Genomewide Nonadditive Gene Regulation in Arabidopsis Allotetraploids

Department of Agronomy, University of Wisconsin, Madison, Wisconsin 53706, USA.
Genetics (Impact Factor: 5.96). 01/2006; 172(1):507-17. DOI: 10.1534/genetics.105.047894
Source: PubMed

ABSTRACT Polyploidy has occurred throughout the evolutionary history of all eukaryotes and is extremely common in plants. Reunification of the evolutionarily divergent genomes in allopolyploids creates regulatory incompatibilities that must be reconciled. Here we report genomewide gene expression analysis of Arabidopsis synthetic allotetraploids, using spotted 70-mer oligo-gene microarrays. We detected >15% transcriptome divergence between the progenitors, and 2105 and 1818 genes were highly expressed in Arabidopsis thaliana and A. arenosa, respectively. Approximately 5.2% (1362) and 5.6% (1469) genes displayed expression divergence from the midparent value (MPV) in two independently derived synthetic allotetraploids, suggesting nonadditive gene regulation following interspecific hybridization. Remarkably, the majority of nonadditively expressed genes in the allotetraploids also display expression changes between the parents, indicating that transcriptome divergence is reconciled during allopolyploid formation. Moreover, >65% of the nonadditively expressed genes in the allotetraploids are repressed, and >94% of the repressed genes in the allotetraploids match the genes that are expressed at higher levels in A. thaliana than in A. arenosa, consistent with the silencing of A. thaliana rRNA genes subjected to nucleolar dominance and with overall suppression of the A. thaliana phenotype in the synthetic allotetraploids and natural A. suecica. The nonadditive gene regulation is involved in various biological pathways, and the changes in gene expression are developmentally regulated. In contrast to the small effects of genome doubling on gene regulation in autotetraploids, the combination of two divergent genomes in allotetraploids by interspecific hybridization induces genomewide nonadditive gene regulation, providing a molecular basis for de novo variation and allopolyploid evolution.

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Available from: Hongmei Jiang, Sep 29, 2015
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    • "Indeed, many plant species include populations with different ploidy levels, with differences in fitness frequently observed as genome dosage changes between diploid and polyploid accessions (Comai, 2005). For instance, such fitness differences are common in allopolyploids formed by the hybridization of two different species, including in hybrid allopolyploid species within the Arabidopsis genus (Chen & Ni, 2006; Wang et al., 2006; Chen, 2010). However, all allopolyploids are, by definition, hybrids, making the separation of genome dosage vs hybridity effects on heterosis challenging. "
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    ABSTRACT: Heterosis is the phenomenon whereby hybrid offspring of genetically divergent parents display superior characteristics compared with their parents. Although hybridity and polyploidy can influence heterosis in hybrid plants, the differential contributions of hybridity vs polyploidy to heterosis effects remain unknown. To address this question, we investigated heterosis effects on rosette size and growth rate of 88 distinct F1 lines of Arabidopsis thaliana consisting of diploids, reciprocal triploids and tetraploids in isogenic and hybrid genetic contexts. 'Heterosis without hybridity' effects on plant size can be generated in genetically isogenic F1 triploid plants. Paternal genome excess F1 triploids display positive heterosis, whereas maternal genome excess F1 s display negative heterosis effects. Paternal genome dosage increases plant size in F1 hybrid triploid plants by, on average, 57% (in contrast with 35% increase displayed by F1 diploid hybrids). Such effects probably derive from differential seed size, as the growth rate of triploids was similar to diploids. Tetraploid plants display a lower growth rate compared with other ploidies, whereas hybrids display increased early stage growth rate. By disaggregating heterosis effects caused by hybridity vs genome dosage, we advance our understanding of heterosis in plants and facilitate novel paternal genome dosage-based strategies to enhance heterosis effects in crop plants.
    New Phytologist 09/2015; DOI:10.1111/nph.13650 · 7.67 Impact Factor
    • "ntly hampered by the lack of genome information for related diatoms . Gene expression systems in allopolyploid ( including allodi - ploid ) organisms have been described in yeasts ( Kodama et al . , 2005 ; Horinouchi et al . , 2010 ) and angiosperms ( e . g . , Coffea arabica allotetraploid [ Bardil et al . , 2011 ] , Arabidopsis allotetraploids [ Wang et al . , 2006 ] , and Gossypium allotetraploids [ Chaudhary et al . , 2009 ] ) . The allopolyploid transcriptome is not likely to be a simple mixture of the parent species but a result of interactions between the regulatory systems derived from each parental spe - cies ( Riddle and Birchler , 2003 ; Pignatta and Comai , 2009 ) , which may facilitate "
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    ABSTRACT: Oleaginous photosynthetic organisms such as microalgae are promising sources for biofuel production through the generation of carbon-neutral sustainable energy. However, the metabolic mechanisms driving high-rate lipid production in these oleaginous organisms remain unclear, thus impeding efforts to improve productivity through genetic modifications. We analyzed the genome and transcriptome of the oleaginous diatom Fistulifera solaris JPCC DA0580. Next-generation sequencing technology provided evidence of an allodiploid genome structure, suggesting unorthodox molecular evolutionary and genetic regulatory systems for reinforcing metabolic efficiencies. Although major metabolic pathways were shared with nonoleaginous diatoms, transcriptome analysis revealed unique expression patterns, such as concomitant upregulation of fatty acid/triacylglycerol biosynthesis and fatty acid degradation (β-oxidation) in concert with ATP production. This peculiar pattern of gene expression may account for the simultaneous growth and oil accumulation phenotype and may inspire novel biofuel production technology based on this oleaginous microalga. © 2015 American Society of Plant Biologists. All rights reserved.
    The Plant Cell 01/2015; 27(1). DOI:10.1105/tpc.114.135194 · 9.34 Impact Factor
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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:
    Journal of Experimental Botany 12/2014; 66(5). DOI:10.1093/jxb/eru486 · 5.53 Impact Factor
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