The chloroplast genome of Utricularia reniformis sheds light on the evolution of the ndh gene complex of terrestrial carnivorous plants from the lentibulariaceae family

Detalhes bibliográficos
Autor(a) principal: Silva, Saura R. [UNESP]
Data de Publicação: 2016
Outros Autores: Diaz, Yani C.A. [UNESP], Penha, Helen Alves [UNESP], Pinheiro, Daniel G. [UNESP], Fernandes, Camila C. [UNESP], Miranda, Vitor F.O. [UNESP], Michael, Todd P., Varani, Alessandro M. [UNESP]
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: http://dx.doi.org/10.1371/journal.pone.0165176
http://hdl.handle.net/11449/173650
Resumo: Lentibulariaceae is the richest family of carnivorous plants spanning three genera including Pinguicula, Genlisea, and Utricularia. Utricularia is globally distributed, and, unlike Pinguicula and Genlisea, has both aquatic and terrestrial forms. In this study we present the analysis of the chloroplast (cp) genome of the terrestrial Utricularia reniformis. U. reniformis has a standard cp genome of 139,725bp, encoding a gene repertoire similar to essentially all photosynthetic organisms. However, an exclusive combination of losses and pseudogenization of the plastid NAD(P)H-dehydrogenase (ndh) gene complex were observed. Comparisons among aquatic and terrestrial forms of Pinguicula, Genlisea, and Utricularia indicate that, whereas the aquatic forms retained functional copies of the eleven ndh genes, these have been lost or truncated in terrestrial forms, suggesting that the ndh function may be dispensable in terrestrial Lentibulariaceae. Phylogenetic scenarios of the ndh gene loss and recovery among Pinguicula, Genlisea, and Utricularia to the ancestral Lentibulariaceae cladeare proposed. Interestingly, RNAseq analysis evidenced that U. reniformis cp genes are transcribed, including the truncated ndh genes, suggesting that these are not completely inactivated. In addition, potential novel RNA-editing sites were identified in at least six U. reniformis cp genes, while none were identified in the truncated ndh genes. Moreover, phylogenomic analyses support that Lentibulariaceae is monophyletic, belonging to the higher core Lamiales clade, corroborating the hypothesis that the first Utricularia lineage emerged in terrestrial habitats and then evolved to epiphytic and aquatic forms. Furthermore, several truncated cp genes were found interspersed with U. reniformis mitochondrial and nuclear genome scaffolds, indicating that as observed in other smaller plant genomes, such as Arabidopsis thaliana, and the related and carnivorous Genlisea nigrocaulis and G. hispidula, the endosymbiotic gene transfer may also shape the U. reniformis genome in a similar fashion. Overall the comparative analysis of the U. reniformis cp genome provides new insight into the ndh genes and cp genome evolution of carnivorous plants from Lentibulariaceae family.
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spelling The chloroplast genome of Utricularia reniformis sheds light on the evolution of the ndh gene complex of terrestrial carnivorous plants from the lentibulariaceae familyLentibulariaceae is the richest family of carnivorous plants spanning three genera including Pinguicula, Genlisea, and Utricularia. Utricularia is globally distributed, and, unlike Pinguicula and Genlisea, has both aquatic and terrestrial forms. In this study we present the analysis of the chloroplast (cp) genome of the terrestrial Utricularia reniformis. U. reniformis has a standard cp genome of 139,725bp, encoding a gene repertoire similar to essentially all photosynthetic organisms. However, an exclusive combination of losses and pseudogenization of the plastid NAD(P)H-dehydrogenase (ndh) gene complex were observed. Comparisons among aquatic and terrestrial forms of Pinguicula, Genlisea, and Utricularia indicate that, whereas the aquatic forms retained functional copies of the eleven ndh genes, these have been lost or truncated in terrestrial forms, suggesting that the ndh function may be dispensable in terrestrial Lentibulariaceae. Phylogenetic scenarios of the ndh gene loss and recovery among Pinguicula, Genlisea, and Utricularia to the ancestral Lentibulariaceae cladeare proposed. Interestingly, RNAseq analysis evidenced that U. reniformis cp genes are transcribed, including the truncated ndh genes, suggesting