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Current Issue of Trends in Genetics


Issue: Trends in Genetics

Jan 01, 2022

Volume 38Issue 1p1-108, e1-e2
Focus issue: Studying genetic variation through an evolutionary lens
Though equal in genomic content, the two parental genomes inherited by a zygote are not equally utilized during early embryonic development. Numerous genes show parent-of-origin-specific gene expression, caused by allele-specific epigenetic differences. Recent studies have characterised a new epigenetic mediator of such genomic imprinting: H3K27me3. H3K27me3 is associated with transcriptional silencing, and it turns out to be heavily biased towards the maternally-derived allele in mouse embryogenesis. The resulting maternal-specific dense chromatin packaging leads to allele-specific expression of the paternally-derived allele. On pages 82–96 of this issue, Raas and Zijlmans et al. review mechanisms and dynamics of H3K27me3-mediated imprinting throughout mouse embryogenesis, and they hypothesise on its evolutionary origins. The cover shows the maternal bias of H3K27me3 (shown in red hexagons) and the more densely-packaged maternal chromatin (pink DNA strand) compared to the paternal chromatin (blue DNA strand). Image credit: Maximilian Raas & Hendrik Marks....
Though equal in genomic content, the two parental genomes inherited by a zygote are not equally utilized during early embryonic development. Numerous genes show parent-of-origin-specific gene expression, caused by allele-specific epigenetic differences. Recent studies have characterised a new epigenetic mediator of such genomic imprinting: H3K27me3. H3K27me3 is associated with transcriptional silencing, and it turns out to be heavily biased towards the maternally-derived allele in mouse embryogenesis. The resulting maternal-specific dense chromatin packaging leads to allele-specific expression of the paternally-derived allele. On pages 82–96 of this issue, Raas and Zijlmans et al. review mechanisms and dynamics of H3K27me3-mediated imprinting throughout mouse embryogenesis, and they hypothesise on its evolutionary origins. The cover shows the maternal bias of H3K27me3 (shown in red hexagons) and the more densely-packaged maternal chromatin (pink DNA strand) compared to the paternal chromatin (blue DNA strand). Image credit: Maximilian Raas & Hendrik Marks.

Forum

  • Gene-dosage issues: a recurrent theme in whole genome duplication events

    • Reiner A. Veitia,
    • James A. Birchler
    Two recent studies have addressed the long-term consequences of whole genome duplications (WGD). Specifically, they analyzed transcriptomes of the plant Arabidopsis thaliana and of four salmonids to assess the impact of WGD on gene expression. These studies point to commonalities in gene expression adjustments after polyploidization that we outline and discuss below.
  • Evolutionary impact of chimeric RNAs on generating phenotypic plasticity in human cells

    • Sumit Mukherjee,
    • Milana Frenkel-Morgenstern
    Chimeric RNAs are generated by the fusion of the exons or introns of two genes. The generation of chimeric RNAs is important for the functional expansion of cells. Here, we describe the functional implications of chimeric RNAs for generating phenotypic plasticity from an evolutionary perspective.
  • Haldane’s duel: intragenomic conflict, selfish Y chromosomes and speciation

    • Scott William Roy
    Haldane’s rule, which states that the heterogametic sex (XY or ZW females) fares more poorly in interspecific hybrids, is generally attributed to absence of one of the two species' X/Z chromosomes. However, Haldane’s rule is also observed in mouse placentas despite paternal X silencing. This pattern could reflect Y chromosomes having evolved to promote growth due to maternal–paternal conflict. If so, balanced sex investment arises from a complex intra- and intergenomic duel.

Opinion

  • The essential but enigmatic regulatory role of HERVH in pluripotency

    • Corinne E. Sexton,
    • Richard L. Tillett,
    • Mira V. Han
    Human specific endogenous retrovirus H (HERVH) is highly expressed in both naive and primed stem cells and is essential for pluripotency. Despite the proven relationship between HERVH expression and pluripotency, there is no single definitive model for the function of HERVH. Instead, several hypotheses of a regulatory function have been put forward including HERVH acting as enhancers, long noncoding RNAs (lncRNAs), and most recently as markers of topologically associating domain (TAD) boundaries.

