Abstract
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 (g s) explains more variation in WUE than does A. Overall, there was a strong genetic correlation between A and g s, 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 (V cmax) 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 (g m) in variation of WUE. We hypothesize that this is due to an effect through g m, and test this hypothesis using the abi4 mutant. We show that mutants of ABI4 have higher SLA, LWC, and g m than wild-type, consistent with variation in leaf anatomy causing variation in g m 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.
Highlights
The efficiency with which plants fix CO2 relative to their rate of H2O loss is called water use efficiency (WUE), and when high, WUE can mitigate the tradeoff between CO2 uptake and H2O loss
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 specific leaf area (SLA), leaf water content (LWC), and gm than wild-type, consistent with variation in leaf anatomy causing variation in gm and d13C
Summary
The efficiency with which plants fix CO2 relative to their rate of H2O loss is called water use efficiency (WUE), and when high, WUE can mitigate the tradeoff between CO2 uptake and H2O loss. Studies in Arabidopsis have identified extensive natural variation in plant–water relations and gas exchange physiology (Juenger et al 2005, 2010; Masle et al 2005; Bouchabke et al 2008; Christman et al 2008; McKay et al 2008; Monda et al 2011; Des Marais et al 2012; Pons 2012). A LI-6400 (Li-Cor Inc., Lincoln, NE, USA) with wholeshoot Arabidopsis cuvette (Fig. 1) was coupled with online isotopic measurements of CO2 entering and leaving the shoot chamber to determine instantaneous carbon isotope discrimination and gm using TDL (Flexas et al 2006; Barbour et al 2007; Heckwolf et al 2011). For d13C, we fit a simpler model including accession as a random variable and experimental run as a fixed effect In this case, factors associated with chamber could not be included because replicates within each experimental run were pooled for mass spectroscopy analysis. We estimated genetic correlations (rG) among TE and d13C as the standard Pearson product-moment correlation between genotype means or BLUPs
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