Natural variation in stomata size contributes to the local adaptation of water‐use efficiency in Arabidopsis thaliana

Abstract

Stomata control gas exchanges between the plant and the atmosphere. How natural variation in stomata size and density contributes to resolve trade-offs between carbon uptake and water loss in response to local climatic variation is not yet understood. We developed an automated confocal microscopy approach to characterize natural genetic variation in stomatal patterning in 330 fully sequenced Arabidopsis thaliana accessions collected throughout the European range of the species. We compared this to variation in water-use efficiency, measured as carbon isotope discrimination (δ C). We detect substantial genetic variation for stomata size and density segregating within Arabidopsis thaliana. A positive correlation between stomata size and δ C further suggests that this variation has consequences on water-use efficiency. Genome wide association analyses indicate a complex genetic architecture underlying not only variation in stomatal patterning but also to its covariation with carbon uptake parameters. Yet, we report two novel QTL affecting δ C independently of stomatal patterning. This suggests that, in A. thaliana, both morphological and physiological variants contribute to genetic variance in water-use efficiency. Patterns of regional differentiation and covariation with climatic parameters indicate that natural selection has contributed to shape some of this variation, especially in Southern Sweden, where water availability is more limited in spring relative to summer. These conditions are expected to favour the evolution of drought avoidance mechanisms over drought escape strategies.

Drought adaptation in Arabidopsis thaliana by extensive genetic loss-of-function

“…However, delayed flowering may ensure that droughts co-occur with vegetative growth rather than during the drought sensitive reproductive phase. This pattern is also consistent with hypotheses explaining the more water conservative water use and stomatal traits observed in late flowering genotypes (McKay et al, 2003; Lovell et al, 2013; Kenney et al, 2014; Kooyers, 2015) and those from spring drought environments (Dittberner et al, 2018). Future experimental work will be valuable to identify other plant physiological traits affected by the LoF alleles associated with drought timing.…”

Linking genes with ecological strategies in Arabidopsis thaliana

“…After accounting for the demographic history of the species, stomatal size variation was found to correlate with water-use efficiency (i.e. rate of carbon fixation to water loss) and both air humidity and the local probability of spring drought severity (Dittberner et al , 2018), in agreement with field measurements (Mojica et al , 2016). The molecular evolution of the gene P5CS, which contributes to the synthesis of proline, a potent osmoprotectant in A. thaliana , suggests that it contributed to local adaptation (Kesari et al , 2012).…”

“…In A. thaliana , local adaptation for increased tolerance to drought stress is not found in the driest regions, because, in these areas, natural selection promoted genotypes with the ability to escape the stress (Kronholm et al , 2012; Vidigal et al , 2016, Mojica et al , 2016; Tabas-Madrid et al , 2018). Genotypes showing smaller stomata, higher water-use efficiency, and longer photosynthetic activity in the face of terminal drought have in fact evolved in Southern Scandinavia, where the growth season is too short to allow an escape from the drier season but dry enough to require improved drought tolerance (Mojica et al , 2016; Dittberner et al , 2018; Exposito-Alonso et al , 2018 c ). Genotypes with a strong vernalization requirement are in fact more frequent in this region, limiting the possibility to escape drought during the growing season (Li et al , 2014).…”

Changes in Foliar Functional Traits of S. pyrenaicus subsp. carpetanus under the Ongoing Climate Change: A Retrospective Survey

“…Inferring ecological trends as the stronger driver for regulating behavior of stomata [17,42], the observed effects of the long-term exposure of S. carpetanus to gradual increases in water deficit during the growing season denotes an apparent higher resilience capacity to the forthcoming climate aggravation in Mediterranean high-mountains. Moreover, the association among reduced SS and, consequently, higher δ 13 C with historic drought regimens in Spanish accessions of Arabidopsis thaliana [43], provides additional evidence inferring the observed adjustments in stomatal morphology in S. carpetanus as the outcome of the ecological trends recorded in the last three decades, i.e., the aggravation of climate in the growing season. However, further studies incorporating photosynthetic and stomatal regulation parameters, added to nutrient status, are encouraged to determine whether these adjustments are sufficient to sustain efficient photosynthetic activity.…”