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1. Gene expression bias between the subgenomes of allopolyploid hybrids is an emergent property of the kinetics of expression

   https://doi.org/10.1371/journal.pcbi.1011803  

   An, Hong; Pires, J Chris; Conant, Gavin C (January 2024, PLOS Computational Biology)

   Zhang, Jianzhi (Ed.)

   Hybridization coupled to polyploidy, or allopolyploidy, has dramatically shaped the evolution of flowering plants, teleost fishes, and other lineages. Studies of recently formed allopolyploid plants have shown that the two subgenomes that merged to form that new allopolyploid do not generally express their genes equally. Instead, one of the two subgenomes expresses its paralogs more highly on average. Meanwhile, older allopolyploidy events tend to show biases in duplicate losses, with one of the two subgenomes retaining more genes than the other. Since reduced expression is a pathway to duplicate loss, understanding the origins of expression biases may help explain the origins of biased losses. Because we expect gene expression levels to experience stabilizing selection, our conceptual frameworks for how allopolyploid organisms form tend to assume that the new allopolyploid will show balanced expression between its subgenomes. It is then necessary to invoke phenomena such as differences in the suppression of repetitive elements to explain the observed expression imbalances. Here we show that, even for phenotypically identical diploid progenitors, the inherent kinetics of gene expression give rise to biases between the expression levels of the progenitor genes in the hybrid. Some of these biases are expected to be gene-specific and not give rise to global differences in progenitor gene expression. However, particularly in the case of allopolyploids formed from progenitors with different genome sizes, global expression biases favoring one subgenome are expected immediately on formation. Hence, expression biases are arguably the expectation upon allopolyploid formation rather than a phenomenon needing explanation. In the future, a deeper understanding of the kinetics of allopolyploidy may allow us to better understand both biases in duplicate losses and hybrid vigor. 

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2. Whole-Genome Duplication and Host Genotype Affect Rhizosphere Microbial Communities

   https://doi.org/10.1128/msystems.00973-21  

   Ponsford, Julian C.; Hubbard, Charley J.; Harrison, Joshua G.; Maignien, Lois; Buerkle, C. Alex; Weinig, Cynthia (February 2022, mSystems)

   Bulgarelli, Davide (Ed.)

   ABSTRACT The composition of microbial communities found in association with plants is influenced by host phenotype and genotype. However, the ways in which specific genetic architectures of host plants shape microbiomes are unknown. Genome duplication events are common in the evolutionary history of plants and influence many important plant traits, and thus, they may affect associated microbial communities. Using experimentally induced whole-genome duplication (WGD), we tested the effect of WGD on rhizosphere bacterial communities in Arabidopsis thaliana . We performed 16S rRNA amplicon sequencing to characterize differences between microbiomes associated with specific host genetic backgrounds (Columbia versus Landsberg) and ploidy levels (diploid versus tetraploid). We modeled relative abundances of bacterial taxa using a hierarchical Bayesian approach. We found that host genetic background and ploidy level affected rhizosphere community composition. We then tested to what extent microbiomes derived from a specific genetic background or ploidy level affected plant performance by inoculating sterile seedlings with microbial communities harvested from a prior generation. We found a negative effect of the tetraploid Columbia microbiome on growth of all four plant genetic backgrounds. These findings suggest an interplay between host genetic background and ploidy level and bacterial community assembly with potential ramifications for host fitness. Given the prevalence of ploidy-level variation in both wild and managed plant populations, the effects on microbiomes of this aspect of host genetic architecture could be a widespread driver of differences in plant microbiomes. IMPORTANCE Plants influence the composition of their associated microbial communities, yet the underlying host-associated genetic determinants are typically unknown. Genome duplication events are common in the evolutionary history of plants and affect many plant traits. Using Arabidopsis thaliana , we characterized how whole-genome duplication affected the composition of rhizosphere bacterial communities and how bacterial communities associated with two host plant genetic backgrounds and ploidy levels affected subsequent plant growth. We observed an interaction between ploidy level and genetic background that affected both bacterial community composition and function. This research reveals how genome duplication, a widespread genetic feature of both wild and crop plant species, influences bacterial assemblages and affects plant growth. 

