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Synthetic allopolyploidy unveils hybridization-driven transcriptional reprogramming underlying thermal adaptation in Cucumis.

Both heterosis (hybrid vigor) resulting from hybridization and genetic plasticity conferred by whole-genome duplication (WGD) are recognized as drivers of evolutionary success and ecological adaptation in plants. Allopolyploids, which combine both hybridization and WGD, are widespread in both natural and agricultural settings and often exhibit superior performance. However, the relative contributions of these two elements to the success of allopolyploids remain poorly understood. Here, we employed an experimentally reconstructed allotetraploid Cucumis species (C. × hytivus, 2n = 4x = 38) and its diploid interspecific hybrid progenitor (allodiploid, 2n = 2x = 19) to decouple and investigate the distinct and combined contributions of hybridization and whole-genome doubling to immediate genetic and phenotypic consequences of allopolyploid formation under environmental stress. Both C. × hytivus and the allodiploid exhibited superior heat tolerance compared with the parental species with significantly higher semi-lethal temperature and enhanced physiological acclimation capacity. While the allodiploid and allotetraploid retain transcriptomic features where differences persist (e.g., WGCNA modules), comparative analysis of the 15,680 homoeologous gene pairs in the allodiploid and allotetraploid under heat stress (45°C) versus control conditions (28°C) revealed conserved heat-responsive transcriptional plasticity, suggesting that enhanced thermotolerance in C. × hytivus is presented as consequences arising dominantly after interspecific hybridization. This study provides mechanistic insights into allopolyploid adaptation through experimental reconstruction of allopolyploid genomes, demonstrating that hybridization initiates key transcriptional and physiological advantages under stress, subsequent WGD stabilizes these adaptations and contributes to the full phenotypic realization. This work decouples the roles of interspecific hybridization and WGD and proposes a synthetic biology approach for developing climate-resilient crops.

Hybridization, Genetic

Unraveling evolutionary pathways: allopolyploidization and introgression in polyploid Prunus (Rosaceae).

Allopolyploidization, resulting from hybridization and subsequent whole-genome duplication (WGD), is a fundamental mechanism driving evolutionary diversification across various lineages within the Tree of Life. The polyploid Prunus (Rosaceae), significant for its economic and agricultural value, provides an ideal model for investigating the evolutionary dynamics associated with allopolyploidy. In this study, we utilized deep genome skimming (DGS) data to demonstrate a comprehensive analytical framework for elucidating the underlying allopolyploidy that includes a newly adapted tool (DGS-Tree2GD) tailored explicitly for accurately detecting WGD events. Additionally, we introduced two methods to evaluate the contribution of incomplete lineage sorting (ILS) to lineage diversification. Phylogenomic discordance analyses revealed that allopolyploidization, rather than ILS, played a dominant role in the origin and dynamics of polyploid Prunus. Moreover, we inferred that the uplift of the Himalayas from the Middle to Late Miocene was a key driver in the rapid diversification of the Maddenia clade, an endemic group in East Asia. This geological event facilitated extensive hybridization and allopolyploidization, particularly the introgression between the Himalayas-Hengduan and Central-Eastern China clades. This case study demonstrates the robustness and efficacy of our analytical approach in precisely identifying WGD events and elucidating the evolutionary mechanisms underlying allopolyploidization in polyploid Prunus.

Polyploidy

Doubled Genomes, Divergent Fates: Genomic Insights Into Diversification in an Allotetraploid Cavefish.

Cave environments impose unique challenges that drive remarkable genetic and phenotypic changes in cave-dwelling organisms. In this study, we investigated the genomic basis of adaptation in the small eye golden-line fish (Sinocyclocheilus microphthalmus), an allotetraploid cavefish endemic to Guangxi, China. Using whole-genome resequencing data from 47 individuals across six cave locations, we examined how neutral and selective forces influence diversification. Our analyses uncovered significant population structure indicative of allopatric divergence, along with evidence of locus-specific selection contributing to genomic differentiation. We identified seven single outlier clusters (SOCs), each tied to the divergence of specific populations, underscoring the role of local processes in driving diversity. Genes associated with vision showed relaxed selection, likely reflecting adaptation to darkness, while positive selection on other loci revealed additional functional shifts. Notably, allopolyploidy was found to fuel divergence through subgenome-specific patterns and asymmetric evolution within SOCs and among homoeologs. Taken together, these findings provide valuable insights into mechanisms of cave evolution and illustrate how allotetraploid genomes can facilitate diversification, potentially contributing to speciation in extreme environments.

Animals

Genomic analyses of three Acanthus L. species provide insight into polyploidization-driven speciation and evolution.

