Comparative Chloroplast Genomes of Nicotiana Species (Solanaceae): Insights Into the Genetic Variation, Phylogenetic Relationship, and Polyploid Speciation

Nicotiana L. is a genus rich in polyploidy, which represents an ideal natural system for investigating speciation, biodiversity, and phytogeography. Despite a wealth of phylogenetic work on this genus, a robust evolutionary framework with a dated molecular phylogeny for the genus is still lacking. I...

Full description

Bibliographic Details
Main Authors: Shuaibin Wang, Junping Gao, Haoyu Chao, Zhaowu Li, Wenxuan Pu, Yaofu Wang, Ming Chen
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-07-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.899252/full
_version_ 1811325295426273280
author Shuaibin Wang
Shuaibin Wang
Junping Gao
Haoyu Chao
Zhaowu Li
Wenxuan Pu
Yaofu Wang
Ming Chen
author_facet Shuaibin Wang
Shuaibin Wang
Junping Gao
Haoyu Chao
Zhaowu Li
Wenxuan Pu
Yaofu Wang
Ming Chen
author_sort Shuaibin Wang
collection DOAJ
description Nicotiana L. is a genus rich in polyploidy, which represents an ideal natural system for investigating speciation, biodiversity, and phytogeography. Despite a wealth of phylogenetic work on this genus, a robust evolutionary framework with a dated molecular phylogeny for the genus is still lacking. In this study, the 19 complete chloroplast genomes of Nicotiana species were assembled, and five published chloroplast genomes of Nicotiana were retrieved for comparative analyses. The results showed that the 24 chloroplast genomes of Nicotiana, ranging from 155,327 bp (N. paniculata) to 156,142 bp (N. heterantha) in size, exhibited typical quadripartite structure. The chloroplast genomes were rather conserved in genome structure, GC content, RNA editing sites, and gene content and order. The higher GC content observed in the IR regions could be a result of the presence of abundant rRNA and tRNA genes, which contained a relatively higher GC content. A total of seven hypervariable regions, as new molecular markers for phylogenetic analysis, were uncovered. Based on 78 protein-coding genes, we constructed a well-supported phylogenetic tree, which was largely in agreement with previous studies, except for a slight conflict in several sections. Chloroplast phylogenetic results indicated that the progenitors of diploid N. sylvestris, N. knightiana, and the common ancestor of N. sylvestris and N. glauca might have donated the maternal genomes of allopolyploid N. tabacum, N. rustica, and section Repandae, respectively. Meanwhile, the diploid section Noctiflorae lineages (N. glauca) acted as the most likely maternal progenitor of section Suaveolentes. Molecular dating results show that the polyploid events range considerably in ~0.12 million (section Nicotiana) to ~5.77 million (section Repandae) years ago. The younger polyploids (N. tabacum and N. rustica) were estimated to have arisen ~0.120 and ~0.186 Mya, respectively. The older polyploids (section Repandae and Suaveolentes) were considered to have originated from a single polyploid event at ~5.77 and ~4.49 Mya, respectively. In summary, the comparative analysis of chloroplast genomes of Nicotiana species has not only revealed a series of new insights into the genetic variation and phylogenetic relationships in Nicotiana but also provided rich genetic resources for speciation and biodiversity research in the future.
first_indexed 2024-04-13T14:30:32Z
format Article
id doaj.art-6aa95ebf306a44cbae56eaf39cc449b8
institution Directory Open Access Journal
issn 1664-462X
language English
last_indexed 2024-04-13T14:30:32Z
publishDate 2022-07-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Plant Science
spelling doaj.art-6aa95ebf306a44cbae56eaf39cc449b82022-12-22T02:43:12ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-07-011310.3389/fpls.2022.899252899252Comparative Chloroplast Genomes of Nicotiana Species (Solanaceae): Insights Into the Genetic Variation, Phylogenetic Relationship, and Polyploid SpeciationShuaibin Wang0Shuaibin Wang1Junping Gao2Haoyu Chao3Zhaowu Li4Wenxuan Pu5Yaofu Wang6Ming Chen7Department of Bioinformatics, State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, ChinaTobacco Research Institute of Technology Centre, China Tobacco Hunan Industrial Corporation, Changsha, ChinaTobacco Research Institute of Technology Centre, China Tobacco Hunan Industrial Corporation, Changsha, ChinaDepartment of Bioinformatics, State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, ChinaState Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University, Nanjing, ChinaTobacco Research Institute of Technology Centre, China Tobacco Hunan Industrial Corporation, Changsha, ChinaTobacco Research Institute of Technology Centre, China Tobacco Hunan Industrial Corporation, Changsha, ChinaDepartment of Bioinformatics, State Key Laboratory of Plant Physiology and Biochemistry, College of Life Sciences, Zhejiang University, Hangzhou, ChinaNicotiana L. is a genus rich in polyploidy, which represents an ideal natural system for investigating speciation, biodiversity, and phytogeography. Despite a wealth of phylogenetic work on this genus, a robust evolutionary