Growth‐defense trade‐offs masked in unadmixed populations are revealed by hybridization

Abstract

Organisms are constantly challenged by pathogens and pests, which can drive the evolution of growth‐defense strategies. Plant stomata are essential for gas exchange during photosynthesis and conceptually lie at the intersection of the physiological demands of growth and exposure to foliar fungal pathogens. Generations of natural selection for locally adapted growth‐defense strategies can eliminate variation between traits, potentially masking trade‐offs and selection conflicts that may have existed in the past. Hybrid populations offer a unique opportunity to reset the clock on selection and to study potentially maladaptive trait variation before selection removes it. We study the interactions of growth, stomatal, ecopysiological, and disease resistance traits in poplars (Populus) after infection by the leaf rust Melampsora medusae. Phenotypes were measured in a common garden and genotyped at 227K SNPs. We isolate the effects of hybridization on trait variance, discover correlations between stomatal, ecophysiology, and disease resistance, examine trade‐offs and selection conflicts, and explore the evolution of growth‐defense strategies potentially mediated by selection for stomatal traits on the upper leaf surface. These results suggest an important role for stomata in determining growth‐defense strategies in organisms susceptible to foliar pathogens, and reinforces the contribution of hybridization studies toward our understanding of trait evolution.

How important are functional and developmental constraints on phenotypic evolution? An empirical test with the stomatal anatomy of flowering plants

“…& A. Gray ex Hook., Populus interspecific crosses, and Solanum interspecific crosses, typically find partial independence of D ab and D ad ; some loci affect both traits, but some loci only affect density on one surface and/or genetic correlations are weak (Ishimaru et al 2001; Ferris et al 2002; Hall et al 2005; Rae et al 2006; Laza et al 2010; Chitwood et al 2013; McKown et al 2014; Muir, Pease, and Moyle 2014; Porth et al 2015; Fetter, Nelson, and Keller 2021). For example, Populus trichocarpa populations have putatively adaptive genetic variation in D ad .…”

“…However, the light environment alone cannot explain why hypostomatous leaves predominate in shade plants (Muir 2019), suggesting that we need to understand the costs of upper stomata better. Upper stomata increase the susceptibility to rust pathogens in Populus (McKown et al 2014, 2019; Fetter, Nelson, and Keller 2021). Amphistomy may also cause the palisade mesophyll to dry out under strong vapor pressure deficits (Buckley et al 2015).…”

“…One factor may be increased vulnerability to pathogens. For example, upper stomata increase susceptibility to rust pathogens in Populus (McKown et al 2014, 2019; Fetter, Nelson, and Keller 2021). Amphistomy may also cause the palisade mesophyll to dry out under strong vapor pressure deficits (Buckley et al 2015).…”

Admixture mapping and selection scans identify genomic regions associated with stomatal patterning and disease resistance in hybrid poplars

“…In a previous study, we found evidence of hybrids expressing a genetic correlation between stomatal traits and resistance to the basidiomycete leaf rust, Melampsora medusae (Fetter et al, 2021).…”

“…After overwintering, ecophysiology, height growth, and bud phenology traits were measured (Table 1). For a detailed explanation of phenotypes, see Fetter et al (2021). Following genotyping and genetic analysis, several hybrid individuals were identified, including hybrids from crosses with P. trichocarpa, P. angustifolia, and P. deltoides (Chhatre et al, 2018;Fetter et al, 2021).…”