Allopolyploidy fundamentally influences plant evolution, yet the genomic dynamics of allotetraploidization remain incompletely understood. We investigated Acanthus tetraploideus (2n = 4x = 96), an ecologically significant allotetraploid true mangrove from Indo-West Pacific intertidal zones. Our prior integrative investigations indicate that A. tetraploideus originated through hybridization of the diploid species A. ilicifolius and A. ebracteatus with subsequent chromosome doubling. Here, we present complete chromosome-scale genome assemblies for all three species, representing the first genomic resources for true mangrove polyploid research. Our analysis reveals that the three species have experienced at least four rounds of polyploidization events, with the most recent, approximately 53 mya, possibly an Acanthus-specific event. The allotetraploid A. tetraploideus, which emerged between 1.5 and 2.2 mya, has A. ebracteatus as its maternal progenitor and A. ilicifolius as its paternal one. Through a comprehensive genomic comparison and analysis of homoeologous gene expression, we propose a gradual evolutionary trajectory for allotetraploidy in A. tetraploideus. Despite the allotetraploidization event dating back to around 2 mya, A. tetraploideus retains a high degree of colinearity with its ancestral genomes, with the majority (76.2%) of duplicated genes retained and no significant sub-genome bias in gene expression. Furthermore, we have identified positive selection in specific genes that may facilitate the adaptation of Acanthus mangrove species to their intertidal habitats. These findings establish A. tetraploideus as a model for studying allopolyploid evolution while providing new insights into mangrove speciation processes.

Genome, Plant

Why Specialized Metabolism Recurrently Emerges in Plants: Chemical and Genomic Biases in Metabolic Diversification.

Specialized metabolism plays a central role in mediating ecological interactions and adaptive responses in plants, while leaving enduring signatures in genome structure and evolution. Here, we synthesize advances in genomics, biochemistry, and evolutionary biology into a metabolite-driven genetic diversification (MGD) framework, in which metabolite chemistry biases the generation, retention, and reuse of genetic variation. When metabolic flux produces reactive, inhibitory, or otherwise costly intermediates, pathways handling these liabilities recurrently recruit gene dosage changes, duplication, and divergence at catalytic and regulatory choke points. These biases do not impose deterministic outcomes; instead, they shape which genomic variants are preferentially sampled and retained under selection, giving rise to predictable patterns of genomic change. Genome multiplication-through whole-genome duplication, allopolyploidy, and cell type-specific endoreduplication-amplifies these effects by altering dosage balance, regulatory context, and retention trajectories. Integrating MGD with genome-scale dosage dynamics explains why specialized metabolism repeatedly converges on similar solutions across plant lineages, even amid extensive genomic turnover and chemical diversity.

Journal Article

Clinical and Genomic Insights into the Allodiploid Hybrid Pathogen Aspergillus latus: A Retrospective Case Series.

Aspergillus latus is an emerging cryptic allodiploid hybrid pathogen within Aspergillus section Nidulantes that closely resembles related species and therefore prone to misidentification by routine diagnostic methods. Therefore, its true clinical burden is likely underestimated. In this study, we retrospectively characterized five patients with A. latus infections identified by metagenomic next-generation sequencing (mNGS) at a tertiary hospital in China. Clinical manifestations varied according to host immune status, ranging from a subclinical pulmonary lesion in an immunocompetent individual to aggressive disease in highly immunocompromised patients. Conventional microbiological methods showed limited sensitivity and consistently misidentified the isolates as A. nidulans, whereas mNGS enabled accurate detection of A. latus together with complex co-infections. Three viable clinical isolates were recovered for morphological characterization, antifungal susceptibility testing, and whole-genome sequencing (WGS). All tested isolates demonstrated reduced susceptibility to echinocandins but remained susceptible to mold-active triazoles and amphotericin B. Furthermore, WGS and macrosynteny analyses confirmed their allodiploid hybrid nature, revealing a mosaic genome derived from A. spinulosporus and an A. quadrilineatus-related lineage. Collectively, these findings highlight that A. latus may be missed by routine diagnostic methods and may exhibit a distinct antifungal susceptibility profile. Molecular approaches such as mNGS and WGS may therefore help achieve accurate species-level identification and support targeted antifungal therapy. Given this small retrospective case series, larger prospective and multicenter studies are needed to validate these observations and better define the epidemiology, clinical spectrum, and therapeutic implications of this emerging allodiploid hybrid pathogen.

Retrospective Studies

Genomic Divergence Shaped the Genetic Regulation of Meiotic Homologous Recombination in Brassica Allopolyploids.

The tight regulation of meiotic recombination between homologs is disrupted in Brassica AAC allotriploids, a genomic configuration that may have facilitated the formation of rapeseed (Brassica napus L.) ∼7,500 years ago. Indeed, the presence of the haploid C genome induces supernumerary crossovers between homologous A chromosomes with dramatically reshaped distribution. However, the genetic mechanisms driving this phenomenon and their divergence between nascent and established lineages remain unclear. To address these concerns, we generated hybrids carrying additional C chromosomes derived either from an established lineage of the allotetraploid B. napus or from its diploid progenitor B. oleracea. We then assessed recombination variation across twelve populations by mapping male meiotic crossovers using single nucleotide polymorphism markers evenly distributed across the sequenced A genome. Our findings reveal that the C09 chromosome of B. oleracea is responsible for the formation of additional crossovers near pericentromeric regions. Interestingly, its counterpart from an established lineage of B. napus shows no significant effect on its own, despite having a similar content of meiotic genes. However, we showed that the B. napus C09 chromosome influences crossover formation through inter-chromosomal epistatic interactions with other specific C chromosomes. These results provide new insights into the genetic regulation of homologous recombination in Brassica and emphasize the role of genomic divergence since the formation of the allopolyploid B. napus.

