Darwin's studies on heterostyly in Primula described two floral morphs, pin and thrum, with reciprocal anther and stigma heights that promote insect-mediated cross-pollination. This key innovation evolved independently in several angiosperm families. Subsequent studies on heterostyly in Primula contributed to the foundation of modern genetic theory and the neo-Darwinian synthesis. The established genetic model for Primula heterostyly involves a diallelic S locus comprising several genes, with rare recombination events that result in self-fertile homostyle flowers with anthers and stigma at the same height. Here we reveal the S locus supergene as a tightly linked cluster of thrum-specific genes that are absent in pins. We show that thrums are hemizygous not heterozygous for the S locus, which suggests that homostyles do not arise by recombination between S locus haplotypes as previously proposed. Duplication of a floral homeotic gene 51.7 million years (Myr) ago, followed by its neofunctionalization, created the current S locus assemblage which led to floral heteromorphy in Primula. Our findings provide new insights into the structure, function and evolution of this archetypal supergene.
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Barrett, S. C. H. The evolution of plant sexual diversity. Nat. Rev. Genet. 3, 274–284 (2002).
Richards, A. J. Primula 2nd edn (Batsford, 2002).
Darwin, C. R. On the two forms or dimorphic condition in the species of Primula, and on their remarkable sexual relations. J. Proc. Linn. Soc. Bot. 6, 77–96 (1862).
Gregory, R. P., De Winton, D. & Bateson, M. A. Genetics of Primula sinensis. J. Genet. 13, 219–253 (1923).
Bateson, W. & Gregory, R. P. On the inheritance of heterostylism in Primula. Proc. R. Soc. Lond. B 76, 581–586 (1905).
Bridges, C. B. The chromosome hypothesis of linkage applied to cases in sweetpeas and Primula. Am. Nat. 48, 524–534 (1914).
Ernst, A. Weitere untersuchungen zur phänanalyse zum fertilitätsproblem und zur genetik heterostyler primeln. II. Primula hortensis. Arch. Julius Klaus Stift. Vererbungsforsch. Sozialanthropol. Rassenhyg. 11, 1–280 (1936).
Ernst, A. Heterostylie-Forschung versuche zur genetischen analyse eines organisations und ‘Anpassungs’ merkmales. Z. Induk. Abstamm. Vererbungsl. 71, 156–230 (1936).
De Winton, D. & Haldane, J. B. S. The genetics of Primula sinensis. III. Linkage in the diploid. J. Genet. 31, 67–100 (1935).
Darlington, C. D. Meiosis in diploid and tetraploid Primula sinensis. J. Genet. 24, 65–95 (1931).
Mather, K. The genetical architecture of heterostyly in Primula sinensis. Evolution 4, 340–352 (1950).
Schwander, T., Libbrecht, R. & Keller, L. Supergenes and complex phenotypes. Curr. Biol. 24, R288–R294 (2014).
Darwin, C. R. The Different Forms of Flowers on Plants of the Same Species (John Murray, 1877).
Dodd, M. E., Silvertown, J. & Chase, M. W. Phylogenetic analysis of trait evolution and species diversity variation among angiosperm families. Evolution 53, 732–744 (1999).
Webster, M. A. & Gilmartin, P. M. Analysis of late stage flower development in primula vulgaris reveals novel differences in cell morphology and temporal aspects of floral heteromorphy. New Phytol. 171, 591–603 (2006).
Shivanna, K. R., Heslop-Harrison, J. & Heslop-Harrison, Y. Heterostyly in primula. 2. Sites of pollen inhibition, and effects of pistil constituents on compatible and incompatible pollen tube growth. Protoplasma 107, 319–337 (1981).
Richards, A. J. & Ibrahim, H. B. The breeding system in primula veris L .II. pollen-Tube growth and seed-Set. New Phytol. 90, 305–314 (1982).
Lewis, D. Comparative incompatibility in angiosperms and fungi. Adv. Genet. 6, 235–285 (1954).
Dowrick, V. P. J. Heterostyly and homostyly in Primula obconica. Heredity 10, 219–236 (1956).
Lloyd, D. G. & Webb, C. J. in Evolution and Function of Heterostyly (ed. Barrett, S. C. H. ) 151–175 (Springer Verlag, 1992).
Charlesworth, D. & Charlesworth, B. Model for the evolution of distyly. Am. Nat. 114, 467–498 (1979).
Bodmer, W. F. The genetics of homostyly in populations of Primula vulgaris. Phil. Trans. R. Soc. Lond. B 242, 517–549 (1960).
Fisher, R. A. A theoretical system of selection for homostyle. Primula Sankhya. 9, 325–342 (1949).
Piper, J. G., Charlesworth, B. & Charlesworth, D. A high-rate of self-fertilization and increased seed fertility of homostyle primroses. Nature. 310, 50–51 (1984).
Crosby, J. L. High proportions of homostyle plants in populations of Primula vulgaris. Nature. 145, 672–673 (1940).
Crosby, J. L. Selection of an unfavourable gene complex. Evol. Ecol. Res. 3, 212–230 (1949).
Webster, M. A. & Gilmartin, P. M. A comparison of early floral ontogeny in wild-type and floral homeotic mutant phenotypes of Primula. Planta 216, 903–917 (2003).
