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 - 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 -