Supergene evolution via stepwise duplications and neofunctionalization of a floral-organ identity gene
- 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 maleHeterostyly 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.…
Verfasserangaben: | Cuong Nguyen HuuORCiD, Barbara KellerORCiD, Elena ContiORCiD, Christian KappelORCiDGND, Michael LenhardORCiDGND |
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DOI: | https://doi.org/10.1073/pnas.2006296117 |
ISSN: | 0027-8424 |
Pubmed ID: | https://pubmed.ncbi.nlm.nih.gov/32868445 |
Titel des übergeordneten Werks (Englisch): | Proceedings of the National Academy of Sciences of the United States of America (PNAS) |
Verlag: | National Academy of Sciences |
Verlagsort: | Washington |
Publikationstyp: | Wissenschaftlicher Artikel |
Sprache: | Englisch |
Datum der Erstveröffentlichung: | 31.08.2020 |
Erscheinungsjahr: | 2020 |
Datum der Freischaltung: | 01.06.2023 |
Freies Schlagwort / Tag: | Primula; gene duplication; heterostyly; neofunctionalization; supergene |
Band: | 117 |
Ausgabe: | 37 |
Seitenanzahl: | 10 |
Erste Seite: | 23148 |
Letzte Seite: | 23157 |
Fördernde Institution: | Deutsche ForschungsgemeinschaftGerman Research Foundation (DFG); [Le1412/19-1]; Schweizerischer NationalfondsSwiss National Science; Foundation (SNSF) [31003A_175556]; Claraz Foundation |
Organisationseinheiten: | Mathematisch-Naturwissenschaftliche Fakultät / Institut für Biochemie und Biologie |
DDC-Klassifikation: | 5 Naturwissenschaften und Mathematik / 57 Biowissenschaften; Biologie / 570 Biowissenschaften; Biologie |
Peer Review: | Referiert |