Population transcriptomic sequencing reveals allopatric divergence and local adaptation in Pseudotaxus chienii (Taxaceae)

Abstract Background Elucidating the effects of geography and selection on genetic variation is critical for understanding the relative importance of adaptation in driving differentiation and identifying the environmental factors underlying its occurrence. Adaptive genetic variation is common in tree...

Full description

Bibliographic Details
Main Authors: Li Liu, Zhen Wang, Yingjuan Su, Ting Wang
Format: Article
Language:English
Published: BMC 2021-05-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-021-07682-3
_version_ 1818833110936059904
author Li Liu
Zhen Wang
Yingjuan Su
Ting Wang
author_facet Li Liu
Zhen Wang
Yingjuan Su
Ting Wang
author_sort Li Liu
collection DOAJ
description Abstract Background Elucidating the effects of geography and selection on genetic variation is critical for understanding the relative importance of adaptation in driving differentiation and identifying the environmental factors underlying its occurrence. Adaptive genetic variation is common in tree species, especially widely distributed long-lived species. Pseudotaxus chienii can occupy diverse habitats with environmental heterogeneity and thus provides an ideal material for investigating the process of population adaptive evolution. Here, we characterize genetic and expression variation patterns and investigate adaptive genetic variation in P. chienii populations. Results We generated population transcriptome data and identified 13,545 single nucleotide polymorphisms (SNPs) in 5037 unigenes across 108 individuals from 10 populations. We observed lower nucleotide diversity (π = 0.000701) among the 10 populations than observed in other gymnosperms. Significant negative correlations between expression diversity and nucleotide diversity in eight populations suggest that when the species adapts to the surrounding environment, gene expression and nucleotide diversity have a reciprocal relationship. Genetic structure analyses indicated that each distribution region contains a distinct genetic group, with high genetic differentiation among them due to geographical isolation and local adaptation. We used F ST outlier, redundancy analysis, and latent factor mixed model methods to detect molecular signatures of local adaptation. We identified 244 associations between 164 outlier SNPs and 17 environmental variables. The mean temperature of the coldest quarter, soil Fe and Cu contents, precipitation of the driest month, and altitude were identified as the most important determinants of adaptive genetic variation. Most candidate unigenes with outlier signatures were related to abiotic and biotic stress responses, and the monoterpenoid biosynthesis and ubiquitin-mediated proteolysis KEGG pathways were significantly enriched in certain populations and deserve further attention in other long-lived trees. Conclusions Despite the strong population structure in P. chienii, genomic data revealed signatures of divergent selection associated with environmental variables. Our research provides SNPs, candidate unigenes, and biological pathways related to environmental variables to facilitate elucidation of the genetic variation in P. chienii in relation to environmental adaptation. Our study provides a promising tool for population genomic analyses and insights into the molecular basis of local adaptation.
first_indexed 2024-12-19T02:13:43Z
format Article
id doaj.art-decb8eec4b5646ec97d2df19524dca9b
institution Directory Open Access Journal
issn 1471-2164
language English
last_indexed 2024-12-19T02:13:43Z
publishDate 2021-05-01
publisher BMC
record_format Article
series BMC Genomics
spelling doaj.art-decb8eec4b5646ec97d2df19524dca9b2022-12-21T20:40:33ZengBMCBMC Genomics1471-21642021-05-0122112110.1186/s12864-021-07682-3Population transcriptomic sequencing reveals allopatric divergence and local adaptation in Pseudotaxus chienii (Taxaceae)Li Liu0Zhen Wang1Yingjuan Su2Ting Wang3School of Life Sciences, Sun Yat-sen UniversitySchool of Life Sciences, Sun Yat-sen UniversitySchool of Life Sciences, Sun Yat-sen UniversityCollege of Life Sciences, South China Agricultural UniversityAbstract Background Elucidating the effects of geography and selection on genetic variation is critical for understanding the relative importance of adaptation in driving