Journal Article

Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing

de Jonge, Ronnie, Bolton, Melvin D, Peter van Esse, H, Santhanam, Parthasarathy, Thomma, Bart P. H. J, Usami, Toshiyuki, Subbarao, Krishna V, Maruthachalam, Karunakaran, Saber, Mojtaba Keykha, Zhang, Zhao, Lievens, Bart

2012

Overview

Fungal plant pathogens secrete effector molecules to establish disease on their hosts, and plants in turn use immune receptors to try 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 Verticillium 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, and 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. 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 toward F. oxysporum in tomato, showing that this immune receptor is involved in resistance against multiple fungal pathogens.

• Publisher: National Academy of Sciences,National Acad Sciences
• Subject: albo-atrum / Alleles / Arabidopsis / Base Sequence / Biological Sciences / Cercospora beticola / Colletotrichum / Disease Resistance / Disease Resistance - genetics / Evolution / Evolution, Molecular / Fungal Proteins / Fungal Proteins - metabolism / Fungi / Fusarium / Fusarium - genetics / Fusarium oxysporum / Gene expression / Gene transfer / Gene Transfer, Horizontal / Genes, Fungal / Genes, Fungal - genetics / Genetic Variation / genetics / genome / Genome, Fungal / Genome, Fungal - genetics / Genomes / Genomics / horizontal gene-transfer / host / hosts / immunology / Lycopersicon esculentum / mechanisms / metabolism / methods / microbiology / Molecular Sequence Data / natriuretic peptides / Nicotiana - genetics / Nicotiana - microbiology / Nicotiana benthamiana / Nucleotide sequence / Open reading frames / pathogenicity / Pathogens / Peptides / physiology / Plant Diseases / Plant Diseases - genetics / Plant Diseases - immunology / Plant Diseases - microbiology / plant pathogenic fungi / Plant pathogens / Plant Proteins / Plant Proteins - metabolism / Plants / Proteins / Receptors / Receptors, Cell Surface / Receptors, Cell Surface - metabolism / resistance / Ribonucleic acid / RNA / Sequence Analysis, RNA / Sequence Analysis, RNA - methods / Sequence Homology, Amino Acid / Sequencing / soil-borne diseases / Solanum lycopersicum / Solanum lycopersicum - immunology / Solanum lycopersicum - microbiology / Solanum lycopersicum var. lycopersicum / Tobacco / Tomatoes / Transcriptome / Transcriptome - genetics / vascular wilt / Verticillium / Verticillium - genetics / Verticillium - pathogenicity / Verticillium albo-atrum / Verticillium dahliae / Virulence / Virulence - genetics / Wilt / wilting / Xanthomonas axonopodis