A genetic link between whole-plant water use efficiency and leaf carbon isotope composition in the C₄ grass Setaria

Abstract

Increasing whole plant water use efficiency (yield per transpiration; WUEplant) through plant breeding can benefit the sustainability of agriculture and improve crop yield under drought. To select for WUEplant, an efficient phenotyping method that reports on the genetic contribution of component traits such as transpiration efficiency (TEi; rate of CO2 assimilation per stomatal conductance) must be developed. Leaf carbon stable isotope composition (δ13Cleaf) has been proposed as a high-throughput proxy for TEi, and a negative correlation between δ13Cleaf and both WUEplant and TEi has previously been demonstrated in several C4 grass species. Therefore, the aim of the research presented here was to determine if the same loci control δ13Cleaf, WUEplant, and TEi under well-watered and water-limited conditions in a recombinant inbred line (RIL) population of closely related C4 grasses Setaria viridis and S. italica. Three quantitative trait loci (QTL) for δ13Cleaf were co-localized with transpiration, biomass, and a linear model of WUE. When WUEplant was calculated for allele classes based on the three QTL for δ13Cleaf, δ13Cleaf was negatively correlated with WUEplant as theory predicts when WUEplant is in part driven by differences in TEi. In any population, multiple traits can influence WUEplant; however, the analysis of δ13Cleaf in this RIL population demonstrates that there is genetic control of TEi that significantly contributes to WUEplant. Furthermore, this research suggests that δ13Cleaf can be used in marker-assisted breeding to select for TEi and as a tool to better understand the physiology and genetic architecture of TEi and WUEplant in C4 species.Significance StatementOverextended water resources and drought are major agricultural problems worldwide. Therefore, selection for increased plant water use efficiency (WUEplant) in food and biofuel crop species is an important trait in plant breeding programs. Leaf carbon isotopic composition (δ13Cleaf) has potential as a rapid and effective high throughput phenotyping method for intrinsic transpiration efficiency (TEi), an important leaf-level component trait of WUEplant. Our research shows that δ13Cleaf and WUEplant share a common genetic architecture through their shared relationship with TEi. This suggests that δ13Cleaf can be used as a screen for TEi in marker-assisted plant breeding programs to improve crop drought resistance and decrease agricultural water consumption.

Carbon isotope composition, water use efficiency, and drought sensitivity are controlled by a common genomic segment in maize

“…4a), observed also in other C 4 species (Henderson et al 1998; Dercon et al 2006; Sharwood et al 2014). A significant difference between NIL B and the recurrent parent in grain δ 13 C was observed only in well-watered conditions, in agreement with findings in the C 4 species Setaria (Ellsworth et al 2018), where differences in δ 13 C were small under water-limited conditions. The authors explain this with lower stomatal conductance leveling differences in transpiration efficiency and hence differences in δ 13 C between genotypes, like it was reported in C 3 species (Adiredjo et al 2014) and maize (Alvarez Prado et al 2018).…”

“…Taken together, the findings in Setaria and our results in maize demonstrate a genetic and physiological association between δ 13 C and WUE in C 4 species, which most probably involves regulation through stomatal conductance. We showed that, in maize, grain δ 13 C is both genetically determined and responsive to drought as it has recently been shown for leaf δ 13 C in Setaria (Ellsworth et al 2018 ). Hence, our results suggest that, in spite of the fact that the underlying mechanisms are still not clear, δ 13 C can be used in maize as a proxy of other variables involved in drought tolerance.…”

“…3d and 4a). Similar observations have been made in Setaria , where correlations of fresh biomass, transpiration, and WUE have been established with leaf δ 13 C in a recombinant inbred line (RIL) population and co-localizing QTL were found for these traits in well-watered conditions (Ellsworth et al 2018). Taken together, the findings in Setaria and our results in maize demonstrate a genetic and physiological association between δ 13 C and WUE in C 4 species, which most probably involves regulation through stomatal conductance.…”

“…Co-localized QTL for WUE and δ 13 C have previously been found in C 3 species (Adiredjo et al 2014; Easlon et al 2014) and recently in the C 4 species Setaria (Ellsworth et al 2018). Welcker et al (2011) showed for maize that responses to both evaporative demand and soil water deficit are affected to a large extent by the same genomic regions.…”

“…The chr 7 segment affected δ 13 C, growth sensitivity to both evaporative demand and decrease in soil water content, as well as WUE plant , i WUE, g s , stomatal density, and leaf ABA content. Co-localized QTL for WUE and δ 13 C have previously been found in C 3 species (Adiredjo et al 2014 ; Easlon et al 2014 ) and recently in the C 4 species Setaria (Ellsworth et al 2018 ). Welcker et al ( 2011 ) showed for maize that responses to both evaporative demand and soil water deficit are affected to a large extent by the same genomic regions.…”