Uncovering the dynamic evolution of nucleotide‐binding site‐leucine‐rich repeat (NBS‐LRR) genes in Brassicaceae

Abstract

Plant genomes harbor dozens to hundreds of nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes; however, the long-term evolutionary history of these resistance genes has not been fully understood. This study focuses on five Brassicaceae genomes and the Carica papaya genome to explore changes in NBS-LRR genes that have taken place in this Rosid II lineage during the past 72 million years. Various numbers of NBS-LRR genes were identified from Arabidopsis lyrata (198), A. thaliana (165), Brassica rapa (204), Capsella rubella (127), Thellungiella salsuginea (88), and C. papaya (51). In each genome, the identified NBS-LRR genes were found to be unevenly distributed among chromosomes and most of them were clustered together. Phylogenetic analysis revealed that, before and after Brassicaceae speciation events, both toll/interleukin-1 receptor-NBS-LRR (TNL) genes and non-toll/interleukin-1 receptor-NBS-LRR (nTNL) genes exhibited a pattern of first expansion and then contraction, suggesting that both subclasses of NBS-LRR genes were responding to pathogen pressures synchronically. Further, by examining the gain/loss of TNL and nTNL genes at different evolutionary nodes, this study revealed that both events often occurred more drastically in TNL genes. Finally, the phylogeny of nTNL genes suggested that this NBS-LRR subclass is composed of two separate ancient gene types: RPW8-NBS-LRR and Coiled-coil-NBS-LRR.

Large-Scale Analyses of Angiosperm Nucleotide-Binding Site-Leucine-Rich Repeat Genes Reveal Three Anciently Diverged Classes with Distinct Evolutionary Patterns

“…Because most nTNL genes encode a coiled-coil (CC) domain at the N terminus, the nTNL genes often are called CC-NBS-LRR (CNL) genes (Meyers et al, 2003;Ameline-Torregrosa et al, 2008). However, recent studies have revealed that apart from CNL genes, a small group of nTNL genes that possess a special N-terminal domain, RPW8 (resistance to powdery mildew8) domain, likely represent a distinct class of NBS genes (RPW8-NBS-LRR [RNL]; Xiao et al, 2001;Cannon et al, 2004;Bonardi et al, 2011;Collier et al, 2011;Shao et al, 2014;Zhang et al, 2016). Investigations of NBS genes in the Fabaceae (rosid I lineage) and Brassicaceae (rosid II lineage) have shown that RNLs and CNLs diverged prior to the divergence of these two families (Shao et al, 2014;Zhang et al, 2016).…”

“…However, recent studies have revealed that apart from CNL genes, a small group of nTNL genes that possess a special N-terminal domain, RPW8 (resistance to powdery mildew8) domain, likely represent a distinct class of NBS genes (RPW8-NBS-LRR [RNL]; Xiao et al, 2001;Cannon et al, 2004;Bonardi et al, 2011;Collier et al, 2011;Shao et al, 2014;Zhang et al, 2016). Investigations of NBS genes in the Fabaceae (rosid I lineage) and Brassicaceae (rosid II lineage) have shown that RNLs and CNLs diverged prior to the divergence of these two families (Shao et al, 2014;Zhang et al, 2016). Interestingly, although both CNL and RNL genes are present in monocots and dicots, TNL genes only are present in dicots (Meyers et al, 2003;Tarr and Alexander, 2009;Andolfo et al, 2013;Shao et al, 2014).…”

Tracking ancestral lineages and recent expansions of NBS-LRR genes in angiosperms

“…However, several recent studies have examined a group of NBS-LRR genes with a special RPW8 domain at the N terminus. 5,7,12 This group of RPW8-NBS-LRR (RNL) genes has not been found to be involved in detecting specific pathogens as most known TNL or CNL type R genes, but functions in signal transductions of disease resistances. 12,13 A controversy was then raised by comparing independent phylogenetic analysis, referring to whether RNL genes are derived from a CNL lineage recently or represent another ancient NBS-LRR class that sister to CNL and TNL genes.…”

“…Benefits from the conserved NBS domain in NBS-LRR proteins, highthroughput bioinformatics methods for genome-wide identification of NBS-LRR genes have been developed, 2,3 with which dozens to hundreds of NBS-LRR genes have been identified from various angiosperm plant genomes. [4][5][6][7][8][9] Previous studies have divided angiosperm NBS-LRR genes into 2 separate classes, TIR-NBS-LRR (TNL) and non-TIR-NBS-LRR (nTNL), based on the presence or absence of a Toll/ IL-1 receptor-like (TIR) domain at the N-terminal of translated proteins. 10,11 The nTNL genes are also called CC-NBS-LRR genes (CNL), which is based on a frequently detected coiledcoil (CC) domain at the N-terminal of nTNL proteins.…”

“…12,13 A controversy was then raised by comparing independent phylogenetic analysis, referring to whether RNL genes are derived from a CNL lineage recently or represent another ancient NBS-LRR class that sister to CNL and TNL genes. 2,5,7 To clarify this basic concept for NBS-LRR gene classification, our recent study 6 performed large-scale phylogenetic analysis of NBS-LRR genes from 22 genomes across major angiosperm lineages. In combination with motif composition analysis of the NBS domain and intron structure and phase detection, our study provides strong evidence that RNL is an ancient NBS-LRR class that has been largely ignored by most previous studies.…”