Asymmetric evolution of protein domains in the leucine-rich repeat receptor-like kinase (LRR-RLK) family of plant developmental coordinators

Abstract

The coding sequences of developmental genes are expected to be conserved over deep time, with cis-regulatory change driving the modulation of gene function. In contrast, proteins with roles in defense are expected to evolve rapidly, in molecular arms-races with pathogens. However, some gene families include both developmental and defense genes. In these families, does the tempo and mode of evolution differ between developmental and defense genes, despite shared ancestry and structure? The leucine-rich repeat receptor-like kinase (LRR-RLKs) protein family includes many members with roles in plant development and defense, thus providing an ideal system for answering this question. LRR-RLKs are receptors that traverse plasma membranes. LRR domains bind extracellular ligands, RLK domains initiate intracellular signaling cascades in response to ligand binding. In LRR-RLKs with roles in defense, LRR domains evolve faster than RLK domains. To determine whether this asymmetry extends to developmental LRR-RLKs, we assessed evolutionary rates and tested for selection acting on eleven clades of LRR-RLK proteins, using deeply sampled protein trees. To assess functional evolution, we performed heterologous complementation assays using Arabidopsis thaliana (arabidopsis) LRR-RLK mutants. We found that the LRR domains of developmental LRR-RLK proteins evolved faster than their cognate RLK domains. LRR-RLKs with roles in development and defense had strikingly similar patterns of molecular evolution. Heterologous transformation experiments revealed that the evolution of developmental LRR-RLKs likely involves multiple mechanisms, including changes to cis-regulation, coding sequence evolution, and escape from adaptive conflict. Our results indicate similar evolutionary pressures acting on developmental and defense signaling proteins, despite divergent organismal functions. In addition, deep understanding of the molecular evolution of developmental receptors can help guide targeted genome engineering in agriculture.