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Polyploidy, or whole-genome duplication (WGD), is a significant evolutionary force. Following allopolyploidy, duplicate gene copies (homeologs) have divergent evolutionary trajectories: some genes are preferentially retained in duplicate, while others tend to revert to single-copy status. Examining the effect of homeolog loss (i.e., changes in gene dosage) on associated phenotypes is essential for unraveling the genetic mechanisms underlying polyploid genome evolution. However, homeolog-specific editing has been demonstrated in only a few crop species and remains unexplored beyond agricultural applications.Tragopogon(Asteraceae) includes an evolutionary model system for studying the immediate consequences of polyploidy in nature. In this study, we developed a CRISPR-mediated homeolog-specific editing platform in allotetraploidT. mirus. Using theMYB10andDFRgenes as examples, we successfully knocked out the targeted homeolog inT. mirus(4x) without editing the other homeolog (i.e., no off-target events). The editing efficiencies, defined as the percentage of plants with at least one allele of the targeted homeolog modified, were 35.7% and 45.5% forMYB10andDFR, respectively. Biallelic modification of the targeted homeolog occurred in the T0generation. These results demonstrate the robustness of homeolog-specific editing in polyploidTragopogon, laying the foundation for future studies of genome evolution following WGD in nature.
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Pangenomes provide new insights into polyploidy in plants
Abstract Polyploidy, also known as whole-genome duplication (WGD), is a significant evolutionary force in green plants, especially angiosperms. The dynamic nature of polyploid genomes generates genetic diversity and drives the evolution of novel traits and adaptations. Pangenomics is emerging as a major frontier in plant genome research, with a rapidly growing number of pangenomes for individual species and associated analyses providing novel agronomic and evolutionary insights. Polyploid genome analysis can be confounded by intraspecific variation when relying on a single reference genome assembly. The use of pangenomes that better represent the genomic diversity of a species helps overcome this limitation. However, a major gap remains between the number of pangenomic studies in polyploid compared to diploid species, despite the widespread prevalence of WGD, limiting the potential of the pangenome framework for characterizing and understanding polyploid genomes. Furthermore, most polyploid pangenome studies have focused on domesticated crop species, and natural populations have rarely been examined. In addition to applications in crop improvement, pangenomes can provide insights into the ecological and evolutionary impact of polyploidy. Here, we summarize recent pangenome studies in polyploid plants and highlight promising topics for future research. We hope this article will encourage the growth of pangenomic studies in polyploid systems, particularly in natural populations.
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- Award ID(s):
- 1923234
- PAR ID:
- 10662353
- Publisher / Repository:
- Linnean Society of London
- Date Published:
- Journal Name:
- Evolutionary Journal of the Linnean Society
- Volume:
- 4
- Issue:
- 1
- ISSN:
- 2752-938X
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Boden, Scott (Ed.)Abstract Polyploidy or whole-genome duplication (WGD) is a significant evolutionary force. However, the mechanisms governing polyploid genome evolution remain unclear, limited largely by a lack of functional analysis tools in organisms that best exemplify the earliest stages of WGD. Tragopogon (Asteraceae) includes an evolutionary model system for studying the immediate consequences of polyploidy. In this study, we significantly improved the transformation system and obtained genome-edited T. porrifolius (2x) and T. mirus (4x) primary generation (T0) individuals. Using CRISPR/Cas9, we knocked out the dihydroflavonol 4-reductase (DFR) gene, which controls anthocyanin synthesis, in both species. All transgenic allotetraploid T. mirus individuals had at least one mutant DFR allele, and 71.4% had all four DFR alleles edited. The resulting mutants lacked anthocyanin, and these mutations were inherited in the T1 generation. This study demonstrates a highly efficient CRISPR platform, producing genome-edited Tragopogon individuals that have completed the life cycle. The approaches used and challenges faced in building the CRISPR system in Tragopogon provide a framework for building similar systems in other non-genetic models. Genome editing in Tragopogon paves the way for novel functional biology studies of polyploid genome evolution and the consequences of WGD on complex traits, holding enormous potential for both basic and applied research.more » « less
