Distinctive plastome evolution in carnivorous angiosperms
Abstract Background Independent origins of carnivory in multiple angiosperm families are fabulous examples of convergent evolution using a diverse array of life forms and habitats. Previous studies have indicated that carnivorous plants have distinct evolutionary trajectories of plastid genome (plas...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-12-01
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| Series: | BMC Plant Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12870-023-04682-1 |
| _version_ | 1797377133254803456 |
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| author | Chao-Nan Fu Susann Wicke An-Dan Zhu De-Zhu Li Lian-Ming Gao |
| author_facet | Chao-Nan Fu Susann Wicke An-Dan Zhu De-Zhu Li Lian-Ming Gao |
| author_sort | Chao-Nan Fu |
| collection | DOAJ |
| description | Abstract Background Independent origins of carnivory in multiple angiosperm families are fabulous examples of convergent evolution using a diverse array of life forms and habitats. Previous studies have indicated that carnivorous plants have distinct evolutionary trajectories of plastid genome (plastome) compared to their non-carnivorous relatives, yet the extent and general characteristics remain elusive. Results We compared plastomes from 9 out of 13 carnivorous families and their non-carnivorous relatives to assess carnivory-associated evolutionary patterns. We identified inversions in all sampled Droseraceae species and four species of Utricularia, Pinguicula, Darlingtonia and Triphyophyllum. A few carnivores showed distinct shifts in inverted repeat boundaries and the overall repeat contents. Many ndh genes, along with some other genes, were independently lost in several carnivorous lineages. We detected significant substitution rate variations in most sampled carnivorous lineages. A significant overall substitution rate acceleration characterizes the two largest carnivorous lineages of Droseraceae and Lentibulariaceae. We also observe moderate substitution rates acceleration in many genes of Cephalotus follicularis, Roridula gorgonias, and Drosophyllum lusitanicum. However, only a few genes exhibit significant relaxed selection. Conclusion Our results indicate that the carnivory of plants have different effects on plastome evolution across carnivorous lineages. The complex mechanism under carnivorous habitats may have resulted in distinctive plastome evolution with conserved plastome in the Brocchinia hechtioides to strongly reconfigured plastomes structures in Droseraceae. Organic carbon obtained from prey and the efficiency of utilizing prey-derived nutrients might constitute possible explanation. |
| first_indexed | 2024-03-08T19:48:21Z |
| format | Article |
| id | doaj.art-6c9b953012e74666b047ebd0507f6954 |
| institution | Directory Open Access Journal |
| issn | 1471-2229 |
| language | English |
| last_indexed | 2024-03-08T19:48:21Z |
| publishDate | 2023-12-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Plant Biology |
| spelling | doaj.art-6c9b953012e74666b047ebd0507f69542023-12-24T12:13:35ZengBMCBMC Plant Biology1471-22292023-12-0123111510.1186/s12870-023-04682-1Distinctive plastome evolution in carnivorous angiospermsChao-Nan Fu0Susann Wicke1An-Dan Zhu2De-Zhu Li3Lian-Ming Gao4CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of SciencesInstitute for Biology, Humboldt-University BerlinGermplasm Bank of Wild Species, Kunming Institute of Botany, Chinese Academy of SciencesCAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of SciencesCAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of SciencesAbstract Background Independent origins of carnivory in multiple angiosperm families are fabulous examples of convergent evolution using a diverse array of life forms and habitats. Previous studies have indicated that carnivorous plants have distinct evolutionary trajectories of plastid genome (plastome) compared to their non-carnivorous relatives, yet the extent and general characteristics remain elusive. Results We compared plastomes from 9 out of 13 carnivorous families and their non-carnivorous relatives to assess carnivory-associated evolutionary patterns. We identified inversions in all sampled Droseraceae species and four species of Utricularia, Pinguicula, Darlingtonia and Triphyophyllum. A few carnivores showed distinct shifts in inverted repeat boundaries and the overall repeat contents. Many ndh genes, along with some other genes, were independently lost in several carnivorous lineages. We detected significant substitution rate variations in most sampled carnivorous lineages. A significant overall substitution rate acceleration characterizes the two largest carnivorous lineages of Droseraceae and Lentibulariaceae. We also observe moderate substitution rates acceleration in many genes of Cephalotus follicularis, Roridula gorgonias, and Drosophyllum lusitanicum. However, only a few genes exhibit significant relaxed selection. Conclusion Our results indicate that the carnivory of plants have different effects on plastome evolution across carnivorous lineages. The complex mechanism under carnivorous habitats may have resulted in distinctive plastome evolution with conserved plastome in the Brocchinia hechtioides to strongly reconfigured plastomes structures in Droseraceae. Organic carbon obtained from prey and the efficiency of utilizing prey-derived nutrients might constitute possible explanation.https://doi.org/10.1186/s12870-023-04682-1CarnivoryPlastomeSubstitution ratesPrey-derived nutrient utilization |
| spellingShingle | Chao-Nan Fu Susann Wicke An-Dan Zhu De-Zhu Li Lian-Ming Gao Distinctive plastome evolution in carnivorous angiosperms BMC Plant Biology Carnivory Plastome Substitution rates Prey-derived nutrient utilization |
| title | Distinctive plastome evolution in carnivorous angiosperms |
| title_full | Distinctive plastome evolution in carnivorous angiosperms |
| title_fullStr | Distinctive plastome evolution in carnivorous angiosperms |
| title_full_unstemmed | Distinctive plastome evolution in carnivorous angiosperms |
| title_short | Distinctive plastome evolution in carnivorous angiosperms |
| title_sort | distinctive plastome evolution in carnivorous angiosperms |
| topic | Carnivory Plastome Substitution rates Prey-derived nutrient utilization |
| url | https://doi.org/10.1186/s12870-023-04682-1 |
| work_keys_str_mv | AT chaonanfu distinctiveplastomeevolutionincarnivorousangiosperms AT susannwicke distinctiveplastomeevolutionincarnivorousangiosperms AT andanzhu distinctiveplastomeevolutionincarnivorousangiosperms AT dezhuli distinctiveplastomeevolutionincarnivorousangiosperms AT lianminggao distinctiveplastomeevolutionincarnivorousangiosperms |