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

John N Ferguson,Kieron D Edwards,Matt Humphry,Rhonda C Meyer,Ulrike Bechtold,Oliver Brendel

doi:10.1111/pce.13527

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 (δ13C). However, in the genetic backgrounds tested here, drought tolerance traits, stomatal conductance, δ13C. 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.

Highlights

Water availability is essential for the optimal allocation of resources to achieve maximal growth and reproductive fitness (Anderson, 2016)
We used a selection of 12 facultative summer annual ecotypes of Arabidopsis that previously demonstrated variation for drought sensitivity (DS) and water use associated traits (Table S1; Ferguson et al, 2018), as well as a recombinant inbred line (RIL) mapping population and associated near‐isogenic lines (NILs) (BC4F3‐4) to examine natural variation of plant water use (PWU) and above ground biomass allocation (Tables S2 and 5)
Two experimental setups were used as part of this study: (a) 12 ecotypes and RILs—a short‐dehydration experiment under predominantly SD conditions to measure a range of leaf‐level water‐use efficiency (WUE) parameters (WUEi, δ13C), vegetative water use (VWU), flowering time, biomass parameters, and DS (Figure 1a; Ferguson et al, 2018) and (b) 12 ecotypes and NILs—a continuous moderate drought experiment under predominantly LD conditions, during which relative soil water content (rSWC) was maintained at moderate drought levels (~40% rSWC) to measure leaf‐level WUE parameters (δ13C), VWU, PWU, flowering time, and biomass parameters (Bechtold et al, 2010; Figure 1b)

Summary

Introduction

Water availability is essential for the optimal allocation of resources to achieve maximal growth and reproductive fitness (Anderson, 2016). The usefulness of drought resistance as a trait to optimize plant productivity has been questioned, as the improvement of various drought resistance‐related traits has been demonstrated to reduce productivity under some circumstances, regardless of the ability of plants to survive the period of drought stress (Blum, 2005, 2009; Passioura, 2007). It is widely accepted that drought resistance facilitates plant survival, but it does not contribute towards the maintenance of yield following drought stress or in water replete conditions (Blum, 2005, 2009; Passioura, 2007). The identification of plant varieties that are able to produce stabilized or improved yields with reduced water inputs is an important goal for plant breeders, physiologists, and molecular biologists alike (Morison, Baker, Mullineaux, & Davies, 2008; Parry, Flexas, & Medrano, 2005)

Results

Discussion

Conclusion