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Title: Evolutionary Analyses of Gene Expression Divergence in Panicum hallii : Exploring Constitutive and Plastic Responses Using Reciprocal Transplants

Journal Article · · Molecular Biology and Evolution

Abstract The evolution of gene expression is thought to be an important mechanism of local adaptation and ecological speciation. Gene expression divergence occurs through the evolution of cis- polymorphisms and through more widespread effects driven by trans-regulatory factors. Here, we explore expression and sequence divergence in a large sample of Panicum hallii accessions encompassing the species range using a reciprocal transplantation experiment. We observed widespread genotype and transplant site drivers of expression divergence, with a limited number of genes exhibiting genotype-by-site interactions. We used a modified FST–QST outlier approach (QPC analysis) to detect local adaptation. We identified 514 genes with constitutive expression divergence above and beyond the levels expected under neutral processes. However, no plastic expression responses met our multiple testing correction as QPC outliers. Constitutive QPC outlier genes were involved in a number of developmental processes and responses to abiotic environments. Leveraging earlier expression quantitative trait loci results, we found a strong enrichment of expression divergence, including for QPC outliers, in genes previously identified with cis and cis–environment interactions but found no patterns related to trans-factors. Population genetic analyses detected elevated sequence divergence of promoters and coding sequence of constitutive expression outliers but little evidence for positive selection on these proteins. Our results are consistent with a hypothesis of cis-regulatory divergence as a primary driver of expression divergence in P. hallii.

Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Grant/Contract Number:
SC0014156; SC0021126; AC02-05CH11231
OSTI ID:
2280395
Alternate ID(s):
OSTI ID: 2472340
Journal Information:
Molecular Biology and Evolution, Journal Name: Molecular Biology and Evolution Journal Issue: 10 Vol. 40; ISSN 0737-4038
Publisher:
Oxford University PressCopyright Statement
Country of Publication:
United States
Language:
English

References (90)

