Intragenic recombination generated two distinct Cf genes that mediate AVR9 recognition in the natural population of Lycopersicon pimpinellifolium

Abstract

Resistance gene Cf-9 of cultivated tomato (Lycopersicon esculentum) confers recognition of the AVR9 elicitor protein of the fungal pathogen Cladosporium fulvum. The Cf-9 locus, containing Cf-9 and four homologs (Hcr9s), originates from Lycopersicon pimpinellifolium (Lp). We examined naturally occurring polymorphism in Hcr9s that confer AVR9 recognition in the Lp population. AVR9 recognition occurs frequently throughout this population. In addition to Cf-9, we discovered a second gene in Lp, designated 9DC, which also confers AVR9 recognition. Compared with Cf-9, 9DC is more polymorphic, occurs more frequently, and is more widely spread throughout the Lp population, suggesting that 9DC is older than Cf-9. The sequences of Cf-9 and 9DC suggest that Cf-9 evolved from 9DC by intragenic recombination between 9DC and another Hcr9. The fact that the 9DC and Cf-9 proteins differ in 61 aa residues, and both mediate recognition of AVR9, shows that in nature Hcr9 proteins with the same recognitional specificity can vary significantly. R ecognition of a diverse range of pathogens, followed by an adequate defense response, is crucial for the survival of plants. Resistance (R) genes, which mediate recognition of products of matching avirulence (Avr) genes, play a key role in the recognition of pathogens (1). Most R gene products contain a leucine-rich repeat (LRR) domain with putative solventexposed amino acid residues that decorate the surface of the protein, where specific interactions with other proteins are thought to occur (2). R proteins with different specificities differ predominantly at putative solvent-exposed positions, which are often thought to result from adaptive evolution (3).Plants need to generate R genes with new specificities because pathogens continuously try to circumvent recognition by the host plant. New R genes are thought to evolve by sequence exchange between homologous genes and by accumulation of random point mutations in codons that encode amino acids located at putative solvent-exposed positions (3, 4).The continuous generation of new recognitional specificities by the host, followed by subsequent adaptation of the pathogen to circumvent this recognition, can be seen as an ''arms race'' between plants and pathogens (5). Recent observations suggest that in nature, this arms race is a slow process and that the battle between plants and pathogens is more likely to be similar to ''trench warfare.'' In this model, frequencies of R genes in the plant population fluctuate in time, following the frequency of the matching Avr gene in the pathogen population (6). Consistent with this model, gene-for-gene pairs like AvrRpm1-RPM1 and AvrPto-Pto are ancient (6, 7), and plants carrying or lacking the RPM1 gene coexist in the plant population (6).The tomato R genes Cf-9 and Cf-4 mediate recognition of strains of the leaf mold fungus Cladosporium fulvum carrying the Avr9 or Avr4 gene, respectively (8). Recognition by resistant plants results in the activation of multiple defense responses that limit further fun...

From Guard to Decoy: A New Model for Perception of Plant Pathogen Effectors

“…First, R genes are typically polymorphic in natural plant populations. This has been observed repeatedly in both single gene studies (e.g., Arabidopsis RPM1 [Stahl et al, 1999] and tomato Cf-9 [Van der Hoorn et al, 2001]) and genome-wide analyses (Bakker et al, 2006;Clark et al, 2007). Second, effector targets are under selection for decreased binding affinity to effectors.…”

Natural Variation in the Pto Pathogen Resistance Gene Within Species of Wild Tomato (Lycopersicon). I. Functional Analysis of Pto Alleles

“…Up until now, studies of the molecular evolution of resistance genes in plants have been limited to a few model plant species and their closest relatives (Caicedo et al 1999;Stahl et al 1999;van der Hoorn et al 2001;Tian et al 2002;Mauricio et al 2003). Here we describe the sequence variability at the Pto locus among seven close relatives of the model plant species L. esculentum.…”

“…Population genetic analyses of allelic variation in Arabidopsis (Rps2, Rpm1, and Rps5) and Lycopersicon spp. (Cf-9) revealed that pathogen recognition specificity corresponded to sequence variation at these loci (Caicedo et al 1999;Stahl et al 1999;van der Hoorn et al 2001;Tian et al 2002;Mauricio et al 2003). Additional sequence-based analyses combined with functional tests are needed to explore the evolutionary consequences of interactions between hosts and pathogens.…”

Evolution of plant resistance at the molecular level: ecological context of species interactions

“…As many as 24 major resistance phenotypes were detectable in this host population. High amounts of molecular diversity both within and among natural populations have also been detected at complex R-loci in Lactuca spp., Lycopersicon pimpinellifolium and Phaseolus vulgaris Neema et al, 2001; Van der Hoorn et al, 2001), and for concentrations of furanocoumarins, which deter herbivores attacking Pastinaca sativa (Berenbaum and Zangerl, 1998). Although genetic variation is common, some host populations appear to lack detectable variation for resistance to insects or pathogens (Nakamura et al, 1995;Burdon and Thrall, 1999).…”

“…Based on the simple genetic determinism emerging from Flor's work (1956), models of resistance evolution have led to the idea that negative frequency-dependent selection might maintain resistance polymorphisms in host plants (reviewed in Leonard, 1997;Bergelson et al, 2001a). Thus, frequency-dependent selection has been invoked to explain maintenance of polymorphisms in A. thaliana and L. pimpinellifolium (Stahl et al, 1999;Bergelson et al, 2001b;Van der Hoorn et al, 2001).…”