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. 2016 Jan 1;66(1):116–121. doi: 10.1270/jsbbs.66.116

Molecular mechanism of the S-RNase-based gametophytic self-incompatibility in fruit trees of Rosaceae

Hidenori Sassa 1,*
PMCID: PMC4780795  PMID: 27069396

Abstract

Self-incompatibility (SI) is a major obstacle for stable fruit production in fruit trees of Rosaceae. SI of Rosaceae is controlled by the S locus on which at least two genes, pistil S and pollen S, are located. The product of the pistil S gene is a polymorphic and extracellular ribonuclease, called S-RNase, while that of the pollen S gene is a protein containing the F-box motif, SFB (S haplotype-specific F-box protein)/SFBB (S locus F-box brothers). Recent studies suggested that SI of Rosaceae includes two different systems, i.e., Prunus of tribe Amygdaleae exhibits a self-recognition system in which its SFB recognizes self-S-RNase, while tribe Pyreae (Pyrus and Malus) shows a non-self-recognition system in which many SFBB proteins are involved in SI, each recognizing subset of non-self-S-RNases. Further biochemical and biological characterization of the S locus genes, as well as other genes required for SI not located at the S locus, will help our understanding of the molecular mechanisms, origin, and evolution of SI of Rosaceae, and may provide the basis for breeding of self-compatible fruit tree cultivars.

Keywords: Rosaceae, self-incompatibility, pistil, pollen, S locus, S-RNase, F-box

Introduction

Many fruit trees of Rosaceae, such as Japanese pear (Pyrus pyrifolia), apple (Malus × domestica), sweet cherry (Prunus avium), almond (Prunus dulcis), mume (Prunus mume), and apricot (Prunus armeniaca), exhibit self-incompatibility (SI) and require pollination with pollen from compatible SI genotypes for stable fruit production. Aside from this practical importance, SI of Rosaceae is interesting from an evolutionary point of view, because the common ancestor of Asterid and Rosid is thought to exhibit S-RNase-based gametophytic self-incompatibility (GSI, see below, Igic and Kohn 2001) which is suggestive of a common origin. To date, S-RNase has been characterized in two families of Asterid, Solanaceae and Plantaginaceae, while it is known in only one family of Rosid, Rosaceae (de Nettancourt 2001, Franklin-Tong 2008, Sassa et al. 2010, Fig. 1). In addition, Rosaceae is likely to include two different systems of SI: a self-recognition system of Prunus of tribe Amygdaleae of subfamily Spiraeoideae (cherry, almond, and apricot), and a non-self-recognition system of tribe Pyreae of subfamily Spiraeoideae (pear and apple). This review focuses on recent findings on different mechanisms of SI in Rosaceae. For the technical advances in the determination of SI genotypes of rosaceous fruit trees, please refer to the following literature; Kato et al. 2012, Okada 2015, Tao and Iezzoni 2010, Yamane and Tao 2009.

Fig. 1.

Fig. 1

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Different self-incompatibility systems in angiosperms. The phylogenetic tree is based on The Angiosperm Phylogeny Group (2009). GSI, SSI and heterostyly denote gametophytic self-incompatibility, sporophytic self-incompatibility and heterostyly self-incompatibility, respectively. Pistil-part and pollen-part determinants are in the parentheses (see text). Nowak et al. (2011) reported S-RNase-like genes of Coffea (Rubiaceae, Asterid), however, it is not clear if the genes are located at the S locus.

Products of the S locus of Rosaceae: pistil determinant S-RNase and pollen determinant F-box proteins SFB and SFBB

Genetically, SI of Rosaceae is controlled by a single S locus with multiple alleles (for Fragaria of subfamily Rosoideae, in addition to the S locus, involvement of another locus was suggested (Bošković et al. 2010)), and when one of the two S alleles of the pistil matches that of a pollen, the pollen is recognized as self, and is rejected (de Nettancourt 2001, Franklin-Tong 2008). However, the S locus contains at least two genes tightly linked with each other, pistil S and pollen S genes, and the pair of pistil S and pollen S alleles is called the S haplotype (de Nettancourt 2001, Franklin-Tong 2008).

