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Homoeolog expression bias and expression level dominance in allopolyploid cotton.

ABSTRACT: Allopolyploidy is an evolutionary and mechanistically intriguing process, in that it entails the reconciliation of two or more sets of diverged genomes and regulatory interactions. In this study, we explored gene expression patterns in interspecific hybrid F(1), and synthetic and natural allopolyploid cotton using RNA-Seq reads from leaf transcriptomes. We determined how the extent and direction of expression level dominance (total level of expression for both homoeologs) and homoeolog expression bias (relative contribution of homoeologs to the transcriptome) changed from hybridization through evolution at the polyploid level and following cotton domestication. Genome-wide expression level dominance was biased toward the A-genome in the diploid hybrid and natural allopolyploids, whereas the direction was reversed in the synthetic allopolyploid. This biased expression level dominance was mainly caused by up- or downregulation of the homoeolog from the 'non-dominant' parent. Extensive alterations in homoeolog expression bias and expression level dominance accompany the initial merger of two diverged diploid genomes, suggesting a combination of regulatory (cis or trans) and epigenetic interactions that may arise and propagate through the transcriptome network. The extent of homoeolog expression bias and expression level dominance increases over time, from genome merger through evolution at the polyploid level. Higher rates of transgressive and novel gene expression patterns as well as homoeolog silencing were observed in natural allopolyploids than in F(1) hybrid and synthetic allopolyploid cottons. These observations suggest that natural selection reconciles the regulatory mismatches caused by initial genomic merger, while new gene expression conditions are generated for evaluation by selection.

SUBMITTER: Yoo MJ

PROVIDER: S-EPMC3554454 | biostudies-literature | 2013 Feb

REPOSITORIES: biostudies-literature

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Homoeolog expression bias and expression level dominance in allopolyploid cotton.

Yoo M-J MJ Szadkowski E E Wendel J F JF

Heredity 20121121 2

Allopolyploidy is an evolutionary and mechanistically intriguing process, in that it entails the reconciliation of two or more sets of diverged genomes and regulatory interactions. In this study, we explored gene expression patterns in interspecific hybrid F(1), and synthetic and natural allopolyploid cotton using RNA-Seq reads from leaf transcriptomes. We determined how the extent and direction of expression level dominance (total level of expression for both homoeologs) and homoeolog expressio ...[more]

PMID: 23169565

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Project description:BACKGROUND:Allopolyploids require rapid genetic and epigenetic modifications to reconcile two or more sets of divergent genomes. To better understand the fate of duplicate genes following genomic mergers and doubling during allopolyploid formation, in this study, we explored the global gene expression patterns in resynthesized allotetraploid Brassica napus (AACC) and its diploid parents B. rapa (AA) and B. oleracea (CC) using RNA sequencing of leaf transcriptomes. RESULTS:We found that allopolyploid B. napus formation was accompanied by extensive changes (approximately one-third of the expressed genes) in the parental gene expression patterns ('transcriptome shock'). Interestingly, the majority (85%) of differentially expressed genes (DEGs) were downregulated in the allotetraploid. Moreover, the homoeolog expression bias (relative contribution of homoeologs to the transcriptome) and expression level dominance (total expression level of both homoeologs) were thoroughly investigated by monitoring the expression of 23,766 B. oleracea-B. rapa orthologous gene pairs. Approximately 36.5% of the expressed gene pairs displayed expression bias with a slight preference toward the A-genome. In addition, 39.6, 4.9 and 9.0% of the expressed gene pairs exhibited expression level dominance (ELD), additivity expression and transgressive expression, respectively. The genome-wide ELD was also biased toward the A-genome in the resynthesized B. napus. To explain the ELD phenomenon, we compared the individual homoeolog expression levels relative to those of the diploid parents and found that ELD in the direction of the higher-expression parent can be explained by the downregulation of homoeologs from the dominant parent or upregulation of homoeologs from the nondominant parent; however, ELD in the direction of the lower-expression parent can be explained only by the downregulation of the nondominant parent or both homoeologs. Furthermore, Gene Ontology (GO) enrichment analysis suggested that the alteration in the gene expression patterns could be a prominent cause of the phenotypic variation between the newly formed B. napus and its parental species. CONCLUSIONS:Collectively, our data provide insight into the rapid repatterning of gene expression at the beginning of Brassica allopolyploidization and enhance our knowledge of allopolyploidization processes.

