested by F-test. Narrow-sense heritabilities were calculated using least square estimates of the genetic parameters (Kearsey and Pooni, 1996).
QTL for the seven physiological traits (chlorophyll concentration, net photosynthesis, transpiration, stomatal conductance, leaf intercellular CO2 concentration, leaf water potential, and relative water content) were resolved by composite interval mapping. QTL Cartographer version 1.13 model 6 was used with 5–12 markers to control for the genetic background on a 10 cm window (Basten et al., 1999). Five markers for PHO and RWC traits, seven markers for CHL, 10 markers for POT, SCO and IC, and 12 markers for TR, respectively, were selected. The experiment threshold level for the test statistic was determined by a permutation test of 1000 permutations at a significance level 
=5%. The individual QTL effects (R2) were estimated as the percentage of the variance explained by the QTL conditioned on the background markers. QTL intervals were determined using the LOD-1 unit rank on the LOD curve.
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Results |
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Quantitative variation and heritabilities
All the trait distributions were continuous, showing their quantitative nature. The descriptive information for seven physiological traits is shown in Table 1
. The mean value of net photosynthesis was 17.3 µmol CO2 fixed m-2 s-1. This activity appeared low in comparison with previous studies which reported activity ranging from 20 to 40 µmol m-2 s-1 (Sims et al., 1999), but it could be explained by culture conditions: greenhouse conditions and winter culture (implying low irradiance). The mean value of stomatal conductance was 1.01 mol H2O m-2 s-1 which is in accordance with values obtained by Jamaux et al. for control plants (Jamaux et al., 1997). The mean values of predawn leaf water potential and relative water content (–0.51 MPa and 89.9%, respectively) indicated that plants were non-water-stressed according to the water status of sunflower in the greenhouse conditions reported earlier (Maury et al., 2000). The correlation coefficients among traits are presented in Table 2. The direction (+ or -) and degree of correlation were consistent with previous observations between transpiration and stomatal conductance (0.687**), leaf intercellular CO2 concentration and stomatal conductance (0.232*) and net photosynthesis and chlorophyll concentration (0.270*). Net photosynthesis and transpiration were positively correlated (0.669**). Leaf water potential and transpiration, and POT and stomatal conductance were negatively correlated (-0.302** and -0.347**, respectively). It is known that stomatal conductance is dependent of the leaf water potential (Fetcher et al., 1993). However, there is no correlation between RWC and the other traits. In the culture conditions used in this study (irrigated and winter conditions), RWC appeared to be constant during the day and did not depend on the other traits.
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The mean values of RIL were intermediate between the two parents for all traits. Some RIL had more extreme values than the parents showing a transgressive segregation. Analysis of variance revealed significant differences between the RIL for all the traits measured, indicating that the traits related to photosynthetic activity and water status are genotype-dependent in sunflower. These results are in accordance with those described by Virgona et al. who showed that the genotypic variation in the ratio of carbon accumulation to transpiration was significant in sunflower (Virgona et al., 1990
). Narrow-sense heritabilities were calculated for all traits measured (Table 1
). Inheritance was low for stomatal conductance (0.26), intercellular CO2 concentration (0.26), leaf water potential (0.25), and relative water content (0.22). These results were confirmed by the coefficient of variation (CV). Chlorophyll concentration, net photosynthesis and transpiration were more heritable with values ranging from 0.37 to 0.57. The coefficient of variation was low for chlorophyll rate, stomatal conductance, internal CO2 concentration, leaf water potential, and relative water content, but higher for net photosynthesis. The coefficient of variation for transpiration was 45.8% indicating that the low heritability observed for this trait may be due to data dispersion. Photosynthetic activity and water-related traits in sunflower seem to be moderately heritable.
QTL for photosynthesis and water status related traits
A total of 19 QTL on 12 linkage groups were detected for the seven physiological traits studied. Map positions and effects of these QTL are summarized in Table 3. The total proportion of the variance explained by the QTL ranged from 9.8% to 62.9% depending on the trait. Three QTL involved in net photosynthesis were identified: pho9.1 and pho9.2 on linkage group IX and pho14.1 on linkage group XIV. These loci explained altogether 62.9% of the genetic variance in this trait. The locus pho9.1 (31.5%) was the most explicit locus. The loci pho9.1 and pho9.2 had additive opposite effects. The chlorophyll content is linked to four QTL, located on linkage groups V, VIII, X, and XVIII, explaining 53% of the variation in the trait. Four chromosomal regions were associated with stomatal movements: sco3.1, sco8.1, sco16.1, and sco17.1, respectively, on linkage groups III, VIII, XVI, and XVII. These QTL explained 61.9% of the variance of the stomatal conductance. The locus sco3.1, had a positive additive effect. Three QTL were detected for transpiration on groups IV, XI and XIV and accounted for 44.3% of the phenotypic variance. For internal leaf CO2 concentration, one QTL was detected on linkage group XI with negative additive effect explaining 15.8% of the genetic variance. Four putative loci associated with water status of sunflower were also identified, based on the evaluation of two different key traits: leaf water potential and relative water content. Three QTL explaining 34.1% of the genetic variation of leaf water potential were identified on linkage group VIII (pot8.1), X (pot10.1) and XIV (pot 14.1). The loci pot10.1 and pot14.1 had negative additive effects whereas pot8.1 had a positive effect. Only one QTL was detected for relative water content on linkage group V (rwc 5.1). A lower R2 (9.8%) was obtained for this QTL, which was also the less heritable trait. So, it appears that undetected regions of the genome control genetic variation of leaf water potential and relative water content.
