Extensive Translational Regulation of Gene Expression in an Allopolyploid (<i>Glycine dolichocarpa</i>)

Coate, Jeremy E.; Bar, Haim; Doyle, Jeff J.

doi:10.1105/tpc.113.119966

Cited by 52 publications

(46 citation statements)

References 83 publications

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“…Homeolog expression bias observed at the transcriptional level was largely preserved in the translatome. Coate et al (40) found that translational regulation preferentially targets genes involved in transcription, translation, and photosynthesis, causing regional and possibly whole-chromosome shifts in expression bias between homeologs, and reduces transcriptional differences between the polyploid and its diploid progenitors. Translational regulation correlates positively with long-term retention of homeologs from a paleopolyploidy event, suggesting that it plays a significant role in polyploid evolution.…”

Section: Coffea Arabicamentioning

confidence: 98%

Nonadditive Gene Expression in Polyploids

et al. 2014

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Allopolyploidy involves hybridization and duplication of divergent parental genomes and provides new avenues for gene expression. The expression levels of duplicated genes in polyploids can show deviation from parental additivity (the arithmetic average of the parental expression levels). Nonadditive expression has been widely observed in diverse polyploids and comprises at least three possible scenarios: (a) The total gene expression level in a polyploid is similar to that of one of its parents (expression-level dominance); (b) total gene expression is lower or higher than in both parents (transgressive expression); and (c) the relative contribution of the parental copies (homeologs) to the total gene expression is unequal (homeolog expression bias). Several factors may result in expression nonadditivity in polyploids, including maternal-paternal influence, gene dosage balance, cis- and/or trans-regulatory networks, and epigenetic regulation. As our understanding of nonadditive gene expression in polyploids remains limited, a new generation of investigators should explore additional phenomena (i.e., alternative splicing) and use other high-throughput "omics" technologies to measure the impact of nonadditive expression on phenotype, proteome, and metabolome.

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Section: Coffea Arabicamentioning

confidence: 98%

Nonadditive Gene Expression in Polyploids

et al. 2014

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“…Thus, where researchers are interested in quantifying changes in expression per gene copy or per cell (absolute regulation), rather than changes in expression per transcriptome (relative regulation), transcriptome-normalized expression is a poor proxy for the actual biological phenomena of interest. It has previously been pointed out that transcript abundance often correlates poorly with protein abundance (e.g., Schwanhausser et al 2011;Coate et al 2014;Ly et al 2014), but transcriptome size variation introduces another, rarely considered disconnect between expression profiling data and biological reality. Consequently, though transcriptional responses per transcriptome have been widely studied, gene expression responses per gene copy or per cell, as well as variation in total transcription, remain largely unexplored, and remarkably, the distinction between these different measures of expression is frequently ignored or overlooked.…”

Section: Introductionmentioning

confidence: 98%

Variation in transcriptome size: are we getting the message?

Coate

Doyle

2014

Chromosoma

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The number of RNA molecules per cell (transcriptome size) is highly variable, differing among and within cell types depending on cell size, stage of the cell cycle, ploidy level, age, disease state, and growth condition. Such variation has been observed at the level of total RNA, ribosomal RNA, messenger RNA (mRNA), and the polyadenylated fraction of mRNA, and these distinct RNA species can also vary in abundance with respect to each other. This variation in transcriptome size has been largely ignored or overlooked, and in fact, standard data normalization procedures for transcript profiling experiments implicitly assume that mRNA transcriptome size is constant. Consequently, variation in transcriptome size has important technical implications for such experiments, as well as profound biological implications for the affected cells and underlying genomes. Here, we review what is known about transcriptome size variation, explore how ignoring this variation introduces systematic bias into standard expression profiling experiments, and present examples of how such biases have led to erroneous conclusions in expression studies of sex chromosome dosage compensation, cancer, Rett syndrome, embryonic development, aging, and polyploidy. We also discuss how quantifying transcriptome size will help to elucidate the selective forces underlying patterns of gene and genome evolution and review the evidence that cells exert tight control over transcriptome size in order to maintain cell size homeostasis and to optimize chemical reactions within the cell, such that loss of control over transcriptome size is associated with cancer and aging. Thus, transcriptome size is an important phenotype in its own right. Finally, we discuss strategies for quantifying transcriptome size and individual gene dosage responses in order to account for and better understand this important biological phenomenon.

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“…Homoploid hybridization and allopolyploidization may disrupt both genetic and epigenomic processes resulting in altered DNA methylation patterns (Shaked et al, 2001;Mittelsten Scheid et al, 2003;Salmon et al, 2005;Lukens et al, 2006;Chen, 2007;Song and Chen, 2015;Rigal et al, 2016), changes in gene expression (Adams et al, 2003;Adams and Wendel, 2005;Buggs et al, 2010;Chelaifa et al, 2010;Coate et al, 2014;Renny-Byfield et al, 2015 and transposable element (TE) reactivation (Dion-Côté et al, 2014), commonly referred to as genomic shock (McClintock, 1984). These genome-wide changes are associated with novel phenotypic variation in newly formed allopolyploids (Madlung et al, 2002;Gaeta et al, 2007), which likely contributed to the survival and ultimate success of polyploids (Kagale et al, 2014;Vanneste et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower

et al. 2017

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Recent studies have shown that one of the parental subgenomes in ancient polyploids is generally more dominant, having retained more genes and being more highly expressed, a phenomenon termed subgenome dominance. The genomic features that determine how quickly and which subgenome dominates within a newly formed polyploid remain poorly understood. To investigate the rate of emergence of subgenome dominance, we examined gene expression, gene methylation, and transposable element (TE) methylation in a natural, <140-year-old allopolyploid (Mimulus peregrinus), a resynthesized interspecies triploid hybrid (M. robertsii), a resynthesized allopolyploid (M. peregrinus), and progenitor species (M. guttatus and M. luteus). We show that subgenome expression dominance occurs instantly following the hybridization of divergent genomes and significantly increases over generations. Additionally, CHH methylation levels are reduced in regions near genes and within TEs in the first-generation hybrid, intermediate in the resynthesized allopolyploid, and are repatterned differently between the dominant and recessive subgenomes in the natural allopolyploid. Subgenome differences in levels of TE methylation mirror the increase in expression bias observed over the generations following hybridization. These findings provide important insights into genomic and epigenomic shock that occurs following hybridization and polyploid events and may also contribute to uncovering the mechanistic basis of heterosis and subgenome dominance.

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Extensive Translational Regulation of Gene Expression in an Allopolyploid (Glycine dolichocarpa)

Cited by 52 publications

References 83 publications

Nonadditive Gene Expression in Polyploids

Nonadditive Gene Expression in Polyploids

Variation in transcriptome size: are we getting the message?

Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower

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