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The complete chloroplast genome of Ulmus mianzhuensis with insights into structural variations, adaptive evolution, and phylogenetic relationships of Ulmus (Ulmaceae)

BACKGROUND: Ulmus mianzhuensis is an endemic tree species in China with high ornamental and economic value. Currently, little is known regarding its genomic architecture, phylogenetic position, or adaptive evolution. Here, we sequenced the complete chloroplast genome (cp genome) of U. mianzhuensis a...

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Autores principales: Lin, Nan, Liu, Rui, Wang, Yakun, Guo, Peng, Wang, Yihan, Liu, Yanpei, Shang, Fude
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10308733/
https://www.ncbi.nlm.nih.gov/pubmed/37386355
http://dx.doi.org/10.1186/s12864-023-09430-1
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author Lin, Nan
Liu, Rui
Wang, Yakun
Guo, Peng
Wang, Yihan
Liu, Yanpei
Shang, Fude
author_facet Lin, Nan
Liu, Rui
Wang, Yakun
Guo, Peng
Wang, Yihan
Liu, Yanpei
Shang, Fude
author_sort Lin, Nan
collection PubMed
description BACKGROUND: Ulmus mianzhuensis is an endemic tree species in China with high ornamental and economic value. Currently, little is known regarding its genomic architecture, phylogenetic position, or adaptive evolution. Here, we sequenced the complete chloroplast genome (cp genome) of U. mianzhuensis and further compared the variations in gene organization and structure within Ulmus species to define their genomic evolution, then reconstructed the phylogenomic relationship of 31 related Ulmus species to explore the systematic position of U. mianzhuensis and the utility of cp genome for resolving phylogenetics among Ulmus species. RESULTS: Our results revealed that all the Ulmus species exhibited a typical quadripartite structure, with a large single copy (LSC) region of 87,170 − 88,408 bp, a small single copy (SSC) region of 18,650 − 19,038 bp and an inverted repeat (IR) region of 26,288 − 26,546 bp. Within Ulmus species, gene structure and content of cp genomes were highly conserved, although slight variations were found in the boundary of SC/IR regions. Moreover, genome-wide sliding window analysis uncovered the variability of ndhC-trnV-UAC, ndhF-rpl32, and psbI-trnS-GCU were higher among 31 Ulmus that may be useful for the population genetics and potential DNA barcodes. Two genes (rps15 and atpF) were further detected under a positive selection of Ulmus species. Comparative phylogenetic analysis based on the cp genome and protein-coding genes revealed consistent topology that U. mianzhuensis is a sister group to U. parvifolia (sect. Microptelea) with a relatively low-level nucleotide variation of the cp genome. Additionally, our analyses also found that the traditional taxonomic system of five sections in Ulmus is not supported by the current phylogenomic topology with a nested evolutionary relationship between sections. CONCLUSIONS: Features of the cp genome length, GC content, organization, and gene order were highly conserved within Ulmus. Furthermore, molecular evidence from the low variation of the cp genome suggested that U. mianzhuensis should be merged into U. parvifolia and regarded as a subspecies of U. parvifolia. Overall, we demonstrated that the cp genome provides valuable information for understanding the genetic variation and phylogenetic relationship in Ulmus. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09430-1.
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spelling pubmed-103087332023-06-30 The complete chloroplast genome of Ulmus mianzhuensis with insights into structural variations, adaptive evolution, and phylogenetic relationships of Ulmus (Ulmaceae) Lin, Nan Liu, Rui Wang, Yakun Guo, Peng Wang, Yihan Liu, Yanpei Shang, Fude BMC Genomics Research BACKGROUND: Ulmus mianzhuensis is an endemic tree species in China with high ornamental and economic value. Currently, little is known regarding its genomic architecture, phylogenetic position, or adaptive evolution. Here, we sequenced the complete chloroplast genome (cp genome) of U. mianzhuensis and further compared the variations in gene organization and structure within Ulmus species to define their genomic evolution, then reconstructed the phylogenomic relationship of 31 related Ulmus species to explore the systematic position of U. mianzhuensis and the utility of cp genome for resolving phylogenetics among Ulmus species. RESULTS: Our results revealed that all the Ulmus species exhibited a typical quadripartite structure, with a large single copy (LSC) region of 87,170 − 88,408 bp, a small single copy (SSC) region of 18,650 − 19,038 bp and an inverted repeat (IR) region of 26,288 − 26,546 bp. Within Ulmus species, gene structure and content of cp genomes were highly conserved, although slight variations were found in the boundary of SC/IR regions. Moreover, genome-wide sliding window analysis uncovered the variability of ndhC-trnV-UAC, ndhF-rpl32, and psbI-trnS-GCU were higher among 31 Ulmus that may be useful for the population genetics and potential DNA barcodes. Two genes (rps15 and atpF) were further detected under a positive selection of Ulmus species. Comparative phylogenetic analysis based on the cp genome and protein-coding genes revealed consistent topology that U. mianzhuensis is a sister group to U. parvifolia (sect. Microptelea) with a relatively low-level nucleotide variation of the cp genome. Additionally, our analyses also found that the traditional taxonomic system of five sections in Ulmus is not supported by the current phylogenomic topology with a nested evolutionary relationship between sections. CONCLUSIONS: Features of the cp genome length, GC content, organization, and gene order were highly conserved within Ulmus. Furthermore, molecular evidence from the low variation of the cp genome suggested that U. mianzhuensis should be merged into U. parvifolia and regarded as a subspecies of U. parvifolia. Overall, we demonstrated that the cp genome provides valuable information for understanding the genetic variation and phylogenetic relationship in Ulmus. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09430-1. BioMed Central 2023-06-29 /pmc/articles/PMC10308733/ /pubmed/37386355 http://dx.doi.org/10.1186/s12864-023-09430-1 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Lin, Nan
Liu, Rui
Wang, Yakun
Guo, Peng
Wang, Yihan
Liu, Yanpei
Shang, Fude
The complete chloroplast genome of Ulmus mianzhuensis with insights into structural variations, adaptive evolution, and phylogenetic relationships of Ulmus (Ulmaceae)
title The complete chloroplast genome of Ulmus mianzhuensis with insights into structural variations, adaptive evolution, and phylogenetic relationships of Ulmus (Ulmaceae)
title_full The complete chloroplast genome of Ulmus mianzhuensis with insights into structural variations, adaptive evolution, and phylogenetic relationships of Ulmus (Ulmaceae)
title_fullStr The complete chloroplast genome of Ulmus mianzhuensis with insights into structural variations, adaptive evolution, and phylogenetic relationships of Ulmus (Ulmaceae)
title_full_unstemmed The complete chloroplast genome of Ulmus mianzhuensis with insights into structural variations, adaptive evolution, and phylogenetic relationships of Ulmus (Ulmaceae)
title_short The complete chloroplast genome of Ulmus mianzhuensis with insights into structural variations, adaptive evolution, and phylogenetic relationships of Ulmus (Ulmaceae)
title_sort complete chloroplast genome of ulmus mianzhuensis with insights into structural variations, adaptive evolution, and phylogenetic relationships of ulmus (ulmaceae)
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10308733/
https://www.ncbi.nlm.nih.gov/pubmed/37386355
http://dx.doi.org/10.1186/s12864-023-09430-1
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