Recent and Ongoing Horizontal Transfer of Mitochondrial Introns Between Two Fungal Tree Pathogens
Two recently introduced fungal plant pathogens (Ceratocystis lukuohia and Ceratocystis huliohia) are responsible for Rapid ‘ōhi‘a Death (ROD) in Hawai‘i. Despite being sexually incompatible, the two pathogens often co-occur in diseased ‘ōhi‘a sapwood, where genetic interaction is possible. We sequen...
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Frontiers Media S.A.
2021-06-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2021.656609/full |
| _version_ | 1818436862172200960 |
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| author | Chase G. Mayers Thomas C. Harrington Alvan Wai Georg Hausner |
| author_facet | Chase G. Mayers Thomas C. Harrington Alvan Wai Georg Hausner |
| author_sort | Chase G. Mayers |
| collection | DOAJ |
| description | Two recently introduced fungal plant pathogens (Ceratocystis lukuohia and Ceratocystis huliohia) are responsible for Rapid ‘ōhi‘a Death (ROD) in Hawai‘i. Despite being sexually incompatible, the two pathogens often co-occur in diseased ‘ōhi‘a sapwood, where genetic interaction is possible. We sequenced and annotated 33 mitochondrial genomes of the two pathogens and related species, and investigated 35 total Ceratocystis mitogenomes. Ten mtDNA regions [one group I intron, seven group II introns, and two autonomous homing endonuclease (HE) genes] were heterogeneously present in C. lukuohia mitogenomes, which were otherwise identical. Molecular surveys with specific primers showed that the 10 regions had uneven geographic distribution amongst populations of C. lukuohia. Conversely, identical orthologs of each region were present in every studied isolate of C. huliohia regardless of geographical origin. Close relatives of C. lukuohia lacked or, rarely, had few and dissimilar orthologs of the 10 regions, whereas most relatives of C. huliohia had identical or nearly identical orthologs. Each region included or worked in tandem with HE genes or reverse transcriptase/maturases that could facilitate interspecific horizontal transfers from intron-minus to intron-plus alleles. These results suggest that the 10 regions originated in C. huliohia and are actively moving to populations of C. lukuohia, perhaps through transient cytoplasmic contact of hyphal tips (anastomosis) in the wound surface of ‘ōhi‘a trees. Such contact would allow for the transfer of mitochondria followed by mitochondrial fusion or cytoplasmic exchange of intron intermediaries, which suggests that further genomic interaction may also exist between the two pathogens. |
| first_indexed | 2024-12-14T17:15:31Z |
| format | Article |
| id | doaj.art-769c0fe8925b4670b6347d87feab733d |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-14T17:15:31Z |
| publishDate | 2021-06-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-769c0fe8925b4670b6347d87feab733d2022-12-21T22:53:26ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-06-011210.3389/fmicb.2021.656609656609Recent and Ongoing Horizontal Transfer of Mitochondrial Introns Between Two Fungal Tree PathogensChase G. Mayers0Thomas C. Harrington1Alvan Wai2Georg Hausner3Department of Plant Pathology and Microbiology, Iowa State University, Ames, IA, United StatesDepartment of Plant Pathology and Microbiology, Iowa State University, Ames, IA, United StatesDepartment of Microbiology, University of Manitoba, Winnipeg, MB, CanadaDepartment of Microbiology, University of Manitoba, Winnipeg, MB, CanadaTwo recently introduced fungal plant pathogens (Ceratocystis lukuohia and Ceratocystis huliohia) are responsible for Rapid ‘ōhi‘a Death (ROD) in Hawai‘i. Despite being sexually incompatible, the two pathogens often co-occur in diseased ‘ōhi‘a sapwood, where genetic interaction is possible. We sequenced and annotated 33 mitochondrial genomes of the two pathogens and related species, and investigated 35 total Ceratocystis mitogenomes. Ten mtDNA regions [one group I intron, seven group II introns, and two autonomous homing endonuclease (HE) genes] were heterogeneously present in C. lukuohia mitogenomes, which were otherwise identical. Molecular surveys with specific primers showed that the 10 regions had uneven geographic distribution amongst populations of C. lukuohia. Conversely, identical orthologs of each region were present in every studied isolate of C. huliohia regardless of geographical origin. Close relatives of C. lukuohia lacked or, rarely, had few and dissimilar orthologs of the 10 regions, whereas most relatives of C. huliohia had identical or nearly identical orthologs. Each region included or worked in tandem with HE genes or reverse transcriptase/maturases that could facilitate interspecific horizontal transfers from intron-minus to intron-plus alleles. These results suggest that the 10 regions originated in C. huliohia and are actively moving to populations of C. lukuohia, perhaps through transient cytoplasmic contact of hyphal tips (anastomosis) in the wound surface of ‘ōhi‘a trees. Such contact would allow for the transfer of mitochondria followed by mitochondrial fusion or cytoplasmic exchange of intron intermediaries, which suggests that further genomic interaction may also exist between the two pathogens.https://www.frontiersin.org/articles/10.3389/fmicb.2021.656609/fullRapid ‘Ōhi‘a DeathRapid Ohia Deathmobile intronshorizontal gene transferforest pathologyMicroascales |
| spellingShingle | Chase G. Mayers Thomas C. Harrington Alvan Wai Georg Hausner Recent and Ongoing Horizontal Transfer of Mitochondrial Introns Between Two Fungal Tree Pathogens Frontiers in Microbiology Rapid ‘Ōhi‘a Death Rapid Ohia Death mobile introns horizontal gene transfer forest pathology Microascales |
| title | Recent and Ongoing Horizontal Transfer of Mitochondrial Introns Between Two Fungal Tree Pathogens |
| title_full | Recent and Ongoing Horizontal Transfer of Mitochondrial Introns Between Two Fungal Tree Pathogens |
| title_fullStr | Recent and Ongoing Horizontal Transfer of Mitochondrial Introns Between Two Fungal Tree Pathogens |
| title_full_unstemmed | Recent and Ongoing Horizontal Transfer of Mitochondrial Introns Between Two Fungal Tree Pathogens |
| title_short | Recent and Ongoing Horizontal Transfer of Mitochondrial Introns Between Two Fungal Tree Pathogens |
| title_sort | recent and ongoing horizontal transfer of mitochondrial introns between two fungal tree pathogens |
| topic | Rapid ‘Ōhi‘a Death Rapid Ohia Death mobile introns horizontal gene transfer forest pathology Microascales |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2021.656609/full |
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