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Allopolyploidization may initiate rapid evolution due to heritable karyotypic changes. The types and extents of these changes, the underlying causes, and their effects on phenotype remain to be fully understood. Here, we designed experimental populations suitable to address these issues using a synthetic allotetraploid wheat. We show that extensive variation in both chromosome number (NCV) and structure (SCV) accumulated in a selfed population of a synthetic allotetraploid wheat (genome S b S b DD). The combination of NCVs and SCVs generated massive organismal karyotypic heterogeneity. NCVs and SCVs were intrinsically correlated and highly variable across the seven sets of homoeologous chromosomes. Both NCVs and SCVs stemmed from meiotic pairing irregularity (presumably homoeologous pairing) but were also constrained by homoeologous chromosome compensation. We further show that homoeologous meiotic pairing was positively correlated with sequence synteny at the subtelomeric regions of both chromosome arms, but not with genic nucleotide similarity per se. Both NCVs and SCVs impacted phenotypic traits but only NCVs caused significant reduction in reproductive fitness. Our results implicate factors influencing meiotic homoeologous chromosome pairing and reveal the type and extent of karyotypic variation and its immediate phenotypic manifestation in synthetic allotetraploid wheat. This has relevance for our understanding of allopolyploid evolution., (© 2023 The Authors New Phytologist © 2023 New Phytologist Foundation.)

Allopolyploidization, which entails interspecific hybridization and whole genome duplication (WGD), is associated with emergent genetic and epigenetic instabilities that are thought to contribute to adaptation and evolution. One frequent genomic consequence of nascent allopolyploidization is homoeologous exchange (HE), which arises from compromised meiotic fidelity and generates genetically and phenotypically variable progenies. Here, we used a genetically tractable synthetic rice segmental allotetraploid system to interrogate genome-wide DNA methylation and gene expression responses and outcomes to the separate and combined effects of hybridization, WGD and HEs. Progenies of the tetraploid rice were genomically diverse due to genome-wide HEs that affected all chromosomes, yet they exhibited overall methylome stability. Nonetheless, regional variation of cytosine methylation states was widespread in the tetraploids. Transcriptome profiling revealed genome-wide alteration of gene expression, which at least in part associates with changes in DNA methylation. Intriguingly, changes of DNA methylation and gene expression could be decoupled from hybridity and sustained and amplified by HEs. Our results suggest that HEs, a prominent genetic consequence of nascent allopolyploidy, can exacerbate, diversify and perpetuate the effects of allopolyploidization on epigenetic and gene expression variation, and hence may contribute to allopolyploid evolution., (© 2019 The Authors. New Phytologist © 2019 New Phytologist Trust.)

Allopolyploidy is a prevalent process in plants, having important physiological, ecological and evolutionary consequences. Transcriptomic responses to genomic merger and doubling have been demonstrated in many allopolyploid systems, encompassing a diversity of phenomena including homoeolog expression bias, genome dominance, expression-level dominance and revamping of co-expression networks. Notwithstanding the foregoing, there remains a need to develop a conceptual framework that will stimulate a deeper understanding of these diverse phenomena and their mechanistic interrelationships. Here we introduce considerations relevant to this framework with a focus on cis-trans interactions among duplicated genes and alleles in hybrids and allopolyploids. By extending classic allele-specific expression analysis to the allopolyploid level, we distinguish the distinct effects of progenitor regulatory interactions from the novel intergenomic interactions that arise from genome merger and allopolyploidization. This perspective informs experiments designed to reveal the molecular genetic basis of gene regulatory control, and will facilitate the disentangling of genetic from epigenetic and higher-order effects that impact gene expression. Finally, we suggest that the extended cis-trans model may help conceptually unify several presently disparate hallmarks of allopolyploid evolution, including genome-wide expression dominance and biased fractionation, and lead to a new level of understanding of phenotypic novelty accompanying polyploidy., (© 2018 The Authors. New Phytologist © 2018 New Phytologist Trust.)

Cotton cultivars have evolved to produce extensive, long, seed-born fibers important for the textile industry, but we know little about the molecular mechanism underlying spinnable fiber formation. Here, we report how PACLOBUTRAZOL RESISTANCE 1 (PRE1) in cotton, which encodes a basic helix-loop-helix (bHLH) transcription factor, is a target gene of spinnable fiber evolution. Differential expression of homoeologous genes in polyploids is thought to be important to plant adaptation and novel phenotypes. PRE1 expression is specific to cotton fiber cells, upregulated during their rapid elongation stage and A-homoeologous biased in allotetraploid cultivars. Transgenic studies demonstrated that PRE1 is a positive regulator of fiber elongation. We determined that the natural variation of the canonical TATA-box, a regulatory element commonly found in many eukaryotic core promoters, is necessary for subgenome-biased PRE1 expression, representing a mechanism underlying the selection of homoeologous genes. Thus, variations in the promoter of the cell elongation regulator gene PRE1 have contributed to spinnable fiber formation in cotton. Overexpression of GhPRE1 in transgenic cotton yields longer fibers with improved quality parameters, indicating that this bHLH gene is useful for improving cotton fiber quality., (© 2018 The Authors. New Phytologist © 2018 New Phytologist Trust.)