Feature Review

  • Advancing human disease research with fish evolutionary mutant models

    • Emily A. Beck,
    • Hope M. Healey,
    • Clayton M. Small,
    • Mark C. Currey,
    • Thomas Desvignes,
    • William A. Cresko,
    • John H. Postlethwait
    Model organism research is essential to understand disease mechanisms. However, laboratory-induced genetic models can lack genetic variation and often fail to mimic the spectrum of disease severity. Evolutionary mutant models (EMMs) are species with evolved phenotypes that mimic human disease. EMMs complement traditional laboratory models by providing unique avenues to study gene-by-environment interactions, modular mutations in noncoding regions, and their evolved compensations. EMMs have improved our understanding of complex diseases, including cancer, diabetes, and aging, and illuminated mechanisms in many organs.

Reviews

  • Genome structural variation in human evolution

    • Edward J. Hollox,
    • Luciana W. Zuccherato,
    • Serena Tucci
    Structural variation (SV) is a large difference (typically >100 bp) in the genomic structure of two genomes and includes both copy number variation and variation that does not change copy number of a genomic region, such as an inversion. Improved reference genomes, combined with widespread genome sequencing using short-read sequencing technology, and increasingly using long-read sequencing, have reignited interest in SV. Recent large-scale studies and functional focused analyses have highlighted the role of SV in human evolution.
  • Retention of duplicated genes in evolution

    • Elena Kuzmin,
    • John S. Taylor,
    • Charles Boone
    Gene duplication is a prevalent phenomenon across the tree of life. The processes that lead to the retention of duplicated genes are not well understood. Functional genomics approaches in model organisms, such as yeast, provide useful tools to test the mechanisms underlying retention with functional redundancy and divergence of duplicated genes, including fates associated with neofunctionalization, subfunctionalization, back-up compensation, and dosage amplification. Duplicated genes may also be retained as a consequence of structural and functional entanglement.
  • Regulatory mechanisms ensuring coordinated expression of functionally related genes

    • Oriana Q.H. Zinani,
    • Kemal Keseroğlu,
    • Ertuğrul M. Özbudak
    Coordinated spatiotemporal expression of large sets of genes is required for the development and homeostasis of organisms. To achieve this goal, organisms use myriad strategies where they form operons, utilize bidirectional promoters, cluster genes, share enhancers among genes by DNA looping, and form topologically associated domains and transcriptional condensates. Coexpression achieved by these different strategies is hypothesized to have functional importance in minimizing gene expression variability, establishing dosage balance to ensure stoichiometry of protein complexes, and minimizing accumulation of toxic intermediate metabolites.
  • There is another: H3K27me3-mediated genomic imprinting

    • Maximilian W.D. Raas,
    • Dick W. Zijlmans,
    • Michiel Vermeulen,
    • Hendrik Marks
    DNA methylation has long been considered the primary epigenetic mediator of genomic imprinting in mammals. Recent epigenetic profiling during early mouse development revealed the presence of domains of trimethylation of lysine 27 on histone H3 (H3K27me3) and chromatin compaction specifically at the maternally derived allele, independent of DNA methylation. Within these domains, genes are exclusively expressed from the paternally derived allele. This novel mechanism of noncanonical imprinting plays a key role in the development of mouse extraembryonic tissues and in the regulation of imprinted X-chromosome inactivation, highlighting the importance of parentally inherited epigenetic histone modifications.
  • The evolution of the GALactose utilization pathway in budding yeasts

    • Marie-Claire Harrison,
    • Abigail L. LaBella,
    • Chris Todd Hittinger,
    • Antonis Rokas
    The Leloir galactose utilization or GAL pathway of budding yeasts, including that of the baker’s yeast Saccharomyces cerevisiae and the opportunistic human pathogen Candida albicans, breaks down the sugar galactose for energy and biomass production. The GAL pathway has long served as a model system for understanding how eukaryotic metabolic pathways, including their modes of regulation, evolve. More recently, the physical linkage of the structural genes GAL1, GAL7, and GAL10 in diverse budding yeast genomes has been used as a model for understanding the evolution of gene clustering.

Genome of the Month

  • Nautilus pompilius

    • Hao Song,
    • Li-na Sun,
    • Hai-yan Wang,
    • Tao Zhang
    Nautilus pompilius, a ‘living fossil’, has many ancestral features, such as an external chambered shell and pinhole eye, despite its long evolutionary history, thus providing an excellent prototypical model for studying cephalopod evolution. It also has a compact, minimalist genome with fewer genes and slower evolutionary rates in both noncoding and coding regions compared with its sister coleoid genomes. The genome retained a conserved molluscan biomineralization toolkit; relevant proteins such as shell matrix proteins, Sushi/SCR/CCP, laminin, and chitin-binding domains show high similarity with proteins in other mollusks and have massive lineage-specific expanded repetitive low-complexity domains, which co-contribute to the production of aragonite crystals, a major component of the nautilus shell.
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