Limits...
Cross-kingdom host shifts of phytomyxid parasites.

Neuhauser S, Kirchmair M, Bulman S, Bass D - BMC Evol. Biol. (2014)

Bottom Line: 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.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Microbiology, Leopold-Franzens University Innsbruck, Technikerstraße 25, 6020 Innsbruck, Austria. Sigrid.Neuhauser@uibk.ac.at.

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.

Show MeSH

Related in: MedlinePlus

Network analysis of plant parasitic Phytomyxea and potential host plants (shown as plant families following the taxonomy suggested onhttp://www.theplantlist.org, 20.06.2013). Phytomyxids can use alternative host plants during their life cycle. for the majority of species only haphazard reports of the host range are available, while for some agriculturally important species like of Spongospora subterranea, Polymyxa graminis, P. betae, and Plasmodiophora brassicae extensive host range studies are available, leading to a seemingly wider host range of these species. It is noteworthy that, despite this bias, all species for which targeted host range studies exist hosts belonging to monocot and dicot host plants can be found. Pink?=?monocot plant families, Blue?=?dicot plant families, Red font?=?Phytomyxids for which hosts belonging to both the monocot and dicot hosts were described.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
getmorefigures.php?uid=PMC4016497&req=5

Figure 4: Network analysis of plant parasitic Phytomyxea and potential host plants (shown as plant families following the taxonomy suggested onhttp://www.theplantlist.org, 20.06.2013). Phytomyxids can use alternative host plants during their life cycle. for the majority of species only haphazard reports of the host range are available, while for some agriculturally important species like of Spongospora subterranea, Polymyxa graminis, P. betae, and Plasmodiophora brassicae extensive host range studies are available, leading to a seemingly wider host range of these species. It is noteworthy that, despite this bias, all species for which targeted host range studies exist hosts belonging to monocot and dicot host plants can be found. Pink?=?monocot plant families, Blue?=?dicot plant families, Red font?=?Phytomyxids for which hosts belonging to both the monocot and dicot hosts were described.

Mentions: Furthermore, plasmodiophorids are known to rarely infect a range of so-called alternative hosts in which very limited (i.e. to single host cells) infections can be observed. Therefore, we conducted a comprehensive literature study to identify and summarise possible alternative hosts (Figure 4, Additional file 1: Table S2). Interactions with alternative hosts remain highly understudied; however one characteristic common to those known is that resting spores are rarely or never formed. According to these data some plasmodiophorid species can infect host plants belonging to two or more plant families; Ligniera junci, Polymyxa graminis, Plasmodiophora brassicae, and Spongospora subterranea are known to parasitize both monocot and eudicot host species (Figure 4). Plasmodiophorid parasites of oomycetes and the phagomyxid M. ectocarpii (Figure 2G) can infect a range of distantly related oomycetes or brown algae respectively (Additional file 1: Table S2).


Cross-kingdom host shifts of phytomyxid parasites.

Neuhauser S, Kirchmair M, Bulman S, Bass D - BMC Evol. Biol. (2014)

Network analysis of plant parasitic Phytomyxea and potential host plants (shown as plant families following the taxonomy suggested onhttp://www.theplantlist.org, 20.06.2013). Phytomyxids can use alternative host plants during their life cycle. for the majority of species only haphazard reports of the host range are available, while for some agriculturally important species like of Spongospora subterranea, Polymyxa graminis, P. betae, and Plasmodiophora brassicae extensive host range studies are available, leading to a seemingly wider host range of these species. It is noteworthy that, despite this bias, all species for which targeted host range studies exist hosts belonging to monocot and dicot host plants can be found. Pink?=?monocot plant families, Blue?=?dicot plant families, Red font?=?Phytomyxids for which hosts belonging to both the monocot and dicot hosts were described.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4016497&req=5

Figure 4: Network analysis of plant parasitic Phytomyxea and potential host plants (shown as plant families following the taxonomy suggested onhttp://www.theplantlist.org, 20.06.2013). Phytomyxids can use alternative host plants during their life cycle. for the majority of species only haphazard reports of the host range are available, while for some agriculturally important species like of Spongospora subterranea, Polymyxa graminis, P. betae, and Plasmodiophora brassicae extensive host range studies are available, leading to a seemingly wider host range of these species. It is noteworthy that, despite this bias, all species for which targeted host range studies exist hosts belonging to monocot and dicot host plants can be found. Pink?=?monocot plant families, Blue?=?dicot plant families, Red font?=?Phytomyxids for which hosts belonging to both the monocot and dicot hosts were described.
Mentions: Furthermore, plasmodiophorids are known to rarely infect a range of so-called alternative hosts in which very limited (i.e. to single host cells) infections can be observed. Therefore, we conducted a comprehensive literature study to identify and summarise possible alternative hosts (Figure 4, Additional file 1: Table S2). Interactions with alternative hosts remain highly understudied; however one characteristic common to those known is that resting spores are rarely or never formed. According to these data some plasmodiophorid species can infect host plants belonging to two or more plant families; Ligniera junci, Polymyxa graminis, Plasmodiophora brassicae, and Spongospora subterranea are known to parasitize both monocot and eudicot host species (Figure 4). Plasmodiophorid parasites of oomycetes and the phagomyxid M. ectocarpii (Figure 2G) can infect a range of distantly related oomycetes or brown algae respectively (Additional file 1: Table S2).

Bottom Line: 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.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.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Microbiology, Leopold-Franzens University Innsbruck, Technikerstraße 25, 6020 Innsbruck, Austria. Sigrid.Neuhauser@uibk.ac.at.

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.

Show MeSH
Related in: MedlinePlus