The Paradox of Self-Fertile Varieties in the Context of Self-Incompatible Genotypes in Olive

Olive (Olea europaea L.) is a perennial diploid species mainly clonally propagated and diffused in the Mediterranean area as one of the oldest tree crops (Loumou and Giourga, 2003; McKey et al., 2010; Zohary et al., 2012; Mousavi et al., 2017). As in many other allochthonous, hermaphrodite, wind-pollinated species, olive is characterized by a plentiful flowering, followed by a poor fruit set, which results in low yields (Cuevas and Polito, 2004; Ben Dhiab et al., 2017; Kassa et al., 2019). Environmental conditions, such as temperature, rainfall, and wind, may strongly affect flowering time, flowering intensity, and fertilization (Fernandez-Escobar et al., 2008; Haberman et al., 2017; Benlloch-González et al., 2018). Efficient pollination depends on many factors, such as the presence of exogenous compatible pollen, the duration of stigma receptivity, the number of pollen grains, pollen-ovule ratio, and stigma morphology (Cruden, 2000; García-Mozo et al., 2004; Pinillos and Cuevas, 2009; Rojo et al., 2016). Despite the importance of these factors, the main constraints responsible for the low fruit setting of olive are undoubtedly self-incompatibility (SI) and a high percentage of ovary abortion of some cultivars (Reale et al., 2009; Seifi et al., 2015).Self-incompatibility is one of the most effective systems adopted by flowering plants to prevent inbreeding and maintain a high diversity within species (Ferrer and Good, 2012). Within the sporophytic (SSI) and gametophytic (GSI) categories, several incompatibility systems have been reported, but only three of them have been characterized at molecular level, one for SSI (Brassicaceae) and two for GSI (one in Solanaceae, Plantaginaceae, and Rosaceae, and one for Papaveraceae) (Higashiyama, 2010). The recent discovery of the diallelic SSI system in olive and other related genera has provided evidence on the SI system operating in the Oleaceae family. In particular, it has been clarified that the inhibition of pollen tube growth takes place at the stigma, and it has been established that there are only two incompatibility groups, i.e., diallelic SI, such that olive cultivars are incompatible within groups and compatible between groups (Saumitou-Laprade et al., 2017a).In light of this evidence, it has become even more difficult to explain the self-fertility of some varieties, which has been confirmed by numerous studies (Seifi et al., 2012; Selak et al., 2014a; Breton et al., 2016; Marchese et al., 2016a). It is also now clear that pseudo-self-compatibility (PSC)--the failure to reject self-pollen despite the presence of a functional SI system--may occur in olive, and all previous reports on olive self-fertility need to be re-interpreted or ignored when not confirmed by paternity tests of seeds deriving from selfing. In this review, we hope to shed some light on the complexity of SI system in olive, particularly focusing on the evidence for PSC, providing a synthesis of the fragmented work on this topic and a new perspective on SI in olive, supported by experimental work from our laboratory