Cargando…

Evolution of Rosaceae Plastomes Highlights Unique Cerasus Diversification and Independent Origins of Fruiting Cherry

Rosaceae comprises numerous types of economically important fruits, ornamentals, and timber. The lack of plastome characteristics has blocked our understanding of the evolution of plastome and plastid genes of Rosaceae crops. Using comparative genomics and phylogenomics, we analyzed 121 Rosaceae pla...

Descripción completa

Detalles Bibliográficos
Autores principales: Zhang, Jing, Wang, Yan, Chen, Tao, Chen, Qing, Wang, Lei, Liu, Zhen-shan, Wang, Hao, Xie, Rui, He, Wen, Li, Ming, Liu, Cong-li, Yang, Shao-feng, Li, Meng-yao, Lin, Yuan-xiu, Zhang, Yun-ting, Zhang, Yong, Luo, Ya, Tang, Hao-ru, Gao, Li-zhi, Wang, Xiao-rong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8639594/
https://www.ncbi.nlm.nih.gov/pubmed/34868119
http://dx.doi.org/10.3389/fpls.2021.736053
_version_ 1784609183487754240
author Zhang, Jing
Wang, Yan
Chen, Tao
Chen, Qing
Wang, Lei
Liu, Zhen-shan
Wang, Hao
Xie, Rui
He, Wen
Li, Ming
Liu, Cong-li
Yang, Shao-feng
Li, Meng-yao
Lin, Yuan-xiu
Zhang, Yun-ting
Zhang, Yong
Luo, Ya
Tang, Hao-ru
Gao, Li-zhi
Wang, Xiao-rong
author_facet Zhang, Jing
Wang, Yan
Chen, Tao
Chen, Qing
Wang, Lei
Liu, Zhen-shan
Wang, Hao
Xie, Rui
He, Wen
Li, Ming
Liu, Cong-li
Yang, Shao-feng
Li, Meng-yao
Lin, Yuan-xiu
Zhang, Yun-ting
Zhang, Yong
Luo, Ya
Tang, Hao-ru
Gao, Li-zhi
Wang, Xiao-rong
author_sort Zhang, Jing
collection PubMed
description Rosaceae comprises numerous types of economically important fruits, ornamentals, and timber. The lack of plastome characteristics has blocked our understanding of the evolution of plastome and plastid genes of Rosaceae crops. Using comparative genomics and phylogenomics, we analyzed 121 Rosaceae plastomes of 54 taxa from 13 genera, predominantly including Cerasus (true cherry) and its relatives. To our knowledge, we generated the first comprehensive map of genomic variation across Rosaceae plastomes. Contraction/expansion of inverted repeat regions and sequence losses of the two single-copy regions underlie large genomic variations in size among Rosaceae plastomes. Plastid protein-coding genes were characterized with a high proportion (over 50%) of synonymous variants and insertion-deletions with multiple triplets. Five photosynthesis-related genes were specially selected in perennial woody trees. Comparative genomic analyses implied divergent evolutionary patterns between pomaceous and drupaceous trees. Across all examined plastomes, unique and divergent evolution was detected in Cerasus plastomes. Phylogenomic analyses and molecular dating highlighted the relatively distant phylogenetic relationship between Cerasus and relatives (Microcerasus, Amygdalus, Prunus, and Armeniaca), which strongly supported treating the monophyletic true cherry group as a separate genus excluding dwarf cherry. High genetic differentiation and distinct phylogenetic relationships implied independent origins and domestication between fruiting cherries, particularly between Prunus pseudocerasus (Cerasus pseudocerasus) and P. avium (C. avium). Well-resolved maternal phylogeny suggested that cultivated P. pseudocerasus originated from Longmenshan Fault zone, the eastern edge of Himalaya-Hengduan Mountains, where it was subjected to frequent genomic introgression between its presumed wild ancestors and relatives.
format Online
Article
Text
id pubmed-8639594
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-86395942021-12-04 Evolution of Rosaceae Plastomes Highlights Unique Cerasus Diversification and Independent Origins of Fruiting Cherry Zhang, Jing Wang, Yan Chen, Tao Chen, Qing Wang, Lei Liu, Zhen-shan Wang, Hao Xie, Rui He, Wen Li, Ming Liu, Cong-li Yang, Shao-feng Li, Meng-yao Lin, Yuan-xiu Zhang, Yun-ting Zhang, Yong Luo, Ya Tang, Hao-ru Gao, Li-zhi Wang, Xiao-rong Front Plant Sci Plant Science Rosaceae comprises numerous types of economically important fruits, ornamentals, and timber. The lack of plastome characteristics has blocked our understanding of the evolution of plastome and plastid genes of Rosaceae crops. Using comparative genomics and phylogenomics, we analyzed 121 Rosaceae plastomes of 54 taxa from 13 genera, predominantly including Cerasus (true cherry) and its relatives. To our knowledge, we generated the first comprehensive map of genomic variation across Rosaceae plastomes. Contraction/expansion of inverted repeat regions and sequence losses of the two single-copy regions underlie large genomic variations in size among Rosaceae plastomes. Plastid protein-coding genes were characterized with a high proportion (over 50%) of synonymous variants and insertion-deletions with multiple triplets. Five photosynthesis-related genes were specially selected in perennial woody trees. Comparative genomic analyses implied divergent evolutionary