Submitted to: Proceedings of the National Academy of Sciences
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/17/2012
Publication Date: 3/13/2012
Citation: Dejonge, R., vanEsse, P., Maruthachalam, K., Bolton, M.D., Santhanam, P., Saber, M.K., Zhang, Z., Usami, T., Lievens, B., Subbarao, K.V., Thomma, B.P. 2012. Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proceedings of the National Academy of Sciences. 109(13):5110-5115. Interpretive Summary: Plant pathogens produce proteins during infection called effectors. These effectors help to establish disease unless they are recognized by resistance proteins in plants. When resistance proteins recognize effectors, a defense reaction occurs that stops the invading pathogen. Tomato plants that have the Ve1 resistance gene are immune to infection by strains of Verticillium dahliae that produce the effector called Ave1. Despite the use of several strategies, cloning of Ave1 has previously proven unsuccessful. In this paper, Ave1 was identified by comparing the genomes of several race 1 isolates that are known to have Ave1 against race 2 isolates that lack Ave1. Interesting, the gene encoding Ave1 is most similar to plant genes, suggesting that V. dahliae obtained the gene directly from plants through a process called horizontal gene transfer. The only plant pathogens known to have the Ave1 gene were Xanthomonas axonopodis, Colletotrichum higginsianum, Cercospora beticola, and Fusarium oxysporum f. sp. lycopersici. The Ave1 genes of F. oxysporum and C. beticola were shown to activate resistance responses in the presence of Ve1 in tobacco. Although C. beticola is a sugar beet pathogen and therefore functional analysis of Ve1 against C. beticola cannot be obtained in tomato, tomato plants harboring Ve1 were resistant to infection by F. oxysporum sp. lycopersici.
Technical Abstract: Fungal plant pathogens secrete effector molecules to establish disease on their hosts, while plants in turn utilize immune receptors to intercept these effectors. The tomato immune receptor Ve1 governs resistance to race 1 strains of the soil-borne vascular wilt fungi Verticillium dahliae and V. albo-atrum, but the corresponding Verticillium effector remained unknown thus far. By high-throughput population genome sequencing, a single 50 Kb sequence stretch was identified that only occurs in race 1 strains, while subsequent transcriptome sequencing of Verticillium-infected Nicotiana benthamiana plants revealed only a single highly expressed ORF in this region, designated Ave1 (for Avirulence on Ve1 tomato). Functional analyses confirmed that Ave1 activates Ve1-mediated resistance and demonstrated that Ave1 markedly contributes to fungal virulence, not only on tomato but also on Arabidopsis. Interestingly, Ave1 is homologous to a widespread family of plant natriuretic peptides (PNPs). Besides plants, homologous proteins were only found in the bacterial plant pathogen Xanthomonas axonopodis and the plant pathogenic fungi Colletotrichum higginsianum, Cercospora beticola and Fusarium oxysporum f. sp. lycopersici. The distribution of Ave1 homologs, coincident with the presence of Ave1 within a flexible genomic region, strongly suggests that Verticillium acquired Ave1 from plants through horizontal gene transfer. Remarkably, by transient expression we show that also the Ave1 homologs from F. oxysporum and C. beticola can activate Ve1-mediated resistance. In line with this observation, Ve1 was found to mediate resistance towards F. oxysporum in tomato, showing that this immune receptor is involved in resistance against multiple fungal pathogens.