Avirulence Genes in Cereal Powdery Mildews: The Gene-for-Gene Hypothesis 2.0

Abstract

The gene-for-gene hypothesis states that for each gene controlling resistance in the host, there is a corresponding, specific gene controlling avirulence in the pathogen. Allelic series of the cereal mildew resistance genes Pm3 and Mla provide an excellent system for genetic and molecular analysis of resistance specificity. Despite this opportunity for molecular research, avirulence genes in mildews remain underexplored. Earlier work in barley powdery mildew (B.g. hordei) has shown that the reaction to some Mla resistance alleles is controlled by multiple genes. Similarly, several genes are involved in the specific interaction of wheat mildew (B.g. tritici) with the Pm3 allelic series. We found that two mildew genes control avirulence on Pm3f: one gene is involved in recognition by the resistance protein as demonstrated by functional studies in wheat and the heterologous host Nicotiana benthamiana. A second gene is a suppressor, and resistance is only observed in mildew genotypes combining the inactive suppressor and the recognized Avr. We propose that such suppressor/avirulence gene combinations provide the basis of specificity in mildews. Depending on the particular gene combinations in a mildew race, different genes will be genetically identified as the "avirulence" gene. Additionally, the observation of two LINE retrotransposon-encoded avirulence genes in B.g. hordei further suggests that the control of avirulence in mildew is more complex than a canonical gene-for-gene interaction. To fully understand the mildew-cereal interactions, more knowledge on avirulence determinants is needed and we propose ways how this can be achieved based on recent advances in the field.

Keywords: avirulence gene; barley; powdery mildew; resistance gene; wheat.

FIGURE 1

Proposed models for Avr–R–Svr interactions in cereal powdery mildews. (A) Structure of the AvrPm3^a2/f2 effector family. Minimum and maximum sizes of each region as observed among family members are given in amino acids (aa) and differentiated with dark and light color shades, respectively. The YxC motif and the conserved cysteines are indicated in red. (B–D) Proposed Avr-R-Svr genetic models for the interpretation of genetic segregation ratios deviating from the canonical 1:1 single gene hypothesis. For readability, active and inactive alleles are distinguished with upper and lower case. Here, we have only considered examples of mildew Avr–R interactions where genetic segregation ratios and mapping data were consistent with at least two genetically independent loci being involved in avirulence. (B) Considering the Avr-R-Svr model and a genetic segregation ratio of 1:0:3, avirulence results from a combination of an inactive suppressor allele (svr) and an active avirulence allele (AVR). In the presence of the active SVR and the active AVR, the interaction result in virulence. A molecular model for this suppression scenario is depicted in (E). (C) Considering the Avr-R-Svr model, a genetic segregation ratio of 3:0:1 can be explained by a model involving one suppressor locus and two loci for avirulence (AVR¹ and AVR²). Importantly, the second locus for avirulence (AVR²) is not polymorphic in this cross, thus only the active allele (AVR²) is present. In this model, the active SVR is only effective in suppressing AVR² but not AVR¹. A molecular model for this suppression scenario is depicted in (F). (D) Considering the Avr-R-Svr model, a genetic segregation ratio of 2:1:1 can be explained by a model involving one suppressor locus and two loci for avirulence (AVR¹ and AVR²). Importantly, the second locus for avirulence (AVR²) is not polymorphic in this cross, thus only the active allele (AVR²) is present. In this model, the active SVR can fully suppress AVR² but is only partially effective on AVR¹, thus resulting in avirulence in the first case and intermediate virulence in the second. A molecular model for this suppression scenario is depicted in (G). (E–G) Proposed suppression scenarios based on the genetic models described in (B–D) and resulting in three major phenotypic classes of avirulence ‘A,’ virulence ‘V,’ and intermediate virulence ‘I.’ Only active suppressor and avirulence proteins are shown. For simplicity, AVR–R interactions are represented as physical binding. Absence of suppression is depicted as a red “X” sign. Partial suppression is depicted as a dotted line and a red “∼” sign. The phenotype resulting from single and combined interactions is indicated.