Despite compelling evidence that adaptation to local climate is common in plant populations, little is known about the evolutionary genetics of traits that contribute to climatic adaptation. A screen of natural accessions of Arabidopsis thaliana revealed Tsu-1 and Kas-1 to be opposite extremes for water-use efficiency and climate at collection sites for these accessions differs greatly. To provide a tool to understand the genetic basis of this putative adaptation, Kas-1 and Tsu-1 were reciprocally crossed to create a new mapping population. Analysis of F 3 families showed segregating variation in both δ 13 C and transpiration rate, and as expected these traits had a negative genetic correlation (r g = −0.3). 346 RILs, 148 with Kas-1 cytoplasm and 198 with Tsu-1 cytoplasm, were advanced to the F 9 and genotyped using 48 microsatellites and 55 SNPs for a total of 103 markers. This mapping population was used for QTL analysis of δ 13 C using F 9 RIL means. Analysis of this reciprocal cross showed a large effect of cytoplasmic background, as well as two QTL for δ 13 C. The Kas-1 × Tsu-1 mapping population provides a powerful new resource for mapping QTL underlying natural variation and for dissecting the genetic basis of water-use efficiency differences.K E Y W O R D S : Adaptation, Arabidopsis thaliana, carbon isotope ratio, correlated traits, drought avoidance, drought escape, drought tolerance, transpiration, water-use efficiency.

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Ecologists and physiologists have documented extensive variation in water use efficiency (WUE) in Arabidopsis thaliana, as well as association of WUE with climatic variation. Here, we demonstrate correlations of whole-plant transpiration efficiency and carbon isotope composition (δ13C) among life history classes of A. thaliana. We also use a whole-plant cuvette to examine patterns of co-variation in component traits of WUE and δ13C. We find that stomatal conductance (gs) explains more variation in WUE than does A. Overall, there was a strong genetic correlation between A and gs, consistent with selection acting on the ratio of these traits. At a more detailed level, genetic variation in A was due to underlying variation in both maximal rate of carboxylation (Vcmax) and maximum electron transport rate (Jmax). We also found strong effects of leaf anatomy, where lines with lower WUE had higher leaf water content (LWC) and specific leaf area (SLA), suggesting a role for mesophyll conductance (gm) in variation of WUE. We hypothesize that this is due to an effect through gm, and test this hypothesis using the abi4 mutant. We show that mutants of ABI4 have higher SLA, LWC, and gm than wild-type, consistent with variation in leaf anatomy causing variation in gm and δ13C. These functional data also add further support to the central, integrative role of ABI4 in simultaneously altering ABA sensitivity, sugar signaling, and CO2 assimilation. Together our results highlight the need for a more holistic approach in functional studies, both for more accurate annotation of gene function and to understand co-limitations to plant growth and productivity.

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