that these are not completely inactivated. In addition, potential novel RNA-editing sites were identified in at least six U. reniformis cp genes, while none were identified in the truncated ndh genes. Moreover, phylogenomic analyses support that Lentibulariaceae is monophyletic, belonging to the higher core Lamiales clade, corroborating the hypothesis that the first Utricularia lineage emerged in terrestrial habitats and then evolved to epiphytic and aquatic forms. Furthermore, several truncated cp genes were found interspersed with U. reniformis mitochondrial and nuclear genome scaffolds, indicating that as observed in other smaller plant genomes, such as Arabidopsis thaliana, and the related and carnivorous Genlisea nigrocaulis and G. hispidula, the endosymbiotic gene transfer may also shape the U. reniformis genome in a similar fashion. Overall the comparative analysis of the U. reniformis cp genome provides new insight into the ndh genes and cp genome evolution of carnivorous plants from Lentibulariaceae family.Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)Instituto de Bioci�ncias UNESP - Univ Estadual Paulista C�mpus BotucatuDepartamento de Biologia Aplicada � Agropecu�ria Faculdade de Ci�ncias Agr�rias e Veterin�rias UNESP - Univ Estadual Paulista C�mpus JaboticabalDepartamento de Tecnologia Faculdade de Ci�ncias Agr�rias e Veterin�rias UNESP - Univ Estadual Paulista C�mpus JaboticabalIbis Bioscience Computational GenomicsInstituto de Bioci�ncias UNESP - Univ Estadual Paulista C�mpus BotucatuDepartamento de Biologia Aplicada � Agropecu�ria Faculdade de Ci�ncias Agr�rias e Veterin�rias UNESP - Univ Estadual Paulista C�mpus JaboticabalDepartamento de Tecnologia Faculdade de Ci�ncias Agr�rias e Veterin�rias UNESP - Univ Estadual Paulista C�mpus JaboticabalFAPESP: 13/25164-6Universidade Estadual Paulista (Unesp)Computational GenomicsSilva, Saura R. [UNESP]Diaz, Yani C.A. [UNESP]Penha, Helen Alves [UNESP]Pinheiro, Daniel G. [UNESP]Fernandes, Camila C. [UNESP]Miranda, Vitor F.O. [UNESP]Michael, Todd P.Varani, Alessandro M. [UNESP]2018-12-11T17:07:04Z2018-12-11T17:07:04Z2016-10-01info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://dx.doi.org/10.1371/journal.pone.0165176PLoS ONE, v. 11, n. 10, 2016.1932-6203http://hdl.handle.net/11449/17365010.1371/journal.pone.01651762-s2.0-849920357322-s2.0-84992035732.pdfScopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengPLoS ONE1,164info:eu-repo/semantics/openAccess2023-10-14T06:06:04Zoai:repositorio.unesp.br:11449/173650Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462023-10-14T06:06:04Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv The chloroplast genome of Utricularia reniformis sheds light on the evolution of the ndh gene complex of terrestrial carnivorous plants from the lentibulariaceae family
title The chloroplast genome of Utricularia reniformis sheds light on the evolution of the ndh gene complex of terrestrial carnivorous plants from the lentibulariaceae family
spellingShingle The chloroplast genome of Utricularia reniformis sheds light on the evolution of the ndh gene complex of terrestrial carnivorous plants from the lentibulariaceae family
Silva, Saura R. [UNESP]
title_short The chloroplast genome of Utricularia reniformis sheds light on the evolution of the ndh gene complex of terrestrial carnivorous plants from the lentibulariaceae family
title_full The chloroplast genome of Utricularia reniformis sheds light on the evolution of the ndh gene complex of terrestrial carnivorous plants from the lentibulariaceae family
title_fullStr The chloroplast genome of Utricularia reniformis sheds light on the evolution of the ndh gene complex of terrestrial carnivorous plants from the lentibulariaceae family
title_full_unstemmed The chloroplast genome of Utricularia reniformis sheds light on the evolution of the ndh gene complex of terrestrial carnivorous plants from the lentibulariaceae family
title_sort The chloroplast genome of Utricularia reniformis sheds light on the evolution of the ndh gene complex of terrestrial carnivorous plants from the lentibulariaceae family
author Silva, Saura R. [UNESP]
author_facet Silva, Saura R. [UNESP]
Diaz, Yani C.A. [UNESP]
Penha, Helen Alves [UNESP]
Pinheiro, Daniel G. [UNESP]
Fernandes, Camila C. [UNESP]
Miranda, Vitor F.O. [UNESP]
Michael, Todd P.
