Diallelic self‐incompatibility is the main determinant of fertilization patterns in olive orchards

TLDR: Paternity analysis showed that the DSI system is the main determinant of fertilization success under field open pollination conditions: G1 cultivars sired seeds exclusively on G2 cultivars, and reciprocally, and no self‐fertilization events were observed.

Abstract: Introduction - Self-incompatibility (SI) in flowering plants potentially represents a major obstacle for sexual reproduction, especially when the number of S-alleles is low. The situation is extreme in the commercially important olive tree, where in vitro pollination assays suggested the existence of a diallelic SI (DSI) system involving only two SI groups (G1 and G2). Varieties belonging to the same SI group cannot fertilize each other, such that successful fruit production is predicted to require pollination between varieties of different groups. Methods and Results – To test this prediction, we explored the extent to which the DSI system determines fertilization patterns under field conditions. 117 olive cultivars were first genotyped using ten highly polymorphic dinucleotide Simple Sequence Repeat (SSR) markers to ascertain varietal identity. Cultivars were then phenotyped through controlled pollination tests to assign each of them to one of the two SI groups. We then collected and genotyped 1,440 open pollinated embryos from five different orchards constituted of seven local cultivars with known group of incompatibility groups. Embryos genotype information were used: (i) to assign embryos to the most likely pollen donor genotype in the neighborhood using paternity analysis, and (ii) to compare the composition of the pollen cloud genetic among recipient trees in the five sites. The paternity analysis showed that the DSI system is the main determinant of fertilization success under field open pollination conditions: G1 cultivars sired seeds exclusively on G2 cultivars, and reciprocally. No self-fertilization events were observed. Moreover, the varietal composition of the pollen cloud differed not only among orchards, but also among individual trees within orchards, with SI phenotype being the main predictor of the composition the pollen cloud fertilizing a given olive producing tree. Discussion - Our results demonstrate that DSI is a potent force determining pollination success among varieties within olive orchards used for production. They have the potential to improve management practices by guiding the selection of compatible varieties to avoid planting orchards containing sets of varieties with strongly unbalanced SI groups, as these would lead to suboptimal olive production. Beyond its scientific interest, the knowledge of the incompatibility groups of the cultivated varieties is a new powerful tool for economic operators involved in olive growing and olive oil production.