Abstract
Leaf thickness is a quantitative trait that is associated with the ability of plants to occupy dry, high irradiance environments. Despite its importance, leaf thickness has been difficult to measure reproducibly, which has impeded progress in understanding its genetic basis, and the associated anatomical mechanisms that pattern it. Here, we used a custom-built dual confocal profilometer device to measure leaf thickness in the Arabidopsis Ler × Cvi recombinant inbred line population and found statistical support for four quantitative trait loci (QTL) associated with this trait. We used publically available data for a suite of traits relating to flowering time and growth responses to light quality and show that three of the four leaf thickness QTL coincide with QTL for at least one of these traits. Using time course photography, we quantified the relative growth rate and the pace of rosette leaf initiation in the Ler and Cvi ecotypes. We found that Cvi rosettes grow slower than Ler, both in terms of the rate of leaf initiation and the overall rate of biomass accumulation. Collectively, these data suggest that leaf thickness is tightly linked with physiological status and may present a tradeoff between the ability to withstand stress and rapid vegetative growth. To understand the anatomical basis of leaf thickness, we compared cross-sections of Cvi and Ler leaves and show that Cvi palisade mesophyll cells elongate anisotropically contributing to leaf thickness. Flow cytometry of whole leaves show that endopolyploidy accompanies thicker leaves in Cvi. Overall, our data suggest that mechanistically, an altered schedule of cellular events affecting endopolyploidy and increasing palisade mesophyll cell length contribute to increase of leaf thickness in Cvi. Ultimately, knowledge of the genetic basis and developmental trajectory leaf thickness will inform the mechanisms by which natural selection acts to produce variation in this adaptive trait.
Highlights
Understanding the developmental basis of evolutionary change in leaf shape presents several major challenges
We found that the leaf thickness peaks on chromosomes 1 and 5, as well as chromosome 3@3 overlap with high LOD score leaf mass per area (LMA) loci, but that the leaf thickness quantitative trait loci (QTL) on chromosome 3@86 is independent of LMA (Figure 1 and Supplementary Table S1)
We used a custom-built dual confocal profilometer device to measure leaf thickness in the Arabidopsis Ler × Cvi recombinant inbred line (RIL) population and found statistical support for four QTL associated with this trait
Summary
Understanding the developmental basis of evolutionary change in leaf shape presents several major challenges. Is leaf shape inherently multidimensional, necessitating multivariate methods for its quantification, but it changes throughout the organ’s ontogeny in response to a complex interplay of genetic and environmental factors. Multivariate analyses have enabled the delineation of global (i.e., spanning taxonomic and biome groups) associations between biogeographic parameters, such as temperature, irradiance, and precipitation and specific leaf traits, which are deemed functional (Wright et al, 2004, 2017). Among these functional traits, leaf mass per area (LMA), the product of a leaf ’s thickness and its density, is robustly associated with the ability of plants to survive arid, highirradiance environments (Wright et al, 2004; Poorter et al, 2009)
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