Cargando…

Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation

BACKGROUND: Understanding how organisms evolve and adapt to extreme habitats is of crucial importance in evolutionary ecology. Altitude gradients are an important determinant of the distribution pattern and range of organisms due to distinct climate conditions at different altitudes. High-altitude r...

Descripción completa

Detalles Bibliográficos
Autores principales: Geng, Yupeng, Guan, Yabin, Qiong, La, Lu, Shugang, An, Miao, Crabbe, M. James C., Qi, Ji, Zhao, Fangqing, Qiao, Qin, Zhang, Ticao
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8296595/
https://www.ncbi.nlm.nih.gov/pubmed/34294107
http://dx.doi.org/10.1186/s12915-021-01079-0
_version_ 1783725674551312384
author Geng, Yupeng
Guan, Yabin
Qiong, La
Lu, Shugang
An, Miao
Crabbe, M. James C.
Qi, Ji
Zhao, Fangqing
Qiao, Qin
Zhang, Ticao
author_facet Geng, Yupeng
Guan, Yabin
Qiong, La
Lu, Shugang
An, Miao
Crabbe, M. James C.
Qi, Ji
Zhao, Fangqing
Qiao, Qin
Zhang, Ticao
author_sort Geng, Yupeng
collection PubMed
description BACKGROUND: Understanding how organisms evolve and adapt to extreme habitats is of crucial importance in evolutionary ecology. Altitude gradients are an important determinant of the distribution pattern and range of organisms due to distinct climate conditions at different altitudes. High-altitude regions often provide extreme environments including low temperature and oxygen concentration, poor soil, and strong levels of ultraviolet radiation, leading to very few plant species being able to populate elevation ranges greater than 4000 m. Field pennycress (Thlaspi arvense) is a valuable oilseed crop and emerging model plant distributed across an elevation range of nearly 4500 m. Here, we generate an improved genome assembly to understand how this species adapts to such different environments. RESULTS: We sequenced and assembled de novo the chromosome-level pennycress genome of 527.3 Mb encoding 31,596 genes. Phylogenomic analyses based on 2495 single-copy genes revealed that pennycress is closely related to Eutrema salsugineum (estimated divergence 14.32–18.58 Mya), and both species form a sister clade to Schrenkiella parvula and genus Brassica. Field pennycress contains the highest percentage (70.19%) of transposable elements in all reported genomes of Brassicaceae, with the retrotransposon proliferation in the Middle Pleistocene being likely responsible for the expansion of genome size. Moreover, our analysis of 40 field pennycress samples in two high- and two low-elevation populations detected 1,256,971 high-quality single nucleotide polymorphisms. Using three complementary selection tests, we detected 130 candidate naturally selected genes in the Qinghai-Tibet Plateau (QTP) populations, some of which are involved in DNA repair and the ubiquitin system and potential candidates involved in high-altitude adaptation. Notably, we detected a single base mutation causing loss-of-function of the FLOWERING LOCUS C protein, responsible for the transition to early flowering in high-elevation populations. CONCLUSIONS: Our results provide a genome-wide perspective of how plants adapt to distinct environmental conditions across extreme elevation differences and the potential for further follow-up research with extensive data from additional populations and species. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-021-01079-0.
format Online
Article
Text
id pubmed-8296595
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-82965952021-07-22 Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation Geng, Yupeng Guan, Yabin Qiong, La Lu, Shugang An, Miao Crabbe, M. James C. Qi, Ji Zhao, Fangqing Qiao, Qin Zhang, Ticao BMC Biol Research Article BACKGROUND: Understanding how organisms evolve and adapt to extreme habitats is of crucial importance in evolutionary ecology. Altitude gradients are an important determinant of the distribution pattern and range of organisms due to distinct climate conditions at different altitudes. High-altitude regions often provide extreme environments including low temperature and oxygen concentration, poor soil, and strong levels