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Insight into early diversification of leucine-rich repeat receptor-like kinases provided by the sequenced moss and hornwort genomes

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Identification of the subfamily X leucine-rich repeat receptor-like kinases in the recently sequenced moss and hornwort genomes points to their diversification into distinct groups during early evolution of land plants.

Abstract

Signal transduction mediated through receptor-ligand interactions plays key roles in controlling developmental and physiological processes of multicellular organisms, and plants employ diverse receptors in signaling. Leucine-rich repeat receptor-like kinases (LRR-RLKs) represent one of the largest receptor classes in plants and are structurally classified into subfamilies. LRR-RLKs of the subfamily X are unique in the variety of their signaling roles; they include receptors for steroid or peptide hormones as well as negative regulators of signaling through binding to other LRR-RLKs, raising a question as to how they diversified. However, our understanding of diversification processes of LRR-RLKs has been hindered by the paucity of genomic data in non-seed plants and limited taxa sampling in previous phylogenetic analyses. Here we analyzed the phylogeny of LRR-RLK X sequences collected from all major land plant lineages and show that this subfamily diversified into six major clades before the divergence between bryophytes and vascular plants. Notably, we have identified homologues of the brassinosteroid receptor, BRASSINOSTEROID INSENSITIVE 1 (BRI1), in the genomes of Sphagnum mosses, hornworts, and ferns, contrary to earlier reports that postulate the origin of BRI1-like LRR-RLKs in the seed plant lineage. The phylogenetic distribution of major clades illustrates that the current receptor repertoire was shaped through lineage-specific gene family expansion and independent gene losses, highlighting dynamic changes in the evolution of LRR-RLKs.

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Acknowledgements

We thank the Department of Energy Joint Genome Institute, Jonathan Shaw (Duke University), and David Weston (ORNL) for pre-publication access to the proteome of Sphagnum fallax and S. magellanicum, which we used to collect LRR-RLK subfamily X and its related sequences. We also thank Hirofumi Nakagami and three anonymous reviewers for valuable comments and suggestions. This work was supported by JSPS KAKENHI (17H03967, 18H04841, 18H04625, 18H05487, and 20H00422 to SS and 20K06770 to CF) and Nakatsuji Foresight Foundation Research Grant to CF.

Funding

This work was supported by JSPS KAKENHI (Grant Nos. 17H03967, 18H04841, 18H04625, 18H05487, and 20H00422 to SS and 20K06770 to CF) and Nakatsuji Foresight Foundation Research Grant to CF.

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CF and SS conceived and designed the experiments. CF conducted the experiments. CF and SS analyzed the data and wrote the paper. All authors read and approved the final manuscript.

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Correspondence to Chihiro Furumizu.

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Furumizu, C., Sawa, S. Insight into early diversification of leucine-rich repeat receptor-like kinases provided by the sequenced moss and hornwort genomes. Plant Mol Biol 107, 337–353 (2021). https://doi.org/10.1007/s11103-020-01100-0

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  • DOI: https://doi.org/10.1007/s11103-020-01100-0

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