Distinct expression and methylation patterns for genes with different fates following a single whole-genome duplication in flowering plants

For most sequenced flowering plants, multiple whole-genome duplications (WGDs) are found. Duplicated genes following WGD often have different fates that can quickly disappear again, be retained for long(er) periods, or subsequently undergo small-scale duplications. However, how different expression, epigenetic regulation, and functional constraints are associated with these different gene fates following a WGD still requires further investigation due to successive WGDs in angiosperms complicating the gene trajectories. In this study, we investigate lotus (Nelumbo nucifera), an angiosperm with a single WGD during the K–pg boundary. Based on improved intraspecific-synteny identification by a chromosome-level assembly, transcriptome, and bisulfite sequencing, we explore not only the fundamental distinctions in genomic features, expression, and methylation patterns of genes with different fates after a WGD but also the factors that shape post-WGD expression divergence and expression bias between duplicates. We found that after a WGD genes that returned to single copies show the highest levels and breadth of expression, gene body methylation, and intron numbers, whereas the long-retained duplicates exhibit the highest degrees of protein–protein interactions and protein lengths and the lowest methylation in gene flanking regions. For those long-retained duplicate pairs, the degree of expression divergence correlates with their sequence divergence, degree in protein–protein interactions, and expression level, whereas their biases in expression level reflecting subgenome dominance are associated with the bias of subgenome fractionation. Overall, our study on the paleopolyploid nature of lotus highlights the impact of different functional constraints on gene fate and duplicate divergence following a single WGD in plant

Origin and evolution of the octoploid strawberry genome.

Cultivated strawberry emerged from the hybridization of two wild octoploid species, both descendants from the merger of four diploid progenitor species into a single nucleus more than 1 million years ago. Here we report a near-complete chromosome-scale assembly for cultivated octoploid strawberry (Fragaria × ananassa) and uncovered the origin and evolutionary processes that shaped this complex allopolyploid. We identified the extant relatives of each diploid progenitor species and provide support for the North American origin of octoploid strawberry. We examined the dynamics among the four subgenomes in octoploid strawberry and uncovered the presence of a single dominant subgenome with significantly greater gene content, gene expression abundance, and biased exchanges between homoeologous chromosomes, as compared with the other subgenomes. Pathway analysis showed that certain metabolomic and disease-resistance traits are largely controlled by the dominant subgenome. These findings and the reference genome should serve as a powerful platform for future evolutionary studies and enable molecular breeding in strawberry

Subgenome Dominance in an Interspecific Hybrid, Synthetic Allopolyploid, and a 140-Year-Old Naturally Established Neo-Allopolyploid Monkeyflower

Recent studies have shown that one of the parental subgenomes in ancient polyploids is generally more dominant, having retained more genes and being more highly expressed, a phenomenon termed subgenome dominance. The genomic features that determine how quickly and which subgenome dominates within a newly formed polyploid remain poorly understood. To investigate the rate of emergence of subgenome dominance, we examined gene expression, gene methylation, and transposable element (TE) methylation in a natural, \u3c140-year-old allopolyploid (Mimulus peregrinus), a resynthesized interspecies triploid hybrid (M. robertsii), a resynthesized allopolyploid (M. peregrinus), and progenitor species (M. guttatus and M. luteus). We show that subgenome expression dominance occurs instantly following the hybridization of divergent genomes and significantly increases over generations. Additionally, CHH methylation levels are reduced in regions near genes and within TEs in the first-generation hybrid, intermediate in the resynthesized allopolyploid, and are repatterned differently between the dominant and recessive subgenomes in the natural allopolyploid. Subgenome differences in levels of TE methylation mirror the increase in expression bias observed over the generations following hybridization. These findings provide important insights into genomic and epigenomic shock that occurs following hybridization and polyploid events and may also contribute to uncovering the mechanistic basis of heterosis and subgenome dominance

Does one subgenome become dominant in the formation and evolution of a polyploid?

Background Polyploids are common in flowering plants and they tend to have more expanded ranges of distributions than their diploid progenitors. Possible mechanisms underlying polyploid success have been intensively investigated. Previous studies showed that polyploidy generates novel changes and that subgenomes in allopolyploid species often differ in gene number, gene expression levels and levels of epigenetic alteration. It is widely believed that such differences are the results of conflicts among the subgenomes. These differences have been treated by some as subgenome dominance, and it is claimed that the magnitude of subgenome dominance increases in polyploid evolution. Scope In addition to changes which occurred during evolution, differences between subgenomes of a polyploid species may also be affected by differences between the diploid donors and changes which occurred during polyploidization. The variable genome components in many plant species are extensive, which would result in exaggerated differences between a subgenome and its progenitor when a single genotype or a small number of genotypes are used to represent a polyploid or its donors. When artificially resynthesized polyploids are used as surrogates for newly formed genotypes which have not been exposed to evolutionary selection, differences between diploid genotypes available today and those involved in the formation of the natural polyploid genotypes must also be considered. Conclusions Contrary to the now widely held views that subgenome biases in polyploids are the results of conflicts among the subgenomes and that one of the parental subgenomes generally retains more genes which are more highly expressed, available results show that subgenome biases mainly reflect legacy from the progenitors and that they can be detected before the completion of polyploidization events. Further, there is no convincing evidence that the magnitudes of subgenome biases have significantly changed during evolution for any of the allopolyploid species assessed

