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Supergenes are non-recombining genomic regions ensuring the co-inheritance of multiple, co-adapted genes. Despite the importance of supergenes in adaptation, little is known on how they originate. A classic example of supergene is the S locus controlling heterostyly, a floral heteromorphism occurring in 28 angiosperm families. In Primula, heterosty...
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... we compared d N /d S values for S-locus genes with those of their respective paralogs. The S-locus genes CYP T and GLO T showed significantly or marginally significantly higher d N /d S values than their respective paralogs, CYP734A51 and GLO1 (table 3 and supplementary table S9 and fig. S32, Supplementary Material online). ...Context 2
... and table S10, Supplementary Material online). Conversely, KFB T and CCM T showed lower pairwise d N / d S than their paralogs (KFB1 and CCM1 ; table 3 and supple- mentary table S9, Supplementary Material online), although significance of these results could not be tested due to insufficient number of comparisons. Finally, no significant differences in substitution rates were detected between the KFB T and KFB1 clades on CodeML, nor between the CCM T and CCM1 clades (likelihood-ratio test P ¼ 0.76 and P ¼ 0.13, respectively; supplementary fig. ...Citations
... Recent efforts have been made to elucidate the genetic architecture of heterostylous supergenes in a handful of distylous systems (reviewed in 12-each belonging to a different angiosperm lineage, have demonstrated that distyly is controlled by several hemizygous genes present in the short-styled morph (S-morph) but absent from the long-styled morph (Lmorph) [14][15][16][17][18][19][20] . For example, in Primula, the S-locus is a hemizygous region containing ve genes controlling the expression of different components of the distylous polymorphism [14][15]21 . ...
Tristyly is a polymorphism characterized by three flower morphs with reciprocal stigma and anther heights controlled by two epistatically interacting diallelic loci (S and M), hypothesized to be supergenes. Chromosome-level genome assemblies of Eichhornia paniculata identified the S- and M-loci. The S-locus is a supergene consisting of two divergent alleles: The S-allele (2.51Mb) with three S-allele specific genes hemizygous in most S-morph plants and the s-allele (596kb) with five s-allele specific genes. Two of the S-allele specific genes, LAZY1-S and HRGP-S, were specifically expressed in styles and stamens, respectively, making them tristyly candidate genes. The M-locus contained one gene (LAZY1-M), homologous to LAZY1-S, that was present in the M-allele but absent from the m-allele. Estimates of allele ages are consistent with the prediction that the S-locus evolved before the M-locus. Re-use of the same gene family highlights the potential role of gene duplication in the evolution of epistatic multilocus polymorphisms.
... However, the molecular and functional characterization of the S-locus has been achieved only recently. The breakthrough occurred in Primula, where the S-locus comprises five genes known as S-genes (CCM T , GLO T , CYP T , PUM T , and KFB T ) and is hemizygous in thrums (S/0) but absent in pins (0/0; Figure 1a; Li et al., 2016;Potente, Léveillé-Bourret, et al., 2022). Four of the five S-genes (i.e., CCM T , GLO T , CYP T , and KFB T ) are the product of gene duplications, and their paralogs (named CCM1, GLO1, CYP734A51, and KFB1) have been localized in Primula veris, where they are scattered throughout the genome (Potente, Léveillé-Bourret, et al., 2022). ...
... The breakthrough occurred in Primula, where the S-locus comprises five genes known as S-genes (CCM T , GLO T , CYP T , PUM T , and KFB T ) and is hemizygous in thrums (S/0) but absent in pins (0/0; Figure 1a; Li et al., 2016;Potente, Léveillé-Bourret, et al., 2022). Four of the five S-genes (i.e., CCM T , GLO T , CYP T , and KFB T ) are the product of gene duplications, and their paralogs (named CCM1, GLO1, CYP734A51, and KFB1) have been localized in Primula veris, where they are scattered throughout the genome (Potente, Léveillé-Bourret, et al., 2022). The function of S-genes has been experimentally characterized only for GLO T and CYP T , which were recently shown to control key traits in thrum flowers: GLO T determines long anthers, while CYP T determines short stigma and female self-incompatibility (Huu et al., 2016(Huu et al., , 2020(Huu et al., , 2022. ...
... The recently published high-quality annotation of the five Sgenes and their four paralogs (Potente, Léveillé-Bourret, et al., 2022), combined with newly generated sequences of these nine genes extracted from WGR data of thrums and homostyles, provide an ideal opportunity to test how the genetic architecture of the S-locus and the transition to homostyly affect genetic variation and selection on S-genes and their paralogs. First, the thrum-specific segregation of the hemizygous S-locus should cause a 3/4th reduction of effective population size (Ne), lowering genetic diversity in S-genes (Huu et al., 2016). ...
