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Supergene Evolution Via Stepwise Duplications and Neofunctionalization of a Floral-Organ Identity Gene

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Supergene Evolution Via Stepwise Duplications and Neofunctionalization of a Floral-Organ Identity Gene Supergene evolution via stepwise duplications and neofunctionalization of a floral-organ identity gene Cuong Nguyen Huua, Barbara Kellerb, Elena Contib, Christian Kappela, and Michael Lenharda,1 aInstitute for Biochemistry and Biology, University of Potsdam, D-14476 Potsdam-Golm, Germany; and bDepartment of Systematic and Evolutionary Botany, University of Zurich, CH-8008 Zurich, Switzerland Edited by June B. Nasrallah, Cornell University, Ithaca, NY, and approved August 5, 2020 (received for review April 7, 2020) Heterostyly represents a fascinating adaptation to promote out- addition, self-incompatibility is present in many distylous species breeding in plants that evolved multiple times independently. (9). In all examined cases, distyly is under simple Mendelian While L-morph individuals form flowers with long styles, short genetic control, with a dominant and a recessive haplotype at the anthers, and small pollen grains, S-morph individuals have flowers single S locus determining the morphs (10). With a few excep- with short styles, long anthers, and large pollen grains. The differ- tions, the dominant S haplotype causes S-morph and the reces- ence between the morphs is controlled by an S-locus “supergene” sive s haplotype L-morph flowers. Rather than a single gene, the consisting of several distinct genes that determine different traits S locus represents a supergene, that is, a chromosomal region of the syndrome and are held together, because recombination with at least two tightly linked genes that determine the different between them is suppressed. In Primula, the S locus is a roughly aspects of a coadapted set of phenotypes (10–12). Similar su- 300-kb hemizygous region containing five predicted genes. How- pergenes underlie many fascinating coadapted phenotypes in ever, with one exception, their roles remain unclear, as does the plants and animals (13–16), and their evolutionary buildup is evolutionary buildup of the S locus. Here we demonstrate that the often only incompletely understood. MADS-box GLOBOSA2 (GLO2) gene at the S locus determines an- The primrose genus Primula is the most studied model for ther position. In Primula forbesii S-morph plants, GLO2 promotes distyly (17). Primula flowers show reciprocal herkogamy, pollen growth by cell expansion in the fused tube of petals and stamen polymorphism, and self-incompatibility, with the dominant S and filaments beneath the anther insertion point; by contrast, neither recessive s haplotypes producing S- and L-morph flowers, re- pollen size nor male incompatibility is affected by GLO2 activity. spectively (3, 18, 19). Based on classical genetic studies, the S PLANT BIOLOGY GLO1 GLO2 The paralogue , from which arose by duplication, has locus supergene has been proposed to contain at least three maintained the ancestral B-class function in specifying petal and separable individual loci: G, controlling style length; A, deter- GLO2 stamen identity, indicating that underwent neofunctionali- mining anther position; and P, controlling pollen size and zation, likely at the level of the encoded protein. Genetic mapping number (10). Style length and female-compatibility type have and phylogenetic analysis indicate that the duplications giving rise CYP734A50 GLO2 never been genetically separated (20, 21); by contrast, male to the style-length-determining gene and to oc- compatibility is likely controlled by a locus distinct from A and P curred sequentially, with the CYP734A50 duplication likely the (21, 22). At the molecular level, the dominant S-locus haplotype first. Together these results provide the most detailed insight into represents a roughly 280-kb-long genomic segment that is the assembly of a plant supergene yet and have important impli- hemizygous; specifically, it is present only on the chromosome cations for the evolution of heterostyly. with the S haplotype but missing from the chromosome with the recessive s haplotype (23–25). Five genes have been predicted to heterostyly | Primula | supergene | gene duplication | neofunctionalization Significance lowering plants have evolved many different adaptations to Fpromote efficient cross-pollination (1, 2). Some of the most fascinating of these are found in the group of stylar polymor- Heterostyly is an adaptation to promote outbreeding in plants. phisms that often combine reciprocal herkogamy with self- In heterostylous primroses, plants form flowers either with incompatibility (1). Individuals of species with stylar polymor- long styles and low anthers or with short styles and high an- phism fall into two or three classes, or morphs, that differ in their thers. This difference is due to a chromosomal segment con- taining five predicted genes, yet their roles and the evolution arrangement of male and female reproductive organs. In