Characteristics of plastid genomes in the genus Ceratostigma inhabiting arid habitats in China and their phylogenomic implications

Abstract Background Ceratostigma, a genus in the Plumbaginaceae, is an ecologically dominant group of shrubs, subshrub and herb mainly distributed in Qinghai-Tibet Plateau and North China. Ceratostigma has been the focal group in several studies, owing to their importance in economic and ecological...

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Main Authors: Yu-Juan Zhao, Jian Liu, Gen-Shen Yin, Xun Gong
Format: Article
Language:English
Published: BMC 2023-06-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-023-04323-7
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author Yu-Juan Zhao
Jian Liu
Gen-Shen Yin
Xun Gong
author_facet Yu-Juan Zhao
Jian Liu
Gen-Shen Yin
Xun Gong
author_sort Yu-Juan Zhao
collection DOAJ
description Abstract Background Ceratostigma, a genus in the Plumbaginaceae, is an ecologically dominant group of shrubs, subshrub and herb mainly distributed in Qinghai-Tibet Plateau and North China. Ceratostigma has been the focal group in several studies, owing to their importance in economic and ecological value and unique breeding styles. Despite this, the genome information is limited and interspecific relationships within the genus Cerotastigma remains unexplored. Here we sequenced, assembled and characterized the 14 plastomes of five species, and conducted phylogenetic analyses of Cerotastigma using plastomes and nuclear ribosomal DNA (nrDNA) data. Results Fourteen Cerotastigma plastomes possess typical quadripartite structures with lengths from 164,076 to 168,355 bp that consist of a large single copy, a small single copy and a pair of inverted repeats, and contain 127–128 genes, including 82–83 protein coding genes, 37 transfer RNAs and eight ribosomal RNAs. All plastomes are highly conservative and similar in gene order, simple sequence repeats (SSRs), long repeat repeats and codon usage patterns, but some structural variations in the border of single copy and inverted repeats. Mutation hotspots in coding (Pi values > 0.01: matK, ycf3, rps11, rps3, rpl22 and ndhF) and non-coding regions (Pi values > 0.02: trnH-psbA, rps16-trnQ, ndhF-rpl32 and rpl32-trnL) were identified among plastid genomes that could be served as potential molecular markers for species delimitation and genetic variation studies in Cerotastigma. Gene selective pressure analysis showed that most protein-coding genes have been under purifying selection except two genes. Phylogenetic analyses based on whole plastomes and nrDNA strongly support that the five species formed a monophyletic clade. Moreover, interspecific delimitation was well resolved except C. minus, individuals of which clustered into two main clades corresponding to their geographic distributions. The topology inferred from the nrDNA dataset was not congruent with the tree derived from the analyses of the plastid dataset. Conclusion These findings represent the first important step in elucidating plastome evolution in this widespread distribution genus Cerotastigma in the Qinghai-Tibet Plateau. The detailed information could provide a valuable resource for understanding the molecular dynamics and phylogenetic relationship in the family Plumbaginaceae. Lineage genetic divergence within C. minus was perhaps promoted by geographic barriers in the Himalaya and Hengduan Mountains region, but introgression or hybridization could not be completely excluded.
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spelling doaj.art-eefaba18142347629f5695f52bf7a6de2023-06-11T11:09:59ZengBMCBMC Plant Biology1471-22292023-06-0123111510.1186/s12870-023-04323-7Characteristics of plastid genomes in the genus Ceratostigma inhabiting arid habitats in China and their phylogenomic implicationsYu-Juan Zhao0Jian Liu1Gen-Shen Yin2Xun Gong3CAS 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 SciencesInstitute of Agriculture and Life Sciences, Kunming UniversityCAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of SciencesAbstract Background Ceratostigma, a genus in the Plumbaginaceae, is an ecologically dominant group of shrubs, subshrub and herb mainly distributed in Qinghai-Tibet Plateau and North China. Ceratostigma has been the focal group in several studies, owing to their importance in economic and ecological value and unique breeding styles. Despite this, the genome information is limited and interspecific relationships within the genus Cerotastigma remains unexplored. Here we sequenced, assembled and characterized the 14 plastomes of five species, and conducted phylogenetic analyses of Cerotastigma using plastomes and nuclear ribosomal DNA (nrDNA) data. Results Fourteen Cerotastigma plastomes possess typical quadripartite structures with lengths from 164,076 to 168,355 bp that consist of a large single copy, a small single copy and a pair of inverted repeats, and contain 127–128 genes, including 82–83 protein coding genes, 37 transfer RNAs and eight ribosomal RNAs. All plastomes are highly conservative and similar in gene order, simple sequence repeats (SSRs), long repeat repeats and codon usage patterns, but some structural variations in the border of single copy and inverted repeats. Mutation hotspots in coding (Pi values > 0.01: matK, ycf3, rps11, rps3, rpl22 and ndhF) and non-coding regions (Pi values > 0.02: trnH-psbA, rps16-trnQ, ndhF-rpl32 and rpl32-trnL) were identified among plastid genomes that could be served as potential molecular markers for species delimitation and genetic variation studies in Cerotastigma. Gene selective pressure analysis showed that most protein-coding genes have been under purifying selection except two genes. Phylogenetic analyses based on whole plastomes and nrDNA strongly support that the five species formed a monophyletic clade. Moreover, interspecific delimitation was well resolved except C. minus, individuals of which clustered into two main clades corresponding to their geographic distributions. The topology inferred from the nrDNA dataset was not congruent with the tree derived from the analyses of the plastid dataset. Conclusion These findings represent the first important step in elucidating plastome evolution in this widespread distribution genus Cerotastigma in the Qinghai-Tibet Plateau. The detailed information could provide a valuable resource for understanding the molecular dynamics and phylogenetic relationship in the family Plumbaginaceae. Lineage genetic divergence within C. minus was perhaps promoted by geographic barriers in the Himalaya and Hengduan Mountains region, but introgression or hybridization could not be completely excluded.https://doi.org/10.1186/s12870-023-04323-7CeratostigmaPlastid genomeComparative analysisInterspecific relationshipPlumbaginaceae
spellingShingle Yu-Juan Zhao
Jian Liu
Gen-Shen Yin
Xun Gong
Characteristics of plastid genomes in the genus Ceratostigma inhabiting arid habitats in China and their phylogenomic implications
BMC Plant Biology
Ceratostigma
Plastid genome
Comparative analysis
Interspecific relationship
Plumbaginaceae
title Characteristics of plastid genomes in the genus Ceratostigma inhabiting arid habitats in China and their phylogenomic implications
title_full Characteristics of plastid genomes in the genus Ceratostigma inhabiting arid habitats in China and their phylogenomic implications
title_fullStr Characteristics of plastid genomes in the genus Ceratostigma inhabiting arid habitats in China and their phylogenomic implications
title_full_unstemmed Characteristics of plastid genomes in the genus Ceratostigma inhabiting arid habitats in China and their phylogenomic implications
title_short Characteristics of plastid genomes in the genus Ceratostigma inhabiting arid habitats in China and their phylogenomic implications
title_sort characteristics of plastid genomes in the genus ceratostigma inhabiting arid habitats in china and their phylogenomic implications
topic Ceratostigma
Plastid genome
Comparative analysis
Interspecific relationship
Plumbaginaceae
url https://doi.org/10.1186/s12870-023-04323-7
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