Accelerated flowering time reduces lifetime water use without penalizing reproductive performance in Arabidopsis

Abstract

Natural selection driven by water availability has resulted in considerable variation for traits associated with drought tolerance and leaf‐level water‐use efficiency ( WUE ). In Arabidopsis, little is known about the variation of whole‐plant water use (PWU) and whole‐plant WUE ( transpiration efficiency ). To investigate the genetic basis of PWU, we developed a novel proxy trait by combining flowering time and rosette water use to estimate lifetime PWU. We validated its usefulness for large‐scale screening of mapping populations in a subset of ecotypes. This parameter subsequently facilitated the screening of water use and drought tolerance traits in a recombinant inbred line population derived from two Arabidopsis accessions with distinct water‐use strategies, namely, C24 (low PWU) and Col‐0 (high PWU). Subsequent quantitative trait loci mapping and validation through near‐isogenic lines identified two causal quantitative trait loci, which showed that a combination of weak and nonfunctional alleles of the FRIGIDA (FRI) and FLOWERING LOCUS C (FLC) genes substantially reduced plant water use due to their control of flowering time. Crucially, we observed that reducing flowering time and consequently water use did not penalize reproductive performance, as such water productivity (seed produced per unit of water transpired) improved. Natural polymorphisms of FRI and FLC have previously been elucidated as key determinants of natural variation in intrinsic WUE (δ 13 C). However, in the genetic backgrounds tested here, drought tolerance traits, stomatal conductance, δ 13 C. and rosette water use were independent of allelic variation at FRI and FLC , suggesting that flowering is critical in determining lifetime PWU but not always leaf‐level traits.

Genetic and physiological bases for variation in water use efficiency in canola

“…These observations provide evidence that FT may be driving variation in WUE in canola. Our findings are consistent with previous studies that found associations between Δ 13 C and flowering time and productivity traits (Ferguson et al, 2019;Fletcher, Mullen, Heiliger, & McKay, 2015;McKay et al, 2003), suggesting that a cross-talk between drought tolerance and drought avoidance mechanisms contributes to effective water use in canola productivity. FT and ELF genes (candidates identified herein) have been shown to regulate stomatal opening in Arabidopsis via the regulation of H + ATPase by blue light in guard cells (Kinoshita et al, 2011).…”

Linking Brassinosteroid and ABA Signaling in the Context of Stress Acclimation

“…The interaction of BR signaling components with FLC (MADS-box transcription factor encoded by flowering locus C) provides a new mechanism for drought resistance, where FLC substantially reduces plant water use [ 49 ]. FLC is also involved in long-term cold adaptation mediated by the epigenetic memory mechanism [ 50 ].…”

Competition-by-drought interactions change phenotypic plasticity and the direction of selection on Arabidopsis traits

“…We found that genetic variation in flowering time was negatively associated with leaf δ 13 C, suggesting that early flowering plants had higher intrinsic leaf-level WUE due to lower stomatal conductance or higher assimilation rate A (Ferguson et al, 2019). This positive correlation between flowering time and δ 13 C might be a result of maladapted late-flowering genotypes having lower A for a given stomatal conductance.…”

“…Our panel of natural genotypes lacked genotypes requiring vernalization , thus these genotypes might partly be responsible for the discrepancies with these publications. Additionally, Ferguson et al (2019)…”

“…Escape may be adaptive when low soil moisture occurs at the end of growing seasons (Kenney et al, 2014) while avoidance may be adaptive when moisture is limited throughout a growing season (Campitelli et al, 2016). Escape has been characterized by rapid flowering, high specific leaf area (SLA), high leaf N, high carbon 85 assimilation rate (A), low root:shoot mass ratio, and low water use efficiency (WUE) (Ludlow, 1989; Des Kenney et al, 2014;El-Soda et al, 2015), while avoidance is characterized by the opposite values (but see Ferguson et al, 2019). Arabidopsis is a rapidly maturing annual, an early successional strategy, which may be adaptive when neighbors are better resource competitors.…”