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.
Sexual self-incompatibility in European pear (Pyrus communis L.) is controlled by a single locus (Slocus) encoding a polymorphic stylar ribonuclease (S-RNase) that is responsible for the female function in pollen-pistil recognition. In this study, genomic DNA sequences corresponding to five new S-RNase alleles (named S 20 , S 21 , S 22 , S 23 , and S 24 ) and to S m were characterized in European pear cultivars. Re-sequencing S q from 'General Le Clerc' showed this S-RNase to encode the same protein as S 12 . Based on these findings, a polymerase chain reaction (PCR)-based method was developed for the molecular typing of cultivars bearing 20 S-RNases (S 1 -S 14 , S m , and S 20 -S 24 ) using consensus and allele-specific primers. Genomic PCR with consensus primers amplified product sizes characteristic of the S-RNases S 1 , S 2 , S 4 , S 10 , S 13 , and S 20 . However, the allele groups S 3 /S 12 , S 6 /S 8 /S 11 /S 22 and S 5 /S 7 /S 9 /S 14 /S m /S 21 / S 23 /S 24 amplified PCR products of similar size. To discriminate between alleles within these groups, primers to specifically amplify each S-RNase were developed. Application of this approach in 19 cultivars with published Salleles allowed re-evaluation of one of the alleles of 'Passe Crassane,' 'Conference,' and 'Condo.' Finally, this method was used to assign S-genotypes to 37 cultivars. Test crosses confirmed molecular results.
The stylar products of the S-locus for the gametophytic self-incompatibility (GSI) system in the Rosaceae are ribonucleases (S-RNases). Recently, sequences for 13 pear S-RNase alleles have been published and named following a letter-symbol nomenclature (S a to S d and S h to S p ). To establish the correspondence between these sequences and the self-incompatibility alleles we have described previously (S 1 to S 5 ), we have amplified genomic DNA with consensus primers from the cultivars, ÔWilliamsÕ (S 1 S 2 ), ÔCosciaÕ (S 3 S 4 ), ÔButirra Precoce MorettiniÕ (S 1 S 3 ), ÔSanta Maria MorettiniÕ (S 2 S 3 ) and ÔDoyenne du ComiceÕ (S 4 S 5 ) and identified PCR products specifically associated with each S allele. Cloning and sequencing of the amplification products has revealed that they correspond to European pear sequences already deposited in the database. This allowed us to link S-RNase sequences with S allele phenotypes and to determine a correspondence between the symbol-letter nomenclature used to name S-RNase sequences and the number-based nomenclature used to name S alleles. Based on this result the prediction of new cross-incompatibilities among pear cultivars is discussed. Finally, we propose a unified number-based nomenclature to avoid future confusion denominating S alleles in pear.
The recent analysis of the S-locus region of apple and Japanese pear, two species of Pyrinae (Rosaceae), suggested multiple and different F-box genes (called SFBBs) as candidates for the male determinant (pollen S) of RNase-based gametophytic self-incompatibility in these two species. Here, we followed a phylogenetic approach to take advantage of the pattern of molecular evolution of the S-locus of Pyrinae in characterizing SFBB homologs belonging to S-haplotypes of apple and three species of Pyrus (European, Japanese, and Chinese pears). Our results suggested that the S-locus region of Pyrinae contains no less than six SFBB members and that its structure seems to be rather conserved between apple and pear species. In accordance with the prevailing theory on S-haplotype evolution, the pollen S is expected to have coevolved with the S-RNase and to show some common features derived from the long-term evolution under frequency-dependent balancing selection, i.e., high sequence diversity, evidence of positive selection, and shared ancestral polymorphisms. Using this conceptual framework, we present evidence that some SFBB genes may be better candidates for pollen S in Pyrinae than others. Overall, the SFBB genes analyzed exhibited much lower sequence diversity than their associated S-RNases; likewise, they showed little or no evidence of positive selection. However, evidence of coevolution with the S-RNase clearly emerged for two of them. Altogether our results suggested different evolutionary histories for different SFBBs putatively derived from their distinct involvement in self-incompatibility.
While stigma anatomy is well documented for a good number of species, little information is available on the acquisition and cessation of stigmatic receptivity. The aim of this work is to characterize the development of stigma receptivity, from anthesis to stigma degeneration, in the pentacarpellar pear (Pyrus communis) flower. Stigma development and stigmatic receptivity were monitored over two consecutive years, as the capacity of the stigmas to offer support for pollen germination and pollen tube growth. In an experiment where hand pollinations were delayed for specified times after anthesis, three different stigmatic developmental stages could be observed: (1) immature stigmas, which allow pollen adhesion but not hydration; (2) receptive stigmas, which allow proper pollen hydration and germination; and (3) degenerated stigmas, in which pollen hydrates and germinates properly, but pollen tube growth is impaired soon after germination. This developmental characterization showed that stigmas in different developmental stages coexist within a flower and that the acquisition and cessation of stigmatic receptivity by each carpel occur in a sequential manner. In this way, while the duration of stigmatic receptivity for each carpel is rather short, the flower has an expanded receptive period. This asynchronous period of receptivity for the different stigmas of a single flower is discussed as a strategy that could serve to maximize pollination resources under unreliable pollination conditions.
European pear, as well as its close relatives Japanese pear and apple, exhibits S-RNase-based gametophytic self-incompatibility. The male determinant of this self-incompatibility mechanism is a pollen-expressed protein containing an F-box domain; in the genera Petunia (Solanaceae), Antirrhinum (Plantaginaceae), and Prunus (Rosaceae), a single F-box gene determines the pollen S. In apple and Japanese pear, however, multiple S-locus F-box genes were recently identified as candidates for the pollen S, and they were named S-locus F-Box Brothers. These genes were considered good candidates for the pollen S determinant since they exhibit S-haplotype-specific polymorphisms, pollen-specific expression, and linkage to the S-RNase. In the present study, S-locus F-Box Brothers homologs have been cloned from two of the most agronomically important European pear varieties, "Abbé Fétel" (S 104-2 /S 105 ) and "Max Red Bartlett" (S 101 /S 102 ), and they have been mapped on a genetic linkage map developed on their progeny. Our results suggest that the number of Fbox genes linked to the S-locus of the European pear is higher than expected according with previous reports for apple and Japanese pear, since up to five genes were found to be linked to a single S-haplotype. Moreover, two of these genes exhibited an incomplete linkage to the S-RNase, allowing the identification of low-frequency recombinant haplotypes, generated by a crossing-over event between the two genes. These F-box genes are most likely placed in close proximity of the S-locus but do not belong to it, and they can thus be excluded from being responsible for the determination of pollen S function.
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