The linear mitochondrial genome of the quarantine chytrid Synchytrium endobioticum; insights into the evolution and recent history of an obligate biotrophic plant pathogen
Abstract Background Chytridiomycota species (chytrids) belong to a basal lineage in the fungal kingdom. Inhabiting terrestrial and aquatic environments, most are free-living saprophytes but several species cause important diseases: e.g. Batrachochytrium dendrobatidis, responsible for worldwide amphi...
| Main Authors: | , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2018-09-01
|
| Series: | BMC Evolutionary Biology |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s12862-018-1246-6 |
| _version_ | 1818692837504450560 |
|---|---|
| author | Bart T. L. H. van de Vossenberg Balázs Brankovics Hai D. T. Nguyen Marga P. E. van Gent-Pelzer Donna Smith Kasia Dadej Jarosław Przetakiewicz Jan F. Kreuze Margriet Boerma Gerard C. M. van Leeuwen C. André Lévesque Theo A. J. van der Lee |
| author_facet | Bart T. L. H. van de Vossenberg Balázs Brankovics Hai D. T. Nguyen Marga P. E. van Gent-Pelzer Donna Smith Kasia Dadej Jarosław Przetakiewicz Jan F. Kreuze Margriet Boerma Gerard C. M. van Leeuwen C. André Lévesque Theo A. J. van der Lee |
| author_sort | Bart T. L. H. van de Vossenberg |
| collection | DOAJ |
| description | Abstract Background Chytridiomycota species (chytrids) belong to a basal lineage in the fungal kingdom. Inhabiting terrestrial and aquatic environments, most are free-living saprophytes but several species cause important diseases: e.g. Batrachochytrium dendrobatidis, responsible for worldwide amphibian decline; and Synchytrium endobioticum, causing potato wart disease. S. endobioticum has an obligate biotrophic lifestyle and isolates can be further characterized as pathotypes based on their virulence on a differential set of potato cultivars. Quarantine measures have been implemented globally to control the disease and prevent its spread. We used a comparative approach using chytrid mitogenomes to determine taxonomical relationships and to gain insights into the evolution and recent history of introductions of this plant pathogen. Results We assembled and annotated the complete mitochondrial genome of 30 S. endobioticum isolates and generated mitochondrial genomes for five additional chytrid species. The mitochondrial genome of S. endobioticum is linear with terminal inverted repeats which was validated by tailing and PCR amplifying the telomeric ends. Surprisingly, no conservation in organisation and orientation of mitochondrial genes was observed among the Chytridiomycota except for S. endobioticum and its sister species Synchytrium microbalum. However, the mitochondrial genome of S. microbalum is circular and comprises only a third of the 72.9 Kbp found for S. endobioticum suggesting recent linearization and expansion. Four mitochondrial lineages were identified in the S. endobioticum mitochondrial genomes. Several pathotypes occur in different lineages, suggesting that these have emerged independently. In addition, variations for polymorphic sites in the mitochondrial genome of individual isolates were observed demonstrating that S. endobioticum isolates represent a community of different genotypes. Such communities were shown to be complex and stable over time, but we also demonstrate that the use of semi-resistant potato cultivars triggers a rapid shift in the mitochondrial haplotype associated with increased virulence. Conclusions Mitochondrial genomic variation shows that S. endobioticum has been introduced into Europe multiple times, that several pathotypes emerged multiple times, and that isolates represent communities of different genotypes. Our study represents the most comprehensive dataset of chytrid mitogenomes, which provides new insights into the extraordinary dynamics and evolution of mitochondrial genomes involving linearization, expansion and reshuffling. |
| first_indexed | 2024-12-17T13:04:08Z |
| format | Article |
| id | doaj.art-e51cffdef14040b9a6b5eb75ef694e51 |
| institution | Directory Open Access Journal |
| issn | 1471-2148 |
| language | English |
| last_indexed | 2024-12-17T13:04:08Z |
| publishDate | 2018-09-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Evolutionary Biology |
| spelling | doaj.art-e51cffdef14040b9a6b5eb75ef694e512022-12-21T21:47:18ZengBMCBMC Evolutionary Biology1471-21482018-09-0118111510.1186/s12862-018-1246-6The linear mitochondrial genome of the quarantine chytrid Synchytrium endobioticum; insights into the evolution and recent history of an obligate biotrophic plant pathogenBart T. L. H. van de Vossenberg0Balázs Brankovics1Hai D. T. Nguyen2Marga P. E. van Gent-Pelzer3Donna Smith4Kasia Dadej5Jarosław Przetakiewicz6Jan F. Kreuze7Margriet Boerma8Gerard C. M. van Leeuwen9C. André Lévesque10Theo A. J. van der Lee11Wageningen UR, Droevendaalsesteeg 1, Biointeractions and Plant Health & Plant BreedingWesterdijk Fungal Biodiversity InstituteAgriculture and Agri-Food CanadaWageningen UR, Droevendaalsesteeg 1, Biointeractions and Plant Health & Plant BreedingCanadian Food Inspection AgencyAgriculture and Agri-Food CanadaPlant Breeding and Acclimatization Institute, National Research InstituteInternational Potato CentreHilbrands Laboratorium BVDutch National Plant Protection Organization, National Reference CentreAgriculture and Agri-Food CanadaWageningen UR, Droevendaalsesteeg 1, Biointeractions and Plant Health & Plant BreedingAbstract Background Chytridiomycota species (chytrids) belong to a basal lineage in the fungal kingdom. Inhabiting terrestrial and aquatic environments, most are free-living saprophytes but several species cause important diseases: e.g. Batrachochytrium dendrobatidis, responsible for worldwide amphibian decline; and Synchytrium endobioticum, causing potato wart disease. S. endobioticum has an obligate biotrophic lifestyle and isolates can be further characterized as pathotypes based on their virulence on a differential set of potato cultivars. Quarantine measures have been implemented globally to control the disease and prevent its spread. We used a