Phylogenomics, plastome degradation and mycoheterotrophy evolution of Neottieae (Orchidaceae), with emphasis on the systematic position and Loess Plateau-Changbai Mountains disjunction of Diplandrorchis
Abstract Background Mycoheterotrophy is a unique survival strategy adapted to dense forests and has attracted biologists’ attention for centuries. However, its evolutionary origin and related plastome degradation are poorly understood. The tribe Neottieae contains various nutrition types, i.e., auto...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2022-11-01
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| Series: | BMC Plant Biology |
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| Online Access: | https://doi.org/10.1186/s12870-022-03906-0 |
| _version_ | 1811329096909586432 |
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| author | Huan-Wen Peng Lian Lian Jun Zhang Andrey S. Erst Wei Wang |
| author_facet | Huan-Wen Peng Lian Lian Jun Zhang Andrey S. Erst Wei Wang |
| author_sort | Huan-Wen Peng |
| collection | DOAJ |
| description | Abstract Background Mycoheterotrophy is a unique survival strategy adapted to dense forests and has attracted biologists’ attention for centuries. However, its evolutionary origin and related plastome degradation are poorly understood. The tribe Neottieae contains various nutrition types, i.e., autotrophy, mixotrophy, and mycoheterotrophy. Here, we present a comprehensive phylogenetic analysis of the tribe based on plastome and nuclear ITS data. We inferred the evolutionary shift of nutrition types, constructed the patterns of plastome degradation, and estimated divergence times and ancestral ranges. We also used an integration of molecular dating and ecological niche modeling methods to investigate the disjunction between the Loess Plateau and Changbai Mountains in Diplandrorchis, a mycoheterotrophic genus endemic to China that was included in a molecular phylogenetic study for the first time. Results Diplandrorchis was imbedded within Neottia and formed a clade with four mycoheterotrophic species. Autotrophy is the ancestral state in Neottieae, mixotrophy independently originated at least five times, and three shifts from mixotrophy to mycoheterotrophy independently occurred. The five mixotrophic lineages possess all plastid genes or lost partial/all ndh genes, whereas each of the three mycoheterotroph lineages has a highly reduced plastome: one lost part of its ndh genes and a few photosynthesis-related genes, and the other two lost almost all ndh, photosynthesis-related, rpo, and atp genes. These three mycoheterotrophic lineages originated at about 26.40 Ma, 25.84 Ma, and 9.22 Ma, respectively. Diplandrorchis had presumably a wide range in the Pliocene and migrated southward in the Pleistocene. Conclusions The Pleistocene climatic fluctuations and the resultant migration resulted in the Loess Plateau-Changbai Mountains disjunction of Diplandrorchis. In the evolution of mycoheterotrophic lineages, the loss of plastid-encoded genes and plastome degradation are staged and irreversible, constraining mycoheterotrophs to inhabit understories with low light levels. Accordingly, the rise of local forests might have promoted the origin of conditions in which mycoheterotrophy is advantageous. |
| first_indexed | 2024-04-13T15:37:50Z |
| format | Article |
| id | doaj.art-a2fc82edd6194abca3f09d65c6d1d11e |
| institution | Directory Open Access Journal |
| issn | 1471-2229 |
| language | English |
| last_indexed | 2024-04-13T15:37:50Z |
| publishDate | 2022-11-01 |
| publisher | BMC |
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| series | BMC Plant Biology |
| spelling | doaj.art-a2fc82edd6194abca3f09d65c6d1d11e2022-12-22T02:41:13ZengBMCBMC Plant Biology1471-22292022-11-0122111310.1186/s12870-022-03906-0Phylogenomics, plastome degradation and mycoheterotrophy evolution of Neottieae (Orchidaceae), with emphasis on the systematic position and Loess Plateau-Changbai Mountains disjunction of DiplandrorchisHuan-Wen Peng0Lian Lian1Jun Zhang2Andrey S. Erst3Wei Wang4State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of SciencesState Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of SciencesState Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of SciencesCentral Siberian Botanical Garden, Russian Academy of SciencesState Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of