Successful search for a resistance gene in tomato targeted against a virulence factor of a fungal pathogen

Laugé, R.; Joosten, M.H.A.J.; Haanstra, J.P.W.; Goodwin, P. H.; Lindhout, P.; Wit, P.J.G.M. de

doi:10.1073/pnas.95.15.9014

Cited by 121 publications

(92 citation statements)

References 29 publications

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“…However, necrotic symptoms developed on the MM-Cf-0 and MM-Cf-4 plants after inoculation with PVX::MfEcp2 were less severe than those developed on the MM-Cf-Ecp2 line and did not lead to lethality. As expected (17), inoculations of MM-Cf-0 and MM-Cf-4 plants with PVX::Ecp2 induced only mosaic symptoms, typical for PVX infections. Finally, inoculations with PVX:: MfEcp2-2 and PVX::MfEcp2-3 did not trigger HR or necrosis on any of the tomato lines tested, but induced only systemic mosaic symptoms typical for PVX infections (Fig.…”

Section: Necrosis-and Hr-associated Recognition Of M Fijiensis Ecp2 Inmentioning

confidence: 69%

Tomato Cf resistance proteins mediate recognition of cognate homologous effectors from fungi pathogenic on dicots and monocots

Stergiopoulos

Burg²,

Ökmen³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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Most fungal effectors characterized so far are species-specific and facilitate virulence on a particular host plant. During infection of its host tomato, Cladosporium fulvum secretes effectors that function as virulence factors in the absence of cognate Cf resistance proteins and induce effector-triggered immunity in their presence. Here we show that homologs of the C. fulvum Avr4 and Ecp2 effectors are present in other pathogenic fungi of the Dothideomycete class, including Mycosphaerella fijiensis, the causal agent of black Sigatoka disease of banana. We demonstrate that the Avr4 homolog of M. fijiensis is a functional ortholog of C. fulvum Avr4 that protects fungal cell walls against hydrolysis by plant chitinases through binding to chitin and, despite the low overall sequence homology, triggers a Cf-4-mediated hypersensitive response (HR) in tomato. Furthermore, three homologs of C. fulvum Ecp2 are found in M. fijiensis, one of which induces different levels of necrosis or HR in tomato lines that lack or contain a putative cognate Cf-Ecp2 protein, respectively. In contrast to Avr4, which acts as a defensive virulence factor, M. fijiensis Ecp2 likely promotes virulence by interacting with a putative host target causing host cell necrosis, whereas Cf-Ecp2 could possibly guard the virulence target of Ecp2 and trigger a Cf-Ecp2-mediated HR. Overall our data suggest that Avr4 and Ecp2 represent core effectors that are collectively recognized by single cognate Cfproteins. Transfer of these Cf genes to plant species that are attacked by fungi containing these cognate core effectors provides unique ways for breeding disease-resistant crops.Cladosporium fulvum | Mycosphaerella fijiensis | effector-triggered immunity | biotrophy | toxigenic peptides

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Section: Necrosis-and Hr-associated Recognition Of M Fijiensis Ecp2 Inmentioning

confidence: 69%

Tomato Cf resistance proteins mediate recognition of cognate homologous effectors from fungi pathogenic on dicots and monocots

Stergiopoulos

Burg²,

Ökmen³

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

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172

212

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“…Accessions that contain 9DC, like PI126946, have been used in breeding programs (23). ‡ Indeed, one AVR9-responsive commercial tomato cultivar was found to ‡ Boukema, I. W., Meeting on Cladosporium fulvum Cke in Tomato, February 26 -27, 1980, Wageningen, The Netherlands.…”

Section: Discussionmentioning

confidence: 99%

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

Hoorn

Kruijt

Roth

et al. 2001

Proc. Natl. Acad. Sci. U.S.A.

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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...

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“…During infection the pathogen secrets proteins into plant extracellular space. Upon expression, the gene encoding one of the secreted proteins, ECP2, induces HR and resistance to recombinant Potato virus X in nonhost plant Nicotiana paniculata (Lauge et al 2000), probably through recognition by Cf-ECP2 (Lauge et al 1998). Therefore ECP2 might be a specific Avr elicitor of C. fulvum nonhost resistance.…”

Section: Introductionmentioning

confidence: 99%

Cladosporium fulvum CfHNNI1 induces hypersensitive necrosis, defence gene expression and disease resistance in both host and nonhost plants

Cai

Zhou

et al. 2007

Plant Mol Biol

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Nonhost resistance as a durable and broadspectrum defence strategy is of great potential for agricultural applications. We have previously isolated a cDNA showing homology with genes encoding bZIP transcription factors from tomato leaf mould pathogen Cladosporium fulvum. Upon expression, the cDNA results in necrosis in C. fulvum host tomato and nonhost tobacco plants and is thus named CfHNNI1 (for C. fulvum host and nonhost plant necrosis inducer 1). In the present study we report the induction of necrosis in a variety of nonhost plant species belonging to three families by the transient in planta expression of CfHNNI1 using virus-based vectors. Additionally, transient expression of CfHNNI1 also induced expression of the HR marker gene LeHSR203 and greatly reduced the accumulation of recombinant Potato virus X. Stable CfHNNI1 transgenic tobacco plants were generated in which the expression of CfHNNI1 is under the control of the pathogeninducible hsr203J promoter. When infected with the oomycetes pathogen Phytophthora parasitica var. nicotianae, these transgenic plants manifested enhanced expression of CfHNNI1 and subsequent accumulation of CfHNNI1 protein, resulting in high expression of the HSR203J and PR genes, and strong resistance to the pathogen. The CfHNNI1 transgenic plants also exhibited induced resistance to Pseudomonas syringae pv. tabaci and Tobacco mosaic virus. Furthermore, CfHNNI1 was highly expressed and the protein was translocated into plant cells during the incompatible interactions between C. fulvum and host and nonhost plants. Our results demonstrate that CfHNNI1 is a potential general elicitor of hypersensitive response and nonhost resistance.

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Successful search for a resistance gene in tomato targeted against a virulence factor of a fungal pathogen

Cited by 121 publications

References 29 publications

Tomato Cf resistance proteins mediate recognition of cognate homologous effectors from fungi pathogenic on dicots and monocots

Tomato Cf resistance proteins mediate recognition of cognate homologous effectors from fungi pathogenic on dicots and monocots

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

Cladosporium fulvum CfHNNI1 induces hypersensitive necrosis, defence gene expression and disease resistance in both host and nonhost plants

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