Pima cotton (Gossypium barbadense) is widely cultivated because of its long, strong seed trichomes ('fibers') used for premium textiles. These agronomically advanced fibers were derived following domestication and thousands of years of human-mediated crop improvement. To gain an insight into fiber development and evolution, we conducted comparative proteomic and transcriptomic profiling of developing fiber from an elite cultivar and a wild accession. Analyses using isobaric tag for relative and absolute quantification (iTRAQ) LC-MS/MS technology identified 1317 proteins in fiber. Of these, 205 were differentially expressed across developmental stages, and 190 showed differential expression between wild and cultivated forms, 14.4% of the proteome sampled. Human selection may have shifted the timing of developmental modules, such that some occur earlier in domesticated than in wild cotton. A novel approach was used to detect possible biased expression of homoeologous copies of proteins. Results indicate a significant partitioning of duplicate gene expression at the protein level, but an approximately equal degree of bias for each of the two constituent genomes of allopolyploid cotton. Our results demonstrate the power of complementary transcriptomic and proteomic approaches for the study of the domestication process. They also provide a rich database for mining for functional analyses of cotton improvement or evolution., (© 2013 The Authors. New Phytologist © 2013 New Phytologist Trust.)

Polyploid formation and processes that create partial genomic duplication generate redundant genomic information, whose fate is of particular interest to evolutionary biologists. Different processes can lead to diversification among duplicate genes, which may be counterbalanced by mechanisms that retard divergence, including gene conversion via nonreciprocal homoeologous exchange. Here, we used genomic resources in diploid and allopolyploid cotton (Gossypium) to detect homoeologous single nucleotide polymorphisms provided by expressed sequence tags from G. arboreum (A genome), G. raimondii (D genome) and G. hirsutum (AD genome), allowing us to identify homoeo-single nucleotide polymorphism patterns indicative of potential homoeologous exchanges. We estimated the proportion of contigs in G. hirsutum that have experienced nonreciprocal homoeologous exchanges since the origin of polyploid cotton 1-2 million years ago (Mya) to be between 1.8% and 1.9%. To address the question of when the intergenomic exchange occurred, we assayed six of the genes affected by homoeo-recombination in all five Gossypium allopolyploids using a phylogenetic approach. This analysis revealed that nonreciprocal homoeologous exchanges have occurred throughout polyploid divergence and speciation, as opposed to saltationally with polyploid formation. In addition, some genomic regions show multiple patterns of homoeologous recombination among species.

Here, we describe the evolution of gene expression among a diversified cohort of five allopolyploid species in the cotton genus (Gossypium). Using this phylogenetic framework and comparisons with expression changes accompanying F(1) hybridization, we provide a temporal perspective on expression diversification following a shared genome duplication. Global patterns of gene expression were studied by the hybridization of petal RNAs to a custom microarray. This platform measures total expression for c. 42 000 duplicated genes, and genome-specific expression for c. 1400 homoeologs (genes duplicated by polyploidy). We report homoeolog expression bias favoring the allopolyploid D genome over the A genome in all species (among five polyploid species, D biases ranging from c. 54 to 60%), in addition to conservation of biases among genes. Furthermore, we find surprising levels of transgressive up- and down-regulation in the allopolyploids, a diminution of the level of bias in genomic expression dominance but not in its magnitude, and high levels of rate variation among allotetraploid species. We illustrate how phylogenetic and temporal components of expression evolution may be partitioned and revealed following allopolyploidy. Overall patterns of expression evolution are similar among the Gossypium allotetraploids, notwithstanding a high level of interspecific rate variation, but differ strikingly from the direction of genomic expression dominance patterns in the synthetic F(1) hybrid.

Duplication is a prominent feature of plant genomic architecture. This has led many researchers to speculate that gene duplication may have played an important role in the evolution of phenotypic novelty within plants. Until recently, however, it was difficult to make this connection. We are now beginning to understand how duplication has contributed to adaptive evolution in plants. In this review we introduce the sources of gene duplication and predictions of the various fates of duplicates. We also highlight several recent and pertinent examples from the literature. These examples demonstrate the importance of the functional characteristics of genes and the source of duplication in influencing evolutionary outcome.

A fundamental precept of evolutionary biology is that natural selection acts on phenotypes determined by DNA sequence variation within natural populations. Recent advances in our understanding of gene regulation, however, have elucidated a spectrum of epigenetic molecular phenomena capable of altering the temporal, spatial, and abundance patterns of gene expression. These modifications may have morphological, physiological, and ecological consequences, and are heritable across generations, suggesting they are important in evolution. A corollary is that genetic variation per se is not always a prerequisite to evolutionary change. Here, we provide an introduction to epigenetic mechanisms in plants, and highlight some of the empirical studies illustrative of the possible connections between evolution and epigenetically mediated alterations in gene expression and morphology.