Meiosis

Bistable Mutation-Selection Equilibria and Violations of Fisher's Theorem in Tetraploids: Insights from Nonlinear Dynamics.

Polyploidy and whole genome duplication (WGD) are widespread biological phenomena with substantial cellular, meiotic, and genetic effects. Despite their prevalence and significance across the tree of life, population genetics theory for polyploids is not well developed. The lack of theoretical models limits our understanding of polyploid evolution and restricts our ability to harness polyploidy for crop improvement amidst increasing environmental stress. To address this gap, we developed and analyzed deterministic models of mutation-selection balance for tetraploids under polysomic (autotetraploid) and disomic (allotetraploid) inheritance patterns and arbitrary dominance relationships. We also introduced a new mathematical framework based on ordinary differential equations and nonlinear dynamics for analyzing the models. We find that autotetraploids approach Hardy-Weinberg Equilibrium 33% faster than allotetraploids, but the different tetraploid inheritance models show little differences in mutation load and allele frequency at mutation-selection balance. Our model also reveals two bistable points of mutation-selection balance for dominant alleles with biased mutation rates over a wide range of selection coefficients in the tetraploid models compared to bistability in only a narrow range for diploids. Finally, using discrete time simulations, we explore the temporal dynamics of allele frequency and fitness change and compare these dynamics to the predictions of Fisher's Fundamental Theorem of Natural Selection. While Fisher's predictions generally hold, we show that the bistable dynamics for dominant mutations fundamentally alter the associated temporal dynamics. Overall, this work develops foundational theoretical models that will facilitate the development of population genetic models and methodologies to study evolution in empirical tetraploid populations.

Fisher’s Fundamental Theorem

Nonadditive gene expression and reduced homoeolog expression bias in an intraspecific hexaploid wheat hybrid.

BACKGROUND: Intraspecific hybridization in allopolyploid plants can generate additive and nonadditive changes in gene expression through interactions between divergent parental genomes. However, how it simultaneously affects gene expression and the relative expression of homoeologs in higher-order polyploids is less well understood. To study this, we sequenced seedling leaf transcriptomes and profiled gene body methylation in two hexaploid wheat (Triticum aestivum L.) cultivars and their F₁ hybrids. RESULTS: Although only 4.3% of genes differed in expression between the parents, 22.3% deviated from mid-parent expression in the hybrids, with many showing transgressive expression. 32.1% of triads contained at least one homoeolog that deviated from mid-parent expression, and all three homoeologs deviated in 11% of triads, substantially more than expected by chance. Triads in which all three homoeologs were overexpressed also showed reduced differences in expression among homoeologs. Greater parental divergence in relative homoeolog expression was associated with nonadditive expression. Genes lacking gene body methylation were also more likely to show dominant or transgressive expression, whereas gene body methylation was associated with more balanced homoeolog expression and additive or conserved expression. CONCLUSIONS: Intraspecific hybridization in hexaploid wheat, even without a change in ploidy, was associated with widespread nonadditive gene expression and altered relative homoeolog expression within triads. These responses were associated with parental differences in homoeolog expression and the absence of gene body methylation. Although our findings are limited to seedling leaves from a single intraspecific cross, they provide a basis for testing the generality of these patterns across tissues, developmental stages, and genetic backgrounds.

Triticum

Genome-wide subgenome-resolved analysis validates chromosome 4 differentiation and prioritizes introgressed Coffea arabica accessions.

Chromosome 4 introgression in Timor hybrid-derived Coffea arabica is established, but the robustness of accession prioritization and the relative strength of cultivated-introgressed differentiation across the canephora-derived (sgC) and eugenioides-derived (sgE) subgenomes remained unclear under explicit subgenome filtering. We reanalyzed public genomic resources from 44 coffee accessions using strict contig-level subgenome filtering, Arabica-only population-structure analysis, SNP-panel sensitivity testing, genome-wide differentiation scans, permutation testing, and direct sequence alignment. Population structure and accession rankings were stable across marker densities and random seeds, and the same six introgressed references were retained throughout. Chromosome 4 ranked first in both subgenomes, with a strong sgC signal and a markedly weaker sgE signal; independent baseline-panel permutation tests supported both chromosome 4-associated signals. Direct alignment supported correspondence to the expected chromosome 4 pseudomolecules while showing incomplete source coverage and unresolved exact boundaries. Alignment-supported blocks contained 88 sgC and 62 sgE provisional defense-, signaling-, and regulatory-associated annotations. These results provide a genome-wide, quantitatively validated framework for prioritizing introgressed germplasm and candidate chromosome 4 regions for phenotype-linked coffee research without implying equivalent introgression, exact liftover, or causal resistance genes.

Coffea arabica