Genome sequencing reveals the genetic architecture of heterostyly and domestication history of common buckwheat

Fawcett, Jeffrey A.; Takeshima, Ryoma; Kikuchi, Shinji; Yazaki, Euki; Katsube-Tanaka, Tomoyuki; Dong, Yumei; Li, Meifang; Hunt, Harriet V.; Jones, Martin K.; Lister, Diane L.; Ohsako, Takanori; Ogiso-Tanaka, Eri; Fujii, Kenichiro; Hara, Takashi; Matsui, Katsuhiro; Mizuno, Nobuyuki; Nishimura, Kazusa; Nakazaki, Tetsuya; Saito, Hiroki; Takeuchi, Naoko; Ueno, Mariko; Matsumoto, Daiki; Norizuki, Miyu; Shirasawa, Kenta; Li, Chengyun; Hirakawa, Hideki; Ota, Tatsuya; Yasui, Yasuo

doi:10.1038/s41477-023-01474-1

Cited by 15 publications

(27 citation statements)

References 109 publications

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“…We then asked whether the S -locus was hemizygous also in P. edelbergii , as found in all other heterostylous species studied to date (Fawcett et al, 2023; Gutiérrez-Valencia et al, 2022; Li et al, 2016; Shore et al, 2019; Yang et al, 2023; Zhao et al, 2023), by checking whether the S -locus region was characterized by halved sequencing depth, an approach commonly used to detect hemizygous supergenes (Gutiérrez-Valencia et al, 2021). The S -locus had approximately the same sequencing depth as the rest of chromosome 2 (mean S -locus depth: 154.6x; mean chromosome 2 depth: 156.1x; Figure 4d ).…”

Section: Resultsmentioning

confidence: 99%

“…Recently, research on the S-locus has expanded from Primula to other genera that independently evolved heterostyly, including Turnera (Henning et al, 2022;Matzke et al, 2020Matzke et al, , 2021Shore et al, 2019), Fagopyrum (Fawcett et al, 2023;Yasui et al, 2012Yasui et al, , 2016, Linum (Gutiérrez-Valencia et al, 2022), Gelsemium (Zhao et al, 2023), and Nymphoides (Yang et al, 2023). Surprisingly, in all these cases the S-locus was found to be hemizygous in thrums and absent from pins, pointing to a remarkable consistency in the genomic architecture of the S-locus across heterostylous taxa.…”

Section: Introductionmentioning

confidence: 99%

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ThePrimula edelbergii S-locus is an example of a jumping supergene

Potente,

Yousefi,

Keller

et al. 2024

Preprint

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Research on supergenes, non-recombining genomic regions housing tightly linked genes that control complex phenotypes, has gained prominence in genomics, with supergenes having been described in most eukaryotic lineages. Heterostyly, a floral heteromorphism promoting outcrossing in several angiosperm families, is controlled by the S-locus supergene. Historically, the S-locus has been studied primarily in closely related Primula species and, more recently, in other groups that independently evolved heterostyly. However, it remains unknown whether genetic architecture and composition of the S-locus are maintained among species that share a common origin of heterostyly and subsequently diverged across larger time scales. To address this research gap, we present a chromosome-scale genome assembly of Primula edelbergii, a species that shares the same origin of heterostyly with Primula veris (whose S-locus has been characterized) but diverged from it ca. 18 million years ago. Comparative genomic analyses between P. edelbergii and P. veris allowed us to show, for the first time, that the S-locus can 'jump' (i.e. translocate) between chromosomes. Additionally, we found that four S-locus genes were maintained across time but were reshuffled within the supergene, seemingly without affecting their expression. Furthermore, we confirmed that S-locus hemizygosity counteracts genetic degeneration, otherwise expected in supergenes. Finally, we investigated P. edelbergii evolutionary history within Ericales in terms of whole genome duplications and transposable element accumulation. In summary, our work provides a valuable resource for comparative analyses aimed at investigating the genetics of heterostyly and the pivotal role of supergenes in shaping the evolution of complex phenotypes.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

ThePrimula edelbergii S-locus is an example of a jumping supergene

Potente,

Yousefi,

Keller

et al. 2024

Preprint

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“…Previous work has identified an ancient whole-genome duplication (WGD) shared by buckwheat and Rumex (Zhang et al 2017, Fawcett et al 2023). In addition, R. acetosella , R. scutatus and R. paucifolius are known to have natural polyploid populations (Löve 1940, Löve 1942, Smith 1968).…”

Section: Resultsmentioning

confidence: 99%

“…The large peak we observed in R. thyrsiflorus is more difficult to explain, as it is much older ( dS ∼0.35) and not shared by other species, and polyploidy has not been observed in the species. While old, the peak is too young to be explained by differential retention of the ancient WGD shared with buckwheat, which occurred ∼70 MYA (Fawcett et al 2023). One potential explanation is a large burst of gene duplication without polyploidy; a large genome size and high percentage of duplicated BUSCO genes in our transcriptome assembly support this idea (Supplementary Data 2).…”