The pistil S gene of Rosaceae encodes a polymorphic and highly expressed extracellular ribonuclease called S-RNase, similar to Solanaceae and Plantaginaceae (de Nettancourt 2001, Franklin-Tong 2008). S-RNase acts as a cytotoxin in self-pollen tubes; however, it is taken up in both self- and non-self-pollen tubes in Solanaceae (Goldraij et al. 2006, Luu et al. 2000), suggesting a mechanism in which the pollen S gene plays a pivotal role in detoxifying non-self-S-RNases. Although identification of the pollen S gene had been challenging probably because of its low expression level, chromosome walking from the Prunus S-RNase gene identified polymorphic and pollen-specific F-box gene called SFB (S haplotype-specific F-box protein) as a good candidate for pollen S (Entani et al. 2003, Ushijima et al. 2003). F-box proteins have also been identified as pollen S candidates in other plants, e.g., SLF of Solanaceae and Plantaginaceae, and SFBB of Pyreae of Rosaceae; however, further analyses suggested that the function of SFB may be different from these F-box proteins, coinciding with their differing S locus duplication effects on their pollen SI function.

Effects of S locus duplication on SI in Pyreae and Prunus

In many SI species, tetraploidy has been associated with the loss of SI function in pollen (de Nettancourt 2001). Genetic analyses have revealed that diploid heteroallelic pollen, such as S1S2, loses SI function and is compatible with pistils with any S genotype, while homoallelic pollen retains SI function. This phenomenon, called ‘competitive interaction’ (CI) (de Nettancourt 2001), was also observed in haploid pollen with a translocated chromosome segment harboring the S locus of Nicotiana (Solanaceae) and Antirrhinum (Plantaginaceae) (Golz et al. 2001, Xue et al. 2009). Golz et al. (2001) conducted a large-scale screening of mutagenized pollen for self-compatible (SC) mutants by incompatible pollination, and recovered SC mutants caused by CI and not by pollen S deletion, suggesting that pollen S is essential for pollen tube growth. In Rosaceae, CI has been well documented in Pyreae, i.e., tetraploids of pear and apple (Adachi et al. 2009, Crane and Lewis 1942) and diploid mutants with translocated S locus fragment of Japanese pear (Mase et al. 2014), although this has not been observed to occur in Prunus (Hauck et al. 2006, Tao and Iezzoni 2010). Naturally occurring tetraploid sour cherry (Prunus cerasus) includes both SI and SC plants (Lansari and Iezzoni 1990), and genetic analyses have shown that heteroallelic pollen is rejected by the pistil with a matching S haplotype, leading to a ‘one-allele-match’ model hypothesizing that the SC of sour cherry is caused by the accumulation of mutations in S genes, but not by CI (Hauck et al. 2006, Tao and Iezzoni 2010). This ‘one-allele-match’ model is consistent with the findings of other studies showing pollen-part SC mutants of cherry (P. avium) with deletion or insertion within the SFB (Sonneveld et al. 2005, Ushijima et al. 2004). These differences in the effect of S locus duplication on pollen SI function suggest differing pollen S functions in Prunus and Pyreae.

