Structural evolution drives diversification of the large LRR-RLK gene family.

Jarrett Man,Madelaine Bartlett,Joseph P Gallagher

doi:10.1111/nph.16455

Abstract

Summary ●Cells are continuously exposed to chemical signals that they must discriminate between and respond to appropriately. In embryophytes, the leucine‐rich repeat receptor‐like kinases (LRR‐RLKs) are signal receptors critical in development and defense. LRR‐RLKs have diversified to hundreds of genes in many plant genomes. Although intensively studied, a well‐resolved LRR‐RLK gene tree has remained elusive.●To resolve the LRR‐RLK gene tree, we developed an improved gene discovery method based on iterative hidden Markov model searching and phylogenetic inference. We used this method to infer complete gene trees for each of the LRR‐RLK subclades and reconstructed the deepest nodes of the full gene family.●We discovered that the LRR‐RLK gene family is even larger than previously thought, and that protein domain gains and losses are prevalent. These structural modifications, some of which likely predate embryophyte diversification, led to misclassification of some LRR‐RLK variants as members of other gene families. Our work corrects this misclassification.●Our results reveal ongoing structural evolution generating novel LRR‐RLK genes. These new genes are raw material for the diversification of signaling in development and defense. Our methods also enable phylogenetic reconstruction in any large gene family.

Highlights

Developmental and defense processes are cued by complex mixtures of extracellular chemical signals
To perceive and relay extracellular signals, most leucine-rich repeat receptor-like kinase (LRR-RLK) localize to the plasma membrane, where each LRR-RLK has an extracellular LRR domain, a single-pass transmembrane domain, and a cytosolic RLK domain
Thresholded hits were consolidated across the subalignments and used for phylogenetic inference under the maximum likelihood criterion. This searching and gene tree inference was repeated until no new genes were recovered as well-supported members of a particular clade (≥ 75% bootstrap support), generally after two rounds (Fig. 1b)

Summary

Introduction

Developmental and defense processes are cued by complex mixtures of extracellular chemical signals. The leucine-rich repeat receptor-like kinase (LRR-RLK) receptors, in particular, comprise the largest plant-specific clade of the eukaryotic kinase superfamily (Shiu & Bleecker, 2001a). LRR-RLKs remain inactive until a signal ligand is bound by the extracellular LRR domain, upon which LRR-RLKs oligomerize to form active complexes (Dievart & Clark, 2004; Meng et al, 2016; Santiago et al, 2016). LRR domains can have exquisite signal specificity and sensitivity, and RLK domains can selectively phosphorylate many proteins downstream of signal perception (Shiu & Bleecker, 2003; Santiago et al, 2016; He et al, 2018; Je et al, 2018)

Methods

Results

Discussion

Conclusion