Molecular bases and evolutionary dynamics of self-incompatibility in the Pyrinae (Rosaceae)

Abstract

The molecular bases of the gametophytic self-incompatibility (GSI) system of species of the subtribe Pyrinae (Rosaceae), such as apple and pear, have been widely studied in the last two decades. The characterization of S-locus genes and of the mechanisms underlying pollen acceptance or rejection have been topics of major interest. Besides the single pistil-side S determinant, the S-RNase, multiple related S-locus F-box genes seem to be involved in the determination of pollen S specificity. Here, we collect and review the state of the art of GSI in the Pyrinae. We emphasize recent genomic data that have contributed to unveiling the S-locus structure of the Pyrinae, and discuss their consistency with the models of self-recognition that have been proposed for Prunus and the Solanaceae. Experimental data suggest that the mechanism controlling pollen-pistil recognition specificity of the Pyrinae might fit well with the collaborative 'non-self' recognition system proposed for Petunia (Solanaceae), whereas it presents relevant differences with the mechanism exhibited by the species of the closely related genus Prunus, which uses a single evolutionarily divergent F-box gene as the pollen S determinant. The possible involvement of multiple pollen S genes in the GSI system of Pyrinae, still awaiting experimental confirmation, opens up new perspectives to our understanding of the evolution of S haplotypes, and of the evolution of S-RNase-based GSI within the Rosaceae family. Whereas S-locus genes encode the players determining self-recognition, pollen rejection in the Pyrinae seems to involve a complex cascade of downstream cellular events with significant similarities to programmed cell death.

Identification and characterization of S-RNase genes and S-genotypes in Prunus and Malus species

“…In addition, loss-offunction of the S-RNase results in self-compatibility in both Prunus and Malus (Okada et al 2008;Ferna´ndez i Martı´et al 2009). However, differently from the general inhibition system of Prunus, in the Maloideae the inhibition of S-RNases is thought to be directly triggered by pollen-S genes, each of them providing recognition of a single or a few S-RNases and tartgeting them to degradation; thus, loss-of-function of pollen-S genes leads to opposite results: in Malus, it is expected to extend cross-incompatibility, while it leads to self-compatibility in Prunus (De Franceschi et al 2012).…”

“…Overall, the genetic variation of both S-RNase and SFB genes in peach is significantly lower than that of S-RNase and SFB genes in self-incompatible Prunus species. Thus, it seems that S-pistil and S-pollen genes may have coevolutionary relationships (Hegeduˆs and Hala´sz 2007;Vieira et al 2010;De Franceschi et al 2012). The observed low genetic diversity of S-RNase genes may be partially due to self-compatibility in peach.…”

Transcriptome Analysis of Self- and Cross-pollinated Pistils of Japanese Apricot (Prunus mume Sieb. et Zucc.)

“…In other words, it is thought that multiple pollen S determinants (SLFs) would collaboratively detoxify the non-self S-RNases in the Solanaceae, while a single pollen S determinant (SFB) would release the cytotoxicity of the self S-RNase in Prunus. The role of the pollen S determinant of Pyrinae (SFBBs) is still unclear but it is suggested that the GSI mechanism of Pyrinae would be similar to that of Solanaceae (De Franceschi et al, 2012). On the other hand, three other types of pollen-expressed F-box genes, SLFL1, SLFL2, and SLFL3 (synonymous with the S locus F-box protein with low allelic sequence polymorphism 1, 2, and 3, respectively), were also found on the S locus of Prunus (Entani et al, 2003;Matsumoto et al, 2008;Ushijima et al, , 2004.…”

Direct genotyping of single pollen grains of a self-compatible mutant of Japanese pear (Pyrus pyrifolia) revealed inheritance of a duplicated chromosomal segment containing a second S-haplotype

“…Thus, this selection is predicted to produce S-heteroallelic pollen grains that are capable of breaking down self-incompatibility by competitive interaction between the two different S factors in the pollen grain (Mase et al 2014). It is an important material for breeding as well as for analyzing the mechanism of competitive interaction, which is now hypothesized to be caused by non-self recognition of S-RNase by two different sets of pollen S-determinants in a single pollen tube (Kubo et al 2010;de Franceschi et al 2012). However, the direct detection of two S-haplotypes in a single pollen grain of a PPM plant has not previously been achieved.…”