Evolution of an avirulence gene, AVR1-CO39, concomitant with the evolution and differentiation of Magnaporthe oryzae.

The significance of AVR1-CO39, an avirulence gene of the blast fungus corresponding to Pi-CO39(t) in rice cultivars, during the evolution and differentiation of the blast fungus was evaluated by studying its function and distribution in Pyricularia spp. When the presence or absence of AVR1-CO39 was plotted on a dendrogram constructed from ribosomal DNA sequences, a perfect parallelism was observed between its distribution and the phylogeny of Pyricularia isolates. AVR1-CO39 homologs were exclusively present in one species, Pyricularia oryzae, suggesting that AVR1-CO39 appeared during the early stage of evolution of P. oryzae. Transformation assays showed that all the cloned homologs tested are functional as an avirulence gene, indicating that selection has maintained their function. Nevertheless, Oryza isolates (isolates virulent on Oryza spp.) in P. oryzae were exceptionally noncarriers of AVR1-CO39. All Oryza isolates suffered from one of the two types of known rearrangements at the Avr1-CO39 locus (i.e., G type and J type). These types were congruous to the two major lineages of Oryza isolates from Japan determined by MGR586 and MAGGY. These results indicate that AVR1-CO39 was lost during the early stage of evolution of the Oryza-specific subgroup of P. oryzae. Interestingly, its corresponding resistance gene, Pi-CO39(t), is not widely distributed in Oryza spp.

Speciation in Pyricularia inferred from multilocus phylogenetic analysis.

Pyricularia isolates from various host plants were subjected to a multilocus phylogenetic analysis based on rDNA-ITS, actin, beta-tubulin, and calmodulin loci. A combined gene tree resolved seven groups with 100% BS support, suggesting that they are monophyletic groups supported concordantly by all four loci. By incorporating biological and morphological species criteria, each of the seven groups was considered to be a current species. However, phylogenetic relationships among these species were unresolved in the single-gene trees and in the combined tree. Furthermore, the transition from concordance to conflict occurred more than once in the combined gene tree. They were interpreted by assuming that Pyricularia has evolved through repeated species radiation. The transition point other than the current species limit was considered to be the limit of the former species.