Life, death and rebirth of avirulence effectors in a fungal pathogen of B rassica crops, L eptosphaeria maculans

Summary In agricultural systems, major (R) genes for resistance in plants exert strong selection pressure on cognate/corresponding avirulence effector genes of phytopathogens. However, a complex interplay often exists between trade‐offs linked to effector function and the need to escape R gene recognition. Here, using the Leptosphaeria maculans–oilseed rape pathosystem we review evolution of effectors submitted to multiple resistance gene selection. Characteristics of this pathosystem include a crop in which resistance genes have been deployed intensively resulting in ‘boom and bust’ cycles; a fungal pathogen with a high adaptive potential in which seven avirulence genes are cloned and for which population surveys have been coupled with molecular analysis of events responsible for virulence. The mode of evolution of avirulence genes, all located in dispensable parts of the ‘two‐speed’ genome, is a highly dynamic gene‐specific process. In some instances, avirulence genes are readily deleted under selection. However, others, even when located in the most plastic genome regions, undergo only limited point mutations or their avirulence phenotype is ‘camouflaged’ by another avirulence gene. Thus, while hundreds of effector genes are present, some effectors are likely to have an important and nonredundant function, suggesting functional redundancy and dispensability of effectors might not be the rule. Contents Summary 526 I. Introduction 526 II. A new crop, novel resistance genes and ‘boom and bust’ cycles 527 III. The ‘two‐speed’ genome and specific genome environment of avirulence genes in Leptosphaeria maculans 527 IV. Deletion and other types of inactivations: the easy way to go? 529 V. Is extinction the common scheme? 529 VI. ‘Rebirth’ of AvrLm3 530 VII.