Genomic analyses of the Linum distyly supergene reveal convergent evolution at the molecular level

Gutiérrez‐Valencia, Juanita; Fracassetti, Marco; Berdan, Emma L.; Bunikis, Ignas; Soler, Lucile; Dainat, Jacques; Kutschera, Verena E.; Losvik, Aleksandra; Désamoré, Aurélie; Hughes, P. William; Foroozani, Alireza; Laenen, Benjamin; Pesquet, Edouard; Abdel‐Aziz, Mohamed S.; Pettersson, Olga Vinnere; Nystedt, Björn; Brennan, Adrian C.; Slotte, Tanja

doi:10.1016/j.cub.2022.08.042

Cited by 31 publications

(113 citation statements)

References 97 publications

(131 reference statements)

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“…Distylous populations contain two floral morphs, the S-morph and L-morph, showing morphological differences ( Figure 1 ) accompanied by self- (and intra-morph) incompatibility (SI). The genetic basis of these characteristics is a supergene called the S -locus; the S -morph is hemizygous for the S -locus in Primula [ 2 ], Turnera [ 3 ], Linum [ 4 ], and likely in Fagopyrum [ 5 ]. Despite its complex phenotype, distyly has evolved across 28 genera with extreme phenotypic consistency [ 1 ], making it a remarkable example of convergent evolution.…”

Section: Introductionmentioning

confidence: 99%

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Annotation of the Turnera subulata (Passifloraceae) Draft Genome Reveals the S-Locus Evolved after the Divergence of Turneroideae from Passifloroideae in a Stepwise Manner

Henning

Roalson

Mir

et al. 2023

Plants

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A majority of Turnera species (Passifloraceae) exhibit distyly, a reproductive system involving both self-incompatibility and reciprocal herkogamy. This system differs from self-incompatibility in Passiflora species. The genetic basis of distyly in Turnera is a supergene, restricted to the S-morph, and containing three S-genes. How supergenes and distyly evolved in Turnera, and the other Angiosperm families exhibiting distyly remain largely unknown. Unraveling the evolutionary origins in Turnera requires the generation of genomic resources and extensive phylogenetic analyses. Here, we present the annotated draft genome of the S-morph of distylous Turnera subulata. Our annotation allowed for phylogenetic analyses of the three S-genes’ families across 56 plant species ranging from non-seed plants to eudicots. In addition to the phylogenetic analysis, we identified the three S-genes’ closest paralogs in two species of Passiflora. Our analyses suggest that the S-locus evolved after the divergence of Passiflora and Turnera. Finally, to provide insights into the neofunctionalization of the S-genes, we compared expression patterns of the S-genes with close paralogs in Arabidopsis and Populus trichocarpa. The annotation of the T. subulata genome will provide a useful resource for future comparative work. Additionally, this work has provided insights into the convergent nature of distyly and the origin of supergenes.

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Section: Introductionmentioning

confidence: 99%

“…The S -locus has been characterized in Primula [ 2 , 6 , 7 , 8 ], Turnera [ 3 ], and Linum [ 4 ]. The S -locus in Primula contains five S -genes [ 2 ], two of which have been characterized.…”

Section: Introductionmentioning

confidence: 99%

Annotation of the Turnera subulata (Passifloraceae) Draft Genome Reveals the S-Locus Evolved after the Divergence of Turneroideae from Passifloroideae in a Stepwise Manner

Henning

Roalson

Mir

et al. 2023

Plants

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“…above the anthers' attachment point), and width of the corolla tube mouth 8 .Having evolved independently in angiosperms at least 13 times 9 , distyly represents an ideal case to study convergent evolution 10 . Research on distyly has mainly focused on Primula (Primulaceae) [11][12][13][14][15][16][17] , Fagopyrum (Polygonaceae) 18,19 , and Turnera (Passifloraceae) [20][21][22][23] , reviewed below, and, to a lesser extent, Linum (Linaceae) 24 and Lithospermum (Boraginaceae) 25,26 . Phenotypic convergence in floral morphology appears to be mirrored by convergence in the genetic architecture of the locus controlling distyly.…”

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confidence: 99%

Comparative transcriptomics reveals commonalities and differences in the genetic underpinnings of a floral dimorphism

Potente

Stubbs

Yousefi

et al. 2022

Sci Rep

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Distyly, a floral dimorphism associated with heteromorphic self-incompatibility and controlled by the S-locus supergene, evolved independently multiple times. Comparative analyses of the first transcriptome atlas for the main distyly model, Primula veris, with other distylous species produced the following findings. A set of 53 constitutively expressed genes in P. veris did not include any of the housekeeping genes commonly used to normalize gene expression in qPCR experiments. The S-locus gene CYPT acquired its role in controlling style elongation via a change in expression profile. Comparison of genes differentially expressed between floral morphs revealed that brassinosteroids and auxin are the main hormones controlling style elongation in P. veris and Fagopyrum esculentum, respectively. Furthermore, shared biochemical pathways might underlie the expression of distyly in the distantly related P. veris, F. esculentum and Turnera subulata, suggesting a degree of correspondence between evolutionary convergence at phenotypic and molecular levels. Finally, we provide the first evidence supporting the previously proposed hypothesis that distyly supergenes of distantly related species evolved via the recruitment of genes related to the phytochrome-interacting factor (PIF) signaling network. To conclude, this is the first study that discovered homologous genes involved in the control of distyly in distantly related taxa.

