Evolutionary Genomics of LysM Genes in Land Plants

Authors: ZHANG, XUE-CHENG - UNIV MISSOURI; Cannon, Steven; STACEY, GARY - UNIV MISSOURI

Submitted to: BMC Evolutionary Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/3/2009
Publication Date: 8/3/2009
Citation: Zhang, X., Cannon, S.B., Stacey, G. 2009. Evolutionary Genomics of LysM Genes in Land Plants. BMC Evolutionary Biology. 9:183.

Interpretive Summary: The legume plant family (including peas, clovers, beans, and many tropical trees) has unique structures (nodules) that develop on the roots. These host Rhizobial bacteria, can convert atmospheric nitrogen to a form of natural fertilizer that is directly usable by the plant. This association provides the largest source of natural nitrogen fertilizer in terrestrial ecosystems. A key molecule that makes this relationship possible is "LysM," which recognizes the presence of the Rhizobium bacterium outside of the roots. We report that relatives of the important LysM gene are found in every plant and animal kingdom, but with variations in each case. In plants, these genes have evolved to produce proteins that recognize and guard against fungal diseases, as well as to recognize and allow the beneficial relationship with nitrogen-fixing bacteria in the legumes. Understanding the evolution of this basic mechanism is important for making best use of these natural relationships, both for encouraging natural plant defenses and relationships with beneficial bacteria.

Technical Abstract: The LysM motif, a ubiquitous protein module, recognizes peptidoglycan, chitooligosaccharides (chitin) and, presumably, other structurally-related oligosaccharides. LysM-containing proteins were first shown to be involved in bacterial cell wall degradation and, more recently, were implicated in perceiving chitin and lipo-chitin (nodulation factors) in flowering plants. However, the majority of LysM genes remain functionally uncharacterized and the evolutionary history of complex LysM genes remains elusive. In this study, we report a domain architecture catalogue of LysM proteins across all kingdoms and describe a comparative and evolutionary genomics study of LysM genes in plant lineages. Although LysM-containing proteins display a wide range of complex domain architectures in nature, only a simple core architecture is conserved across kingdoms. Each individual kingdom appears to have evolved a distinct array of domain architectures, indicating the presence of distinctive evolutionary paths in individual kingdoms. We show that early plant lineages acquired four characteristic architectures, progressively lost several primitive architectures, and underwent significant copy number expansions in the LysM-containing receptor-like kinase (LYK) gene family. We report plant LysM phylogenies and associated gene, protein and genomic features, and infer the relative timing of duplications of LYK genes. One of the two groups of tandemly arrayed plant LYK genes likely resulted from an ancient genome duplication followed by local genomic rearrangement, while the origin of the other groups of tandemly arrayed LYK genes remains obscure. Given the fact that no similar evolutionary study has been performed in metazoa and no metazoan LysM motif-containing genes have been functionally characterized, this study provides clues to functional characterization of plant LysM genes and is also informative with regard to evolutionary and functional studies of metazoan LysM genes.