differentiation and identifying the environmental factors underlying its occurrence. Adaptive genetic variation is common in tree species, especially widely distributed long-lived species. Pseudotaxus chienii can occupy diverse habitats with environmental heterogeneity and thus provides an ideal material for investigating the process of population adaptive evolution. Here, we characterize genetic and expression variation patterns and investigate adaptive genetic variation in P. chienii populations. Results We generated population transcriptome data and identified 13,545 single nucleotide polymorphisms (SNPs) in 5037 unigenes across 108 individuals from 10 populations. We observed lower nucleotide diversity (π = 0.000701) among the 10 populations than observed in other gymnosperms. Significant negative correlations between expression diversity and nucleotide diversity in eight populations suggest that when the species adapts to the surrounding environment, gene expression and nucleotide diversity have a reciprocal relationship. Genetic structure analyses indicated that each distribution region contains a distinct genetic group, with high genetic differentiation among them due to geographical isolation and local adaptation. We used F ST outlier, redundancy analysis, and latent factor mixed model methods to detect molecular signatures of local adaptation. We identified 244 associations between 164 outlier SNPs and 17 environmental variables. The mean temperature of the coldest quarter, soil Fe and Cu contents, precipitation of the driest month, and altitude were identified as the most important determinants of adaptive genetic variation. Most candidate unigenes with outlier signatures were related to abiotic and biotic stress responses, and the monoterpenoid biosynthesis and ubiquitin-mediated proteolysis KEGG pathways were significantly enriched in certain populations and deserve further attention in other long-lived trees. Conclusions Despite the strong population structure in P. chienii, genomic data revealed signatures of divergent selection associated with environmental variables. Our research provides SNPs, candidate unigenes, and biological pathways related to environmental variables to facilitate elucidation of the genetic variation in P. chienii in relation to environmental adaptation. Our study provides a promising tool for population genomic analyses and insights into the molecular basis of local adaptation.https://doi.org/10.1186/s12864-021-07682-3Pseudotaxus chieniiPopulation transcriptomeSNPPopulation structureGenotype-environment associationLocal adaptation
spellingShingle Li Liu
Zhen Wang
Yingjuan Su
Ting Wang
Population transcriptomic sequencing reveals allopatric divergence and local adaptation in Pseudotaxus chienii (Taxaceae)
BMC Genomics
Pseudotaxus chienii
Population transcriptome
SNP
Population structure
Genotype-environment association
Local adaptation
title Population transcriptomic sequencing reveals allopatric divergence and local adaptation in Pseudotaxus chienii (Taxaceae)
title_full Population transcriptomic sequencing reveals allopatric divergence and local adaptation in Pseudotaxus chienii (Taxaceae)
title_fullStr Population transcriptomic sequencing reveals allopatric divergence and local adaptation in Pseudotaxus chienii (Taxaceae)
title_full_unstemmed Population transcriptomic sequencing reveals allopatric divergence and local adaptation in Pseudotaxus chienii (Taxaceae)
title_short Population transcriptomic sequencing reveals allopatric divergence and local adaptation in Pseudotaxus chienii (Taxaceae)
title_sort population transcriptomic sequencing reveals allopatric divergence and local adaptation in pseudotaxus chienii taxaceae
topic Pseudotaxus chienii
Population transcriptome
SNP
Population structure
Genotype-environment association
Local adaptation
url https://doi.org/10.1186/s12864-021-07682-3
work_keys_str_mv AT liliu populationtranscriptomicsequencingrevealsallopatricdivergenceandlocaladaptationinpseudotaxuschieniitaxaceae
AT zhenwang populationtranscriptomicsequencingrevealsallopatricdivergenceandlocaladaptationinpseudotaxuschieniitaxaceae
AT yingjuansu populationtranscriptomicsequencingrevealsallopatricdivergenceandlocaladaptationinpseudotaxuschieniitaxaceae
AT tingwang populationtranscriptomicsequencingrevealsallopatricdivergenceandlocaladaptationinpseudotaxuschieniitaxaceae