Variation in gene expression patterns across a conifer hybrid zone highlights the architecture of adaptive evolution under novel selective pressures

Variation in gene expression among natural populations are key contributors to adaptive evolution. Understanding the architecture underlying adaptive trait evolution provides insights into the adaptive potential of populations exposed to novel selective pressures. We investigated patterns and processes driving trait differentiation under novel climatic conditions by combining common garden experiments with transcriptome-wide datasets obtained from Pinus strobiformis - Pinus flexilis hybrid zone populations. We found strong signals of genotype-environment interactions at the individual transcript and the co-expression module level, a marked influence of drought related variables on adaptive evolution and an environment dependent influence of P. flexilis ancestry on survival. Using co-expression network connectivity as a proxy for pleiotropy we highlight that adaptive transcripts were pleiotropic across both gardens and modules with strong population differentiation exhibited lower preservation across gardens. Our work highlights the utility of integrating transcriptomics with space-for-time substitution studies to evaluate the adaptive potential of long-lived species. We conclude by suggesting that the combination of pleiotropic trait architectures and substantial genetic variation may enable long-lived forest tree species to respond to rapid shift in climatic conditions.

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Can Forest Trees Cope with Climate Change?—Effects of DNA Methylation on Gene Expression and Adaptation to Environmental Change

International Journal of Molecular Sciences ◽

10.3390/ijms222413524 ◽

2021 ◽

Vol 22 (24) ◽

pp. 13524

Author(s):

Ewelina A. Klupczyńska ◽

Ewelina Ratajczak

Keyword(s):

Climate Change ◽

Gene Expression ◽

Dna Methylation ◽

Global Climate ◽

Regional Climate ◽

Expression Patterns ◽

Forest Tree ◽

Epigenetic Modifications ◽

Specific Expression ◽

Epigenome Editing

Epigenetic modifications, including chromatin modifications and DNA methylation, play key roles in regulating gene expression in both plants and animals. Transmission of epigenetic markers is important for some genes to maintain specific expression patterns and preserve the status quo of the cell. This article provides a review of existing research and the current state of knowledge about DNA methylation in trees in the context of global climate change, along with references to the potential of epigenome editing tools and the possibility of their use for forest tree research. Epigenetic modifications, including DNA methylation, are involved in evolutionary processes, developmental processes, and environmental interactions. Thus, the implications of epigenetics are important for adaptation and phenotypic plasticity because they provide the potential for tree conservation in forest ecosystems exposed to adverse conditions resulting from global warming and regional climate fluctuations.

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Gene regulatory evolution in cold-adapted fly populations neutralizes plasticity and may undermine genetic canalization

10.1101/2022.01.14.476421 ◽

2022 ◽

Author(s):

Yuheng Huang ◽

Justin Lack ◽

Grant Hoppel ◽

John E Pool

Keyword(s):

Gene Expression ◽

Alternative Splicing ◽

Adaptive Evolution ◽

Empirical Studies ◽

Natural Populations ◽

Plastic Response ◽

Cold Adapted ◽

Thermal Environments ◽

Gene Regulatory ◽

Transcriptomic Level

The relationships between adaptive evolution, phenotypic plasticity, and canalization remain incompletely understood. Theoretical and empirical studies have made conflicting arguments on whether adaptive evolution may enhance or oppose the plastic response. Gene regulatory traits offer excellent potential to study the relationship between plasticity and adaptation, and they can now be studied at the transcriptomic level. Here we take advantage of three closely-related pairs of natural populations of Drosophila melanogaster from contrasting thermal environments that reflect three separate instances of cold tolerance evolution. We measure the transcriptome-wide plasticity in gene expression levels and alternative splicing (intron usage) between warm and cold laboratory environments. We find that suspected adaptive changes in both gene expression and alternative splicing tend to neutralize the ancestral plastic response. Further, we investigate the hypothesis that adaptive evolution can lead to decanalization of selected gene regulatory traits. We find strong evidence that suspected adaptive gene expression (but not splicing) changes in cold-adapted populations are more vulnerable to the genetic perturbation of inbreeding than putatively neutral changes. We find some evidence that these patterns may reflect a loss of genetic canalization accompanying adaptation, although other processes including hitchhiking recessive deleterious variants may contribute as well. Our findings augment our understanding of genetic and environmental effects on gene regulation in the context of adaptive evolution.

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Gene expression changes of seven stonefly species in responses to a latitudinal-environmental gradient

10.1101/2020.09.22.309179 ◽

2020 ◽

Author(s):

Maribet Gamboa ◽

Yusuke Gotoh ◽

Arnelyn D. Doloiras-Laraño ◽

Kozo Watanabe

Keyword(s):