Section: Discussionmentioning

confidence: 99%

Phylogenomics resolves key relationships inRumexand uncovers a dynamic history of independently evolving sex chromosomes

Hibbins,

Rifkin,

Choudhury

et al. 2023

Preprint

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Sex chromosomes have evolved independently many times across eukaryotes. Despite a considerable body of literature on the evolution of sex chromosomes, the causes and consequences of variation in the formation, degeneration, and turnover of sex chromosomes remain poorly understood. Comparative approaches in groups with sexual system variation can be valuable for understanding these questions. Plants are well-suited to such comparative studies, with many lineages containing relatively recent origins of dioecy and sex chromosomes as well as hermaphroditic close relatives.Rumexis a diverse genus of flowering plants harboring significant sexual system variation, including hermaphroditic and dioecious clades with XY sex chromosomes. Previous disagreement in the phylogenetic relationships among key species have rendered the history of sex chromosome evolution uncertain. Resolving this history is important to the development ofRumexas a system for the comparative study of sex chromosome evolution. Here, we leverage new transcriptome assemblies from 11 species representing the major clades in the genus, along with a whole-genome assembly generated for a pivotal hermaphroditic species, to further resolve the phylogeny and history of sex chromosome evolution inRumex. Using phylogenomic approaches, we find evidence for two independent origins of sex chromosomes and introgression from unsampled taxa in the genus. Comparative genomics reveals massive chromosomal rearrangements in a dioecious species, with evidence for a complex origin of the sex chromosomes through multiple chromosomal fusions. However, we see no evidence of elevated rates of fusion on the sex chromosome in comparison with autosomes, providing no support for an adaptive hypothesis for the sex chromosome expansion. Overall, our results highlight the dynamic nature of sex chromosome systems inRumexand illustrate the utility of the genus as a model for the comparative study of sex chromosome evolution.

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“…One of the most notable, recent discoveries on the S-locus is that it is hemizygous and present only in thrums in all systems where its genetic architecture has been investigated, including Primula (Huu et al, 2016;Li et al, 2016), Turnera (Shore et al, 2019), Fagopyrum (Fawcett et al, 2023;Matsui & Yasui, 2020), Linum (Gutiérrez-Valencia et al, 2022), and Gelsemium (Zhao et al, 2023) is lower than that of their paralogs (CCM1, GLO1, CYP734A51, and KFB1; π S : 0.0034 ± 0.0007) located elsewhere in the genome (Table 3).…”

Section: Population Genetic Consequences Of Hemizygosity and Transiti...mentioning

confidence: 99%

Genomic analyses elucidate S‐locus evolution in response to intra‐specific losses of distyly in Primula vulgaris

Mora‐Carrera,

Stubbs,

Potente

et al. 2024

Ecology and Evolution

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Distyly, a floral dimorphism that promotes outcrossing, is controlled by a hemizygous genomic region known as the S‐locus. Disruptions of genes within the S‐locus are responsible for the loss of distyly and the emergence of homostyly, a floral monomorphism that favors selfing. Using whole‐genome resequencing data of distylous and homostylous individuals from populations of Primula vulgaris and leveraging high‐quality reference genomes of Primula we tested, for the first time, predictions about the evolutionary consequences of transitions to selfing on S‐genes. Our results reveal a previously undetected structural rearrangement in CYPᵀ associated with the shift to homostyly and confirm previously reported, homostyle‐specific, loss‐of‐function mutations in the exons of the S‐gene CYPᵀ. We also discovered that the promoter and intronic regions of CYPᵀ in distylous and homostylous individuals are conserved, suggesting that down‐regulation of CYPᵀ via mutations in its promoter and intronic regions is not a cause of the shift to homostyly. Furthermore, we found that hemizygosity is associated with reduced genetic diversity in S‐genes compared with their paralogs outside the S‐locus. Additionally, the shift to homostyly lowers genetic diversity in both the S‐genes and their paralogs, as expected in primarily selfing plants. Finally, we tested, for the first time, long‐standing theoretical models of changes in S‐locus genotypes during early stages of the transition to homostyly, supporting the assumption that two copies of the S‐locus might reduce homostyle fitness.

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Genome sequencing reveals the genetic architecture of heterostyly and domestication history of common buckwheat

Cited by 15 publications

References 109 publications

ThePrimula edelbergii S-locus is an example of a jumping supergene

ThePrimula edelbergii S-locus is an example of a jumping supergene

Phylogenomics resolves key relationships inRumexand uncovers a dynamic history of independently evolving sex chromosomes

Genomic analyses elucidate S‐locus evolution in response to intra‐specific losses of distyly in Primula vulgaris

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