Effector biology during biotrophic invasion of plant cells

Chaudhari, Prateek; Ahmed, Bulbul; Joly, David L; Germain, Hugo

It is pertinent to demystify the terminological ambiguity around effectors since, until recently, their nomenclature was contingent upon host reactions. When a molecule from a particular pathogen modulates the host's defensive cover to increase the pathogen's fitness, it is called a virulence factor. However, when the same molecule is recognized by host immunoreceptors, thereby failing to augment pathogenicity and instead triggering a defense response, it is referred to as an avirulence factor. This variation in pathogenicity is a commonly-occurring phenomenon. A particular effector may be a virulence factor on one host and an avirulence factor on another, a situation observed even within a single plant species where interactions are race-specific. Because of this inconsistency, terms such as virulence and avirulence have their limitations, since they are dependent on the specific host system in which they have been observed. The above discussed terminology in plant pathology is thus rather different from that employed in the medical field. In plant immunity, the terms virulence and avirulence are mainly related to the plant's ability to resist or succumb to the pathogen, thus depending on plant genotype. 9 In the medical field, avirulence refers to the loss of a virulence component belonging to the pathogen. Consequently, an inclusive and neutral term such as "effector" is preferred, 20 as it accounts for all the molecules secreted by a pathogen during infection that alter host cell structure or function. 21 As mentioned earlier, Flor's work was instrumental in establishing the gene-for-gene concept. 9, 10 Flor was quite foresighted when he noted that, for each gene conditioning a reaction in the host, there is a corresponding gene that conditions pathogenicity in the pathogen. 9 His deduction came from studies on the inheritance of pathogenicity in flax rust (Melampsora lini) and on the inheritance of resistance in flax (Linum usitatissimum). 10 Many years later, the flax/flax rust pathosystem remains instrumental in our understanding of the molecular aspects of genefor-gene interactions. This pathosystem enabled inroads to be made in the molecular interaction between R-and Avr-protein, mainly through studies of L and M resistance genes and their corresponding Avr loci. Flax rust AvrL567 genes, whose products are recognized by the L5, L6, and L7 R-proteins of flax, are highly diverse and under diversifying selection pressure, with 12 sequence variants identified from six rust strains. 22 Ravensdale et al. 23 studied direct molecular interactions between L5 and L6 (two alleles of L) and their avirulence targets in detail. Sitedirected mutagenesis in AvrL567 and the construction of chimeric L-proteins revealed that the recognition specificities of L5 and L6 are conditioned by their leucine-rich repeat regions. Their study indicated that mutations in the TIR or NB-ARC domain also affect recognition, which prompted the authors to suggest that interaction with the Avr ligand directly competes with intramolecular interactions, causing R-protein activation. 23 The AvrM effector from flax rust also interacts directly with the flax R-protein M, and this interaction can also be observed in yeast two-hybrid assays. Catanzariti et al. showed that the C-terminal domain of AvrM is required for M-dependent cell-death, consistent with the fact that it interacts with M-protein in yeast. 24 Furthermore, these authors demonstrated that C-terminal 34 ami