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
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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.
    New Phytologist 10/2015; DOI:10.1111/nph.13678 · 7.67 Impact Factor
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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.
    BMC Genomics 08/2014; 15(1):701. DOI:10.1186/1471-2164-15-701 · 3.99 Impact Factor
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    • "Furthermore, we show by coupled qRT-PCR and pyrosequencing analysis of a subset of ETW versus durum (cv TTR13) downregulated genes that a great majority of the modified expression levels in the BBAA subgenomes are shared by the 21 studied bread wheat cultivars of diverse origins, which suggests the early occurrence and evolutionary persistence of altered expression. Although a similar phenomenon of rapid occurrence and evolutionary conservation of altered gene expression has been observed previously in other plant taxa, such as Arabidopsis (Wang et al., 2006), cotton (Grover et al., 2012), Senecio (Hegarty et al., 2006), and Tragopogon (Buggs et al., 2011), our results represent unequivocal documentation of rapid and functionally distinct transcriptome alterations in subgenomes of any extant allopolyploid organism without the complication of a coexisting subgenome. This can be accomplished only by reliberating the genetically " colonized " subgenomes as fully " independent " organismal genomes. "
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    ABSTRACT: Subgenome integrity in bread wheat (Triticum aestivum; BBAADD) makes possible the extraction of its BBAA component to restitute a novel plant type. The availability of such a ploidy-reversed wheat (extracted tetraploid wheat [ETW]) provides a unique opportunity to address whether and to what extent the BBAA component of bread wheat has been modified in phenotype, karyotype, and gene expression during its evolutionary history at the allohexaploid level. We report here that ETW was anomalous in multiple phenotypic traits but maintained a stable karyotype. Microarray-based transcriptome profiling identified a large number of differentially expressed genes between ETW and natural tetraploid wheat (Triticum turgidum), and the ETW-downregulated genes were enriched for distinct Gene Ontology categories. Quantitative RT-PCR analysis showed that gene expression differences between ETW and a set of diverse durum wheat (T. turgidum subsp durum) cultivars were distinct from those characterizing tetraploid cultivars per se. Pyrosequencing revealed that the expression alterations may occur to either only one or both of the B and A homoeolog transcripts in ETW. A majority of the genes showed additive expression in a resynthesized allohexaploid wheat. Analysis of a synthetic allohexaploid wheat and diverse bread wheat cultivars revealed the rapid occurrence of expression changes to the BBAA subgenomes subsequent to allohexaploidization and their evolutionary persistence.
    The Plant Cell 07/2014; 26(7). DOI:10.1105/tpc.114.128439 · 9.34 Impact Factor
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