Utilization of variation to understand Camelina sativa genome evolution

Camelina sativa is an oilseed crop gaining interest for its oil content, protein content, and potential as a new oilseed for human consumption. The main disadvantages of this crop are its smaller seed size and lower total yield compared to other commercial oilseed crops; however, breeding efforts has been progressing to improve yield traits. A low level of genetic diversity and limited breeding efforts have been identified as impediments in C. sativa crop improvement. This study was designed to improve access to genetic diversity in C. sativa by developing genetic tools and identifying genetic mechanisms to accelerate C. sativa breeding. The objectives of this study were: to explore the genetic diversity in available Camelina germplasm using Genotyping-by-Sequencing (GBS), with a focus on close relatives of C. sativa and a collection from Ukraine and Russia; to develop segregating generations through intra- and interspecific hybridization; and to complete whole genome transcriptome analysis to observe gene expression patterns across subgenomes in hexaploid species of Camelina. Genetic markers in this study were developed using GBS, whereas whole transcriptome analysis was performed for subgenome dominance analysis. The genetic diversity study with 193 genotypes identified two subpopulations in C. sativa, where C. microcarpa was found to be a close relative of this species. Winter C. sativa species, such as C. sativa ssp. pilosa and C. alyssum, formed a separate clade and were closely-associated with C. microcarpa. Principal coordinate and phylogenetic analysis differentiated the genotypes based on species and subpopulations. Mapping of reads to the reference genome identified C. neglecta as a progenitor species for the first subgenome of C. sativa. Likewise, a tetraploid was identified that encompassed the first and second subgenomes, and a novel C. microcarpa species differing from C. sativa in terms of genome structure was also identified. Flow cytometry analysis and chromosome count validated the read mapping and confirmed that the novel C. microcarpa possessed 19 chromosomes (n, haploid number) with a different third subgenome not present in C. sativa. The inter- and intraspecific hybridizations enabled genetic linkage maps to be developed, where a common C. sativa genotype was hybridized with other related species. A mapping study identified four quantitative trait loci (QTL) associated with winter behaviour in C. sativa. The winter trait mapped to one locus on chromosome 8 (subgenome 1) in C. sativa ssp. pilosa, to two loci in C. alyssum on chromosomes 13 (subgenome 2) and 20 (subgenome 3), and to one locus on chromosome 13 (subgenome 2) in C. microcarpa. All of the QTL represented homologous segments in the C. sativa reference genome and were proximate to a major flowering gene, Flowering Locus C (FLC). Differential gene expression analysis between the parents at the early seedling stage suggested FLC could be a candidate gene responsible for vernalization responses in winter C. sativa populations. In addition, interspecific hybridization identified a homoeologous recombination (HeR) event between subgenome 1 of C. sativa with subgenome 3 of C. microcarpa (n = 19), and a number of anueploids were identified, as expected. The nature of HeR could create challenges for the success of conventional breeding activities in Camelina species, as recombination could occur between any subgenomes due to the undifferentiated nature of the subgenomes. However, variation in morphology, such as leaf characteristics, days to flowering and fertility suggested a huge potential for increasing genetic variability in C. sativa by use of distantly-related Camelina species. Subgenome dominance has evolutionary significance and can play an important role in improving phenotypic diversity. Subgenome dominance analysis suggested the third subgenome was dominant in the case of Camelina species with n = 20, whereas the second subgenome was dominant for Camelina species with n = 19 and was correlated with the age of divergence of the subgenomes from C. neglecta. Overall, the results provided insight into the subgenome structure and a first step towards identifying the mechanism of a stepwise whole genome duplication process in polyploid C. sativa, which would be instrumental in developing genetic tools for Camelina breeding activities

Subgenomic Stability of Progenitor Genomes During Repeated Allotetraploid Origins of the Same Grass Brachypodium hybridum