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“…Studies of the S‐morph of Primula and Turnera revealed a hemizygous region at the S ‐locus supergene whose allelic counterparts are absent from the L‐morph (Li et al ., 2016; Cocker et al ., 2018; Shore et al ., 2019; Potente et al ., 2022). There also appear to be similar genetic architectures involving hemizygosity at the S ‐locus in distylous Fagopyrum (Yasui et al ., 2012) and Linum (Ushijima et al ., 2012; Gutiérrez‐Valencia et al ., 2022). Consistent with these findings, the candidate S ‐locus genes GeCYP , GeFRS6 , and GeGA3OX in G. elegans are also hemizygous, suggesting that this type of genetic architecture may be a common feature among heterostylous species.…”

Section: Discussionmentioning

confidence: 99%

“…An S ‐locus supergene model has been proposed governing style length, anther position, and the self‐ and intra‐morph incompatibility system in distylous species (Mather, 1950; reviewed in D. Charlesworth & B. Charlesworth, 1979; Lewis & Jones, 1992). However, the molecular basis of the supergene determining the L‐ and S‐morphs has been revealed only during the past decade in a few unrelated distylous taxa, primarily Primula (Primulaceae) (Huu et al ., 2016; Li et al ., 2016; Potente et al ., 2022) and Turnera (Turneraceae) (Shore et al ., 2019; Matzke et al ., 2020), although detailed molecular investigations of the distyly linkage group have also been conducted in Fagopyrum (Polygonaceae) (Yasui et al ., 2012; Takeshima et al ., 2019) and Linum (Linaceae) (Ushijima et al ., 2012; Gutiérrez‐Valencia et al ., 2022,; reviewed in Kappel et al ., 2017). Two different genes determine style length in Primula ( CYP734A50 ) and Turnera ( TsBAHD ), and both are involved in the metabolism of brassinosteroids (BRs) and cause short styles in the S‐morph by the inactivation of BRs (Huu et al ., 2016; Li et al ., 2016; Shore et al ., 2019).…”

Section: Introductionmentioning

confidence: 99%

Genomic evidence supports the genetic convergence of a supergene controlling the distylous floral syndrome

et al. 2022

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Summary Heterostyly, a plant sexual polymorphism controlled by the S‐locus supergene, has evolved numerous times among angiosperm lineages and represents a classic example of convergent evolution in form and function. Determining whether underlying molecular convergence occurs could provide insights on constraints to floral evolution. Here, we investigated S‐locus genes in distylous Gelsemium (Gelsemiaceae) to determine whether there is evidence of molecular convergence with unrelated distylous species. We used several approaches, including anatomical measurements of sex‐organ development and transcriptome and whole‐genome sequencing, to identify components of the S‐locus supergene. We also performed evolutionary analysis with candidate S‐locus genes and compared them with those reported in Primula and Turnera. The candidate S‐locus supergene of Gelsemium contained four genes, of which three appear to have originated from gene duplication events within Gelsemiaceae. The style‐length genes GeCYP in Gelsemium and CYP734A50 in Primula likely arose from duplication of the same gene, CYP734A1. Three out of four S‐locus genes in Gelsemium elegans were hemizygous, as previously reported in Primula and Turnera. We provide genomic evidence on the genetic convergence of the supergene underlying distyly among distantly related angiosperm lineages and help to illuminate the genetic architecture involved in the evolution of heterostyly.

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Genomic analyses of the Linum distyly supergene reveal convergent evolution at the molecular level

Cited by 31 publications

References 97 publications

Annotation of the Turnera subulata (Passifloraceae) Draft Genome Reveals the S-Locus Evolved after the Divergence of Turneroideae from Passifloroideae in a Stepwise Manner

Annotation of the Turnera subulata (Passifloraceae) Draft Genome Reveals the S-Locus Evolved after the Divergence of Turneroideae from Passifloroideae in a Stepwise Manner

Comparative transcriptomics reveals commonalities and differences in the genetic underpinnings of a floral dimorphism

Genomic evidence supports the genetic convergence of a supergene controlling the distylous floral syndrome

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