TY - JOUR A1 - Potente, Giacomo A1 - Léveillé-Bourret, Étienne A1 - Yousefi, Narjes A1 - Choudhury, Rimjhim Roy A1 - Keller, Barbara A1 - Diop, Seydina Issa A1 - Duijsings, Daniël A1 - Pirovano, Walter A1 - Lenhard, Michael A1 - Szövényi, Péter A1 - Conti, Elena T1 - Comparative genomics elucidates the origin of a supergene controlling floral heteromorphism JF - Molecular biology and evolution : MBE N2 - Supergenes are nonrecombining genomic regions ensuring the coinheritance of multiple, coadapted 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, heterostyly is characterized by the cooccurrence of two complementary, self-incompatible floral morphs and is controlled by five genes clustered in the hemizygous, ca. 300-kb S locus. Here, we present the first chromosome-scale genome assembly of any heterostylous species, that of Primula veris (cowslip). By leveraging the high contiguity of the P. veris assembly and comparative genomic analyses, we demonstrated that the S-locus evolved via multiple, asynchronous gene duplications and independent gene translocations. Furthermore, we discovered a new whole-genome duplication in Ericales that is specific to the Primula lineage. We also propose a mechanism for the origin of S-locus hemizygosity via nonhomologous recombination involving the newly discovered two pairs of CFB genes flanking the S locus. Finally, we detected only weak signatures of degeneration in the S locus, as predicted for hemizygous supergenes. The present study provides a useful resource for future research addressing key questions on the evolution of supergenes in general and the S locus in particular: How do supergenes arise? What is the role of genome architecture in the evolution of complex adaptations? Is the molecular architecture of heterostyly supergenes across angiosperms similar to that of Primula? KW - genome architecture KW - supergene KW - heterostyly KW - evolutionary genomics KW - chromosome-scale genome assembly KW - primula Y1 - 2022 U6 - https://doi.org/10.1093/molbev/msac035 SN - 0737-4038 SN - 1537-1719 VL - 39 IS - 2 PB - Oxford Univ. Press CY - Oxford ER - TY - GEN A1 - Huu, Cuong Nguyen A1 - Plaschil, Sylvia A1 - Himmelbach, Axel A1 - Kappel, Christian A1 - Lenhard, Michael T1 - Female self-incompatibility type in heterostylous Primula is determined by the brassinosteroid-inactivating cytochrome P450 CYP734A50 T2 - Current biology N2 - Most flowering plants are hermaphrodites, with flowers having both male and female reproductive organs. One widespread adaptation to limit self-fertilization is self-incompatibility (SI), where self-pollen fails to fertilize ovules.(1,2) In homomorphic SI, many morphologically indistinguishable mating types are found, although in heteromorphic SI, the two or three mating types are associated with different floral morphologies.(3-6) In heterostylous Primula, a hemizygous supergene determines a short-styled S-morph and a long-styled L-morph, corresponding to two different mating types, and full seed set only results from inter morph crosses.(7-9) Style length is controlled by the brassinosteroid (BR)-inactivating cytochrome P450 CYP734A50,(10) yet it remains unclear what defines the male and female incompatibility types. Here, we show that CYP734A50 also determines the female incompatibility type. Inactivating CYP734A50 converts short S-morph styles into long styles with the same incompatibility behavior as L-morph styles, and this effect can be mimicked by exogenous BR treatment. In vitro responses of S-and L-morph pollen grains and pollen tubes to increasing BR levels could only partly explain their different in vivo behavior, suggesting both direct and indirect effects of the different BR levels in S-versus L-morph stigmas and styles in controlling pollen performance. This BR-mediated SI provides a novel mechanism for preventing self-fertilization. The joint control of morphology and SI by CYP734A50 has important implications for the evolutionary buildup of the heterostylous syndrome and provides a straightforward explanation for why essentially all of the derived self-compatible homostylous Primula species are long homostyles.