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Evolution of Self-Incompatibility in the Brassicaceae Evolution of self-incompatibility in the Brassicaceae: Lessons from a textbook example of natural selection Éléonore Durand, Maxime Chantreau, Audrey Le Veve, Roman Stetsenko, Manu Dubin, Mathieu Genete, Violaine Llaurens, Céline Poux, Camille Roux, Sylvain Billiard, et al. To cite this version: Éléonore Durand, Maxime Chantreau, Audrey Le Veve, Roman Stetsenko, Manu Dubin, et al.. Evolu- tion of self-incompatibility in the Brassicaceae: Lessons from a textbook example of natural selection. Evolutionary Applications, Blackwell, 2020, 10.1111/eva.12933. hal-02784711 HAL Id: hal-02784711 https://hal.archives-ouvertes.fr/hal-02784711 Submitted on 4 Jun 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Received: 15 November 2019 | Revised: 25 January 2020 | Accepted: 29 January 2020 DOI: 10.1111/eva.12933 SPECIAL ISSUE REVIEW AND SYNTHESES Evolution of self-incompatibility in the Brassicaceae: Lessons from a textbook example of natural selection Eléonore Durand1 | Maxime Chantreau1 | Audrey Le Veve1 | Roman Stetsenko1 | Manu Dubin1 | Mathieu Genete1 | Violaine Llaurens2 | Céline Poux1 | Camille Roux1 | Sylvain Billiard1 | Xavier Vekemans1 | Vincent Castric1 1CNRS, Univ. Lille, UMR 8198 - Evo-Eco- Paleo, F-59000 Lille, France Abstract 2Institut de Systématique, Evolution et Self-incompatibility (SI) is a self-recognition genetic system enforcing outcrossing in Biodiversité (ISYEB), Muséum national hermaphroditic flowering plants and results in one of the arguably best understood d'Histoire naturelle, CNRS, Sorbonne Université, EPHE, Université des Antilles CP forms of natural (balancing) selection maintaining genetic variation over long evo- 50, 57 rue Cuvier, 75005 Paris, France lutionary times. A rich theoretical and empirical population genetics literature has Correspondence considerably clarified how the distribution of SI phenotypes translates into fitness Eléonore Durand, CNRS, Univ. Lille, UMR differences among individuals by a combination of inbreeding avoidance and rare- 8198 - Evo-Eco-Paleo, F-59000 Lille, France. Email: [email protected] allele advantage. At the same time, the molecular mechanisms by which self-pollen is specifically recognized and rejected have been described in exquisite details in Funding information European Research Council, Grant/Award several model organisms, such that the genotype-to-phenotype map is also pretty Number: 648321; Agence Nationale de la well understood, notably in the Brassicaceae. Here, we review recent advances in Recherche, Grant/Award Number: ANR-11- JSV7-008 these two fronts and illustrate how the joint availability of detailed characterization of genotype-to-phenotype and phenotype-to-fitness maps on a single genetic sys- tem (plant self-incompatibility) provides the opportunity to understand the evolu- tionary process in a unique perspective, bringing novel insight on general questions about the emergence, maintenance, and diversification of a complex genetic system. KEYWORDS allelic diversification, balancing selection, dominance/recessivity interactions, plant mating systems, sexual reproduction 1 | INTRODUCTION physical proximity with the entry of female reproductive tracts (the stigma). It follows that the structure of this reproductive organ can The flower is the defining organ of angiosperms and is associated cause self-pollination to be very common, such that the potential with the spectacular diversification of this group of plants (Soltis & for sexual reproduction by selfing is high. To avoid the deleterious Soltis, 2014). While flowers in extant species display an astonishing effects of inbreeding depression (Charlesworth & Charlesworth, diversity of sizes, shapes, colors, and functions, a central feature of 1987), reproductive mechanisms preventing selfing have been re- their ancestral state, hermaphroditism, has remained widespread peatedly selected in the course of evolution (Barrett, 2010). Yet, the (Sauquet et al., 2017), bringing pollen-producing anthers in close transition from outcrossing to selfing is one of the most commonly This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2020 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd Evolutionary Applications. 