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.
... The multiplicity of ontogenetic patterns 78,79 and sporophytic and gametophytic self-incompatibility systems or their lack 49,51,80-82 associated with style-length polymorphism suggest diverse evolutionary mechanisms underlying its origin. As a model system for the study of supergenes, advances in new genomic data sets and comparative analyses e.g., [83][84][85][86] are shedding light onto the molecular pathways of convergent evolution in independent stylelength polymorphic lineages, and our results can help to optimise the choice of future study systems. ...
Since the insights by Charles Darwin, heterostyly, a floral polymorphism with morphs bearing stigmas and anthers at reciprocal heights, has become a model system for the study of natural selection. Based on his archetypal heterostylous flower, including regular symmetry, few stamens and a tube, Darwin hypothesised that heterostyly evolved to promote outcrossing through efficient pollen transfer between morphs involving different areas of a pollinator’s body, thus proposing his seminal pollination-precision hypothesis. Here we update the number of heterostylous and other style-length polymorphic taxa to 247 genera belonging to 34 families, notably expanding known cases by 20%. Using phylogenetic and comparative analyses across the angiosperms, we show numerous independent origins of style-length polymorphism associated with actinomorphic, tubular flowers with a low number of sex organs, stamens fused to the corolla, and pollination by long-tongued insects. These associations provide support for the Darwinian pollination-precision hypothesis as a basis for convergent evolution of heterostyly across angiosperms.
... This implies that the transition to self-compatible and long-homostyle plants can occur through a single loss-of-function mutation in the dual-function gene as demonstrated in Primula 35 and here in Fagopyrum, instead of recombination as inferred from the classical heterozygous model. Moreover, CYP734A50 in Primula also originated by gene duplication before the evolution of heterostylous SI 36,37 . Thus, the evolution of heterostylous SI by a duplicated gene acquiring a dual role regulating style length and female compatibility, and its breakdown to self-compatible, long-homostyle plants by the disruption of this gene, may be common evolutionary pathways. ...
Common buckwheat, Fagopyrum esculentum, is an orphan crop domesticated in southwest China that exhibits heterostylous self-incompatibility. Here we present chromosome-scale assemblies of a self-compatible F. esculentum accession and a self-compatible wild relative, Fagopyrum homotropicum, together with the resequencing of 104 wild and cultivated F. esculentum accessions. Using these genomic data, we report the roles of transposable elements and whole-genome duplications in the evolution of Fagopyrum. In addition, we show that (1) the breakdown of heterostyly occurs through the disruption of a hemizygous gene jointly regulating the style length and female compatibility and (2) southeast Tibet was involved in common buckwheat domestication. Moreover, we obtained mutants conferring the waxy phenotype for the first time in buckwheat. These findings demonstrate the utility of our F. esculentum assembly as a reference genome and promise to accelerate buckwheat research and breeding.
... However, the molecular and functional characterization of the S-locus has been performed only recently. The breakthrough occurred in the Primula system, where the S-locus comprises five genes (CCM T ,CYP T , GLO T ,KFB T , and PUM T ) and is hemizygous in thrums (S/0) but absent in pins (0/0; Figure 1A; Liet al. , 2016;Potente et al. , 2022). Two S-locus genes were recently shown to control key traits in thrum flowers:GLO T determines high anthers, whileCYP T determines short stigma and self-incompatibility (Huu et al ., 2016;2022). ...
... Determining whether homostyly in P. vulgaris arose multiple times via independent mutations inCYP T exons or once through a shared structural rearrangement involving CYP T exons or a mutation in the CYP T promoter requires the mapping against a genomic reference of extensive genomic sequences covering both the S-locus and its upstream region. Both types of resources are now available from whole genome resequencing data (WGR) and published genomes for P. vulgaris (Cocker et al ., 2018) and its close relative P. veris (Potente et al ., 2022) Furthermore, the availability of WGR data and reference genomes in the selected study group facilitates the testing of population genetic predictions concerning the evolution of the entire S-locus and S-locus geneparalogs in thrums, pins and homostyles. First, the thrum-specific segregation of the hemizygous S-locus should cause a 3/4th reduction of effective population size (Ne ) (Huu et al., 2016), hence a decrease of genetic diversity in S-locus genes compared to the rest of the genome (Gutiérrez-Valencia et al. , 2021). ...