par- of this segment remain unclear. Here we identify the gene ticular, male and female organs are physically separated within a responsible for raising the anthers in short-styled flowers. This flower, and this herkogamy is reciprocal between the morphs in gene arose by duplication from a classical floral-organ identity most species, with anthers in one morph located in the analogous gene and gained a novel function. Surprisingly, the responsible position to the style in the other, and vice versa. As a result, pollen chromosomal segment appears to have evolved by stepwise from the different morphs is deposited in a spatially segregated gene duplications rather than duplication of an entire chro- manner on the bodies of pollinators (3), resulting in preferential mosomal block. These findings thus provide detailed insight cross-pollination between the morphs and preventing pollen into the evolution of complex polymorphisms involving dif- wastage and the formation of less fit inbred progeny. Often, re- ferent individual traits. ciprocal herkogamy is complemented by self-incompatibility to prevent self-fertilization; with only two or three compatibility types Author contributions: C.N.H., B.K., E.C., C.K., and M.L. designed research; C.N.H., B.K., and corresponding to the different morphs this manifests as an intra- C.K. performed research; C.N.H., B.K., C.K., and M.L. analyzed data; and M.L. wrote morph incompatibility (4, 5). the paper. An intensively studied stylar polymorphism is heterostyly The authors declare no competing interest. (6–8). In the simplest case, distyly, individuals either form This article is a PNAS Direct Submission. flowers with short styles and high anthers (S-morph) or flowers Published under the PNAS license. with long styles and low anthers (L-morph). Additional poly- 1To whom correspondence may be addressed. Email: [email protected]. morphisms can be associated with this reciprocal herkogamy; for This article contains supporting information online at https://www.pnas.org/lookup/suppl/ example, in many species S-morph flowers produce larger, but doi:10.1073/pnas.2006296117/-/DCSupplemental. fewer, pollen grains compared to L-morph flowers (9). In www.pnas.org/cgi/doi/10.1073/pnas.2006296117 PNAS Latest Articles | 1of10 Downloaded by guest on October 1, 2021 reside in this 280-kb segment based on its sequence in Primula brassinosteroids, a class of phytohormones promoting cell elon- vulgaris and the closely related Primula veris (25). This archi- gation, and thus suppresses style elongation in S-morph flowers. tecture of the S locus with a large hemizygous region appears to Despite this important progress, a number of key questions be conserved in five species belonging to different clades of the remain unanswered. One concerns the identity of the other two genus Primula (25), yet whether all five predicted genes are genetically defined loci, A and P, which determine anther posi- present at the S locus throughout the different Primula species is tion and pollen size, respectively. The GLO2 gene represents a unknown. The five genes predicted in P. vulgaris and P. veris are plausible candidate for the A locus; in fact, a transposon inser- tion in GLO2 of P. vulgaris has been reported to result in a short- CYP734A50, encoding a cytochrome P450; GLOBOSA2 (also homostyle phenotype (23). However, no description of the mutant known as GLOT), coding for a B-class homoeotic MADS- phenotype has been provided, nor has this finding been confirmed domain transcription factor; a KELCH F-BOX PROTEIN by an independent allele. Thus, the identity of the GLO2 gene (KFBT) gene; a gene encoding a PUMILIO RNA-binding pro- T with the A locus remains to be firmly established. As for P,no tein (PUM ); and a gene encoding a CONSERVED C-TER- information is currently available about its molecular nature. T MINAL DOMAIN (CCM ) protein. [Naming of the genes The second major unresolved question concerns the evolu- follows priority regarding their first publications (23, 26, 27).] Of tionary buildup of the S locus, both regarding its chromosomal these, CYP734A50 has been shown to correspond to the G locus assembly and the sequence of trait changes. Clear paralogues of (26). The encoded cytochrome P450 monooxygenase inactivates CYP734A50, GLO2, and CCMT are found outside of the S locus, A B C ns ns GLO1 GLO2 ns *** Relative expression of Relative expression of GLO2 GLO2 GLO2 GLO2 L-morph L-morph S-morph S-morph S-morph S-morph L-morph L-morph VIGS-GLO2 VIGS-GLO2 L-morph VIGS- L-morph VIGS- S-morph VIGS- S-morph VIGS- DFEGH ns *** 6.0 2.5 40 * 4.0 * *** *** 2.0 30 *** *** 30 3.0 4.0 *** 1.5 *** *** 20 2.0 1.0 20 2.0 Anther height (mm) 1.0 0.5 10 Length of corolla tube (mm) 10 Cell length (below anther) (µm) Cell length (above anther) (µm) Diameter of corolla mouth mm) 0.0 0.0 0.0 GLO2 GLO2 GLO2 GLO2 GLO2 L-morph L-morph L-morph S-morph S-morph L-morph S-morph S-morph L-morph S-morph S-morph VIGS- S-morph VIGS- S-morph VIGS- S-morph VIGS- S-morph VIGS- Fig. 1. VIGS of GLO2 results in short-homostylous flowers.
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