Transcriptomic Shock Generates Evolutionary Novelty in a Newly Formed, Natural Allopolyploid Plant

Department of Biology, University of Florida, Gainesville, FL 32611, USA.
Current biology: CB (Impact Factor: 9.57). 03/2011; 21(7):551-6. DOI: 10.1016/j.cub.2011.02.016
Source: PubMed


New hybrid species might be expected to show patterns of gene expression intermediate to those shown by parental species. "Transcriptomic shock" may also occur, in which gene expression is disrupted; this may be further modified by whole genome duplication (causing allopolyploidy). "Shock" can include instantaneous partitioning of gene expression between parental copies of genes among tissues. These effects have not previously been studied at a population level in a natural allopolyploid plant species. Here, we survey tissue-specific expression of 144 duplicated gene pairs derived from different parental species (homeologs) in two natural populations of 40-generation-old allotetraploid Tragopogon miscellus (Asteraceae) plants. We compare these results with patterns of allelic expression in both in vitro "hybrids" and hand-crossed F(1) hybrids between the parental diploids T. dubius and T. pratensis, and with patterns of homeolog expression in synthetic (S(1)) allotetraploids. Partitioning of expression was frequent in natural allopolyploids, but F(1) hybrids and S(1) allopolyploids showed less partitioning of expression than the natural allopolyploids and the in vitro "hybrids" of diploid parents. Our results suggest that regulation of gene expression is relaxed in a concerted manner upon hybridization, and new patterns of partitioned expression subsequently emerge over the generations following allopolyploidization.

