Complex Interactions between Fungal Avirulence Genes and Their Corresponding Plant Resistance Genes and Consequences for Disease Resistance Management.

Yohann Petit-Houdenot,Isabelle Fudal

doi:10.3389/fpls.2017.01072

Abstract

During infection, pathogens secrete an arsenal of molecules, collectively called effectors, key elements of pathogenesis which modulate innate immunity of the plant and facilitate infection. Some of these effectors can be recognized directly or indirectly by resistance (R) proteins from the plant and are then called avirulence (AVR) proteins. This recognition usually triggers defense responses including the hypersensitive response and results in resistance of the plant. R—AVR gene interactions are frequently exploited in the field to control diseases. Recently, the availability of fungal genomes has accelerated the identification of AVR genes in plant pathogenic fungi, including in fungi infecting agronomically important crops. While single AVR genes recognized by their corresponding R gene were identified, more and more complex interactions between AVR and R genes are reported (e.g., AVR genes recognized by several R genes, R genes recognizing several AVR genes in distinct organisms, one AVR gene suppressing recognition of another AVR gene by its corresponding R gene, two cooperating R genes both necessary to recognize an AVR gene). These complex interactions were particularly reported in pathosystems showing a long co-evolution with their host plant but could also result from the way agronomic crops were obtained and improved (e.g., through interspecific hybridization or introgression of resistance genes from wild related species into cultivated crops). In this review, we describe some complex R—AVR interactions between plants and fungi that were recently reported and discuss their implications for AVR gene evolution and R gene management.

Highlights

During infection, pathogens secrete an arsenal of molecules, collectively called effectors, key elements of pathogenesis which modulate innate immunity of the plant and facilitate infection (Oliva et al, 2010)
Under the selection pressure exerted by R genes, pathogens can become virulent through evolution of their AVR gene repertoire
Mechanisms leading to virulence include complete deletion, inactivation, or down-regulation of the AVR gene, or point mutations allowing recognition to be evaded while maintaining the virulence function of the AVR protein (Jones and Dangl, 2006; Guttman et al, 2014)

Summary

INTRODUCTION

Pathogens secrete an arsenal of molecules, collectively called effectors, key elements of pathogenesis which modulate innate immunity of the plant and facilitate infection (Oliva et al, 2010). NLR are multi-domain proteins containing a C-terminal leucinerich repeat (LRR) domain, a central nucleotide-binding (NB) domain and a N-terminal domain often composed of a Toll/interleukin-1 receptor (TIR) or a coiled-coil (CC) domain (Takken and Goverse, 2012) Their multi-domain structure allows R proteins to simultaneously recognize AVR proteins and trigger plant defense reactions. LepR3 resistance was rapidly overcome in parts of Australia soon after its introduction (Sprague et al, 2006) as a consequence of the previous use of Rlm cultivars and the deletion of AvrLm1 in a high proportion of Australian L. maculans isolates (Gout et al, 2007). The first molecular events leading to virulence toward Rlm mainly corresponded to drastic events (deletion, accumulation of mutations) and to three amino acid changes without major modification of protein structure (Daverdin et al, 2012; Blondeau et al, 2015). In contrast to the AvrLm1/Rlm1–LepR3 interaction, the Frontiers in Plant Science | www.frontiersin.org

A BIPARTITE AVIRULENCE GENE NECESSARY FOR RECOGNITION BY ONE RESISTANCE GENE

CONCLUDING REMARKS