Flagel LE, Udall J, Nettleton D, Wendel J. Duplicate gene expression in allopolyploid Gossypium reveals two temporally distinct phases of expression evolution. BMC Biol 6: 16

Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, IA 50011, USA.
BMC Biology (Impact Factor: 7.98). 02/2008; 6(1):16. DOI: 10.1186/1741-7007-6-16
Source: PubMed


Polyploidy has played a prominent role in shaping the genomic architecture of the angiosperms. Through allopolyploidization, several modern Gossypium (cotton) species contain two divergent, although largely redundant genomes. Owing to this redundancy, these genomes can play host to an array of evolutionary processes that act on duplicate genes.
We compared homoeolog (genes duplicated by polyploidy) contributions to the transcriptome of a natural allopolyploid and a synthetic interspecific F1 hybrid, both derived from a merger between diploid species from the Gossypium A-genome and D-genome groups. Relative levels of A- and D-genome contributions to the petal transcriptome were determined for 1,383 gene pairs. This comparison permitted partitioning of homoeolog expression biases into those arising from genomic merger and those resulting from polyploidy. Within allopolyploid Gossypium, approximately 24% of the genes with biased (unequal contributions from the two homoeologous copies) expression patterns are inferred to have arisen as a consequence of genomic merger, indicating that a substantial fraction of homoeolog expression biases occur instantaneously with hybridization. The remaining 76% of biased homoeologs reflect long-term evolutionary forces, such as duplicate gene neofunctionalization and subfunctionalization. Finally, we observed a greater number of genes biased toward the paternal D-genome and that expression biases have tended to increases during allopolyploid evolution.
Our results indicate that allopolyploidization entails significant homoeolog expression modulation, both immediately as a consequence of genomic merger, and secondarily as a result of long-term evolutionary transformations in duplicate gene expression.

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    • "Detection of different copies expected in these genomes may be challenging, because individual gene duplications (resulting in paralogs in both diploid and polyploid genomes) usually add an additional layer of complexity (Ainouche et al. 2012). Detection and analysis of homeologs is central to polyploidy research, and several studies have focused on the detection of different copies in polyploid genomes such as in Glycine (Ilut et al. 2012), Gossypium (Flagel et al. 2008; Salmon et al. 2009), Coffea (Combes et al. 2011) or Triticum (Akhunova et al. 2010) species. In these systems, the diploid parental (or related) representatives are known and can be used to identify duplicated homeologs in the allotetraploids. "
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    ABSTRACT: Gene and whole-genome duplications are widespread in plant nuclear genomes, resulting in sequence heterogeneity. Identification of duplicated genes may be particularly challenging in highly redundant genomes, especially when there are no diploid parents as reference. Here, we developed a pipeline to detect the different copies in the ribosomal RNA gene family in the hexaploid grass Spartina maritima from Next Generation Sequencing (Roche-454) reads. The heterogeneity of the different domains of the highly repeated 45S unit was explored by identifying Single Nucleotide Polymorphisms (SNPs), and assembling reads based on shared polymorphisms. SNPs were validated using comparisons with Illumina sequence data sets and by cloning and Sanger-(re)sequencing. Using this approach, 29 validated polymorphisms and 11 validated haplotypes were reported (out of 34 and 20, respectively, which were initially predicted by our program). The rDNA domains of S. maritima have similar lengths to those found in other Poaceae, apart from the 5'-ETS which is about twice longer in S. maritima. Sequence homogeneity was encountered in coding regions and both internal transcribed spacers (ITS), while high intra-genomic variability was detected in the intergenic spacer (IGS) and the external transcribed spacer (ETS). Molecular cytogenetic analysis by Fluorescent In Situ Hybridization (FISH) revealed the presence of one pair of 45S rDNA signals on the chromosomes of S. maritima instead of three expected pairs for a hexaploid genome, indicating loss of duplicated homeologous loci through the diploidization process. The procedure developed here may be employed at any ploidy level and using different sequencing technologies.
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    • "Differential geneexpression patterns among diploids and tetraploids have been studied to investigate the effects of natural and synthetic polyploidy for novel organ development and resistance to abiotic stresses (Chen and Ni, 2006; Doyle et al., 2008). The molecular basis of evolutionary advantage could be related to gene expression changes, which have been demonstrated in resynthesized polyploids in Arabidopsis (Wang et al., 2006), Brassica (Gaeta et al., 2009), and Gossypium (Flagel et al., 2008). RNA sequencing (RNA-seq) revealed the differential expression of ~50% of paralogues among 18 000 duplicated genes in soybean; the genes showed subfunctionalization on testing seven different tissues (Roulin et al., 2013). "
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    ABSTRACT: The exploitation of synthetic polyploids for producing seedless fruits is well known in watermelon. Tetraploid progenitors of triploid watermelon plants, compared with their diploid counterparts, exhibit wide phenotypic differences. Although many factors modulate alternative splicing (AS) in plants, the effects of autopolyploidization on AS are still unknown. In this study, we used tissues of leaf, stem, and fruit of diploid and tetraploid sweet watermelon to understand changes in gene expression and the occurrence of AS. RNA-sequencing analysis was performed along with reverse transcription quantitative PCR and rapid amplification of cDNA ends (RACE)-PCR to demonstrate changes in expression and splicing. All vegetative tissues except fruit showed an increased level of AS in the tetraploid watermelon throughout the growth period. The ploidy levels of diploids and the tetraploid were confirmed using a ploidy analyser. We identified 5362 and 1288 genes that were up- and downregulated, respectively, in tetraploid as compared with diploid plants. We further confirmed that 22 genes underwent AS events across tissues, indicating possibilities of generating different protein isoforms with altered functions of important transcription factors and transporters. Arginine biosynthesis, chlorophyllide synthesis, GDP mannose biosynthesis, trehalose biosynthesis, and starch and sucrose degradation pathways were upregulated in autotetraploids. Phloem protein 2, chloroplastic PGR5-like protein, zinc-finger protein, fructokinase-like 2, MYB transcription factor, and nodulin MtN21 showed AS in fruit tissues. These results should help in developing high-quality seedless watermelon and provide additional transcriptomic information related to other cucurbits. © The Author 2014. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email:
    Full-text · Article · Dec 2014 · Journal of Experimental Botany
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    • "This discrepancy between transcriptomes in two newly-generated hexaploids might be due to the tissues examined (young seedling vs. flower bud) and/or genome constitutions (Hegarty et al., 2006, 2008). 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). "
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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.
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