Leaf shape in Populus tremula is a complex, omnigenic trait.

Niklas Mähler,Stefan Jansson,Matej Vučak,Chanaka Mannapperuma,Nathaniel R Street,Mark E S Bailey,Torgeir R Hvidsten,Barbara K Terebieniec,Bastian Schiffthaler,Kathryn M Robinson

doi:10.1002/ece3.6691

Niklas Mähler, Stefan Jansson + Show 8 more

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https://doi.org/10.1002/ece3.6691

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Abstract

Leaf shape is a defining feature of how we recognize and classify plant species. Although there is extensive variation in leaf shape within many species, few studies have disentangled the underlying genetic architecture. We characterized the genetic architecture of leaf shape variation in Eurasian aspen (Populus tremula L.) by performing genome‐wide association study (GWAS) for physiognomy traits. To ascertain the roles of identified GWAS candidate genes within the leaf development transcriptional program, we generated RNA‐Seq data that we used to perform gene co‐expression network analyses from a developmental series, which is publicly available within the PlantGenIE resource. We additionally used existing gene expression measurements across the population to analyze GWAS candidate genes in the context of a population‐wide co‐expression network and to identify genes that were differentially expressed between groups of individuals with contrasting leaf shapes. These data were integrated with expression GWAS (eQTL) results to define a set of candidate genes associated with leaf shape variation. Our results identified no clear adaptive link to leaf shape variation and indicate that leaf shape traits are genetically complex, likely determined by numerous small‐effect variations in gene expression. Genes associated with shape variation were peripheral within the population‐wide co‐expression network, were not highly connected within the leaf development co‐expression network, and exhibited signatures of relaxed selection. As such, our results are consistent with the omnigenic model.

Highlights

Leaf shape is a defining feature of how we recognize and classify plant species and, as such, is an important component of our relationship with nature
We examined the developmental profiles of genome-wide association study (GWAS) candidate genes and explored their co-expression network centrality
Despite the vast variation in leaf shape within and between species, we still have a rather limited understanding of the gene regulatory network underlying the process of leaf development and of the genetic determinants of leaf shape variation among individuals

Summary

| INTRODUCTION

Leaf shape is a defining feature of how we recognize and classify plant species and, as such, is an important component of our relationship with nature. A number of genes with a central role in the control of leaf primordia initiation and subsequent leaf development and pattern formation have been identified from forward genetic screens, largely in Arabidopsis thaliana (Tsukaya, 2005). Forward genetic screens have identified genes acting during leaf organogenesis, most studies have been conducted using A. thaliana mutants that target single genes Those genes can be shown to be essential for, or to contribute to, the control of leaf development, they are not necessarily those underlying natural variation. Street et al (2008), Street, Jansson, and Hvidsten (2011) performed system biology analyses to link available microarray expression data to leaf physiognomy QTLs, identifying GRFs (growth-regulating factors) as candidate genes controlling leaf development. Our results indicate that leaf shape variation in aspen is highly polygenic and is associated with numerous small-effect size variants affecting genes expressed during leaf development

| MATERIALS AND METHODS

Findings

| DISCUSSION