ReviewStructure, function and evolution of plant disease resistance genes
Introduction
Five classes of gene-for-gene disease resistance (R) genes have been defined according to the structural characteristics of their predicted protein products (see 1, 2 for recent reviews published in this series). Data from the genetic analysis of plant–pathogen interactions and more recent, but limited, data from molecular analysis support the model in which the products of R genes act as receptors for the direct or indirect products (i.e. ligands) of pathogen avirulence (avr) genes. The receptor–ligand interactions are very specific and mutations that modify or inactivate avr genes allow pathogens to avoid recognition. Thus, two pertinent evolutionary questions are what is the molecular basis of R-gene specificity and how do new resistance specificities evolve?
Section snippets
NBS-LRR genes
The majority of R genes cloned so far encode proteins with a nucleotide-binding site (NBS) and a leucine-rich repeat (LRR) region. Several NBS-LRR-containing R genes have been cloned for the first time in the past year 3•, 4•, 5•, 6, 7•, 8•. Although extremely divergent in DNA sequence, the gene products of the NBS-LRR class are readily recognised by several distinctive motifs in their amino-terminal half, which are conserved in amino-acid sequence and order, and by carboxy-terminal LRRs [9•].
The extracellular LRR class
The extracellular LRR class of R genes includes the rice Xa21 gene for resistance against bacterial blight (Xanthomonas resistance) and the Cf genes of tomato for resistance against the fungal pathogen Cladosporium fulvum. The Xa21 product has the classic receptor-kinase format — an extracellular LRR, a membrane-spanning region and an intracellular protein-kinase domain (see [1] for references of the earlier literature). The Cf gene products contain extracellular LRRs and a transmembrane
The Pseudomonas tomato resistance (Pto) gene
The Pto gene for bacterial speck resistance in tomato, which encodes a serine/threonine protein kinase (PK) with no LRR region, requires the presence of the linked NBS-LRR gene Prf (Pseudomonas resistance and fenthion sensitivity) for activity (see 1, 2 for earlier original references). No other R genes in the PK class have been identified to date. An extensive mutational analysis has been reported recently that confirms that Pto is the receptor for the corresponding ligand encoded by the
The molecular basis of R-gene specificity
The flax L gene, a member of the TIR-NBS-LRR subclass, has provided an excellent system in which to analyse the molecular basis of R-gene specificity. Eleven alleles of the flax L gene, ten of which encode different flax rust resistance specificities, have been sequenced [16••]. The comparison of the allele sequences revealed that most alleles contain polymorphic bases spread across the whole coding region, with the largest variation in the LRR-coding region. Comparison of the predicted
Evolution of R genes and specificities
For an increasing number of R genes, including the NBS-LRR genes, evidence of the selection for diversity of codons encoding residues in the LRR region that are predicted to be solvent exposed, and hence may constitute ligand contact points, has been observed 6, 10••, 13, 17, 18, 19, 20. Like the initial analysis of Cf genes in tomato [17], subsequent comparison of DNA sequences within NBS-LRR gene loci has revealed evidence of past exchanges of blocks of sequence by recombination 6, 10••, 16••
The role of unequal exchange events at complex R loci
Re-assortment of sequence polymorphism by meiotic recombination is a principal factor in R-gene evolution. Where R genes exist as complexes of directly repeated genes that are related in sequence, two alternatives for sequence exchange are possible. First, ‘equal exchange’ in which the first gene in the complex may only recombine with the first gene in the homologous complex, the second gene with the second homologue, and so on. Second, ‘unequal exchange’ in which each gene in the sequence may
Molecular population genetics of R genes
Population genetic analysis of wild plant species can provide information concerning the frequencies and diversity of resistance alleles in nature, and on the selection forces maintaining resistance and leading to the evolution of new specificities in natural populations. The high level of genomic/molecular biological information that is accumulating on Arabidopsis and Arabidopsis–pathogen interactions is stimulating the increased use of this wild plant in population analysis of host–pathogen
Downstream resistance signalling components
Although not the topic of this review, one recent report is relevant to R-gene evolution. The authors cloned the Bs2 gene (for Xanthomonas blight resistance) from pepper and demonstrated that it functions in several Solanaceous species but not in species outside of the Solanceae [7•]. One interpretation of this observation is that downstream components of R-gene signalling pathways are co-adapted within species to particular R-gene products; a phenomenon referred to as ‘restricted taxonomic
Conclusions and future directions
Significant progress has been made during the past year in understanding the determinants of R-gene specificity and how these specificities evolve. In particular, mutational analysis of Pto in tomato and recombinational analysis of L alleles in flax have identified features of the two distinct classes of proteins encoded by these genes that are involved in recognition and signalling processes. In addition, the large-scale sequence analysis of complex R-gene haplotypes has shed light on the
Update
Since the submission of this review several new publications relevant to this topic have appeared. The cloning of a further Peronospora resistance gene from Arabidopsis, RPP13, has been reported [33]. Three specificities have been identified at the locus, which appears to be a single gene with highly variable multiple alleles that are subject to diversifying selection in the LRR region.
The first analysis demonstrating a biological role of alternative products, a feature shared by all
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
• of special interest
•• of outstanding interest
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