3.2 Compatibility groups

Incompatibility is the phenomenon by which pollen deposited on the stigma surface of a flower is usually unable to germinate, grow and fertilise the ovules, thus inhibiting fruit setting. In olive, incompatibility reaction occurs shortly after the pollen grains land on an incompatible stigma and pollen tube growth stops in the first layers of stigmatic cells. (Figure 1).

Most olive varieties were known as self-incompatible (Seifi et al., 2011; Sánchez-Estrada and Cuevas, 2018), but, recently, it has been discovered that, in addition to this, they may also be inter-incompatible.

Recent advances on the genetic and molecular mechanisms underlying self- and inter-incompatibility in olive have highlighted a peculiar system, observed for the first time in numerous genera of the Oleaceae family, including Fraxinus (Saumitou-Laprade et al., 2018), Phillyrea (Carré et al., 2021), Ligustrum (De Cauwer et al., 2021) and Olea (Saumitou-Laprade et al., 2017), known as diallelic self-incompatibility (DSI).

DSI is controlled by a single locus with two alleles, a dominant allele S and a recessive allele s. These alleles lead to only two possible genotypic combinations (Ss and ss), corresponding to the incompatibility groups G1 and G2, respectively, where all varieties of G1 group are self- and inter-incompatible with each other and compatible with all G2 varieties and vice versa.

In a study conducted on an F1 progeny derived by the cross of a G1 and a G2 cultivars, the DSI locus has been identified (Mariotti et al., 2020), spanning a physical length of approximately 300 Kb in chromosome 18 of the wild olive genome (Unver et al., 2017).

The most recent studies performed on olive and on Phillyrea angustifolia are pointing out the presence of a hemizygous incompatibility locus, carrying a long deletion and leading to the identification of genes related to hormone regulation, potentially responsible for the incompatibility reaction (Castric et al., 2024; Raimondeau et al., 2024).

In contrast to this reproductive system, it has been observed that some olive varieties are able to produce fruits and seeds from self-fertilisation, despite the persistence of the phenomenon of incompatibility on self-pollinated stigmas. The phenomenon has not yet been clarified, but several hypotheses have been formulated to explain this paradox (Alagna et al., 2019).

The incompatibility system based on only two incompatibility groups has been tested on a large number of varieties through stigma tests and the use of markers associated with the S and s alleles, confirming that the two groups persist in all analysed varieties. The existence of the two groups was also confirmed at field level through the genotyping of thousands of embryos derived from the open pollination of different varieties, all derived exclusively from the cross between G1 and G2 varieties (Mariotti et al., 2021; Vuletin Selak et al., 2021).

The diallelic incompatibility system certainly represents a barrier to the reproductive possibilities of the olive and explains the low productivity of most varieties (Vuletin Selak et al., 2011; 2013). However, knowledge of this reproductive system may allow to improve management practices by guiding the selection of inter-compatible varieties, therefore increasing the possibilities of inter-fertilisation and fruit production and avoiding the planting of orchards containing sets of varieties with strongly unbalanced SI groups.

  Figure 1. Pollen grains on the stigma surface. A: Incompatible reaction without any pollen germination, B: Compatible reaction with abundant pollen tubes growing towards the style.

References

• Alagna, F., Caceres, M. E., Pandolfi, S., Collani, S., Mousavi, S., Mariotti, R., et al. (2019). The paradox of self-fertile varieties in the context of self-incompatible genotypes in olive. Front. Plant Sci., 10, 452724.
• Carré, A., Gallina, S., Santoni, S., Vernet, P., Godé, C., Castric, V., Saumitou-Laprade, P. (2021). Genetic mapping of sex and self-incompatibility determinants in the androdioecious plant Phillyrea angustifolia. Peer Comm. J., 1.
• Castric, V., Batista, R. A., Carre, A., Mousavi, S., Mazoyer, C., Gode, C., et al. (2023). The diallelic self-incompatibility system in Oleaceae is controlled by a hemizygous genomic region expressing a gibberellin pathway gene. bioRxiv, 2023-12.
• De Cauwer, I., Vernet, P., Billiard, S., Godé, C., Bourceaux, A., Ponitzki, C., Saumitou-Laprade, P. (2021). Widespread coexistence of self-compatible and self-incompatible phenotypes in a diallelic self-incompatibility system in Ligustrum vulgare (Oleaceae). Heredity, 127(4), 384-392.
• Mariotti, R., Fornasiero, A., Mousavi, S., Cultrera, N. G., Brizioli, F., Pandolfi, S., et al. (2020). Genetic mapping of the incompatibility locus in olive and development of a linked sequence-tagged site marker. Front. Plant Sci., 10, 494090.
• Mariotti, R., Pandolfi, S., De Cauwer, I., Saumitou-Laprade, P., Vernet, P., Rossi, M., et al. (2021). Diallelic self-incompatibility is the main determinant of fertilization patterns in olive orchards. Evol. Appl., 14(4), 983-995.
• Raimondeau, P., Marande, W., Cheptou, P. O., Vautrin, S., Manzi, S., Chave, J., et al. (2024). Hemizygous supergene controls homomorphic di-allelic self-incompatibility in olive. Mining high-throughput genomic datasets to investigate the evolutionary history of Oleaceae. PhD Thesis, Chapter 3, 74-98.
• Sánchez-Estrada, A., Cuevas, J. (2018). ‘Arbequina’ olive is self-incompatible. Sci. Hortic., 230, 50-55.
• Saumitou-Laprade, P., Vernet, P., Dowkiw, A., Bertrand, S., Billiard, S., Albert, B., et al. (2018). Polygamy or subdioecy? the impact of diallelic self-incompatibility on the sexual system in Fraxinus excelsior (Oleaceae). Proc. R. Soc. B. Biol. Sci. 285, 20180004.
• Saumitou-Laprade, P., Vernet, P., Vekemans, X., Billiard, S., Gallina, S., Essalouh, L., et al. (2017). Elucidation of the genetic architecture of self-incompatibility in olive: evolutionary consequences and perspectives for orchard management. Evol. Appl. 10(9), 867–880.
  Seifi, E., Guerin, J., Kaiser, B., Sedgley, M. (2012). Sexual compatibility of the olive cultivar ‘Kalamata’ assessed by paternity analysis. Span. J. Agric. Res., 10(3), 731-740.
• Unver, T., Wu, Z., Sterck, L., Turktas, M., Lohaus, R., Li, Z., et al. (2017). Genome of wild olive and the evolution of oil biosynthesis. PNAS, 114(44), E9413-E9422.
• Vuletin Selak, G., Baruca Arbeiter, A., Cuevas, J., Perica, S., Pujic, P., Raboteg Božiković, M., Bandelj, D. (2021). Seed paternity analysis using SSR markers to assess successful pollen donors in mixed olive orchards. Plants, 10(11), 2356.
• Vuletin Selak, G., Perica, S., Ban, S.G., Poljak, M. (2013). The effect of temperature and genotype on pollen performance in olive (Olea europaea L.). Sci. Hortic., 156, 38-46.
• Vuletin Selak, G., Perica, S., Goreta Ban, S., Radunić, M., Poljak, M. (2011). Reproductive success after self-pollination and cross-pollination of olive cultivars in Croatia. HortSci., 46(2), 186-191.