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Open Access Highly Accessed Research article

Cross-kingdom host shifts of phytomyxid parasites

Sigrid Neuhauser12*, Martin Kirchmair1, Simon Bulman3 and David Bass2

Author Affiliations

1 Institute of Microbiology, Leopold-Franzens University Innsbruck, Technikerstraße 25, 6020 Innsbruck, Austria

2 Department of Life Sciences, Natural History Museum London, Cromwell Road, London SW7 5BD, UK

3 The New Zealand Institute for Plant & Food Research Limited, Private Bag 4704, Christchurch 8140, New Zealand

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BMC Evolutionary Biology 2014, 14:33  doi:10.1186/1471-2148-14-33

Published: 23 February 2014

Abstract

Background

Phytomyxids (plasmodiophorids and phagomyxids) are cosmopolitan, obligate biotrophic protist parasites of plants, diatoms, oomycetes and brown algae. Plasmodiophorids are best known as pathogens or vectors for viruses of arable crops (e.g. clubroot in brassicas, powdery potato scab, and rhizomania in sugar beet). Some phytomyxid parasites are of considerable economic and ecologic importance globally, and their hosts include important species in marine and terrestrial environments. However most phytomyxid diversity remains uncharacterised and knowledge of their relationships with host taxa is very fragmentary.

Results

Our molecular and morphological analyses of phytomyxid isolates–including for the first time oomycete and sea-grass parasites–demonstrate two cross-kingdom host shifts between closely related parasite species: between angiosperms and oomycetes, and from diatoms/brown algae to angiosperms. Switching between such phylogenetically distant hosts is generally unknown in host-dependent eukaryote parasites. We reveal novel plasmodiophorid lineages in soils, suggesting a much higher diversity than previously known, and also present the most comprehensive phytomyxid phylogeny to date.

Conclusion

Such large-scale host shifts between closely related obligate biotrophic eukaryote parasites is to our knowledge unique to phytomyxids. Phytomyxids may readily adapt to a wide diversity of new hosts because they have retained the ability to covertly infect alternative hosts. A high cryptic diversity and ubiquitous distribution in agricultural and natural habitats implies that in a changing environment phytomyxids could threaten the productivity of key species in marine and terrestrial environments alike via host shift speciation.

Keywords:
Plasmodiophorid; Plant pathogen; Evolution; Taxonomy; Host range; Plasmodiophora; Polymyxa; Woronina; Sorosphaerula; Spongospora