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3. Little evidence for homoeologous gene conversion and homoeologous exchange events in Gossypium allopolyploids

   https://doi.org/10.1002/ajb2.16386  

   Conover, Justin L; Grover, Corrinne E; Sharbrough, Joel; Sloan, Daniel B; Peterson, Daniel G; Wendel, Jonathan F (August 2024, American Journal of Botany)

   Abstract PremiseA complicating factor in analyzing allopolyploid genomes is the possibility of physical interactions between homoeologous chromosomes during meiosis, resulting in either crossover (homoeologous exchanges) or non‐crossover products (homoeologous gene conversion). Homoeologous gene conversion was first described in cotton by comparing SNP patterns in sequences from two diploid progenitors with those from the allopolyploid subgenomes. These analyses, however, did not explicitly consider other evolutionary scenarios that may give rise to similar SNP patterns as homoeologous gene conversion, creating uncertainties about the reality of the inferred gene conversion events. MethodsHere, we use an expanded phylogenetic sampling of high‐quality genome assemblies from seven allopolyploidGossypiumspecies (all derived from the same polyploidy event), four diploid species (two closely related to each subgenome), and a diploid outgroup to derive a robust method for identifying potential genomic regions of gene conversion and homoeologous exchange. ResultsWe found little evidence for homoeologous gene conversion in allopolyploid cottons, and that only two of the 40 best‐supported events were shared by more than one species. We did, however, reveal a single, shared homoeologous exchange event at one end of chromosome 1, which occurred shortly after allopolyploidization but prior to divergence of the descendant species. ConclusionsOverall, our analyses demonstrated that homoeologous gene conversion and homoeologous exchanges are uncommon inGossypium, affecting between zero and 24 genes per subgenome (0.0–0.065%) across the seven species. More generally, we highlighted the potential problems of using simple four‐taxon tests to investigate patterns of homoeologous gene conversion in established allopolyploids. 

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4. Genome‐material costs and functional trade‐offs in the autopolyploid Solidago gigantea (giant goldenrod) series

   https://doi.org/10.1002/ajb2.16218  

   Walczyk, Angela M.; Hersch‐Green, Erika I. (September 2023, American Journal of Botany)

   Abstract PremiseIncreased genome‐material costs of N and P atoms inherent to organisms with larger genomes have been proposed to limit growth under nutrient scarcities and to promote growth under nutrient enrichments. Such responsiveness may reflect a nutrient‐dependent diploid versus polyploid advantage that could have vast ecological and evolutionary implications, but direct evidence that material costs increase with ploidy level and/or influence cytotype‐dependent growth, metabolic, and/or resource‐use trade‐offs is limited. MethodsWe grew diploid, autotetraploid, and autohexaploidSolidago giganteaplants with one of four ambient or enriched N:P ratios and measured traits related to material costs, primary and secondary metabolism, and resource‐use. ResultsRelative to diploids, polyploids invested more N and P into cells, and tetraploids grew more with N enrichments, suggesting that material costs increase with ploidy level. Polyploids also generally exhibited strategies that could minimize material‐cost constraints over both long (reduced monoploid genome size) and short (more extreme transcriptome downsizing, reduced photosynthesis rates and terpene concentrations, enhanced N‐use efficiencies) evolutionary time periods. Furthermore, polyploids had lower transpiration rates but higher water‐use efficiencies than diploids, both of which were more pronounced under nutrient‐limiting conditions. ConclusionsN and P material costs increase with ploidy level, but material‐cost constraints might be lessened by resource allocation/investment mechanisms that can also alter ecological dynamics and selection. Our results enhance mechanistic understanding of how global increases in nutrients might provide a release from material‐cost constraints in polyploids that could impact ploidy (or genome‐size)‐specific performances, cytogeographic patterning, and multispecies community structuring. 

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5. Plant neopolyploidy and genetic background differentiate the microbiome of duckweed across a variety of natural freshwater sources

   https://doi.org/10.1111/mec.17142  

   Anneberg, Thomas J.; Turcotte, Martin M.; Ashman, Tia‐Lynn (November 2023, Molecular Ecology)

   Abstract Whole‐genome duplication has long been appreciated for its role in driving phenotypic novelty in plants, often altering the way organisms interface with the abiotic environment. Only recently, however, have we begun to investigate how polyploidy influences interactions of plants with other species, despite the biotic niche being predicted as one of the main determinants of polyploid establishment. Nevertheless, we lack information about how polyploidy affects the diversity and composition of the microbial taxa that colonize plants, and whether this is genotype‐dependent and repeatable across natural environments. This information is a first step towards understanding whether the microbiome contributes to polyploid establishment. We, thus, tested the immediate effect of polyploidy on the diversity and composition of the bacterial microbiome of the aquatic plantSpirodela polyrhizausing four pairs of diploids and synthetic autotetraploids. Under controlled conditions, axenic plants were inoculated with pond waters collected from 10 field sites across a broad environmental gradient. Autotetraploids hosted 4%–11% greater bacterial taxonomic and phylogenetic diversity than their diploid progenitors. Polyploidy, along with its interactions with the inoculum source and genetic lineage, collectively explained 7% of the total variation in microbiome composition. Furthermore, polyploidy broadened the core microbiome, with autotetraploids having 15 unique bacterial taxa in addition to the 55 they shared with diploids. Our results show that whole‐genome duplication directly leads to novelty in the plant microbiome and importantly that the effect is dependent on the genetic ancestry of the polyploid and generalizable over many environmental contexts. 

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