Self-recognition by a single pollen S protein in Prunus

In Rosaceae, the pollen-part determinant was first identified in Prunus species by chromosome walking from the S-RNase gene and subsequent sequence analyses of the region (Entani et al. 2003, Ushijima et al. 2003). The identified gene SFB (S haplotype-specific F-box protein) encodes an F-box protein, is specifically expressed in pollen, and shows high allelic polymorphism, comparable to that of the S-RNase. Analyses of pollen-part SC mutants identified 4 bp deletion in the SFB4’ gene of cherry (P. avium) and 6.8 kb insertion in the SFBf gene of Japanese apricot (P. mume), further supporting the involvement of SFB in pollen SI function (Ushijima et al. 2004). Given that the major role of the F-box proteins is, as a component of SCF ubiquitin ligase, recognition of target proteins to be ubiquitinated for degradation by the 26S proteasome, SFB was initially assumed to mediate ubiquitination and degradation of non-self-S-RNases while differentially interacting with self-S-RNase and leaving it intact (Ushijima et al. 2003). However, a pollen-part SC haplotype of cherry, S3’, was found to lack the SFB-containing genomic region. This suggested that ubiquitination of non-self-S-RNases by SCFSFB was unlikely; deletion of SFB would result in the inability to degrade non-self-S-RNases, arresting pollen tube growth in pistils with any S haplotype (Sonneveld et al. 2005). Instead, it is likely that non-self-S-RNases taken up by the pollen tube are detoxified by an unidentified ‘general inhibitor’, while self-S-RNase is protected from the ‘general inhibitor’ by the function of SFB as a ‘blocker’, and acts as a cytotoxin to arrest the growth of a self-pollen tube (Luu et al. 2001, Sonneveld et al. 2005). This model suggests that SI of Prunus is of the ‘self recognition by a single factor’ type, and is consistent with the probable absence of CI in Prunus.

Non-self-recognition by multiple pollen S proteins in Pyreae

The chromosome walking strategy was also adopted to identify the pollen S gene in apple (M. × domestica) and Japanese pear (Pyrus pyrifolia), which belong to tribe Pyreae, and detected pollen-specific F-box genes at the S locus region, similar to Prunus. However, unlike Prunus, more than two pollen-specific F-box genes, homologous with each other, were identified and named SFBB (S locus F-box brothers) (Sassa et al. 2007). Further analyses showed that more than ten SFBB genes are clustered at the S locus region of Pyreae (De Franceschi et al. 2011, Minamikawa et al. 2010, Okada et al. 2011, 2013). Genetic analysis showed tight linkage of these genes with the S-RNase, consistent with the heterochromatic nature of the S locus region (Minamikawa et al. 2010), which may contribute to suppress recombination in this region (Wang et al. 2012).

Multiple F-box genes at the S locus were also characterized in the solanaceous plant, Petunia (Kubo et al. 2010, 2015). The function of SLF, a pollen S F-box gene of Petunia, was revealed by CI when transgenic pollen with introduced heteroallelic SLF gene showed breakdown of SI (Sijacic et al. 2004). However, further analysis showed that transformation of SLF does not always cause breakdown of SI (e.g., S7-SLF causes CI for S9 and S17 pollen, but not for S5 and S11 pollen) suggesting that SLF is not the sole determinant of pollen specificity, and other factors may also be involved in SI (Kubo et al. 2010). Kubo et al. (2010) cloned five additional types of SLF-like F-box genes, and named SLF2~SLF6. These genes were expressed in pollen and linked to the S-RNase. Functional analysis showed that the newly identified SLF genes induced CI for particular S haplotypes (e.g., S7-SLF2 causes CI for S9, S11, and S19 pollen, but not for S5 and S17 pollen). Based on these findings, the ‘collaborative non-self recognition’ model was proposed for SI of Petunia, i.e., multiple SLF proteins are involved in pollen specificity, and each targets a subset of non-self-S-RNases for detoxification (Kubo et al. 2010). This discovery in Petunia hinted at the significance of the SFBB cluster at the S locus of Pyreae. Kakui et al. (2011) cloned eight types of SFBB genes from S1~S6 haplotypes, and showed that the allelic sequence diversity within the same SFBB type is very low, while the sequence diversity of SFBB genes within the same S haplotype is high and comparable to the allelic diversity of the S-RNase. This is consistent with the hypothesis that multiple SFBB genes are involved in pollen specificity in SI of Pyreae, with each SFBB targeting a subset of non-self-S-RNases. This hypothesis was supported by findings from a mutant haplotype, S4sm, which lacks S4-RNase and an SFBB gene, S4F-box0/SFBB1-S4 (Kakui et al. 2011, Okada et al. 2008, Sassa et al. 1997). The S4sm pollen was rejected not only by S4 pistils, but also by S1 pistils, while it was accepted by pistils of other S haplotypes. This suggests that S4F-box0/SFBB1-S4 is the only factor in the S4 haplotype to detoxify S1-RNase, and that it is not involved in targeting other non-self-S-RNases (Kakui et al. 2011, Saito et al. 2012). Analyses of the evolutionary pattern of SFBB genes of Sorbus aucuparia (Pyreae) have also support the non-self-recognition hypothesis (Aguiar et al. 2013). Together, these findings suggest that SI of Pyreae may differ from that of Prunus ‘self-recognition by single factor’, but may be similar to that of Petunia of Solanaceae, with a ‘non-self-recognition by multiple factors’ system (Table 1).