of ultraviolet radiation, leading to very few plant species being able to populate elevation ranges greater than 4000 m. Field pennycress (Thlaspi arvense) is a valuable oilseed crop and emerging model plant distributed across an elevation range of nearly 4500 m. Here, we generate an improved genome assembly to understand how this species adapts to such different environments. RESULTS: We sequenced and assembled de novo the chromosome-level pennycress genome of 527.3 Mb encoding 31,596 genes. Phylogenomic analyses based on 2495 single-copy genes revealed that pennycress is closely related to Eutrema salsugineum (estimated divergence 14.32–18.58 Mya), and both species form a sister clade to Schrenkiella parvula and genus Brassica. Field pennycress contains the highest percentage (70.19%) of transposable elements in all reported genomes of Brassicaceae, with the retrotransposon proliferation in the Middle Pleistocene being likely responsible for the expansion of genome size. Moreover, our analysis of 40 field pennycress samples in two high- and two low-elevation populations detected 1,256,971 high-quality single nucleotide polymorphisms. Using three complementary selection tests, we detected 130 candidate naturally selected genes in the Qinghai-Tibet Plateau (QTP) populations, some of which are involved in DNA repair and the ubiquitin system and potential candidates involved in high-altitude adaptation. Notably, we detected a single base mutation causing loss-of-function of the FLOWERING LOCUS C protein, responsible for the transition to early flowering in high-elevation populations. CONCLUSIONS: Our results provide a genome-wide perspective of how plants adapt to distinct environmental conditions across extreme elevation differences and the potential for further follow-up research with extensive data from additional populations and species. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-021-01079-0. BioMed Central 2021-07-22 /pmc/articles/PMC8296595/ /pubmed/34294107 http://dx.doi.org/10.1186/s12915-021-01079-0 Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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 Article
Geng, Yupeng
Guan, Yabin
Qiong, La
Lu, Shugang
An, Miao
Crabbe, M. James C.
Qi, Ji
Zhao, Fangqing
Qiao, Qin
Zhang, Ticao
Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
title Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
title_full Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
title_fullStr Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
title_full_unstemmed Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
title_short Genomic analysis of field pennycress (Thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
title_sort genomic analysis of field pennycress (thlaspi arvense) provides insights into mechanisms of adaptation to high elevation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8296595/
https://www.ncbi.nlm.nih.gov/pubmed/34294107
http://dx.doi.org/10.1186/s12915-021-01079-0
work_keys_str_mv AT gengyupeng genomicanalysisoffieldpennycressthlaspiarvenseprovidesinsightsintomechanismsofadaptationtohighelevation
AT guanyabin genomicanalysisoffieldpennycressthlaspiarvenseprovidesinsightsintomechanismsofadaptationtohighelevation
AT qiongla genomicanalysisoffieldpennycressthlaspiarvenseprovidesinsightsintomechanismsofadaptationtohighelevation
AT lushugang genomicanalysisoffieldpennycressthlaspiarvenseprovidesinsightsintomechanismsofadaptationtohighelevation
AT anmiao genomicanalysisoffieldpennycressthlaspiarvenseprovidesinsightsintomechanismsofadaptationtohighelevation
AT crabbemjamesc genomicanalysisoffieldpennycressthlaspiarvenseprovidesinsightsintomechanismsofadaptationtohighelevation
AT qiji genomicanalysisoffieldpennycressthlaspiarvenseprovidesinsightsintomechanismsofadaptationtohighelevation
AT zhaofangqing genomicanalysisoffieldpennycressthlaspiarvenseprovidesinsightsintomechanismsofadaptationtohighelevation
AT qiaoqin genomicanalysisoffieldpennycressthlaspiarvenseprovidesinsightsintomechanismsofadaptationtohighelevation
AT zhangticao genomicanalysisoffieldpennycressthlaspiarvenseprovidesinsightsintomechanismsofadaptationtohighelevation