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

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,
do 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.