SciencesAbstract Background Mycoheterotrophy is a unique survival strategy adapted to dense forests and has attracted biologists’ attention for centuries. However, its evolutionary origin and related plastome degradation are poorly understood. The tribe Neottieae contains various nutrition types, i.e., autotrophy, mixotrophy, and mycoheterotrophy. Here, we present a comprehensive phylogenetic analysis of the tribe based on plastome and nuclear ITS data. We inferred the evolutionary shift of nutrition types, constructed the patterns of plastome degradation, and estimated divergence times and ancestral ranges. We also used an integration of molecular dating and ecological niche modeling methods to investigate the disjunction between the Loess Plateau and Changbai Mountains in Diplandrorchis, a mycoheterotrophic genus endemic to China that was included in a molecular phylogenetic study for the first time. Results Diplandrorchis was imbedded within Neottia and formed a clade with four mycoheterotrophic species. Autotrophy is the ancestral state in Neottieae, mixotrophy independently originated at least five times, and three shifts from mixotrophy to mycoheterotrophy independently occurred. The five mixotrophic lineages possess all plastid genes or lost partial/all ndh genes, whereas each of the three mycoheterotroph lineages has a highly reduced plastome: one lost part of its ndh genes and a few photosynthesis-related genes, and the other two lost almost all ndh, photosynthesis-related, rpo, and atp genes. These three mycoheterotrophic lineages originated at about 26.40 Ma, 25.84 Ma, and 9.22 Ma, respectively. Diplandrorchis had presumably a wide range in the Pliocene and migrated southward in the Pleistocene. Conclusions The Pleistocene climatic fluctuations and the resultant migration resulted in the Loess Plateau-Changbai Mountains disjunction of Diplandrorchis. In the evolution of mycoheterotrophic lineages, the loss of plastid-encoded genes and plastome degradation are staged and irreversible, constraining mycoheterotrophs to inhabit understories with low light levels. Accordingly, the rise of local forests might have promoted the origin of conditions in which mycoheterotrophy is advantageous.https://doi.org/10.1186/s12870-022-03906-0BiogeographyLoess Plateau-Changbai Mountains disjunctionMycoheterotrophyOrchidaceaePhylogenomicsPlastome degradation |
| spellingShingle | Huan-Wen Peng Lian Lian Jun Zhang Andrey S. Erst Wei Wang Phylogenomics, plastome degradation and mycoheterotrophy evolution of Neottieae (Orchidaceae), with emphasis on the systematic position and Loess Plateau-Changbai Mountains disjunction of Diplandrorchis BMC Plant Biology Biogeography Loess Plateau-Changbai Mountains disjunction Mycoheterotrophy Orchidaceae Phylogenomics Plastome degradation |
| title | Phylogenomics, plastome degradation and mycoheterotrophy evolution of Neottieae (Orchidaceae), with emphasis on the systematic position and Loess Plateau-Changbai Mountains disjunction of Diplandrorchis |
| title_full | Phylogenomics, plastome degradation and mycoheterotrophy evolution of Neottieae (Orchidaceae), with emphasis on the systematic position and Loess Plateau-Changbai Mountains disjunction of Diplandrorchis |
| title_fullStr | Phylogenomics, plastome degradation and mycoheterotrophy evolution of Neottieae (Orchidaceae), with emphasis on the systematic position and Loess Plateau-Changbai Mountains disjunction of Diplandrorchis |
| title_full_unstemmed | Phylogenomics, plastome degradation and mycoheterotrophy evolution of Neottieae (Orchidaceae), with emphasis on the systematic position and Loess Plateau-Changbai Mountains disjunction of Diplandrorchis |
| title_short | Phylogenomics, plastome degradation and mycoheterotrophy evolution of Neottieae (Orchidaceae), with emphasis on the systematic position and Loess Plateau-Changbai Mountains disjunction of Diplandrorchis |
| title_sort | phylogenomics plastome degradation and mycoheterotrophy evolution of neottieae orchidaceae with emphasis on the systematic position and loess plateau changbai mountains disjunction of diplandrorchis |
| topic | Biogeography Loess Plateau-Changbai Mountains disjunction Mycoheterotrophy Orchidaceae Phylogenomics Plastome degradation |
| url | https://doi.org/10.1186/s12870-022-03906-0 |
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