Varani, Alessandro M. [UNESP]
author_role author
author2 Diaz, Yani C.A. [UNESP]
Penha, Helen Alves [UNESP]
Pinheiro, Daniel G. [UNESP]
Fernandes, Camila C. [UNESP]
Miranda, Vitor F.O. [UNESP]
Michael, Todd P.
Varani, Alessandro M. [UNESP]
author2_role author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Universidade Estadual Paulista (Unesp)
Computational Genomics
dc.contributor.author.fl_str_mv Silva, Saura R. [UNESP]
Diaz, Yani C.A. [UNESP]
Penha, Helen Alves [UNESP]
Pinheiro, Daniel G. [UNESP]
Fernandes, Camila C. [UNESP]
Miranda, Vitor F.O. [UNESP]
Michael, Todd P.
Varani, Alessandro M. [UNESP]
description Lentibulariaceae is the richest family of carnivorous plants spanning three genera including Pinguicula, Genlisea, and Utricularia. Utricularia is globally distributed, and, unlike Pinguicula and Genlisea, has both aquatic and terrestrial forms. In this study we present the analysis of the chloroplast (cp) genome of the terrestrial Utricularia reniformis. U. reniformis has a standard cp genome of 139,725bp, encoding a gene repertoire similar to essentially all photosynthetic organisms. However, an exclusive combination of losses and pseudogenization of the plastid NAD(P)H-dehydrogenase (ndh) gene complex were observed. Comparisons among aquatic and terrestrial forms of Pinguicula, Genlisea, and Utricularia indicate that, whereas the aquatic forms retained functional copies of the eleven ndh genes, these have been lost or truncated in terrestrial forms, suggesting that the ndh function may be dispensable in terrestrial Lentibulariaceae. Phylogenetic scenarios of the ndh gene loss and recovery among Pinguicula, Genlisea, and Utricularia to the ancestral Lentibulariaceae cladeare proposed. Interestingly, RNAseq analysis evidenced that U. reniformis cp genes are transcribed, including the truncated ndh genes, suggesting that these are not completely inactivated. In addition, potential novel RNA-editing sites were identified in at least six U. reniformis cp genes, while none were identified in the truncated ndh genes. Moreover, phylogenomic analyses support that Lentibulariaceae is monophyletic, belonging to the higher core Lamiales clade, corroborating the hypothesis that the first Utricularia lineage emerged in terrestrial habitats and then evolved to epiphytic and aquatic forms. Furthermore, several truncated cp genes were found interspersed with U. reniformis mitochondrial and nuclear genome scaffolds, indicating that as observed in other smaller plant genomes, such as Arabidopsis thaliana, and the related and carnivorous Genlisea nigrocaulis and G. hispidula, the endosymbiotic gene transfer may also shape the U. reniformis genome in a similar fashion. Overall the comparative analysis of the U. reniformis cp genome provides new insight into the ndh genes and cp genome evolution of carnivorous plants from Lentibulariaceae family.
publishDate 2016
dc.date.none.fl_str_mv 2016-10-01
2018-12-11T17:07:04Z
2018-12-11T17:07:04Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://dx.doi.org/10.1371/journal.pone.0165176
PLoS ONE, v. 11, n. 10, 2016.
1932-6203
http://hdl.handle.net/11449/173650
10.1371/journal.pone.0165176
2-s2.0-84992035732
2-s2.0-84992035732.pdf
url http://dx.doi.org/10.1371/journal.pone.0165176
http://hdl.handle.net/11449/173650
identifier_str_mv PLoS ONE, v. 11, n. 10, 2016.
1932-6203
10.1371/journal.pone.0165176
2-s2.0-84992035732
2-s2.0-84992035732.pdf
dc.language.iso.fl_str_mv eng
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