Gene Expression ◽

Environmental Stress ◽

Environmental Conditions ◽

Latitudinal Gradient ◽

Environmental Changes ◽

Expression Patterns ◽

Gene Expression Patterns ◽

Adaptive Potential ◽

Geographical Regions ◽

Multiple Species

AbstractLatitudinal variation has been known to create strong selection pressure for genomic variation that enables the adaptation and survival of organisms. By altering gene expression patterns, organisms can modify their adaptive potential to heterogeneous environmental conditions along a latitudinal gradient; however, there is a gap in our understanding of how physiological consequences in wild species are affected and how changing environmental conditions act on multiple species. Here, we investigated how seven stream stonefly species sampled from four geographical regions in Japan differ in their responses to latitudinal variations by measuring gene expression (RNA-sequencing) differences within species and gene co-expression among species. We found that a large number of genes (622) were differentially expressed along the latitudinal gradient. The high species-specific gene expression diversity found at higher latitude regions was probably associated with low temperatures and high water discharge, which suggests the adaptive potential of stonefly specie. In contrast, similar gene expression patterns among species was observed at lower latitudes, which suggests that strong environmental stress occurs in warmer regions. Weighted gene co-expression network analysis (WGCNA) identified 22 genes with similar expression patterns among species along the latitudinal gradient. Among the four geographical regions, high differential expression patterns in the co-expressed genes from two regions were found, suggesting that the local environment strongly affects gene expression patterns among species in these regions. Respiration, metabolism, and developmental co-expressed genes exhibited a latitudinal cline, showing clear evidence of divergent adaptive responses to latitude. Our findings demonstrate that stonefly species are differentially adapted to local environmental conditions, and imply that adaptation in gene expression could be shared by multiple species under environmental stress conditions. This study highlights the importance of considering multiple species when evaluating the consequences of environmental changes on aquatic insect communities, and possible mechanisms to cope with environmental changes.

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Systematic changes in gene expression patterns following adaptive evolution in yeast

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.96.17.9721 ◽

1999 ◽

Vol 96 (17) ◽

pp. 9721-9726 ◽

Cited By ~ 327

Author(s):

T. L. Ferea ◽

D. Botstein ◽

P. O. Brown ◽

R. F. Rosenzweig

Keyword(s):

Gene Expression ◽

Adaptive Evolution ◽

Expression Patterns ◽

Gene Expression Patterns

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Linking gene expression patterns with survival studies elucidates adaptive potential in changing environments

Molecular Ecology ◽

10.1111/mec.15389 ◽

2020 ◽

Vol 29 (6) ◽

pp. 1031-1034 ◽

Cited By ~ 1

Author(s):

Mariah H. Meek

Keyword(s):

Gene Expression ◽

Expression Patterns ◽

Gene Expression Patterns ◽

Adaptive Potential ◽

Changing Environments ◽

Survival Studies

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Complexities of gene expression patterns in natural populations of an extremophile fish (Poecilia mexicana , Poeciliidae)

Molecular Ecology ◽

10.1111/mec.14198 ◽

2017 ◽

Vol 26 (16) ◽

pp. 4211-4225 ◽

Cited By ~ 13

Author(s):

Courtney N. Passow ◽

Anthony P. Brown ◽

Lenin Arias-Rodriguez ◽

Muh-Ching Yee ◽

Alexandra Sockell ◽

...

Keyword(s):

Gene Expression ◽

Expression Patterns ◽

Natural Populations ◽

Gene Expression Patterns ◽

Poecilia Mexicana

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Homogenization of sub-genome secretome gene expression patterns in the allodiploid fungus Verticillium longisporum

10.1101/341636 ◽

2018 ◽

Cited By ~ 4

Author(s):

Jasper R.L. Depotter ◽

Fabian van Beveren ◽

Luis Rodriguez-Moreno ◽

Grardy C.M. van den Berg ◽

Thomas A. Wood ◽

...

Keyword(s):

Gene Expression ◽

Plant Pathogens ◽

Genome Duplication ◽

Expression Patterns ◽

Secreted Proteins ◽

Plant Colonization ◽

Gene Expression Patterns ◽

Adaptive Potential ◽

Verticillium Longisporum ◽

Genes Encoding

AbstractAllopolyploidization, genome duplication through interspecific hybridization, is an important evolutionary mechanism that can enable organisms to adapt to environmental changes or stresses. The increased adaptive potential of allopolyploids can be particularly relevant for plant pathogens in their ongoing quest for host immune response evasion. To this end, plant pathogens secrete a plethora of molecules that enable host colonization. Allodiploidization has resulted in the new plant pathogen Verticillium longisporum that infects different hosts than haploid Verticillium species. To reveal the impact of allodiploidization on plant pathogen evolution, we studied the genome and transcriptome dynamics of V. longisporum using next-generation sequencing. V. longisporum genome evolution is characterized by extensive chromosomal rearrangements, between as well as within parental chromosome sets, leading to a mosaic genome structure. In comparison to haploid Verticillium species, V. longisporum genes display stronger signs of positive selection. The expression patterns of the two sub-genomes show remarkable resemblance, suggesting that the parental gene expression patterns homogenized upon hybridization. Moreover, whereas V. longisporum genes encoding secreted proteins frequently display differential expression between the parental sub-genomes in culture medium, expression patterns homogenize upon plant colonization. Collectively, our results illustrate of the adaptive potential of allodiploidy mediated by the interplay of two sub-genomes.Author summaryHybridization followed by whole-genome duplication, so-called allopolyploidization, provides genomic flexibility that is beneficial for survival under stressful conditions or invasiveness into new habitats. Allopolyploidization has mainly been studied in plants, but also occurs in other organisms, including fungi. Verticillium longisporum, an emerging fungal pathogen on brassicaceous plants, arose by allodiploidization between two Verticillium spp. We used comparative genomics to reveal the plastic nature of the V. longisporum genomes, showing that parental chromosome sets recombined extensively, resulting in a mosaic genome pattern. Furthermore, we show that non-synonymous substitutions frequently occurred in V. longisporum. Moreover, we reveal that expression patterns of genes encoding secreted proteins homogenized between the V. longisporum sub-genomes upon plant colonization. In conclusion, our results illustrate the large adaptive potential upon genome hybridization for fungi mediated by genomic plasticity and interaction between sub-genomes.

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