Paternity Tests Support a Diallelic Self-Incompatibility System in a Wild Olive (Olea Europaea Subsp. Laperrinei, Oleaceae)

Paternity Tests Support a Diallelic Self-Incompatibility System in a Wild Olive (Olea Europaea Subsp. Laperrinei, Oleaceae)

Paternity tests support a diallelic self-incompatibility system in a wild olive (Olea europaea subsp. laperrinei, Oleaceae) Guillaume Besnard, Pierre-olivier Cheptou, Malik Debbaoui, Pierre Lafont, Bernard Hugueny, Julia Dupin, Djamel Baali-cherif To cite this version: Guillaume Besnard, Pierre-olivier Cheptou, Malik Debbaoui, Pierre Lafont, Bernard Hugueny, et al.. Paternity tests support a diallelic self-incompatibility system in a wild olive (Olea europaea subsp. laperrinei, Oleaceae). Ecology and Evolution, Wiley Open Access, 2020, 10 (4), pp.1876-1888. 10.1002/ece3.5993. hal-02627180 HAL Id: hal-02627180 https://hal.archives-ouvertes.fr/hal-02627180 Submitted on 26 May 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: 24 October 2019 | Revised: 16 December 2019 | Accepted: 20 December 2019 DOI: 10.1002/ece3.5993 ORIGINAL RESEARCH Paternity tests support a diallelic self-incompatibility system in a wild olive (Olea europaea subsp. laperrinei, Oleaceae) Guillaume Besnard1 | Pierre-Olivier Cheptou2 | Malik Debbaoui1 | Pierre Lafont1 | Bernard Hugueny1 | Julia Dupin1 | Djamel Baali-Cherif3 1EDB, UMR 5174, CNRS-IRD-UPS, Université Paul Sabatier, Toulouse cedex, Abstract France Self-incompatibility (SI) is the main mechanism that favors outcrossing in plants. By 2 CEFE, Univ Montpellier, CNRS, EPHE, IRD, limiting compatible matings, SI interferes in fruit production and breeding of new Univ Paul Valery Montpellier 3, Montpellier, France cultivars. In the Oleeae tribe (Oleaceae), an unusual diallelic SI system (DSI) has been 3Laboratoire de Recherche sur les Zones proposed for three distantly related species including the olive (Olea europaea), but Arides, USTHB/ENSA, Alger, Algeria empirical evidence has remained controversial for this latter. The olive domestication Correspondence is a complex process with multiple origins. As a consequence, the mixing of S-alleles Guillaume Besnard and Djamel Baali-Cherif, Laboratoire de Recherche sur les Zones from two distinct taxa, the possible artificial selection of self-compatible mutants and Arides, USTHB/ENSA, BP44, Alger, Algeria. the large phenological variation of blooming may constitute obstacles for decipher- Emails: [email protected] (GB); [email protected] (DB) ing SI in olive. Here, we investigate cross-genotype compatibilities in the Saharan wild olive (O. e. subsp. laperrinei). As this taxon was geographically isolated for thou- Funding information ERA-NET BiodivERsA INFRAGECO, Grant/ sands of years, SI should not be affected by human selection. A population of 37 Award Number: ANR-16-EBI3-0014; Labex mature individuals maintained in a collection was investigated. Several embryos per TULIP, Grant/Award Number: ANR-10- LABX-0041 mother were genotyped with microsatellites in order to identify compatible fathers that contributed to fertilization. While the pollination was limited by distance inside the collection, our results strongly support the DSI hypothesis, and all individuals were assigned to two incompatibility groups (G1 and G2). No self-fertilization was observed in our conditions. In contrast, crosses between full or half siblings were frequent (ca. 45%), which is likely due to a nonrandom assortment of related trees in the collection. Finally, implications of our results for orchard management and the conservation of olive genetic resources are discussed. KEYWORDS diallelic self-incompatibility system, microsatellites, Olea europaea L., Oleaceae, paternity 1 | INTRODUCTION concerned (ca. 40% of angiosperms) belong to distantly related fam- ilies, such as Brassicaceae, Rosaceae, or Solanaceae (Igic, Lande, & Self-incompatibility (SI) is the main mechanism that prevents self-fer- Kohn, 2008; de Nettancourt, 1977; Taiz et al., 2015). In addition to tilization and promotes outcrossing in flowering plants (Taiz, Zeiger, preventing self-fertilization, SI can also act as a barrier between in- Moller, & Murphy, 2015). A few, independent evolution events dividuals sharing the same SI phenotype and, thus, influences pol- of SI have been documented, and the self-incompatible lineages len-mediated gene flow by limiting compatible matings (Bateman, 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. Ecology and Evolution published by John Wiley & Sons Ltd. 1876 | www.ecolevol.org Ecology and Evolution. 