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Role of host specificity in the speciation of Ascochyta pathogens of cool season food legumes

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Abstract

Ascochyta/legume interactions are attractive systems for addressing evolutionary questions about the role of host specificity in fungal speciation because many wild and cultivated cool season food legumes are infected by Ascochyta spp. and most of these fungi have described teleomorphs (Didymella spp.) that can be induced in the laboratory. Recent multilocus phylogenetic analyses of a worldwide sample of Ascochyta fungi causing ascochyta blights of chickpea (Cicer arietinum), faba bean (Vicia faba), lentil (Lens culinaris), and pea (Pisum sativum) have revealed that fungi causing disease on each host formed a monophyletic group. Host inoculations of these fungi demonstrated that they were host-specific, causing disease only on the host species from which they were isolated. In contrast to the strict association between monophyletic group and host observed for pathogens of cultivated legumes, Ascochyta fungi causing disease on wild bigflower vetch (Vicia grandiflora) were polyphyletic. Genetic crosses between several pairs of closely related, host-specific, and phylogenetically distinct Ascochyta fungi were fully sexually compatible. Progeny from these crosses had normal cultural morphology and segregation of molecular markers indicating a lack of intrinsic, post-zygotic mating barriers between the parental taxa. However, when progeny from a cross between a faba bean-adapted isolate (A. fabae) and a pea-adapted isolate (A. pisi) were assessed for their pathogenicity to the parental hosts, almost all progeny were non-pathogenic to either faba bean or pea. These results suggest that although these fungi have retained the ability to mate and produce progeny with normal saprophytic fitness, progeny are severely compromised in parasitic fitness. The host specificity of these fungi, coupled with the inability of hybrid progeny to colonize and reproduce on a host, may constitute strong extrinsic, pre-zygotic and post-zygotic mating barriers in these fungi and promote the genetic isolation and speciation of host-specific taxa. A phylogeny of the host plants is also being developed, and with more extensive sampling of pathogens and hosts from sympatric populations in the centre of origin, the hypothesis of cospeciation of pathogens and hosts will be tested. The objectives of this review are: (1) to summarize recent phylogenetic, host specificity and speciation studies of Ascochyta fungi, and (2) to suggest how current and future research using these pathosystems may lead to a better understanding of the role of host specificity in the speciation of plant-pathogenic fungi and the cospeciation of pathogens and their hosts.

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Acknowledgements

The author would like to thank Kelly Steele and Martin Wojciechowski, Arizona State University, for providing unpublished data presented in Fig. 2. The author would also like to thank Martin Chilvers, Washington State University, and an anonymous referee for greatly improving the manuscript.

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Correspondence to Tobin L. Peever.

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Peever, T.L. Role of host specificity in the speciation of Ascochyta pathogens of cool season food legumes. Eur J Plant Pathol 119, 119–126 (2007). https://doi.org/10.1007/s10658-007-9148-2

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