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Co-locations between QTL for photosynthetic activity, stomatal movements and water status are described on linkage groups V, VIII and XIV (Fig. 1
). One coincidental location corresponding to stomatal movement and water status was observed on linkage group VIII (sco8.1 and pot8.1). This co-location is supported by the negative correlation between stomatal conductance and leaf water potential (Table 2). Likewise, an unexpected co-location occurred on chromosome V between chlorophyll rate (chl5.1) and leaf water status (rwc5.1). At least a 32 cM genomic region on linkage group XIV showed three QTL involved in water potential (pot14.1), transpiration (tr14.1) and photosynthetic activity (pho14.1). This result is in accordance with the correlation coefficients between net photosynthesis and transpiration, and leaf water potential and transpiration.
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Discussion |
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TopAbstractIntroductionMaterials and methodsResultsDiscussionReferences |
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Significant genetic variability for leaf chlorophyll concentration, net photosynthesis, stomatal movements (measured by conductance and transpiration), and water status (estimated by leaf water potential and relative water content) was observed in recombinant inbred lines of sunflower. Narrow-sense heritability values were low to medium making breeding for these traits difficult by conventional techniques. Only a few data have been published on the inheritance of photosynthesis and water status in other crops. Broad-sense heritability for apparent photosynthesis ranged from 0.36 to 0.57 in soybean and from 0.29 to 0.42 in wheat (Wiebold et al., 1981
; Simon, 1994). Teulat et al. showed that the heritabilities of relative water content decreased with the environmental effect in barley and ranged from 0.04 in irrigated treatments to 0.44 in water-stress conditions (Teulat et al., 1998). The water status parameters are strongly influenced by environmental effects and are usually measured to evaluate the water stress level of the plant. Relative water content and leaf water potential are commonly used as environmental covariables; it is thus unexpected that they appear to be genotype-dependent in sunflower.
Nineteen chromosomal regions related to photosynthetic activity and water status were detected in sunflower in irrigated culture. The low number of loci detected per physiological trait (1–4 QTL) may be due to culture under non-stressed conditions. For example, in maize, Pelleschi et al. detected four QTL for invertase activity under control conditions but described nine QTL under stress conditions (Pelleschi et al., 1999). Prioul et al. concluded that more QTL were revealed in stress conditions than in non-stressed ones (Prioul et al., 1999).
Genome regions associated with only one physiological trait are described. For example, the most significant QTL for net photosynthesis (pho9.1 and pho9.2) were located on linkage group IX without co-location with any other measured trait. This observation suggests that this interval may contain genes encoding specific enzymes for photosynthesis such as genes involved in photosystems (Mullet, 1993). QTL for chlorophyll concentration (chl8.1, chl10.1 and chl18.1) were detected on linkage groups VIII, X and XVIII without co-location with any other QTL suggesting they contain genes involved in chlorophyll turnover. Only one locus involved in internal CO2 concentration (ic11.1) was detected on linkage group XI. No other QTL was detected in this region, and it should correspond to genes implied in CO2 assimilation, like Rubisco. Three regions appeared to be linked only to stomatal closure: linkage groups III (sco3.1), XVI (sco16.1) and XVII (sco17.1). Therefore, it is hypothesized that these loci correspond to genes encoding proteins important for guard cell function (Muller-Rober et al., 1998).
One co-location of QTL between water status and stomatal movement on linkage group VIII has been described. Locus pot8.1 implied in predawn leaf water potential was near those associated with stomatal conductance (sco8.1) on linkage group VIII (interval 18 cM to 36 cM). This result is supported by the negative correlation between leaf water potential and stomatal conductance. It suggests that common genes exist for stomatal closure and water status.
Concerning the linkage group V, the present results show a co-location on a 19 cM region with rwc5.1 and chl5.1 for related water content and chlorophyll concentration. However, these traits are not correlated in this study and there is still no example of a relationship between RWC and leaf chlorophyll content. As the 19 cM interval is likely too high, a more precise location of these QTL should confirm or not our observation. A co-location was observed for RWC and traits related to water status and stomatal movement as a correlation was found. Predawn leaf water potential and RWC are two independent measurements of water status in plant. RWC measures the water content of the leaf during the day, although the predawn leaf water potential measures the pressure difference between soil and plant after the night.
In sunflower, the limitation of photosynthetic rate appeared mainly to be due to stomatal closure and the alteration of photosynthetic machinery (Guidi and Soldatini, 1997). A co-location of QTL involved in water status, transpiration and photosynthesis (pho14.1, tr14.1 and pot14.1) was noted on linkage group XIV. These traits are mutually dependent as shown by the correlations between leaf water potential and transpiration and between net photosynthesis and transpiration. It has also been reported that net photosynthesis is correlated with leaf water potential in sunflower (Mojayad and Planchon, 1994).
A comparison of QTL detected under stressed and non-stressed conditions could be a valuable tool to confirm the results presented in this study. From this point of view the use of RIL in association with AFLP is of particular interest as they could be replicated in many different environmental conditions. This study constitutes the first knowledge of genetic determinism of photosynthesis and water status in sunflower, and has led to the description of important markers for breeding programmes. The next step will be the characterization of QTL by positional cloning and localization of candidate genes involved in photosynthesis and water status.
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Acknowledgments |
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The authors would like to thank Olivier Berseille and Marie-José Tavella for their technical assistance, Marie-Françoise Jardineau for scientific assistance, and ANRT, Caussade Semences and Maïsadour Semences for financial support.
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Notes |
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1 To whom correspondence should be addressed. Fax: +33 5 62 19 35 89. gentz{at}ensat.fr
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Abbreviations |
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CHL, chlorophyll concentration; IC, internal CO2 concentration; PHO, net photosynthesis; POT, predawn leaf water potential; QTL, quantitative trait loci; RIL, recombinant inbred lines; RWC, relative water content; SCO, stomatal conductance; TR, transpiration..
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References |
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