Both homeologous exchanges and homeologous expression bias are generally found in most allopolyploid species. Whether homeologous exchanges and homeologous expression bias differ between repeated allopolyploid speciation events from the same progenitor species remains unknown. Here, we detected a third independent and recent allotetraploid origin for the model grass Brachypodium hybridum. Our homeologous exchange with replacement analyses indicated the absence of significant homeologous exchanges in any of the three types of wild allotetraploids, supporting the integrity of their progenitor subgenomes and the immediate creation of the amphidiploids. Further homeologous expression bias tests did not uncover significant subgenomic dominance in different tissues and conditions of the allotetraploids. This suggests a balanced expression of homeologs under similar or dissimilar ecological conditions in their natural habitats. We observed that the density of transposons around genes was not associated with the initial establishment of subgenome dominance; rather, this feature is inherited from the progenitor genome. We found that drought response genes were highly induced in the two subgenomes, likely contributing to the local adaptation of this species to arid habitats in the third allotetraploid event. These findings provide evidence for the consistency of subgenomic stability of parental genomes across multiple allopolyploidization events that led to the same species at different periods. Our study emphasizes the importance of selecting closely related progenitor species genomes to accurately assess homeologous exchange with replacement in allopolyploids, thereby avoiding the detection of false homeologous exchanges when using less related progenitor species genomes

Biased Gene Fractionation and Dominant Gene Expression among the Subgenomes of Brassica rapa

Polyploidization, both ancient and recent, is frequent among plants. A “two-step theory" was proposed to explain the meso-triplication of the Brassica “A" genome: Brassica rapa. By accurately partitioning of this genome, we observed that genes in the less fractioned subgenome (LF) were dominantly expressed over the genes in more fractioned subgenomes (MFs: MF1 and MF2), while the genes in MF1 were slightly dominantly expressed over the genes in MF2. The results indicated that the dominantly expressed genes tended to be resistant against gene fractionation. By re-sequencing two B. rapa accessions: a vegetable turnip (VT117) and a Rapid Cycling line (L144), we found that genes in LF had less non-synonymous or frameshift mutations than genes in MFs; however mutation rates were not significantly different between MF1 and MF2. The differences in gene expression patterns and on-going gene death among the three subgenomes suggest that “two-step" genome triplication and differential subgenome methylation played important roles in the genome evolution of B. rapa

Gradual evolution of allopolyploidy in Arabidopsis suecica.

Most diploid organisms have polyploid ancestors. The evolutionary process of polyploidization is poorly understood but has frequently been conjectured to involve some form of 'genome shock', such as genome reorganization and subgenome expression dominance. Here we study polyploidization in Arabidopsis suecica, a post-glacial allopolyploid species formed via hybridization of Arabidopsis thaliana and Arabidopsis arenosa. We generated a chromosome-level genome assembly of A. suecica and complemented it with polymorphism and transcriptome data from all species. Despite a divergence around 6 million years ago (Ma) between the ancestral species and differences in their genome composition, we see no evidence of a genome shock: the A. suecica genome is colinear with the ancestral genomes; there is no subgenome dominance in expression; and transposon dynamics appear stable. However, we find changes suggesting gradual adaptation to polyploidy. In particular, the A. thaliana subgenome shows upregulation of meiosis-related genes, possibly to prevent aneuploidy and undesirable homeologous exchanges that are observed in synthetic A. suecica, and the A. arenosa subgenome shows upregulation of cyto-nuclear processes, possibly in response to the new cytoplasmic environment of A. suecica, with plastids maternally inherited from A. thaliana. These changes are not seen in synthetic hybrids, and thus are likely to represent subsequent evolution

Cytonuclear interactions remain stable during allopolyploid evolution despite repeated whole-genome duplications in Brassica

Several plastid macromolecular protein complexes are encoded by both nuclear and plastid genes. Therefore, cytonuclear interactions are held in place to prevent genomic conflicts that may lead to incompatibilities. Allopolyploidy resulting from hybridization and genome doubling of two divergent species can disrupt these fine-tuned interactions, as newly formed allopolyploid species confront biparental nuclear chromosomes with a uniparentally inherited plastid genome. To avoid any deleterious effects of unequal genome inheritance, preferential transcription of the plastid donor over the other donor has been hypothesized to occur in allopolyploids. We used Brassica as a model to study the effects of paleopolyploidy in diploid parental species, as well as the effects of recent and ancient allopolyploidy in Brassica napus, on genes implicated in plastid protein complexes. We first identified redundant nuclear copies involved in those complexes. Compared with cytosolic protein complexes and with genome-wide retention rates, genes involved in plastid protein complexes show a higher retention of genes in duplicated and triplicated copies. Those redundant copies are functional and are undergoing strong purifying selection. We then compared transcription patterns and sequences of those redundant gene copies between resynthesized allopolyploids and their diploid parents. The neopolyploids showed no biased subgenome expression or maternal homogenization via gene conversion, despite the presence of some non-synonymous substitutions between plastid genomes of parental progenitors. Instead, subgenome dominance was observed regardless of the maternal progenitor. Our results provide new insights on the evolution of plastid protein complexes that could be tested and generalized in other allopolyploid species

Chromosome-Level Genome Assembly of Chinese Sucker (Myxocyprinus asiaticus) Reveals Strongly Conserved Synteny Following a Catostomid-Specific Whole-Genome Duplication

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