... On the other hand, similarly to what happens in the Y sex-chromosome (Gossmann et al ., 2011), selection to maintain function of S-locus genes and the exposure of recessive deleterious mutations under hemizygosity should enhance the efficacy of purifying selection. However, the extent to which the efficacy of purifying selection differs between genes within and outside the S-locus remains poorly understood (Potente et al ., 2022). Finally, the transition to homostyly could also reduce genetic diversity in S-locus genes due to increased homozygosity in homostyles (Mora-Carrera et al., 2021). ...
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-locus genes. Our results confirm the presence of previously reported homostyle-specific, loss-of-function mutations in the exons of the S-locus gene CYPᵀ , while also revealing a previously undetected structural rearrangement in CYPᵀ associated with the shift to homostyly. Additionally, we discovered that the promoter region of CYPᵀ in distylous and homostylous individuals is identical, suggesting that down-regulation of CYPᵀ via mutations in its promoter region is not a cause of shift to homostyly. Furthermore, we found that hemizygosity leads to reduced genetic diversity and less efficient purifying selection in S-locus genes compared to genes outside the S-locus, and that the shift to homostyly further lowers genetic diversity, as expected for mating-system shifts. 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 (diploid) copies of the S-locus might reduce homostyle viability.
... CYP734A50 determines style length and female mating type via inactivation of brassinosteroids (BR) [9,10]. Recent phylogenetic analyses of Primula's five S-genes suggest that four arose via independent duplication events followed by translocation to the pre-S-locus [11]. The S-locus has been characterized in Primula [2,[6][7][8], Turnera [3], and Linum [4]. ...
... CYP734A50 determines style length and female mating type via inactivation of brassinosteroids (BR) [9,10]. Recent phylogenetic analyses of Primula's five S-genes suggest that four arose via independent duplication events followed by translocation to the pre-S-locus [11]. ...
... The basis of style length and female mating type in both Primula and Turnera is inactivation of BR. Indirect alterations to the Phytochrome Interacting Factor (PIF) signaling hubs via inactivation of BR or direct alteration of PIF signaling hubrelated genes may be the basis of repression of style elongation in Fagopyrum, Primula, and Turnera [16], a hypothesis that has been computationally supported [11]. Auxin appears to play a role in stamen elongation in Fagopyrum [11], potentially similar to filament elongation in Turnera, as suggested by computational analysis [16]. ...
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.
... 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) 20-23 , 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. ...
... Phenotypic convergence in floral morphology appears to be mirrored by convergence in the genetic architecture of the locus controlling distyly. Specifically, in all studied species, distyly is controlled by a set of genes clustered together in the same genomic region, forming the so-called S-locus supergene, known to be hemizygous in S-morphs and absent from L-morphs in Primula, Fagopyrum Turnera, and Linum 12,17,19,20,24 . ...
... One of the most popular ornamental plants in Europe 27 , Primula (primrose) has served as the canonical model to study distyly since Darwin 2 . Extensive genomic resources are available for this genus, including a chromosomescale genome assembly for Primula veris, in which the S-locus is a ~ 260 kb region containing five genes (CCM T , GLO T , CYP T , PUM T , KFB T ) 12,17 . Two S-locus genes have been functionally characterized in Primula: GLO T , homologous to the highly-conserved B-class floral homeotic gene GLOBOSA, determines high anther position in S-morphs 15 and CYP T , a member of the cytochrome P450 CYP734A family that degrades brassinosteroids 28 , determines short styles 13 and female incompatibility in S-morphs 16 . ...
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 CYP T 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.
... In Primula, the entire S-locus has been characterized and is composed of five S-genes, CCM, GLO2, CYP734A50, PUM, and KFB, each apparently having been incorporated into the S-locus via independent duplication events [13][14][15]. Empirical evidence has demonstrated that CYP734A50 controls female morphology and the female mating type [16,17]. The mechanism by which CYP734A50 affects the female phenotype is by inactivating brassinosteroid (BR) to decrease active levels of this hormone in S-morph pistils [16]. ...
... Interestingly, seed set with self-pollination was always lower than with the outcrosses. Similar results were observed in Primula forbesii; knockdowns of the female determinant gene CYP734A50 resulted in individuals with altered mating types that set less seed when selfed than when outcrossed [14]. This may suggest an additional layer to SI, as wild heterostylous self-compatible populations of Primula oreodoxa [75], Hedyotis acutangula [76], Narcissus albimarginatus [77], and Ophiorrhiza japonica [78], to name a few species, show greater seed set when outcrossed than when selfed, or it may simply reflect inbreeding depression in these obligately outbreeding species. ...