patterns between pomaceous and drupaceous trees. Across all examined plastomes, unique and divergent evolution was detected in Cerasus plastomes. Phylogenomic analyses and molecular dating highlighted the relatively distant phylogenetic relationship between Cerasus and relatives (Microcerasus, Amygdalus, Prunus, and Armeniaca), which strongly supported treating the monophyletic true cherry group as a separate genus excluding dwarf cherry. High genetic differentiation and distinct phylogenetic relationships implied independent origins and domestication between fruiting cherries, particularly between Prunus pseudocerasus (Cerasus pseudocerasus) and P. avium (C. avium). Well-resolved maternal phylogeny suggested that cultivated P. pseudocerasus originated from Longmenshan Fault zone, the eastern edge of Himalaya-Hengduan Mountains, where it was subjected to frequent genomic introgression between its presumed wild ancestors and relatives. Frontiers Media S.A. 2021-11-19 /pmc/articles/PMC8639594/ /pubmed/34868119 http://dx.doi.org/10.3389/fpls.2021.736053 Text en Copyright © 2021 Zhang, Wang, Chen, Chen, Wang, Liu, Wang, Xie, He, Li, Liu, Yang, Li, Lin, Zhang, Zhang, Luo, Tang, Gao and Wang. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Zhang, Jing
Wang, Yan
Chen, Tao
Chen, Qing
Wang, Lei
Liu, Zhen-shan
Wang, Hao
Xie, Rui
He, Wen
Li, Ming
Liu, Cong-li
Yang, Shao-feng
Li, Meng-yao
Lin, Yuan-xiu
Zhang, Yun-ting
Zhang, Yong
Luo, Ya
Tang, Hao-ru
Gao, Li-zhi
Wang, Xiao-rong
Evolution of Rosaceae Plastomes Highlights Unique Cerasus Diversification and Independent Origins of Fruiting Cherry
title Evolution of Rosaceae Plastomes Highlights Unique Cerasus Diversification and Independent Origins of Fruiting Cherry
title_full Evolution of Rosaceae Plastomes Highlights Unique Cerasus Diversification and Independent Origins of Fruiting Cherry
title_fullStr Evolution of Rosaceae Plastomes Highlights Unique Cerasus Diversification and Independent Origins of Fruiting Cherry
title_full_unstemmed Evolution of Rosaceae Plastomes Highlights Unique Cerasus Diversification and Independent Origins of Fruiting Cherry
title_short Evolution of Rosaceae Plastomes Highlights Unique Cerasus Diversification and Independent Origins of Fruiting Cherry
title_sort evolution of rosaceae plastomes highlights unique cerasus diversification and independent origins of fruiting cherry
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8639594/
https://www.ncbi.nlm.nih.gov/pubmed/34868119
http://dx.doi.org/10.3389/fpls.2021.736053
work_keys_str_mv AT zhangjing evolutionofrosaceaeplastomeshighlightsuniquecerasusdiversificationandindependentoriginsoffruitingcherry
AT wangyan evolutionofrosaceaeplastomeshighlightsuniquecerasusdiversificationandindependentoriginsoffruitingcherry
AT chentao evolutionofrosaceaeplastomeshighlightsuniquecerasusdiversificationandindependentoriginsoffruitingcherry
AT chenqing evolutionofrosaceaeplastomeshighlightsuniquecerasusdiversificationandindependentoriginsoffruitingcherry
AT wanglei evolutionofrosaceaeplastomeshighlightsuniquecerasusdiversificationandindependentoriginsoffruitingcherry
AT liuzhenshan evolutionofrosaceaeplastomeshighlightsuniquecerasusdiversificationandindependentoriginsoffruitingcherry
AT wanghao evolutionofrosaceaeplastomeshighlightsuniquecerasusdiversificationandindependentoriginsoffruitingcherry
AT xierui evolutionofrosaceaeplastomeshighlightsuniquecerasusdiversificationandindependentoriginsoffruitingcherry
AT hewen evolutionofrosaceaeplastomeshighlightsuniquecerasusdiversificationandindependentoriginsoffruitingcherry
AT liming evolutionofrosaceaeplastomeshighlightsuniquecerasusdiversificationandindependentoriginsoffruitingcherry
AT liucongli evolutionofrosaceaeplastomeshighlightsuniquecerasusdiversificationandindependentoriginsoffruitingcherry
AT yangshaofeng evolutionofrosaceaeplastomeshighlightsuniquecerasusdiversificationandindependentoriginsoffruitingcherry
AT limengyao evolutionofrosaceaeplastomeshighlightsuniquecerasusdiversificationandindependentoriginsoffruitingcherry
AT linyuanxiu evolutionofrosaceaeplastomeshighlightsuniquecerasusdiversificationandindependentoriginsoffruitingcherry
AT zhangyunting evolutionofrosaceaeplastomeshighlightsuniquecerasusdiversificationandindependentoriginsoffruitingcherry
AT zhangyong evolutionofrosaceaeplastomeshighlightsuniquecerasusdiversificationandindependentoriginsoffruitingcherry
AT luoya evolutionofrosaceaeplastomeshighlightsuniquecerasusdiversificationandindependentoriginsoffruitingcherry
AT tanghaoru evolutionofrosaceaeplastomeshighlightsuniquecerasusdiversificationandindependentoriginsoffruitingcherry
AT gaolizhi evolutionofrosaceaeplastomeshighlightsuniquecerasusdiversificationandindependentoriginsoffruitingcherry
AT wangxiaorong evolutionofrosaceaeplastomeshighlightsuniquecerasusdiversificationandindependentoriginsoffruitingcherry