Project description:BACKGROUND:Allopolyploidy is a genomic structure wherein two or more sets of chromosomes derived from divergent parental species coexist within an organism. It is a prevalent genomic configuration in plants, as an important source of genetic variation, and also frequently confers environmental adaptability and increased crop productivity. We previously reported the oleaginous marine diatom Fistulifera solaris JPCC DA0580 to be a promising host for biofuel production and that its genome is allopolyploid, which had never previously been reported in eukaryotic microalgae. However, the study of allopolyploidy in F. solaris was hindered by the difficulty in classifying the homoeologous genes based on their progenitor origins, owing to the shortage of diatom genomic references. RESULTS:In this study, the allopolyploid genome of F. solaris was tentatively classified into two pseudo-parental subgenomes using sequence analysis based on GC content and codon frequency in each homoeologous gene pair. This approach clearly separated the genome into two distinct fractions, subgenome Fso_h and Fso_l, which also showed the potency of codon usage analysis to differentiate the allopolyploid subgenome. Subsequent homoeolog expression bias analysis revealed that, although both subgenomes appear to contribute to global transcription, there were subgenomic preferences in approximately 61% of homoeologous gene pairs, and the majority of these genes showed continuous bias towards a specific subgenome during lipid accumulation. Additional promoter analysis indicated the possibility of promoter motifs involved in biased transcription of homoeologous genes. Among these subgenomic preferences, genes involved in lipid metabolic pathways showed interesting patterns in that biosynthetic and degradative pathways showed opposite subgenomic preferences, suggesting the possibility that the oleaginous characteristics of F. solaris derived from one of its progenitors. CONCLUSIONS:We report the detailed genomic structure and expression patterns in the allopolyploid eukaryotic microalga F. solaris. The allele-specific patterns reported may contribute to the oleaginous characteristics of F. solaris and also suggest the robust oleaginous characteristics of one of its progenitors. Our data reveal novel aspects of allopolyploidy in a diatom that is not only important for evolutionary studies but may also be advantageous for biofuel production in microalgae.

Project description:BACKGROUND: Interaction 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. RESULTS: Affymetrix 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. CONCLUSIONS: Here, 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.

Project description:BACKGROUND:Allopolyploidy is widespread in angiosperms, and they can coordinate two or more different genomes through genetic and epigenetic modifications to exhibit stronger vigor and adaptability. To explore the changes in homologous gene expression patterns in the natural allotetraploid Brassica napus (AnAnCnCn) relative to its two diploid progenitors, B. rapa (ArAr) and B. oleracea (CoCo), after approximately 7500?years of domestication, the global gene pair expression patterns in four major tissues (stems, leaves, flowers and siliques) of these three species were analyzed using an RNA sequencing approach. RESULTS:The results showed that the 'transcriptomic shock' phenomenon was alleviated in natural B. napus after approximately 7500?years of natural domestication, and most differentially expressed genes (DEGs) in B. napus were downregulated relative to those in its two diploid progenitors. The KEGG analysis indicated that three pathways related to photosynthesis were enriched in both comparison groups (AnAnCnCn vs ArAr and AnAnCnCn vs CoCo), and these pathways were all downregulated in four tissues of B. napus. In addition, homoeolog expression bias and expression level dominance (ELD) in B. napus were thoroughly studied through analysis of expression levels of 27,609 B. rapa-B. oleracea orthologous gene pairs. The overwhelming majority of gene pairs (an average of 86.7%) in B. napus maintained their expression pattern in two diploid progenitors, and approximately 78.1% of the gene pairs showed expression bias with a preference toward the A subgenome. Overall, an average of 48, 29.7 and 22.3% homologous gene pairs exhibited additive expression, ELD and transgressive expression in B. napus, respectively. The ELD bias varies from tissue to tissue; specifically, more gene pairs in stems and siliques showed ELD-A, whereas the opposite was observed in leaves and flowers. More transgressive upregulation, rather than downregulation, was observed in gene pairs of B. napus. CONCLUSIONS:In general, these results may provide a comprehensive understanding of the changes in homologous gene expression patterns in natural B. napus after approximately 7500?years of evolution and domestication and may enhance our understanding of allopolyploidy.

