title: The AVR2-SIX5 gene pair is required to activate I-2-mediated immunity in tomato.
abstract: Plant-invading microbes betray their presence to a plant by exposure of antigenic molecules such as small, secreted proteins called 'effectors'. In Fusarium oxysporum f. sp. lycopersici (Fol) we identified a pair of effector gene candidates, AVR2-SIX5, whose expression is controlled by a shared promoter. The pathogenicity of AVR2 and SIX5 Fol knockouts was assessed on susceptible and resistant tomato (Solanum lycopersicum) plants carrying I-2. The I-2 NB-LRR protein confers resistance to Fol races carrying AVR2. Like Avr2, Six5 was found to be required for full virulence on susceptible plants. Unexpectedly, each knockout could breach I-2-mediated disease resistance. So whereas Avr2 is sufficient to induce I-2-mediated cell death, Avr2 and Six5 are both required for resistance. Avr2 and Six5 interact in yeast two-hybrid assays as well as in planta. Six5 and Avr2 accumulate in xylem sap of plants infected with the reciprocal knockouts, showing that lack of I-2 activation is not due to a lack of Avr2 accumulation in the SIX5 mutant. The effector repertoire of a pathogen determines its host specificity and its ability to manipulate plant immunity. Our findings challenge an oversimplified interpretation of the gene-for-gene model by showing requirement of two fungal genes for immunity conferred by one resistance gene.
authors.affiliation: Molecular Plant Pathology, SILS, Faculty of Science, University of Amsterdam, Amsterdam, the Netherlands.
authors.forename: Lisong
authors.initials: L
authors.lastname: Ma
authors.affiliation: Molecular Plant Pathology, SILS, Faculty of Science, University of Amsterdam, Amsterdam, the Netherlands.
authors.forename: Petra M
authors.initials: PM
authors.lastname: Houterman
authors.affiliation: Molecular Plant Pathology, SILS, Faculty of Science, University of Amsterdam, Amsterdam, the Netherlands.
authors.forename: Fleur
authors.initials: F
authors.lastname: Gawehns
authors.affiliation: Molecular Plant Pathology, SILS, Faculty of Science, University of Amsterdam, Amsterdam, the Netherlands.
authors.forename: Lingxue
authors.initials: L
authors.lastname: Cao
authors.affiliation: Molecular Plant Pathology, SILS, Faculty of Science, University of Amsterdam, Amsterdam, the Netherlands.|Department of Agricultural, Forest and Food Sciences, University of Turin, I-10095, Grugliasco, Italy.
authors.forename: Fabiano
authors.initials: F
authors.lastname: Sillo
authors.affiliation: Molecular Plant Pathology, SILS, Faculty of Science, University of Amsterdam, Amsterdam, the Netherlands.
authors.forename: Hanna
authors.initials: H
authors.lastname: Richter
authors.affiliation: Molecular Plant Pathology, SILS, Faculty of Science, University of Amsterdam, Amsterdam, the Netherlands.
authors.forename: Myriam J
authors.initials: MJ
authors.lastname: Clavijo-Ortiz
authors.affiliation: Molecular Plant Pathology, SILS, Faculty of Science, University of Amsterdam, Amsterdam, the Netherlands.
authors.forename: Sarah M
authors.initials: SM
authors.lastname: Schmidt
authors.affiliation: Laboratory of Biochemistry, Wageningen University, Wageningen, the Netherlands.
authors.forename: Sjef
authors.initials: S
authors.lastname: Boeren
authors.affiliation: Laboratory of Biochemistry, Wageningen University, Wageningen, the Netherlands.
authors.forename: Jacques
authors.initials: J
authors.lastname: Vervoort
authors.affiliation: Molecular Plant Pathology, SILS, Faculty of Science, University of Amsterdam, Amsterdam, the Netherlands.
authors.forename: Ben J C
authors.initials: BJ
authors.lastname: Cornelissen
authors.affiliation: Molecular Plant Pathology, SILS, Faculty of Science, University of Amsterdam, Amsterdam, the Netherlands.
authors.forename: Martijn
authors.initials: M
authors.lastname: Rep
authors.affiliation: Molecular Plant Pathology, SILS, Faculty of Science, University of Amsterdam, Amsterdam, the Netherlands.
authors.forename: Frank L W
authors.initials: FL
authors.lastname: Takken
mesh_terms: D016923:Cell Death; D060467:Disease Resistance / Q000276:immunology; D005656:Fungal Proteins / Q000235:genetics* / Q000378:metabolism; D005670:Fusarium / Q000235:genetics / Q000472:pathogenicity; D055786:Gene Knockout Techniques; D005800:Genes, Fungal; D018551:Solanum lycopersicum / Q000166:cytology / Q000276:immunology* / Q000382:microbiology*; D010935:Plant Diseases / Q000276:immunology / Q000382:microbiology; D057865:Plant Immunity; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism*; D011485:Protein Binding; D014026:Nicotiana / Q000166:cytology; D020798:Two-Hybrid System Techniques; D052584:Xylem / Q000378:metabolism
chemical_list: D005656:Fungal Proteins; D010940:Plant Proteins
keywords: Fusarium oxysporum; I-2; avirulence; disease resistance; effector proteins; gene-for-gene; tomato (Solanum lycopersicum)