comparative approach using chytrid mitogenomes to determine taxonomical relationships and to gain insights into the evolution and recent history of introductions of this plant pathogen. Results We assembled and annotated the complete mitochondrial genome of 30 S. endobioticum isolates and generated mitochondrial genomes for five additional chytrid species. The mitochondrial genome of S. endobioticum is linear with terminal inverted repeats which was validated by tailing and PCR amplifying the telomeric ends. Surprisingly, no conservation in organisation and orientation of mitochondrial genes was observed among the Chytridiomycota except for S. endobioticum and its sister species Synchytrium microbalum. However, the mitochondrial genome of S. microbalum is circular and comprises only a third of the 72.9 Kbp found for S. endobioticum suggesting recent linearization and expansion. Four mitochondrial lineages were identified in the S. endobioticum mitochondrial genomes. Several pathotypes occur in different lineages, suggesting that these have emerged independently. In addition, variations for polymorphic sites in the mitochondrial genome of individual isolates were observed demonstrating that S. endobioticum isolates represent a community of different genotypes. Such communities were shown to be complex and stable over time, but we also demonstrate that the use of semi-resistant potato cultivars triggers a rapid shift in the mitochondrial haplotype associated with increased virulence. Conclusions Mitochondrial genomic variation shows that S. endobioticum has been introduced into Europe multiple times, that several pathotypes emerged multiple times, and that isolates represent communities of different genotypes. Our study represents the most comprehensive dataset of chytrid mitogenomes, which provides new insights into the extraordinary dynamics and evolution of mitochondrial genomes involving linearization, expansion and reshuffling.http://link.springer.com/article/10.1186/s12862-018-1246-6Mitochondrial haplotypesPest introductionPopulation dynamicsFungal communitiesPathotype formationChytridiomycota |
| spellingShingle | Bart T. L. H. van de Vossenberg Balázs Brankovics Hai D. T. Nguyen Marga P. E. van Gent-Pelzer Donna Smith Kasia Dadej Jarosław Przetakiewicz Jan F. Kreuze Margriet Boerma Gerard C. M. van Leeuwen C. André Lévesque Theo A. J. van der Lee The linear mitochondrial genome of the quarantine chytrid Synchytrium endobioticum; insights into the evolution and recent history of an obligate biotrophic plant pathogen BMC Evolutionary Biology Mitochondrial haplotypes Pest introduction Population dynamics Fungal communities Pathotype formation Chytridiomycota |
| title | The linear mitochondrial genome of the quarantine chytrid Synchytrium endobioticum; insights into the evolution and recent history of an obligate biotrophic plant pathogen |
| title_full | The linear mitochondrial genome of the quarantine chytrid Synchytrium endobioticum; insights into the evolution and recent history of an obligate biotrophic plant pathogen |
| title_fullStr | The linear mitochondrial genome of the quarantine chytrid Synchytrium endobioticum; insights into the evolution and recent history of an obligate biotrophic plant pathogen |
| title_full_unstemmed | The linear mitochondrial genome of the quarantine chytrid Synchytrium endobioticum; insights into the evolution and recent history of an obligate biotrophic plant pathogen |
| title_short | The linear mitochondrial genome of the quarantine chytrid Synchytrium endobioticum; insights into the evolution and recent history of an obligate biotrophic plant pathogen |
| title_sort | linear mitochondrial genome of the quarantine chytrid synchytrium endobioticum insights into the evolution and recent history of an obligate biotrophic plant pathogen |
| topic | Mitochondrial haplotypes Pest introduction Population dynamics Fungal communities Pathotype formation Chytridiomycota |
| url | http://link.springer.com/article/10.1186/s12862-018-1246-6 |
| work_keys_str_mv | AT barttlhvandevossenberg thelinearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen AT balazsbrankovics thelinearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen AT haidtnguyen thelinearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen AT margapevangentpelzer thelinearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen AT donnasmith thelinearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen AT kasiadadej thelinearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen AT jarosławprzetakiewicz thelinearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen AT janfkreuze thelinearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen AT margrietboerma thelinearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen AT gerardcmvanleeuwen thelinearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen AT candrelevesque thelinearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen AT theoajvanderlee thelinearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen AT barttlhvandevossenberg linearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen AT balazsbrankovics linearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen AT haidtnguyen linearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen AT margapevangentpelzer linearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen AT donnasmith linearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen AT kasiadadej linearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen AT jarosławprzetakiewicz linearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen AT janfkreuze linearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen AT margrietboerma linearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen AT gerardcmvanleeuwen linearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen AT candrelevesque linearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen AT theoajvanderlee linearmitochondrialgenomeofthequarantinechytridsynchytriumendobioticuminsightsintotheevolutionandrecenthistoryofanobligatebiotrophicplantpathogen |