McCubbin, A. G., Lee, C. & Hetrick, A. Identification of genes showing differential expression between morphs in developing flowers of Primula vulgaris. Sex. Plant Reprod. 19, 63–72 (2006).
Li, J., Webster, M. A., Furuya, M. & Gilmartin, P. M. Identification and characterization of pin and thrum alleles of two genes that co-segregate with the Primula S locus. Plant J. 51, 18–31 (2007).
Manfield, I. W. et al. Molecular characterization of DNA sequences from the Primula vulgaris S locus. J. Exp. Bot. 56, 1177–1188 (2005).
Cocker, J. et al. Oakleaf: an S locus-linked mutation of Primula vulgaris that affects leaf and flower development. New Phytol. 208, 149–161 (2015).
Li, J. et al. Hose in Hose, an S locus-linked mutant of Primula vulgaris is caused by an unstable mutation at the Globosa locus. Proc. Natl Acad. Sci. USA 107, 5664–5668 (2010).
Li, J. et al. The S locus-linked Primula homeotic mutant sepaloid shows characteristics of a B-function mutant but does not result from mutation in a B-function gene. Plant J. 56, 1–12 (2008).
Yoshida, Y. et al. QTL analysis of heterostyly in Primula sieboldii and its application for morph identification in wild populations. Ann. Bot. 108, 133–142 (2011).
Li, J. et al. Integration of genetic and physical maps of the Primula vulgaris S locus and localization by chromosome in situ hybridisation. New Phytol. 208, 137–148 (2015).
Nowak, M. D. et al. The draft genome of Primula veris yields insight into the molecular basis of heterostyly. Genome Biol. 16, 16 (2015).
Verhoef, N. et al. Brassinosteroid biosynthesis and signalling in Petunia hybrida. J. Exp. Bot. 64, 2435–2448 (2013).
Turk, E. M. et al. CYP72B1 inactivates brassinosteroid hormones: an intersection between photomorphogenesis and plant steroid signal transduction. Plant Physiol. 133, 1643–1653 (2003).
Abbasi, N., Park, Y.-I. & Choi, S.-B. Pumilio Puf domain RNA-binding proteins in Arabidopsis. Plant Signal. Behav. 6, 364–368 (2011).
Kim, H. J., Chiang, Y.-H., Kieber, J. J. & Schaller, G. E. SCFKMD controls cytokinin signaling by regulating the degradation of type-B response regulators. Proc. Natl Acad. Sci. USA 110, 10028–10033 (2013).
Webster, M. A. & Grant, C. J. The inheritance of calyx morph variants in Primula vulgaris (Huds). Heredity 64, 121–124 (1990).
Viaene, T. et al. Pistillata-duplications as a mode for floral diversification in (Basal) asterids. Mol. Biol. Evol. 26, 2627–2645 (2009).
Xia, X. DAMBE5: a comprehensive software package for data analysis in molecular biology and evolution. Mol. Biol. Evol. 30, 1720–1728 (2013).
Magallón, S., Gómez-Acevedo, S., Sánchez-Reyes, L. L. & Hernández-Hernández, T. A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity. New Phytol. 207, 437–453 (2015).
Bell, C. D., Soltis, D. E. & Soltis, P. S. The age and diversification of the angiosperms re-revisited. Am. J. Bot. 97, 1296–1303 (2010).
Mast, A. R. et al. Phylogenetic relationships in Primula L. and related genera (Primulaceae) based on noncoding chloroplast DNA. Int. J. Plant Sci. 162, 1381–1400 (2001).
Joron, M. et al. Chromosomal rearrangements maintain a polymorphic supergene controlling butterfly mimicry. Nature 477, 203–206 (2011).
Thomas, J. W. et al. The chromosomal polymorphism linked to variation in social behavior in the white-throated sparrow (Zonotrichia albicollis) is a complex rearrangement and suppressor of recombination. Genetics 179, 1455–1468 (2008).
Wang, J. et al. A Y-like social chromosome causes alternative colony organization in fire ants. Nature 493, 664–668 (2013).
Turgeon, B. G. & Yoder, O. C. Proposed nomenclature for mating type genes of filamentous ascomycetes. Fungal Genet. Biol. 31, 1–5 (2000).
We thank M. Lappage, M. Hughes and P. Wells for horticultural support; colleagues at TGAC for Illumina sequencing; A. Thanki for TGAC Browser support; O. Kent for P. elatior GLO and GLOT sequences; Norfolk Wildlife Trust, Suffolk Wildlife Trust and Norfolk County Council for permission to sample P. veris, P. elatior and P. vulgaris respectively; M. Gage, B. Davies and D. Bowles for comments on the manuscript; W. Wang for advice on k-means analysis; BBSRC for funding via grant BB/H019278/2, and prior awards G11027 and P11021; The Gatsby Foundation for early stage funding; University of Leeds, Durham University and University of East Anglia for support to P.M.G. over several years of the project. CvO was funded by the Earth & Life Systems Alliance (ELSA). P.M.G.'s laboratory is hosted at the John Innes Centre under the UEA-JIC Norwich Research Park collaboration.
The authors declare no competing financial interests.
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Li, J., Cocker, J., Wright, J. et al. Genetic architecture and evolution of the S locus supergene in Primula vulgaris. Nature Plants 2, 16188 (2016). https://doi.org/10.1038/nplants.2016.188