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Summary Recently formed allopolyploid species offer unprecedented insights into the early stages of polyploid evolution. This review examines seven well‐studied neopolyploids (we use ‘neopolyploid’ to refer to very recently formed polyploids, i.e. during the past 300 years), spanning different angiosperm families, exploring commonalities and differences in their evolutionary trajectories. Each neopolyploid provides a unique case study, demonstrating both shared patterns, such as rapid genomic and phenotypic changes, and unique responses to hybridization and genome doubling. While previous studies of these neopolyploids have improved our understanding of polyploidy, significant knowledge gaps remain, highlighting the need for further research into the varied impacts of whole‐genome duplication on gene expression, epigenetic modifications, and ecological interactions. Notably, all of these neopolyploids have spontaneously arisen due to human activity in natural environments, underscoring the profound consequences of polyploidization in a rapidly changing world. Understanding the immediate effects of polyploidy is crucial not only for evolutionary biology but also for applied practices, as polyploidy can lead to novel traits, as well as stress tolerance and increased crop yields. Future research directions include investigating the genetic and epigenetic mechanisms underlying polyploid evolution, as well as exploring the potential of neopolyploids for crop improvement and environmental adaptation.more » « less
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Abstract BackgroundCapturing the genetic diversity of wild relatives is crucial for improving crops because wild species are valuable sources of agronomic traits that are essential to enhance the sustainability and adaptability of domesticated cultivars. Genetic diversity across a genus can be captured in super-pangenomes, which provide a framework for interpreting genomic variations. ResultsHere we report the sequencing, assembly, and annotation of nine wild North American grape genomes, which are phased and scaffolded at chromosome scale. We generate a reference-unbiased super-pangenome using pairwise whole-genome alignment methods, revealing the extent of the genomic diversity among wild grape species from sequence to gene level. The pangenome graph captures genomic variation between haplotypes within a species and across the different species, and it accurately assesses the similarity of hybrids to their parents. The species selected to build the pangenome are a great representation of the genus, as illustrated by capturing known allelic variants in the sex-determining region and for Pierce’s disease resistance loci. Using pangenome-wide association analysis, we demonstrate the utility of the super-pangenome by effectively mapping short reads from genus-wide samples and identifying loci associated with salt tolerance in natural populations of grapes. ConclusionsThis study highlights how a reference-unbiased super-pangenome can reveal the genetic basis of adaptive traits from wild relatives and accelerate crop breeding research.more » « less
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Summary Eukaryotic genomes harbor many forms of variation, including nucleotide diversity and structural polymorphisms, which experience natural selection and contribute to genome evolution and biodiversity. However, harnessing this variation for agriculture hinges on our ability to detect, quantify, catalog, and utilize genetic diversity.Here, we explore seven complete genomes of the emerging biofuel crop pennycress (Thlaspi arvense) drawn from across the species’s current genetic diversity to catalogue variation in genome structure and content.Across this new pangenome resource, we find contrasting evolutionary modes in different genomic regions. Gene-poor, repeat-rich pericentromeric regions experience frequent rearrangements, including repeated centromere repositioning. In contrast, conserved gene-dense chromosome arms maintain large-scale synteny across accessions, even in fast-evolving immune genes where microsynteny breaks down across species but the macrosynteny of gene cluster positioning is maintained.Our findings highlight that multiple elements of the genome experience dynamic evolution that conserves functional content on the chromosome scale but allows rearrangement and presence-absence variation on a local scale. This diversity is invisible to classical reference-based approaches and highlights the strength and utility of pangenomic resources. These results provide a valuable case study of rapid genomic structural evolution within a species and powerful resources for crop development in an emerging biofuel crop.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1093/evolinnean/kzaf010