Expression Divergence Is Correlated with Sequence Evolution but Not Positive Selection in Conifers journal February 2016
Determinants of Substitution Rates in Mammalian Genes: Expression Pattern Affects Selection Intensity but Not Mutation Rate journal January 2000
Variation in Recombination Rate Is Shaped by Domestication and Environmental Conditions in Barley journal June 2019
Inheritance of Gene Expression Level and Selective Constraints on Trans- and Cis-Regulatory Changes in Yeast journal June 2013
Genomic mechanisms of climate adaptation in polyploid bioenergy switchgrass journal January 2021
Genomic Determinants of Protein Evolution and Polymorphism in Arabidopsis journal January 2011
Cis- and trans-regulatory divergence between progenitor species determines gene-expression novelty in Arabidopsis allopolyploids journal January 2012
Natural selection on gene expression journal August 2006
Genetical genomics: combining genetics with gene expression analysis journal October 2005
pixy : Unbiased estimation of nucleotide diversity and divergence in the presence of missing data journal February 2021
Recombination rate estimation in the presence of hotspots journal July 2007
Emerging principles of regulatory evolution journal May 2007
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega journal January 2011
Genetics of gene expression surveyed in maize, mouse and man journal March 2003
A Yeast Hybrid Provides Insight into the Evolution of Gene Expression Regulation journal April 2009
Evolutionary trade-offs between baseline and plastic gene expression in two congeneric oyster species journal June 2019
A High-Throughput 3′-Tag RNA Sequencing for Large-Scale Time-Series Transcriptome Studies book October 2021
Regulatory changes underlying expression differences within and between Drosophila species journal February 2008
Natural variation in growth and leaf ion homeostasis in response to salinity stress in Panicum hallii journal October 2022
Selection on adaptive and maladaptive gene expression plasticity during thermal adaptation to urban heat islands journal October 2021
Detecting Adaptive Differentiation in Structured Populations with Genomic Data and Common Gardens journal January 2019
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies journal January 2014
Discriminant analysis of principal components: a new method for the analysis of genetically structured populations journal January 2010
A population genetic transect of Panicum hallii (Poaceae) journal March 2013
The genetics of divergence and reproductive isolation between ecotypes of Panicum hallii journal September 2014
adegenet 1.3-1: new tools for the analysis of genome-wide SNP data journal September 2011
The genomic landscape of molecular responses to natural drought stress in Panicum hallii journal December 2018
Rethinking long‐term vegetation dynamics: multiple glacial refugia and local expansion of a species complex journal February 2019
The variant call format and VCFtools journal June 2011
Comparative studies of gene expression and the evolution of gene regulation journal June 2012
Variation within and among species in gene expression: raw material for evolution journal March 2006
Gene Expression and Protein Length Influence Codon Usage and Rates of Sequence Evolution in Populus tremula journal December 2006
Variable gene expression in eukaryotes: a network perspective journal May 2007
Local adaptation contributes to gene expression divergence in maize journal January 2021
Reassessment of Mendelian gene pathogenicity using 7,855 cardiomyopathy cases and 60,706 reference samples journal August 2016
variancePartition: interpreting drivers of variation in complex gene expression studies journal November 2016
Inference of Population Structure Using Multilocus Genotype Data: Linked Loci and Correlated Allele Frequencies journal August 2003
Inference of Population Structure Using Multilocus Genotype Data journal June 2000
Evolutionary dynamics of coding and non-coding transcriptomes journal October 2014
A One-Penny Imputed Genome from Next-Generation Reference Panels journal September 2018
Detecting signatures of selection on gene expression journal May 2022
Active and adaptive plasticity in a changing climate journal July 2022
Statistical significance for genomewide studies journal July 2003
Evolutionary Dynamics of Regulatory Changes Underlying Gene Expression Divergence among Saccharomyces Species journal April 2017
Between‐population differences in constitutive and infection‐induced gene expression in threespine stickleback journal October 2021
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 journal December 2014
BBMerge – Accurate paired shotgun read merging via overlap journal October 2017
Connecting theory and data to understand recombination rate evolution journal November 2017
Low Rates of Expression Profile Divergence in Highly Expressed Genes and Tissue-Specific Genes During Mammalian Evolution journal March 2006
Resurrecting the role of Transcription Factor Change in Developmental Evolution journal September 2008
Gene regulatory divergence between locally adapted ecotypes in their native habitats journal October 2018
Gene expression plasticity as a mechanism of coral adaptation to a variable environment journal November 2016
Strong control, conservative point estimation and simultaneous conservative consistency of false discovery rates: a unified approach journal February 2004
STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method journal October 2011
The strength and pattern of natural selection on gene expression in rice journal February 2020
Expression level is a major modifier of the fitness landscape of a protein coding gene journal November 2021
Monitoring plant and soil water status: established and novel methods revisited and their relevance to studies of drought tolerance journal November 2006
Genotype-by-Environment Interaction and Plasticity: Exploring Genomic Responses of Plants to the Abiotic Environment journal November 2013
Pleiotropic effects of trans-regulatory mutations on fitness and gene expression journal July 2022
The loci of Evolution: how Predictable is Genetic Evolution? journal September 2008
Evaluating the role of natural selection in the evolution of gene regulation journal May 2007
Neutral and adaptive variation in gene expression journal March 2006
A test of the Neutral Model of Expression Change in Natural Populations of House Mouse Subspecies journal February 2010
Detecting the number of clusters of individuals using the software structure: a simulation study journal July 2005
Cutadapt removes adapter sequences from high-throughput sequencing reads journal May 2011
Allelic variation and heterosis in maize: How do two halves make more than a whole? journal February 2007
PAML 4: Phylogenetic Analysis by Maximum Likelihood journal April 2007
The roles of cis- and trans-regulation in the evolution of regulatory incompatibilities and sexually dimorphic gene expression journal September 2013
Allelic Variation of Gene Expression in Maize Hybrids journal June 2004
Divergence in Gene Expression Is Uncoupled from Divergence in Coding Sequence in a Secondarily Woody Sunflower journal September 2013
Drought responsive gene expression regulatory divergence between upland and lowland ecotypes of a perennial C 4 grass journal March 2016
The Genetic Architecture of Shoot and Root Trait Divergence Between Mesic and Xeric Ecotypes of a Perennial Grass journal April 2019
Local Regulatory Variation in Saccharomyces cerevisiae journal August 2005
Common Pattern of Evolution of Gene Expression Level and Protein Sequence in Drosophila journal July 2004
The Sequence Alignment/Map format and SAMtools journal June 2009
Constraints on the evolution of phenotypic plasticity: limits and costs of phenotype and plasticity journal February 2015
A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w journal April 2012
Key Questions on the Role of Phenotypic Plasticity in Eco-Evolutionary Dynamics journal August 2015
Fast and accurate short read alignment with Burrows-Wheeler transform journal May 2009
PLINK: A Tool Set for Whole-Genome Association and Population-Based Linkage Analyses journal September 2007
Recombination Landscape Divergence Between Populations is Marked by Larger Low-Recombining Regions in Domesticated Rye journal June 2022
The Baldwin Effect and Genetic Assimilation: Revisiting two Mechanisms of Evolutionary Change Mediated by Phenotypic Plasticity journal November 2007
Adaptive Evolution of Gene Expression in Drosophila journal August 2017
Modularity Facilitates Flexible Tuning of Plastic and Evolutionary Gene Expression Responses during Early Divergence journal December 2017
featureCounts: an efficient general purpose program for assigning sequence reads to genomic features journal November 2013
Crossover Interference in the Mouse journal March 2002
Gene expression stasis and plasticity following migration into a foreign environment journal August 2017
Plant phenotypic plasticity in a changing climate journal December 2010
The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data journal July 2010
Geographic patterns of genomic diversity and structure in the C4 grass Panicum hallii across its natural distribution journal January 2021