Homoeolog-specific transcriptional bias in allopolyploid wheat

Abstract

BackgroundInteraction between parental genomes is accompanied by global changes in gene expression which, eventually, contributes to growth vigor and the broader phenotypic diversity of allopolyploid species. In order to gain a better understanding of the effects of allopolyploidization on the regulation of diverged gene networks, we performed a genome-wide analysis of homoeolog-specific gene expression in re-synthesized allohexaploid wheat created by the hybridization of a tetraploid derivative of hexaploid wheat with the diploid ancestor of the wheat D genome Ae. tauschii.ResultsAffymetrix wheat genome arrays were used for both the discovery of divergent homoeolog-specific mutations and analysis of homoeolog-specific gene expression in re-synthesized allohexaploid wheat. More than 34,000 detectable parent-specific features (PSF) distributed across the wheat genome were used to assess AB genome (could not differentiate A and B genome contributions) and D genome parental expression in the allopolyploid transcriptome. In re-synthesized polyploid 81% of PSFs detected mid-parent levels of gene expression, and only 19% of PSFs showed the evidence of non-additive expression. Non-additive expression in both AB and D genomes was strongly biased toward up-regulation of parental type of gene expression with only 6% and 11% of genes, respectively, being down-regulated. Of all the non-additive gene expression, 84% can be explained by differences in the parental genotypes used to make the allopolyploid. Homoeolog-specific co-regulation of several functional gene categories was found, particularly genes involved in photosynthesis and protein biosynthesis in wheat.ConclusionsHere, we have demonstrated that the establishment of interactions between the diverged regulatory networks in allopolyploids is accompanied by massive homoeolog-specific up- and down-regulation of gene expression. This study provides insights into interactions between homoeologous genomes and their role in growth vigor, development, and fertility of allopolyploid species.

Extensive and Heritable Epigenetic Remodeling and Genetic Stability Accompany Allohexaploidization of Wheat

“…Therefore, this type of rapid genetic instability likely has played some roles in the initial establishment and eventual speciation of T. aestivum (Levy and Feldman 2004;Feldman and Levy 2005;Feldman and Levy 2009). Similarly, genome-wide changes in gene expression in the early generations of nascent allohexaploid wheat have also been documented as a general occurrence in multiple independent lines (Pumphrey et al 2009;Akhunova et al 2010;Chague et al 2010;our unpublished data), so were in other studied plant taxa (reviewed in Osborn et al 2003;Adams and Wendel 2005b;Comai 2005;Chen and Ni 2006;Adams 2007;Chen 2007;Doyle et al 2008;Hegarty and Hiscock 2008;Flagel and Wendel 2009;Jackson and Chen 2009;Soltis and Soltis 2009).…”

Homoeologous copy-specific expression patterns of MADS-box genes for floral formation in allopolyploid wheat

“…The concept of 'genomic expression dominance' has been developed in allotetraploid cotton; in this species, homoeolog expression is biased in favor of the D genome over the A genome (Rapp et al, 2009;Flagel and Wendel, 2010). Genomic expression dominance has also been reported in synthetic hexaploid wheat which shows a biased contribution from the AB genome of the tetraploid parent (Akhunova et al, 2010). The AB genome homoeologs involved in protein biosynthesis and photosynthesis were up-regulated, suggesting that they may contribute to restoration of growth vigor in allopolyploid wheat.…”

“…This study indicated that expression patterns could be classified into two major groups: genes that are almost equally expressed from all three genomes; and genes that are expressed differentially in the three genomes, and which vary between tissues. Subsequently, the differential expression of homoeologs was measured using cDNASSCPs and microarray analysis (Pumphrey et al, 2009), while more recently, genome-wide gene expression changes during allopolyploidization were investigated using Affymetrix GeneChip Wheat Genome Arrays (Changué et al, 2010;Akhunova et al, 2010;Qi et al, 2012) and an Agilent 38K oligo-DNA microarray (Jung et al, 2014). These studies indicate that up to 20% of genes show non-additive expression with homoeolog-specific upor down-regulation.…”

Genomic Imprinting Was Evolutionarily Conserved during Wheat Polyploidization

“…It is thought that homoeologs make unequal contributions to total gene expression levels in polyploid wheat and that gene expression is regulated in a complex manner during grain development, possibly due to crosstalk between genomes during polyploidization (Akhunova et al, 2010;Chagué et al, 2010;Leach et al, 2014;Liu et al, 2015;Han et al, 2016). In this study, a major proportion of homoeologous gene pairs (65.8%) indeed exhibited divergent expression patterns in terms of genomic imprinting in polyploid wheat.…”