Project description:Allopolyploidization is accompanied by changes in gene expression that are thought to contribute to phenotypic diversification. Here we describe global changes in the single-celled cotton fiber proteome of two natural allopolyploid species (Gossypium hirsutum and G. barbadense) and living models of their diploid parents using two different proteomic approaches. In total, 1323 two-dimensional gel electrophoresis spots and 1652 identified proteins by isobaric tags for relative and absolute quantitation were quantitatively profiled during fiber elongation. Between allopolyploids and their diploid A- and D-genome progenitors, amounts of differential expression ranged from 4.4 to 12.8%. Over 80% of the allopolyploid proteome was additively expressed with respect to progenitor diploids. Interestingly, the fiber proteome of G. hirsutum resembles the parental A-genome more closely, where long, spinable fiber first evolved, than does the fiber proteome of G. barbadense. More protein expression patterns were A-dominant than D-dominant in G. hirsutum, but in G. barbadense, the direction of expression-level dominance switched from the D-genome to the A-genome during fiber development. Comparison of developmental changes between the two allopolyploid species revealed a high level of proteomic differentiation despite their shared ancestry, relatively recent evolutionary divergence, and similar gross morphology. These results suggest that the two allopolyploid species have achieved superficially similar modern fiber phenotypes through different evolutionary routes at the proteome level. We also detected homeolog-specific expression for 1001 proteins and present a novel approach to infer the relationship between homeolog-specific and duplicate expression patterns. Our study provides a proteomic perspective on understanding evolutionary consequences of allopolyploidization, showing how protein expression has been altered by polyploidization and subsequently has diversified among species.

Project description:Background:Allopolyploid plants often show wider environmental tolerances than their ancestors; this is expected to be due to the merger of multiple distinct genomes with a fixed heterozygosity. The complex homoeologous gene expression could have been evolutionarily advantageous for the adaptation of allopolyploid plants. Despite multiple previous studies reporting homoeolog-specific gene expression in allopolyploid species, there are no clear examples of homoeolog-specific function in acclimation to a long-term stress condition. Results:We found that the allopolyploid grass Brachypodium hybridum and its ancestor Brachypodium stacei show long-term heat stress tolerance, unlike its other ancestor, Brachypodium distachyon. To understand the physiological traits of B. hybridum, we compared the transcriptome of the 3 Brachypodium species grown under normal and heat stress conditions. We found that the expression patterns of approximately 26% and approximately 38% of the homoeolog groups in B. hybridum changed toward nonadditive expression and nonancestral expression, respectively, under normal condition. Moreover, we found that B. distachyon showed similar expression patterns between normal and heat stress conditions, whereas B. hybridum and B. stacei significantly altered their transcriptome in response to heat after 3 days of stress exposure, and homoeologs that were inherited from B. stacei may have contributed to the transcriptional stress response to heat in B. hybridum. After 15 days of heat exposure, B. hybridum and B. stacei maintained transcriptional states similar to those under normal conditions. These results suggest that an earlier response to heat that was specific to homoeologs originating from B. stacei contributed to cellular homeostasis under long-term heat stress in B. hybridum. Conclusions:Our results provide insights into different regulatory events of the homoeo-transcriptome that are associated with stress acclimation in allopolyploid plants.

Dataset Information

Homoeolog expression bias and expression level dominance in allopolyploid cotton.

Publications

Homoeolog expression bias and expression level dominance in allopolyploid cotton.

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