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Trajectories of Homoeolog-Specific Expression in Allotetraploid Tragopogon castellanus Populations of Independent Origins.

ABSTRACT: Polyploidization can have a significant ecological and evolutionary impact by providing substantially more genetic material that may result in novel phenotypes upon which selection may act. While the effects of polyploidization are broadly reviewed across the plant tree of life, the reproducibility of these effects within naturally occurring, independently formed polyploids is poorly characterized. The flowering plant genus Tragopogon (Asteraceae) offers a rare glimpse into the intricacies of repeated allopolyploid formation with both nascent (< 90 years old) and more ancient (mesopolyploids) formations. Neo- and mesopolyploids in Tragopogon have formed repeatedly and have extant diploid progenitors that facilitate the comparison of genome evolution after polyploidization across a broad span of evolutionary time. Here, we examine four independently formed lineages of the mesopolyploid Tragopogon castellanus for homoeolog expression changes and fractionation after polyploidization. We show that expression changes are remarkably similar among these independently formed polyploid populations with large convergence among expressed loci, moderate convergence among loci lost, and stochastic silencing. We further compare and contrast these results for T. castellanus with two nascent Tragopogon allopolyploids. While homoeolog expression bias was balanced in both nascent polyploids and T. castellanus, the degree of additive expression was significantly different, with the mesopolyploid populations demonstrating more non-additive expression. We suggest that gene dosage and expression noise minimization may play a prominent role in regulating gene expression patterns immediately after allopolyploidization as well as deeper into time, and these patterns are conserved across independent polyploid lineages.

SUBMITTER: Boatwright JL

PROVIDER: S-EPMC8261302 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundAlthough polyploidy has long been recognized as a major force in the evolution of plants, most of what we know about the genetic consequences of polyploidy comes from the study of crops and model systems. Furthermore, although many polyploid species have formed repeatedly, patterns of genome evolution and gene expression are largely unknown for natural polyploid populations of independent origin. We therefore examined patterns of loss and expression in duplicate gene pairs (homeologs) in multiple individuals from seven natural populations of independent origin of Tragopogon mirus (Asteraceae), an allopolyploid that formed repeatedly within the last 80 years from the diploids T. dubius and T. porrifolius.ResultsUsing cDNA-AFLPs, we found differential band patterns that could be attributable to gene silencing, novel expression, and/or maternal/paternal effects between T. mirus and its diploid parents. Subsequent cleaved amplified polymorphic sequence (CAPS) analyses of genomic DNA and cDNA revealed that 20 of the 30 genes identified through cDNA-AFLP analysis showed additivity, whereas nine of the 30 exhibited the loss of one parental homeolog in at least one individual. Homeolog loss (versus loss of a restriction site) was confirmed via sequencing. The remaining gene (ADENINE-DNA GLYCOSYLASE) showed ambiguous patterns in T. mirus because of polymorphism in the diploid parent T. dubius. Most (63.6%) of the homeolog loss events were of the T. dubius parental copy. Two genes, NUCLEAR RIBOSOMAL DNA and GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE, showed differential expression of the parental homeologs, with the T. dubius copy silenced in some individuals of T. mirus.ConclusionsGenomic and cDNA CAPS analyses indicated that plants representing multiple populations of this young natural allopolyploid have experienced frequent and preferential elimination of homeologous loci. Comparable analyses of synthetic F1 hybrids showed only additivity. These results suggest that loss of homeologs and changes in gene expression are not the immediate result of hybridization, but are processes that occur following polyploidization, occurring during the early (<40) generations of the young polyploid. Both T. mirus and a second recently formed allopolyploid, T. miscellus, exhibit more homeolog losses than gene silencing events. Furthermore, both allotetraploids undergo biased loss of homeologs contributed by their shared diploid parent, T. dubius. Further studies are required to assess whether the results for the 30 genes so far examined are representative of the entire genome.

Project description:BackgroundAllopolyploidy 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.ResultsThe 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.ConclusionsIn 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: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.

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Trajectories of Homoeolog-Specific Expression in Allotetraploid Tragopogon castellanus Populations of Independent Origins.

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