Structural evolution drives diversification of the large LRR‐RLK gene family

Abstract

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.

The Sequenced Genomes of Non-Flowering Land Plants Reveal the (R)Evolutionary History of Peptide Signaling

“…An additional twist when investigating potential peptide-receptor interactions is the presence of modified amino acid residues, in particular sulfated Tyr and hydroxylated Pro. We have confirmed that GSO and RGI homologues are present in non-flowering plants (Bowman et al, 2017;Liu et al, 2017;Man et al, 2020), and hypothesized that their respective ligands are conserved in the species where presumptive receptors are present. Using PHI-BLASTp, as described, we indeed retrieved ligand candidates from several species (Figure 1 and 5).…”

Moonlighting Proteins Shine New Light on Molecular Signaling Niches

“…LRR RLKs form the major clade of membrane receptor proteins in plants and most contain an extracellular ligand binding domain, a membrane spanning domain and an intracellular kinase domain [ 46 , 62 , 63 , 64 , 65 , 66 , 67 ]. RLK is a large family with over 600 genes in Arabidopsis forming over 2% of the total protein [ 65 ].…”

“…Plant RLKs form part of the monophyletic RLK and Pelle gene family sharing common ancestors with animal receptor kinases; in particular the kinase domain has similarities with Drosophila melanogaster Pelle kinase and interleukin 1 receptor associated kinases (IRAK) [ 46 , 65 , 68 ]. Diversity between the RLK and Pelle clades is massive amongst plants with rice for instance having more than twice the number of RLKs found in Arabidopsis [ 46 , 64 , 65 , 66 , 68 ], but quite limited in animals with four IRAK members in vertebrates [ 69 ]. This phenomenon is no doubt due to the need of plants to recognize and respond actively to environmental challenges.…”

“…This phenomenon is no doubt due to the need of plants to recognize and respond actively to environmental challenges. Animals can escape these challenges but plants due to their sessile nature need to withstand or tolerate them [ 46 , 64 , 65 , 66 , 68 , 70 ]. Plant RLK diversification has resulted in great variation in the extracellular domain that contributes to their diverse roles mediating all aspects of plant growth and development and responses to the environment, notably to biotic stresses (for reviews, see for instance: [ 65 , 71 , 72 , 73 ]).…”

“…The degree of peptide signaling in plants is perhaps surprising but can be considered an adaptive evolutionary investment [ 77 ]. Recent work has attempted to resolve how extracellular domains of RLKs respond by binding or recognizing PAMPs, DAMPs and other signals contribute to the diversity of plant RLKs at genetic and structural levels [ 64 , 78 , 79 ]. Phylogenetic analyses reveal that the kinase domain is relatively conserved compared to the extracellular domain of RLKs including LRR RLKs [ 62 , 63 , 64 , 66 ].…”