NB-LRR protein required for HR signalling mediated by both extra- and intracellular resistance proteins

• Published in: The Plant journal : for cell and molecular biology 2007-04, Vol.50 (1), p.14-28
• Main Authors: Gabriëls, Suzan H.E.J, Vossen, Jack H, Ekengren, Sophia K, Ooijen, Gerben van, Abd-El-Haliem, Ahmed M, Berg, Grardy C.M. van den, Rainey, Daphne Y, Martin, Gregory B, Takken, Frank L.W, Wit, Pierre J.G.M. de, Joosten, Matthieu H.A.J
• Format: Article
• Language: English
• Subjects: Agronomy. Soil science and plant productions; Amino Acid Sequence; arc domain; AVR gene; Biological and medical sciences; Botany; Cell death; Cf-4; Cladosporium - growth & development; Cladosporium - pathogenicity; Cladosporium fulvum; Cladosporium/growth & development/pathogenicity; confers resistance; dna interactions; Fulvia fulva; functional-analysis; Fundamental and applied biological sciences. Psychology; Fungi; Gene Expression Regulation, Plant; Gene Silencing; gene-products; Genes, Plant; Genetics; Genetics and breeding of economic plants; Hypersensitive response; Immunity, Innate - genetics; Intracellular signalling; Lycopersicon esculentum; Lycopersicon esculentum - genetics; Lycopersicon esculentum - metabolism; Lycopersicon esculentum - microbiology; Lycopersicon esculentum/genetics/metabolism/microbiology; MAP kinase; Molecular Sequence Data; Mutation; Nicotiana benthamiana; NRC1; Pest resistance; Plant Diseases - genetics; Plant Diseases - microbiology; Plant Diseases/genetics/microbiology; Plant pathogens; Plant Proteins - genetics; Plant Proteins - physiology; Plant Proteins/genetics/physiology; plant-disease resistance; Plants, Genetically Modified; Proteins; R protein; resistance protein analogue; Reverse Transcriptase Polymerase Chain Reaction; Signal transduction; Signal Transduction - genetics; Signal Transduction - physiology; Signal Transduction/genetics/physiology; Solanum; tobacco-mosaic-virus; tomato; tomatoes; Varietal selection. Specialized plant breeding, plant breeding aims; Virulence - genetics
• ISSN: 0960-7412; 1365-313X; 1365-313X
• DOI: 10.1111/j.1365-313X.2007.03027.x

Tomato (Solanum lycopersicum) Cf resistance genes confer hypersensitive response (HR)-associated resistance to strains of the pathogenic fungus Cladosporium fulvum that express the matching avirulence (Avr) gene. Previously, we identified an Avr4- responsive tomato (ART) gene that is required for Cf-4/Avr4-induced HR in Nicotiana benthamiana as demonstrated by virus-induced gene silencing (VIGS). The gene encodes a CC-NB-LRR type resistance (R) protein analogue that we have designated NRC1 ( NB-LRR protein required for HR-associated cell death 1). Here we describe that knock-down of NRC1 in tomato not only affects the Cf-4/Avr4-induced HR but also compromises Cf-4-mediated resistance to C. fulvum. In addition, VIGS using NRC1 in N. benthamiana revealed that this protein is also required for the HR induced by the R proteins Cf-9, LeEix, Pto, Rx and Mi. Transient expression of NRC1D⁴⁸¹V, which encodes a constitutively active NRC1 mutant protein, triggers an elicitor-independent HR. Subsequently, we transiently expressed this auto-activating protein in N. benthamiana silenced for genes known to be involved in HR signalling, thereby allowing NRC1 to be positioned in an HR signalling pathway. We found that NRC1 requires RAR1 and SGT1 to be functional, whereas it does not require NDR1 and EDS1. As the Cf-4 protein requires EDS1 for its function, we hypothesize that NRC1 functions downstream of EDS1. We also found that NRC1 acts upstream of a MAP kinase pathway. We conclude that Cf-mediated resistance signalling requires a downstream NB-LRR protein that also functions in cell death signalling pathways triggered by other R proteins.