In heterostylous, self-incompatible Turnera species, a member of the YUCCA gene family, YUC6, resides at the S-locus and has been hypothesized to determine the male mating type. YUCCA gene family members synthesize the auxin, indole-3-acetic acid, via a two-step process involving the TAA gene family. Consequently, it has been speculated that differences in auxin concentration in developing anthers are the biochemical basis underlying the male mating type. Here, we provide empirical evidence that supports this hypothesis. Using a transgenic knockdown approach, we show that YUC6 acts pleiotropically to control both the male physiological mating type and pollen size, but not the filament length dimorphism associated with heterostyly in Turnera. Using qPCR to assess YUC6 expression in different transgenic lines, we demonstrate that the level of YUC6 knockdown correlates with the degree of change observed in the male mating type. Further assessment of YUC6 expression through anther development, in the knockdown lines, suggests that the male mating type is irreversibly determined during a specific developmental window prior to microsporogenesis, which is consistent with the genetically sporophytic nature of this self-incompatibility system. These results represent the first gene controlling male mating type to be characterized in any species with heterostyly.
... Phenotypic convergence in oral morphology appears to be mirrored by convergence in the genetic architecture of the locus controlling distyly. Speci cally, in all studied species, distyly is controlled by a set of genes clustered together in the same genomic region, forming the so-called S-locus supergene, known to be hemizygous in S-morphs and absent from Lmorphs in Primula, Fagopyrum and Turnera [12][13][14][15] . ...
... One of the most popular ornamental plants in Europe 16 , Primula (primrose) has served as the canonical model to study distyly since Darwin 2 . Extensive genomic resources are available for this genus, including a chromosome-scale genome assembly for Primula veris, in which the S locus is a ~ 260 kb region containing ve genes (CCM T , GLO T , CYP T , PUM T , KFB T ) 12,13 . Two S-locus genes have been functionally characterized in Primula: GLO T , homologous to the highly-conserved B-class oral homeotic gene GLOBOSA, determines high anther position in S-morphs 17 and CYP T , a member of the cytochrome P450 CYP734A family which degrades brassinosteroids 18 , determines short styles 19 and female incompatibility in S-morphs 20 . ...
... The functions of the other three S-locus genes (CCM T , PUM T , KFB T ) remain unknown. Four S-locus genes originated via gene duplication, and their closest paralogs have been identi ed (CCM1, GLO1, CYP734A51, KFB1) 12,13,19 . A key open question on the evolution of distyly is how the S-locus genes acquired their role in controlling distyly. ...
Distyly is a floral dimorphism associated with a heteromorphic self-incompatibility mechanism that prevents inbreeding and promotes outcrossing in 28 angiosperm families. Distyly is controlled by a cluster of genes, i.e. the S-locus supergene, that evolved independently in all distylous species studied to date. Here we present a transcriptome atlas for Primula veris , the main model for studying distyly since Darwin, which helped to elucidate the mechanism through which the S-locus gene CYP T acquired its role in controlling style elongation. We also identified genes that are differentially expressed between the two floral morphs of P. veris and Fagopyrum esculentum , revealing the main molecular mechanisms and hormones underlying the expression of distyly in these two species. Further, we discovered shared homologous genes that likely control distyly in P. veris , F. esculentum and Turnera subulata , suggesting that the convergent evolution of distyly at the phenotypic level is coupled, to some extent, also at the molecular level. Additionally, we provided statistical support to the hypothesis that distyly supergenes of different species evolved by the recruitment of genes related to the phytochrome-interacting factor (PIF) signaling network. Overall, this is the first study to identify homologous genes that underlie the control of distyly in distantly-related taxa.
Secoviruses are single-stranded RNA viruses that infect plants. In the present study, we identified 61 putative novel secoviral genomes in various plant species by mining publicly available plant transcriptome data. These viral sequences represent the genomes of 13 monopartite and 48 bipartite secovirids. The genome sequences of 52 secovirids were coding-complete, and nine were partial. Except for small open reading frames (ORFs) determined in waikaviral genomes and RNA2 of torradoviruses, all of the recovered genomes/genome segments contained a large ORF encoding a polyprotein. Based on genome organization and phylogeny, all but three of the novel secoviruses were assigned to different genera. The genome organization of two identified waika-like viruses resembled that of the recently identified waika-like virus Triticum aestivum secovirus. Phylogenetic analysis revealed a pattern of host-virus co-evolution in a few waika- and waika-like viruses and increased phylogenetic diversity of nepoviruses. The study provides a basis for further investigation of the biological properties of these novel secoviruses.