2020;10:1876–1888. BESNARD ET AL. | 1877 1952). Moreover, by interfering with plant production and breeding, of varieties (with the possible vegetative propagation of SI mutants), SI is a major obstacle for constant fruit production in crop species pollen contamination, and neglection of stigma receptivity (with large (Sassa, 2016), as well as for the breeding of new cultivars and the phenological variations among cultivars and years), could also all ex- development of inbred lines (Matsumoto, 2014). Deciphering the SI plain such inconsistencies (Díaz, Martín, Rallo, & de la Rosa, 2007; system of plants is therefore of great interest in agronomy, horticul- Mookerjee, Guerin, Collins, Ford, & Sedgley, 2005; Saumitou-Laprade, ture, and forestry. Vernet, Vekemans, Castric, et al., 2017). In contrast, methods based In the Olive tribe (Oleeae), the SI system has been recently on both intra- and interspecific stigma tests on a representative sam- subject to investigations in the genera Phillyrea, Fraxinus, and ple of olive cultivars indicated that Olea, Phillyrea, and Fraxinus share Olea (Saumitou-Laprade et al., 2010; Saumitou-Laprade, Vernet, the same DSI system (Saumitou-Laprade, Vernet, Vekemans, Billiard, Vekemans, Billiard, et al., 2017; Saumitou-Laprade et al., 2018; et al., 2017). Some authors have, however, expressed doubts about Breton et al., 2014; Vernet et al., 2016). In the regular SI system, these results due to strong divergences with their previous studies negative frequency-dependent advantage promotes the emergence (i.e., asymmetry of incompatibilities in reciprocal crosses and pol- of new S-alleles and their maintenance across speciation (Igic et al., len germination not sustaining DSI; Breton, Koubouris, Villemur, & 2008; Wright, 1939). In Oleeae on the other hand, an unusual, di- Bervillé, 2017; Farinelli et al., 2018). Such disagreeing findings, thus, allelic SI system (DSI) has been proposed for those three distantly call for accurate SI tests on a homogeneous genetic pool, ideally on related lineages (Saumitou-Laprade et al., 2010) that have diverged natural populations of O. europaea. Considering the two alternative from a common polyploid ancestor during the Eocene (Olofsson hypotheses, distinct patterns of cross-compatibility between individ- et al., 2019; Taylor, 1945; Wallander & Albert, 2000). This homo- uals are expected within a population, with only two groups of recip- morphic DSI system is composed of an S-locus with two alleles, S2 rocal compatibility under the DSI hypothesis, while a more complex and S1 (with S2 dominant over S1), that produces two incompatibil- pattern should be observed for the alternative multigroups hypothe- ity groups, G1 (S2S1) and G2 (S1S1; Billiard et al., 2015). Further, in sis implying some nonreciprocal compatibilities among individuals or Oleeae, the reciprocity of compatibilities between Phillyrea angusti- groups of incompatibility. Under this latter hypothesis, incompatibility folia L., Fraxinus ornus L., and Olea europaea L. suggests identical rec- groups could thus be difficult to define, and the required number of ognition specificities between these three taxa (Saumitou-Laprade, observations will increase with the number of S-alleles involved. Vernet, Vekemans, Billiard, et al., 2017; Vernet et al., 2016). The DSI In this work, we aimed to phenotype the SI system of the wild system could, thus, be conserved among Oleeae species, and it was Laperrine's olive [O. europaea subsp. laperrinei (Batt. & Trab.) Cif.] also suggested to be linked to the evolution and maintenance of an- using paternity tests. The Laperrine's olive is endemic to the Saharan drodioecy in Phillyrea and Fraxinus section Ornus (Billiard et al., 2015; mountain ranges (above 1,200 m), and most of its populations have Husse, Billiard, Lepart, Vernet, & Saumitou-Laprade, 2013; Van de been isolated from the Mediterranean basin long before olive do- Paer, Saumitou-Laprade, Vernet, & Billiard, 2015). While the pres- mestication (excepted in the Tassili'n Ajjer; Baali-Cherif & Besnard, ence of a DSI system in Phillyrea and Fraxinus is recognized by the 2005; Besnard et al., 2013). Indeed, investigating the SI system in scientific community (Pannell & Voillemot, 2015), the doubt remains this wild subspecies is relevant because it should not be affected in the cultivated olive tree (O. e. subsp. europaea) because the few by human-related selective effects or recent admixture (Besnard, studies that investigated the mating system in the species present Anthelme, & Baali-Cherif,

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