Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily

Abstract

Summary The nucleotide binding site (NBS) is a characteristic domain of many plant resistance gene products. An increasing number of NBS‐encoding sequences are being identified through gene cloning, PCR amplification with degenerate primers, and genome sequencing projects. The NBS domain was analyzed from 14 known plant resistance genes and more than 400 homologs, representing 26 genera of monocotyledonous, dicotyle‐donous and one coniferous species. Two distinct groups of diverse sequences were identified, indicating divergence during evolution and an ancient origin for these sequences. One group was comprised of sequences encoding an N‐terminal domain with Toll/Interleukin‐1 receptor homology (TIR), including the known resistance genes, N, M, L6, RPP1 and RPP5. Surprisingly, this group was entirely absent from monocot species in searches of both random genomic sequences and large collections of ESTs. A second group contained monocot and dicot sequences, including the known resistance genes, RPS2, RPM1, I2, Mi, Dm3, Pi‐B, Xa1, RPP8, RPS5 and Prf. Amino acid signatures in the conserved motifs comprising the NBS domain clearly distinguished these two groups. The Arabidopsis genome is estimated to contain approximately 200 genes that encode related NBS motifs; TIR sequences were more abundant and outnumber non‐TIR sequences threefold. The Arabidopsis NBS sequences currently in the databases are located in approximately 21 genomic clusters and 14 isolated loci. NBS‐encoding sequences may be more prevalent in rice. The wide distribution of these sequences in the plant kingdom and their prevalence in the Arabidopsis and rice genomes indicate that they are ancient, diverse and common in plants. Sequence inferences suggest that these genes encode a novel class of nucleotide‐binding proteins.

Identification of resistance gene analogs linked to a powdery mildew resistance locus in grapevine

“…Two major sub-classes of NBS-LRR proteins have been identified (Meyers et al 1999). One class comprises sequences encoding an amino-terminal Toll/interleukin-1 receptor homology region (TIR).…”

“…This approach is based on the observation that genes that confer resistance against a diverse range of pathogens, from a variety of plants, show a high degree of structural and amino-acid sequence conservation. In particular, the majority of cloned resistance (R) genes contain a nucleotide-binding site (NBS) and a leucine-rich repeat (LRR) domain (Meyers et al 1999;Ellis et al 2000;Young 2000). Two kinds of N termini have been identified in NBS-LRR resistance genes.…”

“…The first type shows homology to a region in Drosophila Toll and the human Interleukin-1 Receptor (TIR-like), and the other contains a coiled-coil (CC) thought to be involved in protein-protein interactions (non-TIR-like) (Meyers et al 1999;Pan et al 2000a). The NBS sequences of R genes are characterised by the presence of up to seven conserved domains including the P-loop, kinase-2 and GLPL motifs (Meyers et al 1999). The presence of these conserved domains has facilitated the cloning of resistance gene analogs (RGAs) from diverse species by PCR using degenerate oligonucleotide primers.…”

Resistance gene homologues in melon are linked to genetic loci conferring disease and pest resistance

“…Leister et al 1996Leister et al , 1998Yu et al 1996). To obtain a collection of RGH sequences from melon, we applied degenerate PCR primers designed to bind to the P-loop, Kinase-2 and the GLPL (also called 'Hydrophobic Domain') elements in the NBS-LRR gene family (Traut 1994;Meyers et al 1999). We report the cloning and characterization of 15 NBS homologues.…”

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

“…[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. 2 This early-proposed classification system has been largely followed in the past 10 y of NBS-LRR gene investigations.…”