Formae speciales of cereal powdery mildew: close or distant relatives?

Powdery mildew is an important disease of cereals, affecting both grain yield and end-use quality. The causal agent of powdery mildew on cereals, Blumeria graminis, has been classified into eight formae speciales (ff.spp.), infecting crops and wild grasses. Advances in research on host specificity and resistance, and on pathogen phylogeny and origins, have brought aspects of the subspecific classification system of B. graminis into ff.spp. into question, because it is based on adaptation to certain hosts rather than strict host specialization. Cereals therefore cannot be considered as typical non-hosts to non-adapted ff.spp. We introduce the term 'non-adapted resistance' of cereals to inappropriate ff.spp. of B. graminis, which involves both pathogen-associated molecular pattern-triggered immunity (PTI) and effector-triggered immunity (ETI). There is no clear distinction between the mechanisms of resistance to adapted and non-adapted ff.spp. Molecular evolutionary data suggest that the taxonomic grouping of B. graminis into different ff.spp. is not consistent with the phylogeny of the fungus. Imprecise estimates of mutation rates and the lack of genetic variation in introduced populations may explain the uncertainty with regard to divergence times, in the Miocene or Holocene epochs, of ff.spp. of B. graminis which infect cereal crop species. We propose that most evidence favours divergence in the Holocene, during the course of early agriculture. We also propose that the forma specialis concept should be retained for B. graminis pathogenic on cultivated cereals to include clades of the fungus which are strongly specialized to these hosts, i.e. ff.spp. hordei, secalis and tritici, as well as avenae from cultivated A. sativa, and that the forma specialis concept should no longer be applied to B. graminis from most wild grasses.

Genetic and forma specialis diversity in Blumeria graminis of cereals and its implications for host-pathogen co-evolution.

SUMMARY The grass powdery mildew fungus, Blumeria graminis is classified into eight formae speciales (ff.spp.) based on strict host specialization. However, evidence suggests that host ranges extend to more than one genus and are particularly diverse among samples from the Middle East, the proposed centre of origin and diversification of crop plants. This study investigated whether geographical origin, host species or both determine the genetic variation in B. graminis that is found in cereals, sampled from Europe, Asia and North America, and whether there is any evidence for co-evolution between pathogen and host. Phylogenetic analysis of nucleotide sequence variation within the ribosomal DNA Internal Transcribed Spacer (ITS) regions and the beta-tubulin (tub2) gene gives rise to two dendrograms with different topologies. In both trees, isolates of B. graminis from cultivated cereals are grouped according to their principal host genus. This grouping was supported by amplified fragment length polymorphism (AFLP) analysis and cross-infectivity tests. However, there was no evidence of co-evolution. There was far greater divergence between ff.spp. in tub2 sequences than ITS regions and a faster rate of mutation of tub2, especially in the third base position of exons. It is proposed that variation in the rDNA-ITS regions is constrained either by their functional role in the processing of rDNA precursor molecules or by concerted evolution, hence limiting their use in phylogenetic studies. AFLP data suggests an overall lack of correlation between geographical and genetic distances. This may be related to the long distance dispersal exhibited by B. graminis.