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1. Nuclear–cytoplasmic balance: whole genome duplications induce elevated organellar genome copy number

   https://doi.org/10.1111/tpj.15436  

   Fernandes Gyorfy, Matheus; Miller, Emma R.; Conover, Justin L.; Grover, Corrinne E.; Wendel, Jonathan F.; Sloan, Daniel B.; Sharbrough, Joel (August 2021, The Plant Journal)

   SUMMARY The plant genome is partitioned across three distinct subcellular compartments: the nucleus, mitochondria, and plastids. Successful coordination of gene expression among these organellar genomes and the nuclear genome is critical for plant function and fitness. Whole genome duplication (WGD) events in the nucleus have played a major role in the diversification of land plants and are expected to perturb the relative copy number (stoichiometry) of nuclear, mitochondrial, and plastid genomes. Thus, elucidating the mechanisms whereby plant cells respond to the cytonuclear stoichiometric imbalance that follows WGDs represents an important yet underexplored question in understanding the evolutionary consequences of genome doubling. We used droplet digital PCR to investigate the relationship between nuclear and organellar genome copy numbers in allopolyploids and their diploid progenitors in both wheat and Arabidopsis. Polyploids exhibit elevated organellar genome copy numbers per cell, largely preserving the cytonuclear stoichiometry observed in diploids despite the change in nuclear genome copy number. To investigate the timescale over which cytonuclear stoichiometry may respond to WGD, we also estimated the organellar genome copy number inArabidopsissynthetic autopolyploids and in a haploid‐induced diploid line. We observed corresponding changes in organellar genome copy number in these laboratory‐generated lines, indicating that at least some of the cellular response to cytonuclear stoichiometric imbalance is immediate following WGD. We conclude that increases in organellar genome copy numbers represent a common response to polyploidization, suggesting that maintenance of cytonuclear stoichiometry is an important component in establishing polyploid lineages. 

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2. 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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3. Variation in heteroploid reproduction and gene flow across a polyploid complex: One size does not fit all

   https://doi.org/10.1002/ece3.7791  

   Sutherland, Brittany L.; Galloway, Laura F. (June 2021, Ecology and Evolution)

   Abstract Whole‐genome duplication is considered an important speciation mechanism in plants. However, its effect on reproductive isolation between higher cytotypes is not well understood. We used backcrosses between different ploidy levels and surveys of mixed‐ploidy contact zones to determine how reproductive barriers differed with cytotype across a polyploid complex. We backcrossed F1 hybrids derived from 2X‐4X and 4X‐6X crosses in theCampanula rotundifoliaautopolyploid complex, measured backcross fitness, and estimated backcross DNA cytotype. We then sampled four natural mixed‐ploidy contact zones (two 2X‐4X and two 4X‐6X), estimated ploidy, and genotyped individuals across each contact zone. Reproductive success and capacity for gene flow was markedly lower for 2X‐4X than 4X‐6X hybrids. In fact, 3X hybrids could not backcross; all 2X‐4X backcross progeny resulted from neotetraploid F1 hybrids. Further, no 3X individuals were found in 2X‐4X contact zones, and 2X and 4X individuals were genetically distinct. By contrast, backcrosses of 5X hybrids were relatively successful, particularly when crossed to 6X individuals. In 4X‐6X contact zones, 5X individuals and aneuploids were common and all cytotypes were largely genetically similar and spatially intermixed. Taken together, these results provide strong evidence that reproduction is low between 2X and 4X cytotypes, primarily occurring via unreduced gamete production, but that reproduction and gene flow are ongoing between 4X and 6X cytotypes. Further, it suggests whole‐genome duplication can result in speciation between diploids and polyploids, but is less likely to create reproductive barriers between different polyploid cytotypes, resulting in two fundamentally different potentials for speciation across polyploid complexes. 

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4. 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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5. Interaction among ploidy, breeding system and lineage diversification

   https://doi.org/10.1111/nph.16184  

   Zenil‐Ferguson, Rosana; Burleigh, J. Gordon; Freyman, William A.; Igić, Boris; Mayrose, Itay; Goldberg, Emma E. (October 2019, New Phytologist)

   Summary If particular traits consistently affect rates of speciation and extinction, broad macroevolutionary patterns can be interpreted as consequences of selection at high levels of the biological hierarchy. Identifying traits associated with diversification rates is difficult because of the wide variety of characters under consideration and the statistical challenges of testing for associations from comparative phylogenetic data. Ploidy (diploid vs polyploid states) and breeding system (self‐incompatible vs self‐compatible states) are both thought to be drivers of differential diversification in angiosperms.We fit 29 diversification models to extensive trait and phylogenetic data in Solanaceae and investigate how speciation and extinction rate differences are associated with ploidy, breeding system, and the interaction between these traits.We show that diversification patterns in Solanaceae are better explained by breeding system and an additional unobserved factor, rather than by ploidy. We also find that the most common evolutionary pathway to polyploidy in Solanaceae occurs via direct breakdown of self‐incompatibility by whole genome duplication, rather than indirectly via breakdown followed by polyploidization.Comparing multiple stochastic diversification models that include complex trait interactions alongside hidden states enhances our understanding of the macroevolutionary patterns in plant phylogenies. 

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