Sequence divergence and loss‐of‐function phenotypes of S locus F‐box brothers genes are consistent with non‐self recognition by multiple pollen determinants in self‐incompatibility of Japanese pear (Pyrus pyrifolia)

Abstract

SUMMARYThe S-RNase-based gametophytic self-incompatibility (SI) of Rosaceae, Solanaceae, and Plantaginaceae is controlled by at least two tightly linked genes located at the complex S locus; the highly polymorphic S-RNase for pistil specificity and the F-box gene (SFB/SLF) for pollen. Self-incompatibility in Prunus (Rosaceae) is considered to represent a 'self recognition by a single factor' system, because loss-of-function of SFB is associated with self-compatibility, and allelic divergence of SFB is high and comparable to that of S-RNase. In contrast, Petunia (Solanaceae) exhibits 'non-self recognition by multiple factors'. However, the distribution of 'self recognition' and 'non-self recognition' SI systems in different taxa is not clear. In addition, in 'non-self recognition' systems, a loss-of-function phenotype of pollen S is unknown. Here we analyze the divergence of SFBB genes, the multiple pollen S candidates, of a rosaceous plant Japanese pear (Pyrus pyrifolia) and show that intrahaplotypic divergence is high and comparable to the allelic diversity of S-RNase while interhaplotypic divergence is very low. Next, we analyzed loss-of-function of the SFBB1 type gene. Genetic analysis showed that pollen with the mutant haplotype S 4sm lacking SFBB1-S 4 is rejected by pistils with an otherwise compatible S 1 while it is accepted by other non-self pistils. We found that the S 5 haplotype encodes a truncated SFBB1 protein, even though S 5 pollen is accepted normally by pistils with S 1 and other non-self haplotypes. These findings suggest that Japanese pear has a 'non-self recognition by multiple factors' SI system, although it is a species of Rosaceae to which Prunus also belongs.

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

“…This suggests that the S 4 F-box0 gene does not encode the pollen S-determinant. However, the fact that pollen with an S 4 sm -haplotype is rejected by a pistil of an S 1 -haplotype indicates that selfincompatibility in pear is controlled by multiple factors in a non-self recognition system (Kakui et al 2011). Such a system is the product of a single SFB gene within an S-haplotype that is capable of interacting with a subset of non-self S-RNases, and that products of multiple types are required for the entire suite of nonself S-RNases to be collectively recognized and/or detoxified (Kubo et al 2010).…”

“…Unlike Prunus species, the S-locus in both apple and pear have multiple SFB genes, and all SFB genes are exclusively expressed in pollen Okada et al 2008Okada et al , 2011Minamikawa et al 2010;Kakui et al 2011). These SFBs in apple and pear can be divided into two groups, I and II (Okada et al 2011).…”

“…However, genes for the pollen S-determinant in Malus species, belonging to the Maloideae subfamily, have not been functionally characterized (Cheng et al 2006;Kakui et al 2007Kakui et al , 2011Okada et al 2008Okada et al , 2011Sassa et al 2007Sassa et al , 2010.…”

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

“…In contrast, the pollen factors in the Rosaceae are currently classified into two different types. In Prunus, there is a single F-box protein called SLF (S-locus F-box) (Entani et al 2003) or SFB (S haplotype-specific F-box protein) (Ushijima et al 2003) that is predicted to recognize self S-RNase, whereas in the Pyrinae, there are multiple F-box proteins called SFBB (S locus F-box brothers) (Sassa et al 2007;Minamikawa et al 2010) that are predicted to collaborate in recognizing non-self S-RNase (Kakui et al 2011;Saito et al 2012). In either case, these plants require cross pollination with other cultivars to set fruit.…”

Self-Incompatibility System of Ipomoea trifida, a Wild-Type Sweet Potato

“…In S -RNase-based GSI, S -RNases are abundantly expressed in the transmitting tract of the style, and they directly inhibit the growth of self-pollen tubes (Lee et al 1994 ). The pollen determinant genes, SFB / SLF and related genes, are expressed in developing pollen grains and pollen tubes (Ushijima et al 2003 ;Entani et al 2003 ;Sijacic et al 2004 ;Sassa et al 2007Sassa et al , 2010Meng et al 2010 ;Kakui et al 2011 ), and they recognize self or non-self S -RNases (Meng et al 2010 ;Sassa et al 2010 ). In Papaver plants, the female S -gene product, PrsS, is an extracellular signaling molecule that acts as a ligand to the self male S -gene product, PrpS, a transmembrane ion-channel/receptor.…”