Cross‐kingdom transcriptomic trends in the evolution of hybrid gene expression

Behling, Anna H; Winter, David J.; Ganley, Austen R. D.; Cox, Murray P.

doi:10.1111/jeb.14059

Cited by 3 publications

References 88 publications

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Asymmetric genome merging leads to gene expression novelty through nucleo-cytoplasmic disruptions and transcriptomic shock inChlamydomonastriploids

Prost-Boxoen,

Bafort,

Van de Vloet

et al. 2024

Preprint

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Genome merging is a common phenomenon in many organisms, causing a wide range of consequences on phenotype, adaptation, and gene expression, among other effects, yet its broader implications are not well understood. Two consequences of genome merging on gene expression remain poorly understood: dosage effects and evolution of expression. In this study, we employedChlamydomonas reinhardtiias a model to investigate the effects of asymmetric genome merging by crossing a diploid with a haploid strain to create a novel triploid line. Five independent clonal lineages derived from this triploid line were evolved for 425 asexual generations in a laboratory natural selection (LNS) experiment. Utilizing fitness assays, qPCR, and RNA-Seq, we assessed the immediate consequences of genome merging and subsequent evolution over time. Our findings reveal substantial alterations in gene expression, protein homeostasis (proteostasis) and cytonuclear stoichiometry. Notably, gene expression exhibited expression level dominance and transgressivity (i.e., expression level higher or lower than either parent). Ongoing expression level dominance and a pattern of “functional dominance” from the haploid parent was observed, alongside remarkable stability in expression patterns across generations. Despite major nucleo-cytoplasmic disruptions, enhanced fitness was detected in the triploid strain. By comparing gene expression across generations, our results indicate that proteostasis restoration is a critical component of rapid adaptation following genome merging inChlamydomonas reinhardtiiand possibly other systems.

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Asymmetric genome merging leads to gene expression novelty through nucleo-cytoplasmic disruptions and transcriptomic shock inChlamydomonastriploids

Prost-Boxoen,

Bafort,

Van de Vloet

et al. 2024

Preprint

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Cross‐kingdom transcriptomic trends in the evolution of hybrid gene expression

Behling

Winter

Ganley

et al. 2022

J of Evolutionary Biology

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Hybridization is a route to speciation that occurs widely across the eukaryote tree of life. The success of allopolyploids (hybrid species with increased ploidy) and homoploid hybrids (with unchanged ploidy) is well documented. However, their formation and establishment is not straightforward, with a suite of near‐instantaneous and longer term biological repercussions faced by the new species. Central to these challenges is the rewiring of gene regulatory networks following the merger of distinct genomes inherited from both parental species. Research on the evolution of hybrid gene expression has largely involved studies on a single hybrid species or a few gene families. Here, we present the first standardized transcriptome‐wide study exploring the fates of genes following hybridization across three kingdoms: animals, plants and fungi. Within each kingdom, we pair an allopolyploid system with a closely related homoploid hybrid to decouple the influence of increased ploidy from genome merger. Genome merger, not changes in ploidy, has the greatest effect on posthybridization expression patterns across all study systems. Strikingly, we find that differentially expressed genes in parent species preferentially switch to more similar expression in hybrids across all kingdoms, likely as a consequence of regulatory trans‐acting cross‐talk within the hybrid nucleus. We also highlight the prevalence of gene loss or silencing among extremely differentially expressed genes in hybrid species across all kingdoms. These shared patterns suggest that the evolutionary process of hybridization leads to common high‐level expression outcomes, regardless of the particular species or kingdom.

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Hybridization and gene expression: Beyond differentially expressed genes

Runemark,

Moore,

Larson

2024

Molecular Ecology

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Gene expression has a key role in reproductive isolation, and studies of hybrid gene expression have identified mechanisms causing hybrid sterility. Here, we review the evidence for altered gene expression following hybridization and outline the mechanisms shown to contribute to altered gene expression in hybrids. Transgressive gene expression, transcending that of both parental species, is pervasive in early generation sterile hybrids, but also frequently observed in viable, fertile hybrids. We highlight studies showing that hybridization can result in transgressive gene expression, also in established hybrid lineages or species. Such extreme patterns of gene expression in stabilized hybrid taxa suggest that altered hybrid gene expression may result in hybridization‐derived evolutionary novelty. We also conclude that while patterns of misexpression in hybrids are well documented, the understanding of the mechanisms causing misexpression is lagging. We argue that jointly assessing differences in cell composition and cell‐specific changes in gene expression in hybrids, in addition to assessing changes in chromatin and methylation, will significantly advance our understanding of the basis of altered gene expression. Moreover, uncovering to what extent evolution of gene expression results in altered expression for individual genes, or entire networks of genes, will advance our understanding of how selection moulds gene expression. Finally, we argue that jointly studying the dual roles of altered hybrid gene expression, serving both as a mechanism for reproductive isolation and as a substrate for hybrid ecological adaptation, will lead to significant advances in our understanding of the evolution of gene expression.

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Cross‐kingdom transcriptomic trends in the evolution of hybrid gene expression

Cited by 3 publications

References 88 publications

Asymmetric genome merging leads to gene expression novelty through nucleo-cytoplasmic disruptions and transcriptomic shock inChlamydomonastriploids

Asymmetric genome merging leads to gene expression novelty through nucleo-cytoplasmic disruptions and transcriptomic shock inChlamydomonastriploids

Cross‐kingdom transcriptomic trends in the evolution of hybrid gene expression

Hybridization and gene expression: Beyond differentially expressed genes

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