Dataset Information

On the road to diploidization? Homoeolog loss in independently formed populations of the allopolyploid Tragopogon miscellus (Asteraceae).

ABSTRACT: BACKGROUND: Polyploidy (whole-genome duplication) is an important speciation mechanism, particularly in plants. Gene loss, silencing, and the formation of novel gene complexes are some of the consequences that the new polyploid genome may experience. Despite the recurrent nature of polyploidy, little is known about the genomic outcome of independent polyploidization events. Here, we analyze the fate of genes duplicated by polyploidy (homoeologs) in multiple individuals from ten natural populations of Tragopogon miscellus (Asteraceae), all of which formed independently from T. dubius and T. pratensis less than 80 years ago. RESULTS: Of the 13 loci analyzed in 84 T. miscellus individuals, 11 showed loss of at least one parental homoeolog in the young allopolyploids. Two loci were retained in duplicate for all polyploid individuals included in this study. Nearly half (48%) of the individuals examined lost a homoeolog of at least one locus, with several individuals showing loss at more than one locus. Patterns of loss were stochastic among individuals from the independently formed populations, except that the T. dubius copy was lost twice as often as T. pratensis. CONCLUSION: This study represents the most extensive survey of the fate of genes duplicated by allopolyploidy in individuals from natural populations. Our results indicate that the road to genome downsizing and ultimate genetic diploidization may occur quickly through homoeolog loss, but with some genes consistently maintained as duplicates. Other genes consistently show evidence of homoeolog loss, suggesting repetitive aspects to polyploid genome evolution.

SUBMITTER: Tate JA

PROVIDER: S-EPMC2708164 | biostudies-literature | 2009

REPOSITORIES: biostudies-literature

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On the road to diploidization? Homoeolog loss in independently formed populations of the allopolyploid Tragopogon miscellus (Asteraceae).

Tate Jennifer A JA Joshi Prashant P Soltis Kerry A KA Soltis Pamela S PS Soltis Douglas E DE

BMC plant biology 20090627

<h4>Background</h4>Polyploidy (whole-genome duplication) is an important speciation mechanism, particularly in plants. Gene loss, silencing, and the formation of novel gene complexes are some of the consequences that the new polyploid genome may experience. Despite the recurrent nature of polyploidy, little is known about the genomic outcome of independent polyploidization events. Here, we analyze the fate of genes duplicated by polyploidy (homoeologs) in multiple individuals from ten natural po ...[more]

PMID: 19558696

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Project description:Polyploidy is an important evolutionary mechanism and is prevalent among land plants. Most polyploid species examined have multiple origins, which provide genetic diversity and may enhance the success of polyploids. In some polyploids, recurrent origins can result from reciprocal crosses between the same diploid progenitors. Although great progress has been made in understanding the genetic consequences of polyploidy, the genetic implications of reciprocal polyploidization remain poorly understood, especially in natural polyploids. Tragopogon (Asteraceae) has become an evolutionary model system for studies of recent and recurrent polyploidy. Allotetraploid T. miscellus has formed reciprocally in nature with resultant distinctive floral and inflorescence morphologies (i.e., short- vs. long-liguled forms). In this study, we performed comparative inflorescence transcriptome analyses of reciprocally formed T. miscellus and its diploid parents, T. dubius and T. pratensis. In both forms of T. miscellus, homeolog expression of ?70% of the loci showed vertical transmission of the parental expression patterns (i.e., parental legacy), and ?20% of the loci showed biased homeolog expression, which was unbalanced toward T. pratensis. However, 17.9% of orthologous pairs showed different homeolog expression patterns between the two forms of T. miscellus. No clear effect of cytonuclear interaction on biased expression of the maternal homeolog was found. In terms of the total expression level of the homeologs studied, 22.6% and 16.2% of the loci displayed non-additive expression in short- and long-liguled T. miscellus, respectively. Unbalanced expression level dominance toward T. pratensis was observed in both forms of T. miscellus. Significantly, genes annotated as being involved in pectin catabolic processes were highly expressed in long-liguled T. miscellus relative to the short-liguled form, and the majority of these differentially expressed genes were transgressively down-regulated in short-liguled T. miscellus. Given the known role of these genes in cell expansion, they may play a role in the differing floral and inflorescence morphologies of the two forms. In summary, the overall inflorescence transcriptome profiles are highly similar between reciprocal origins of T. miscellus. However, the dynamic homeolog-specific expression and non-additive expression patterns observed in T. miscellus emphasize the importance of reciprocal origins in promoting the genetic diversity of polyploids.

Project description:BackgroundTragopogon mirus and T. miscellus are allotetraploids (2n = 24) that formed repeatedly during the past 80 years in eastern Washington and adjacent Idaho (USA) following the introduction of the diploids T. dubius, T. porrifolius, and T. pratensis (2n = 12) from Europe. In most natural populations of T. mirus and T. miscellus, there are far fewer 35S rRNA genes (rDNA) of T. dubius than there are of the other diploid parent (T. porrifolius or T. pratensis). We studied the inheritance of parental rDNA loci in allotetraploids resynthesized from diploid accessions. We investigate the dynamics and directionality of these rDNA losses, as well as the contribution of gene copy number variation in the parental diploids to rDNA variation in the derived tetraploids.ResultsUsing Southern blot hybridization and fluorescent in situ hybridization (FISH), we analyzed copy numbers and distribution of these highly reiterated genes in seven lines of synthetic T. mirus (110 individuals) and four lines of synthetic T. miscellus (71 individuals). Variation among diploid parents accounted for most of the observed gene imbalances detected in F1 hybrids but cannot explain frequent deviations from repeat additivity seen in the allotetraploid lines. Polyploid lineages involving the same diploid parents differed in rDNA genotype, indicating that conditions immediately following genome doubling are crucial for rDNA changes. About 19% of the resynthesized allotetraploid individuals had equal rDNA contributions from the diploid parents, 74% were skewed towards either T. porrifolius or T. pratensis-type units, and only 7% had more rDNA copies of T. dubius-origin compared to the other two parents. Similar genotype frequencies were observed among natural populations. Despite directional reduction of units, the additivity of 35S rDNA locus number is maintained in 82% of the synthetic lines and in all natural allotetraploids.ConclusionsUniparental reductions of homeologous rRNA gene copies occurred in both synthetic and natural populations of Tragopogon allopolyploids. The extent of these rDNA changes was generally higher in natural populations than in the synthetic lines. We hypothesize that locus-specific and chromosomal changes in early generations of allopolyploids may influence patterns of rDNA evolution in later generations.

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: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.

Dataset Information

On the road to diploidization? Homoeolog loss in independently formed populations of the allopolyploid Tragopogon miscellus (Asteraceae).

Publications

On the road to diploidization? Homoeolog loss in independently formed populations of the allopolyploid Tragopogon miscellus (Asteraceae).

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