2020;00:1–19. wileyonlinelibrary.com/journal/eva | 1 2 | DURAND ET AL. observed evolutionary transitions in flowering plants. In fact, a sub- In recent years, the field has been in the unique situation to merge stantial part of the developmental and morphological diversity of these two scientific communities and take advantage of a genetic flowers is believed to be driven by these reproductive strategies system in which the genotype-to-phenotype relationship has been along the selfing-outcrossing continuum (Barrett, 2010). considerably clarified, in a context where the phenotype-to-fitness Self-incompatibility (SI) is a widespread mechanism to avoid self- map is also properly understood. Building upon these strong foun- ing in flowering plants, whereby fertile plants are capable of self-pol- dations, our group, along with others, has contributed to a better len recognition and rejection and require compatible outcross pollen understanding of how SI phenotypes are controlled at the molecu- to produce seeds. At the phenotypic level, SI is typically determined lar level and a more precise understanding of how natural selection by the segregation of a finite (often large) number of mating types, maintains the system in spite of the many forces that could lead to corresponding to as many distinct pollen–stigma recognition speci- its disruption, eventually allowing its long-term diversification in nat- ficities. Beyond the sole avoidance of self-fertilization, SI thus also ural populations. prevents fertilization between unrelated individuals expressing Here, we review this set of recent advances to illustrate how the identical recognition specificities (de Nettancourt, 1977). In popu- study of such a model system can provide insight into more general lations where the number of such specificities is small, the seed set biological phenomena such as the emergence of evolutionary nov- can thus be impaired, potentially causing viability issues in endan- elty in a complex genetic system and the evolution of dominance. gered species (Wagenius, Lonsdorf, & Neuhauser, 2007). We highlight areas where more discoveries are likely to be made in SI has been a model biological system in two distinct scientific the future. We focus in particular on how the scientific questions in communities. First in the plant molecular biology community, who the field have matured, spanning from the study of the signatures developed SI as a model for how cells perceive external stimuli (self of natural selection to the emergence of functional and regulatory vs. outcross pollen) and mount a specific and appropriate cellular re- novelties. sponse (pollen tube rejection vs. acceptance). Identification of the SI genes in a handful of plant families revealed entirely different molecular and physiological processes, making it clear that SI arose 2 | THE RISE AND FALL OF SI SYSTEMS: independently several times (Franklin-Tong, 2008). Much progress THE SI GENES ARE MORE LABILE THAN WE has been done in the last 15 years in some of these families toward THOUGHT a clearer understanding of how SI is controlled. In Brassicaceae, for example, SI is controlled by a highly diversified allelic series made of 2.1 | Conditions for the maintenance of SI are co-adapted receptor–ligand combinations encoded by tightly linked drastically restricted by a variety of different genes in the so-called “S-locus” (generally SCR/SP11 and SRK that processes, leaving the existence of SI species an encode for male and female specificities, respectively, Kusaba et al., evolutionary puzzle 2001; Schopfer, Nasrallah, & Nasrallah, 1999; but see below for some interesting exceptions). The pollen determinant of SI is sporophyti- SI is one of many strategies (e.g., herkogamy, dichogamy, dicliny, cally controlled by the paternal parent and involves complex dom- etc…) by which plants favor outcrossing and avoid selfing or crossing inance interactions between SI alleles in heterozygotes (reviewed between related individuals (Barrett, 2002). Hence, self-incompati- in Fujii & Takayama, 2018; Schoen & Busch, 2009). In Petunia, in bility is thought to have evolved in response to the negative selec- contrast, SI is achieved by a very different mechanism involving tion generated by inbreeding depression, caused by the expression complex non-self-recognition, where several linked paralogs game- of recessive deleterious alleles in homozygotes (Charlesworth & tophytically expressed in the pollen tube collectively determine the Charlesworth, 1987). The conditions allowing the maintenance of spectrum of recognition specificities (Fuji, Kubo, & Takayama, 2016). SI are linked to the relative fitness of SI individuals
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