(11) KW - heteromorphic self-incompatibility KW - heterostyly KW - Primula forbesii KW - brassinosteroid KW - CYP734A50 KW - supergene KW - pleiotropy Y1 - 2022 U6 - https://doi.org/10.1016/j.cub.2021.11.046 SN - 0960-9822 SN - 1879-0445 VL - 32 IS - 3 SP - 671 EP - 676, E1-E5 PB - Cell Press CY - Cambridge, Mass. ER - TY - JOUR A1 - Huu, Cuong Nguyen A1 - Keller, Barbara A1 - Conti, Elena A1 - Kappel, Christian A1 - Lenhard, Michael T1 - Supergene evolution via stepwise duplications and neofunctionalization of a floral-organ identity gene JF - Proceedings of the National Academy of Sciences of the United States of America (PNAS) N2 - Heterostyly represents a fascinating adaptation to promote outbreeding in plants that evolved multiple times independently. While L-morph individuals form flowers with long styles, short anthers, and small pollen grains, S-morph individuals have flowers with short styles, long anthers, and large pollen grains. The difference between the morphs is controlled by an S-locus "supergene" consisting of several distinct genes that determine different traits of the syndrome and are held together, because recombination between them is suppressed. In Primula, the S locus is a roughly 300-kb hemizygous region containing five predicted genes. However, with one exception, their roles remain unclear, as does the evolutionary buildup of the S locus. Here we demonstrate that the MADS-box GLOBOSA2 (GLO2) gene at the S locus determines anther position. In Primula forbesii S-morph plants, GLO2 promotes growth by cell expansion in the fused tube of petals and stamen filaments beneath the anther insertion point; by contrast, neither pollen size nor male incompatibility is affected by GLO2 activity. The paralogue GLO1, from which GLO2 arose by duplication, has maintained the ancestral B-class function in specifying petal and stamen identity, indicating that GLO2 underwent neofunctionalization, likely at the level of the encoded protein. Genetic mapping and phylogenetic analysis indicate that the duplications giving rise to the style-length-determining gene CYP734A50 and to GLO2 occurred sequentially, with the CYP734A50 duplication likely the first. Together these results provide the most detailed insight into the assembly of a plant supergene yet and have important implications for the evolution of heterostyly. KW - heterostyly KW - Primula KW - supergene KW - gene duplication KW - neofunctionalization Y1 - 2020 U6 - https://doi.org/10.1073/pnas.2006296117 SN - 0027-8424 VL - 117 IS - 37 SP - 23148 EP - 23157 PB - National Academy of Sciences CY - Washington ER - TY - JOUR A1 - Kappel, Christian A1 - Cuong Nguyen Huu, A1 - Lenhard, Michael T1 - A short story gets longer: recent insights into the molecular basis of heterostyly JF - Journal of experimental botany N2 - Heterostyly is a fascinating adaptation to promote outbreeding and a classical paradigm of botany. In the most common type of heterostyly, plants either form flowers with long styles and short stamens, or short styles and long stamens. This reciprocal organ positioning reduces pollen wastage and promotes cross-pollination, thus increasing male fitness. In addition, in many heterostylous species selfing and the generation of unfit progeny due to inbreeding depression is limited by a self-incompatibility system, thus promoting female fitness. The two floral forms are genetically determined by the S locus as a complex supergene, namely a chromosomal region containing several individual genes that control the different traits, such as style or stamen length, and are held together by very tight linkage due to suppressed recombination. Recent molecular-genetic studies in several systems, including Turnera, Fagopyrum, Linum, and Primula have begun to identify and characterize the causal heterostyly genes residing at the S locus. An emerging theme from several families is that the dominant S haplotype represents a hemizygous region not present on the recessive s haplotype. This provides an explanation for the suppressed recombination and suggests a scenario for the chromosomal evolution of the S locus. In this review, we discuss the results from recent molecular-genetic analyses in light of the classical models on the genetics and evolution of heterostyly. KW - CYP734A50 KW - distyly KW - GLOBOSA2 KW - hemizygosity KW - heterostyly KW - Primula KW - S locus KW - supergene KW - tristyly Y1 - 2017 U6 - https://doi.org/10.1093/jxb/erx387 SN - 0022-0957 SN - 1460-2431 VL - 68 SP - 5719 EP - 5730 PB - Oxford Univ. Press CY - Oxford ER -