Natural variation, differentiation, and genetic trade-offs of ecophysiological traits in response to water limitation in Brachypodium distachyon and its descendent allotetraploid B. hybridum (Poaceae)

Abstract

Differences in tolerance to water stress may underlie ecological divergence of closely related ploidy lineages. However, the mechanistic basis of physiological variation governing ecogeographical cytotype segregation is not well understood. Here, using Brachypodium distachyon and its derived allotetraploid B. hybridum as model, we test the hypothesis that, for heteroploid annuals, ecological divergence of polyploids in drier environments is based on trait differentiation enabling drought escape. We demonstrate that under water limitation allotetraploids maintain higher photosynthesis and stomatal conductance and show earlier flowering than diploids, concordant with a drought-escape strategy to cope with water stress. Increased heterozygosity and greater genetic variability and plasticity of polyploids could confer a superior adaptive capability. Consistent with these predictions, we document (1) greater standing within-population genetic variation in water-use efficiency (WUE) and flowering time in allotetraploids, and (2) the existence of (nonlinear) environmental clines in physiology across allotetraploid populations. Increased gas exchange and diminished WUE occurred at the driest end of the gradient, consistent with a drought-escape strategy. Finally, we found that allotetraploids showed weaker genetic correlations than diploids congruous with the expectation of relaxed pleiotropic constraints in polyploids. Our results suggest evolutionary divergence of ecophysiological traits in each ploidy lineage.

Keywords: Adaptation; flowering time; gas exchange; genetic correlations; hybridization; polyploidy.

FIGURE 1

Variation (LS-MEANS adjusted model values ± 1 SE) in a) whole plant photosynthesis (A); b) stomatal conductance (gs); c) carbon isotope composition (δ13C ‰) between two watering treatments (WW = well watered, WR = water restricted) and two levels of ploidy variation: B.distachyon diploids (dashed line) and B. hybridum allotetraploids (solid line). P-values in the graphs are results from test of the slices interactions comparing both ploidy levels in each treatment. Only results from significant tests are shown.

FIGURE 2

The probability of flowering for B.distachyon diploid and B. hybridum allotetraploid individuals in each watering treatment as a function of time (number of days). Shading indicates 95 % confidence intervals.

FIGURE 3

Relationships between annual precipitation and annual soil moisture deficit and the genetic population means of ecophysiological traits under water-restricted conditions: a,b) stomatal conductance (g_s); c,d) carbon isotope composition (δ13C ‰). Soil moisture deficit is defined as potential evapotranspiration minus precipitation. In all cases, the solid line depicts the best quadratic regression fit between variables, and dashed lines are its 95% confidence intervals. Only data for B. hybridum allotetraploids are depicted (red triangles).

FIGURE 4

Relationships between annual precipitation, annual soil moisture deficit and population means of plasticity in ecophysiological traits: a) carbon isotope composition; b,c) flowering time (FT). Soil moisture deficit is defined as potential evapotranspiration minus precipitation. Plasicity values come from trait differences between the two watering treatments. In all cases, solid lines depict the best linear or quadratic regression fit between variables. Only data for B. distachyon diploids are depicted by green circles in the graphs.