framework with a dated molecular phylogeny for the genus is still lacking. In this study, the 19 complete chloroplast genomes of Nicotiana species were assembled, and five published chloroplast genomes of Nicotiana were retrieved for comparative analyses. The results showed that the 24 chloroplast genomes of Nicotiana, ranging from 155,327 bp (N. paniculata) to 156,142 bp (N. heterantha) in size, exhibited typical quadripartite structure. The chloroplast genomes were rather conserved in genome structure, GC content, RNA editing sites, and gene content and order. The higher GC content observed in the IR regions could be a result of the presence of abundant rRNA and tRNA genes, which contained a relatively higher GC content. A total of seven hypervariable regions, as new molecular markers for phylogenetic analysis, were uncovered. Based on 78 protein-coding genes, we constructed a well-supported phylogenetic tree, which was largely in agreement with previous studies, except for a slight conflict in several sections. Chloroplast phylogenetic results indicated that the progenitors of diploid N. sylvestris, N. knightiana, and the common ancestor of N. sylvestris and N. glauca might have donated the maternal genomes of allopolyploid N. tabacum, N. rustica, and section Repandae, respectively. Meanwhile, the diploid section Noctiflorae lineages (N. glauca) acted as the most likely maternal progenitor of section Suaveolentes. Molecular dating results show that the polyploid events range considerably in ~0.12 million (section Nicotiana) to ~5.77 million (section Repandae) years ago. The younger polyploids (N. tabacum and N. rustica) were estimated to have arisen ~0.120 and ~0.186 Mya, respectively. The older polyploids (section Repandae and Suaveolentes) were considered to have originated from a single polyploid event at ~5.77 and ~4.49 Mya, respectively. In summary, the comparative analysis of chloroplast genomes of Nicotiana species has not only revealed a series of new insights into the genetic variation and phylogenetic relationships in Nicotiana but also provided rich genetic resources for speciation and biodiversity research in the future.https://www.frontiersin.org/articles/10.3389/fpls.2022.899252/fullNicotiana L.chloroplast genomegenetic variationphylogenetic relationshipdivergence time estimationpolyploid speciation
spellingShingle Shuaibin Wang
Shuaibin Wang
Junping Gao
Haoyu Chao
Zhaowu Li
Wenxuan Pu
Yaofu Wang
Ming Chen
Comparative Chloroplast Genomes of Nicotiana Species (Solanaceae): Insights Into the Genetic Variation, Phylogenetic Relationship, and Polyploid Speciation
Frontiers in Plant Science
Nicotiana L.
chloroplast genome
genetic variation
phylogenetic relationship
divergence time estimation
polyploid speciation
title Comparative Chloroplast Genomes of Nicotiana Species (Solanaceae): Insights Into the Genetic Variation, Phylogenetic Relationship, and Polyploid Speciation
title_full Comparative Chloroplast Genomes of Nicotiana Species (Solanaceae): Insights Into the Genetic Variation, Phylogenetic Relationship, and Polyploid Speciation
title_fullStr Comparative Chloroplast Genomes of Nicotiana Species (Solanaceae): Insights Into the Genetic Variation, Phylogenetic Relationship, and Polyploid Speciation
title_full_unstemmed Comparative Chloroplast Genomes of Nicotiana Species (Solanaceae): Insights Into the Genetic Variation, Phylogenetic Relationship, and Polyploid Speciation
title_short Comparative Chloroplast Genomes of Nicotiana Species (Solanaceae): Insights Into the Genetic Variation, Phylogenetic Relationship, and Polyploid Speciation
title_sort comparative chloroplast genomes of nicotiana species solanaceae insights into the genetic variation phylogenetic relationship and polyploid speciation
topic Nicotiana L.
chloroplast genome
genetic variation
phylogenetic relationship
divergence time estimation
polyploid speciation
url https://www.frontiersin.org/articles/10.3389/fpls.2022.899252/full
work_keys_str_mv AT shuaibinwang comparativechloroplastgenomesofnicotianaspeciessolanaceaeinsightsintothegeneticvariationphylogeneticrelationshipandpolyploidspeciation
AT shuaibinwang comparativechloroplastgenomesofnicotianaspeciessolanaceaeinsightsintothegeneticvariationphylogeneticrelationshipandpolyploidspeciation
AT junpinggao comparativechloroplastgenomesofnicotianaspeciessolanaceaeinsightsintothegeneticvariationphylogeneticrelationshipandpolyploidspeciation
AT haoyuchao comparativechloroplastgenomesofnicotianaspeciessolanaceaeinsightsintothegeneticvariationphylogeneticrelationshipandpolyploidspeciation
AT zhaowuli comparativechloroplastgenomesofnicotianaspeciessolanaceaeinsightsintothegeneticvariationphylogeneticrelationshipandpolyploidspeciation
AT wenxuanpu comparativechloroplastgenomesofnicotianaspeciessolanaceaeinsightsintothegeneticvariationphylogeneticrelationshipandpolyploidspeciation
AT yaofuwang comparativechloroplastgenomesofnicotianaspeciessolanaceaeinsightsintothegeneticvariationphylogeneticrelationshipandpolyploidspeciation
AT mingchen comparativechloroplastgenomesofnicotianaspeciessolanaceaeinsightsintothegeneticvariationphylogeneticrelationshipandpolyploidspeciation