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Available from: Richard Buggs, Jan 03, 2014
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    • " the course of domestication of hexaploid common wheat ( Yang et al . , 2014 ) . It is expected that the rapidly emerging genomic or transcrip - tomic asymmetry following allopolyploid speciation will con - tinue to evolve under natural and / or human selections , as clearly documented in cotton ( Renny - Byfield & Wendel , 2014 ) and Tragopogon ( Buggs et al . , 2011 ) . Here , we compared the global homeolog expression patterns between the synthetic and natural tetraploid wheats . We found that , relative to the synthetic allote - traploid wheat ( AT2 ) , the spectra of homeolog expression diver - gence were significantly enlarged in all three types of natural tetraploid wheats ( TD , TTR13 and ETW"
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    ABSTRACT: Allopolyploidization has occurred frequently within the Triticum-Aegilops complex which provides a suitable system to investigate how allopolyploidization shapes the expression patterns of duplicated homeologs. We have conducted transcriptome-profiling of leaves and young inflorescences in wild and domesticated tetraploid wheats, Triticum turgidum ssp. dicoccoides (BBAA) and ssp. durum (BBAA), an extracted tetraploid (BBAA), and a synthetic tetraploid (S(l) S(l) AA) wheat together with its diploid parents, Aegilops longissima (S(l) S(l) ) and Triticum urartu (AA). The two diploid species showed tissue-specific differences in genome-wide ortholog expression, which plays an important role in transcriptome shock-mediated homeolog expression rewiring and hence transcriptome asymmetry in the synthetic tetraploid. Further changes of homeolog expression apparently occurred in natural tetraploid wheats, which led to novel transcriptome asymmetry between the two subgenomes. In particular, our results showed that extremely biased homeolog expression can occur rapidly upon the allotetraploidzation and this trend is further enhanced in the course of domestication and evolution of polyploid wheats. Our results suggest that allopolyploidization is accompanied by distinct phases of homeolog expression changes, with parental legacy playing major roles in the immediate rewiring of homeolog expression upon allopolyploidization, while evolution and domestication under allotetraploidy drive further homeolog-expression changes toward re-established subgenome expression asymmetry.
    Full-text · Article · Oct 2015 · New Phytologist
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    • "Preferential suppression of either genome usually takes place in interspecific hybrids and their amphidiploids (Wang et al., 2006; Flagel et al., 2008). Although sudden reunification of divergent genomes may induce genome instability (Adams et al., 2003; Wang et al., 2004; Doyle et al., 2008; Buggs et al., 2011), hybrid-or allopolyploidy-induced incompatibilities may be " settled " by gene expression modulation through chromatin modifications (Osborn et al., 2003; Chen et al., 2004; Ha et al., 2011), transcription factors (Barbash et al., 2003; Shi et al., 2012) and/or RNA interference in the selfing progeny (Wang et al., 2006; Ng et al., 2012). Our comparison of the genome-wide gene expression patterns between a synthetic triploid line and its genome-doubled allohexaploid and stable hexaploid expression changes in allopolyploidization lines has revealed changes arising from hybridization, genome doubling and genome stabilization during allopolyploidization. Since gene expression profiles in hybrid wheats are still unclear, further investigations are needed to clarify the mechanism(s) for gene regulation of allohexaploid wheat. "
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    ABSTRACT: Allopolyploidization is an important evolutionary event in plants, but its genome-wide effects are not fully understood. Common wheat, Triticum aestivum (AABBDD), evolved through amphidiploidization between T. turgidum (AABB) and Aegilops tauschii (DD). Here, global gene expression patterns in the seedlings of a synthetic triploid wheat line (ABD), its chromosome-doubled hexaploid (AABBDD) and stable synthetic hexaploid (AABBDD), and the parental lines T. turgidum (AABB) and Ae. tauschii (DD) were compared using an oligo-DNA microarray to identify metabolic pathways affected by the genome conflict that occurs during allopolyploidization and genome stabilization. Characteristic gene expression patterns of non-additively expressed genes were detected in the newly synthesized triploid and hexaploid, and in the stable synthetic hexaploid. Hierarchical clustering of all differentially expressed and non-additively expressed genes revealed that the gene expression patterns of the triploid (ABD) were similar to those of the maternal parent (AABB), and that expression patterns in successive generations arising from self-pollination became closer to that of the pollen parent (DD). The non-additive gene expression profiles markedly differed between the triploid (ABD) and chromosome-doubled hexaploid (AABBDD), as supported by Gene Ontology (GOSlim) analysis. Four hundred and nineteen non-additively expressed genes were commonly detected in all three generations. GOSlim analysis indicated that these non-additively expressed genes were predominantly involved in "biological pathways". Notably, four of 11 genes related to sugar metabolism displayed elevated expression throughout allopolyploidization. These may be useful candidates for promoting heterosis and adaptation in plants.
    Full-text · Article · Oct 2014 · Genes & Genetic Systems
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    • "Curiously, in the case of rDNA, although T. dubius homeologs are more frequently lost from the polyploid genomes, transcription rates of remaining T. dubius copies are higher than T. pratensis copies [67]. As T. miscellus has shown a high frequency of homeolog loss, but little gene silencing based on the studies to date [21, 41–43, 69], a more comprehensive genome-wide analysis of methylation would help to determine the role of this epigenetic mechanism in shaping the evolution of Tragopogon allopolyploid genomes. "
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    ABSTRACT: Background Hybridization coupled with whole-genome duplication (allopolyploidy) leads to a variety of genetic and epigenetic modifications in the resultant merged genomes. In particular, gene loss and gene silencing are commonly observed post-polyploidization. Here, we investigated DNA methylation as a potential mechanism for gene silencing in Tragopogon miscellus (Asteraceae), a recent and recurrently formed allopolyploid. This species, which also exhibits extensive gene loss, was formed from the diploids T. dubius and T. pratensis. Results Comparative bisulfite sequencing revealed CG methylation of parental homeologs for three loci (S2, S18 and TDF-44) that were previously identified as silenced in T. miscellus individuals relative to the diploid progenitors. One other locus (S3) examined did not show methylation, indicating that other transcriptional and post-transcriptional mechanisms are likely responsible for silencing that homeologous locus. Conclusions These results indicate that Tragopogon miscellus allopolyploids employ diverse mechanisms, including DNA methylation, to respond to the potential shock of genome merger and doubling. Electronic supplementary material The online version of this article (doi:10.1186/1471-2164-15-701) contains supplementary material, which is available to authorized users.
    Full-text · Article · Aug 2014 · BMC Genomics
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