Table 1.

Different systems of the S-RNase based GSI

Family Tribe Genus CI Copy number of pollen S Effect of deletion of pollen S Type of SI
Rosaceae Pyreae Pyrus, Malus + multiple Incompatibility to non-self pistils Non-self-recognition
Amygdaleae Prunus −a single SCa Self-recognition
Solanaceae Petunia, Nicotiana, Solanum + multiple Incompatibility to non-self pistils Non-self-recognition
Plantaginaceae Antirrhinum + multiple? ? Non-self-recognition?
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a

CI is reported to be absent in Prunus (Hauck et al. 2006, Tao and Iezzoni 2010), except for the case of Chinese cherry (Gu et al. 2011, Huang et al. 2008).

Concluding remarks

The SI of Rosaceae is intriguing due to the coexistence of different SI types such as the self-recognition system of Prunus and non-self-recognition system of Pyreae. However, the self-recognition model of SI of Prunus is based on the analyses of naturally occurring tetraploids (Tao and Iezzoni 2010), and previous studies of another natural tetraploid, Prunus pseudocerasus, suggested the possibility of CI in this species (Gu et al. 2013, Huang et al. 2008). Analyses of artificial tetraploids may further clarify the self-recognition model of SI of Prunus.

Biochemical analyses have identified several probable components involved in the SI systems of Rosaceae. Interestingly, both the SFB of Prunus and SFBB of Pyreae have been suggested to form similar SCF complexes, in which an Skp1-like protein, SSK1, bridges SFB/SFBB and Cullin (Matsumoto et al. 2012, Minamikawa et al. 2014, Yuan et al. 2014). Yeast two-hybrid screening using S-RNase as the bait identified actin and an ABC transporter as probable interacting partners of the cherry and apple S-RNases, respectively (Matsumoto and Tao 2012, Meng et al. 2014). However, the biological significance of these protein-protein interactions observed in these in vitro experiments remains to be elucidated. Further biochemical and biological analyses may clarify the molecular bases for the self-recognition and non-self-recognition of the Prunus and the Pyreae systems, respectively.

The products of the S locus have been shown to be not sufficient for SI function, and other factors not linked to the S locus may also be required. Such non-S-specific factors have been characterized in Solanaceae, e.g., HT-B and 120 k proteins (McClure et al. 2011), but not in Rosaceae. Furthemore, non-S locus pollen-part mutations (PPM) have been reported in Prunus avium (sweet cherry) and P. armeniaca (apricot) (Cachi et al. 2011, Zuriaga et al. 2012). Interestingly, the two non-S locus PPM have been mapped to a similar region of linkage group 3 (LG3), which shows synteny to apple (M. × domestica) LG17, where the apple S locus is located. Although it is not clear if the two non-S locus PPMs of sweet cherry and apricot are due to the same gene, identification of the gene(s) will help our understanding of the SI mechanism. Further characterization of the S and non-S locus SI genes, together with evolutionary studies (Aguiar et al. 2015, Morimoto et al. 2015), will shed light on the origin and evolution of self-recognition and non-self-recognition SI systems in Rosaceae.

Acknowledgements

I’m grateful to Dr. Hiroyuki Kakui for comments. The work conducted at the author’s lab was supported by a Grants-in-Aid for Scientific Research (B, 24380004) from Japan Society for the Promotion of Science (JSPS).

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