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


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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    • "We now know all angiosperms to be paleopolyploid and many to be neopolyploid, with adaptation to the duplicated state characterized by recurring patterns of chromosome number reduction, loss of duplicated members of specific gene functional groups, divergence of expression of duplicated gene pairs, and other changes. While synthetic polyploids formed experimentally offer intriguing insight into first reactions of a genome to duplication including loss and restructuring of low-copy DNA sequences (Song et al., 1995; Feldman et al., 1997; Ozkan et al., 2001, 2002; Shaked et al., 2001; Kashkush et al., 2002), activation of genes and retrotransposons (O'Neill et al., 2002; Kashkush et al., 2003), gene silencing (Chen and Pikaard, 1997a, 1997b; Comai et al., 2000; Lee and Chen, 2001; Wang et al., 2006), and subfunctionalization of gene expression patterns (Adams et al., 2003, 2004), these reactions could alternatively be symptoms of imminent extinction of the lineage. Indeed, the extinction hypothesis seems more likely, given that most higher organisms pass through different ploidy levels at different stages of development (Galitski et al., 1999; Hughes et al., 2000) and continuously produce aberrant unreduced gametes at low rates but exceedingly few result in successful lineages and that polyploids generally exhibit lower speciation rates and higher extinction rates than diploids (Mayrose et al., 2011). "
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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
    • "Newly synthesized allopolyploids, which parental forms are known, are a very useful material to study both genetic and epigenetic changes emerging in the early stages of their evolution. Intraspecific crossing and polyploidization result in the formation of new allopolyploids with extensive changes, such as genomic rearrangements, changes in the regulation of gene expression, activation of mobile elements, deletion or amplification of highly repeated or unique sequences, as well as various epigenetic modifications (Kashkush et al. 2002, Adams and Wendel 2005, Wang et al. 2006, Liu et al. 2009, Kraithstein et al. 2010, Jiang et al. 2011). Many researchers have analyzed changes occurring in the nucleotide sequence of triticale using different molecular techniques, such as amplified fragment length polymorphism (AFLP), restriction fragment length polymorphism (RFLP) (Ma et al. 2004, Ma and Gustafson 2008, Bento et al. 2011), single sequence repeat (SSR) (Vaillancourt et al. 2008), the IRAP, REMAP, and ISSR (Bento et al. 2008, Kalinka 2010). "
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    ABSTRACT: Analysis of structural changes of octoploid triticale genomes was conducted in F2 and F3 generations. The plants were derived from crosses of five cultivars and breeding lines of hexaploid wheat (Triticum aestivum L.) with one cultivar of rye (Secale cereale L). The study used four marker systems: inter-simple sequence repeat (ISSR), inter-retrotransposon amplified polymorphism (IRAP), retrotransposon-microsatellite amplified polymorphism (REMAP), and a technique named inter-transposon amplified polymorphism (ITAP) developed by the authors. Most frequently, elimination of specific bands was observed, especially of rye bands. Depending on the cross combination, the percentage of eliminated rye bands ranged from 73.6 to 80.6 %. A lower percentage of wheat bands was eliminated, i.e., from 57.6 to 76.48 %, depending on the combination of crosses. The emergence of new types of bands in hybrids absent in the parental forms was the rarest phenomenon (14.5–17.9 %). The results indicate the ongoing process of genome rearrangements at the molecular level in the early generations of plant crosses that also involve repeated nucleotide sequences of DNA.
    Biologia Plantarum 09/2015; · 1.85 Impact Factor
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