<i>S Locus F-Box Brothers</i>: Multiple and Pollen-Specific F-Box Genes With<i>S</i>Haplotype-Specific Polymorphisms in Apple and Japanese Pear

Sassa, Hidenori; Kakui, Hiroyuki; Miyamoto, Mayu; Suzuki, Yusuke; Hanada, Teiichi; Ushijima, Koichiro; Kusaba, Makoto; Hirano, Hisashi; Koba, Takato

doi:10.1534/genetics.106.068858

Cited by 162 publications

(195 citation statements)

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“…In these families, pistil-S is a secreted ribonuclease termed S-RNase, which exerts cytotoxic effects that inhibit the elongation of self-pollen tubes by degrading RNA [1][2][3][4] ; consequently, the SI system in these families is referred to as S-RNase-based SI. The pollen-S is a set of F-box protein(s), termed S-locus F-box (SLF [1][2][3][4] , also called S-haplotype-specific F-box, SFB 6 , or S-haplotype-specific F-box brothers, SFBB 7 in Rosaceae), and function as a component of the SCF (Skp1-Cullin1-F-box)-type E3 ubiquitin ligase which generally mediates ubiquitination of target proteins for degradation by the 26S proteasome 8 . Previously, we proposed that S-RNase-based SI in Solanaceae is a collaborative non-self recognition system, in which the product of each SLF interacts with a subset of non-self S-RNases, and the products of multiple SLF types are required for the entire suite of non-self S-RNases to be collectively recognized and detoxified 9 .…”

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confidence: 99%

Gene duplication and genetic exchange drive the evolution of S-RNase-based self-incompatibility in Petunia

et al. 2015

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Self-incompatibility (SI) systems in flowering plants distinguish self-and non-self pollen to prevent inbreeding. While other SI systems rely on the self-recognition between specific male-and femaledeterminants, the Solanaceae family has a non-self recognition system resulting in the detoxification of female-determinants of S-ribonucleases (S-RNases), expressed in pistils, by multiple male-determinants of S-locus F-box proteins (SLFs), expressed in pollen. It is not known how many SLF components of this non-self recognition system there are in Solanaceae species, or how they evolved. We identified 16-20 SLFs in each S-haplotype in SI Petunia, from a total of 168 SLF sequences using large-scale nextgeneration sequencing and genomic polymerase chain reaction (PCR) techniques. We predicted the target S-RNases of SLFs by assuming that a particular S-allele must not have a conserved SLF that recognizes its own S-RNase, and validated these predictions by transformation experiments. A simple mathematical model confirmed that 16-20 SLF sequences would be adequate to recognize the vast majority of target S-RNases. We found evidence of gene conversion events, which we suggest are essential to the constitution of a non-self recognition system and also contribute to self-compatible mutations. Self-incompatibility (SI) systems in flowering plants distinguish self and non-self pollen to prevent inbreeding. While all other SI systems studied to date rely on the self-recognition between each single male-and female-determinants, the Solanaceae plants has a non-self recognition system that functions through the detoxification of non-self female-determinants of S-ribonucleases (S-RNases), expressed in pistils, by multiple male-determinants of S-locus F-box proteins (SLFs), expressed in pollen.However, little is known about how many SLF components constitute such a non-self recognition system and how they evolve. Here we conducted large-scale next-generation sequencing and genomic PCR and identified 16-20 SLFs in each S-haplotype in SI Petunia, for a total of 168 SLF sequences. We predicted the target S-RNases of SLFs by assuming that a particular S-allele must not have a conserved SLF that recognizes its own S-RNase, and validated them by transformation experiments. A simple mathematical model showed that 16-20 SLF sequences would be adequate to recognize the vast majority of target S-RNases. We found evidence of gene conversion events, which we suggest are essential to constitute a non-self recognition system and as well as contributed to self-compatible mutations.SI is a genetically controlled reproductive barrier in angiosperms that allows the pistil to reject self (genetically-related) pollen and accept non-self (genetically-unrelated) pollen [1][2][3][4] . In most cases, this self/non-self discrimination is controlled by male-and

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Gene duplication and genetic exchange drive the evolution of S-RNase-based self-incompatibility in Petunia

et al. 2015

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“…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.…”

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

Wang

Korban

et al. 2015

Can. J. Plant Sci.

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. 2015. Identification and characterization of S-RNase genes and S-genotypes in Prunus and Malus species. Can. J. Plant Sci. 95: 213Á225. Most Rosaceae fruit trees such as Prunus and Malus species exhibit gametophytic self-incompatibility that is genetically controlled by the S-locus. In turn, the S-locus contains at least two tightly-linked S-determinant genes, a pistil S-RNase and a pollen SFB. In this study, S-genotypes of 120 cultivated and wild Prunus accessions (peach) and seven wild Malus accessions (crabapple) have been characterized. Among cultivated Prunus genotypes, four S-RNase alleles, designated S 1 , S 2 , S 3 , and S 4 , have been identified, and they share typical structural features of S-RNases from all other self-incompatible Prunus species. Four S-genotypes, S 1 S 2 , S 1 S 3 , S 1 S 4 , and S 2 S 2 , were identified in peach cultivars, while only one S-genotype S 1 S 2 for wild Prunus species. The S 1 S 2 genotype is predominant in peach cultivars, accounting for 58.3% of all evaluated accessions. Similarly, four SFB alleles were identified in peach cultivars and wild accessions. However, all the four SFB alleles encode truncated proteins due to a frame-shift mutation, resulting in loss of hyper-variable and/or variable regions. For Malus species, a total of 14 S-RNase alleles are identified, and of those, two alleles encode truncated proteins. 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 Malus and/or Prunus species. The relationship between the genetic variation of SFB genes and the diversification of S-RNase genes in Rosaceae is also discussed.Key words: Prunus, Malus, Self-incompatibility, S-genotypes, S-RNase, Pollen, S-determinant Gu, C., Wang, L., Korban, S. S. et Han, Y. 2015. Identification et caracte´risation des ge`nes de la S-RNase et des ge´notypes-S chez les espe`ces des genres Prunus et Malus. Can. J. Plant Sci. 95: 213Á225. La plupart des arbres fruitiers de la famille des Rosace´es comme ceux des espe`ces des genres Prunus et Malus illustrent une auto-incompatibilite´game´tophytique que controˆle ge´ne´tiquement le locus-S. Ce dernier regroupe au moins deux ge`nes S-de´terminants e´troitement lie´s, un ge`ne S-RNase du pistil et un ge`ne SFB du pollen. Les auteurs ont caracte´rise´le ge´notype-S de 120 obtentions domestique´es et sauvages de peˆcher (Prunus) et de sept obtentions sauvages de pommetier (Malus). Chez les ge´notypes domestique´s de Prunus, ils ont identifie´quatre alle`les du ge`ne S-RNase, baptise´s S 1 , S 2 , S 3 , et S 4 . Ces alle`les partagent les particularite´s structurales communes aux S-RNases des autres espe`ces auto-incompatibles du genre Prunus. Quatre ge´notypes-S, S 1 S 2 , S 1 S 3 , S 1 S 4 , et S 2 S 2 ont aussi e´te´identifie´s chez les cultivars de peˆcher, mais un seul chez les espe`ces sauvages, S 1 S 2 . Le ge´notype S 1 S 2 pre´domine chez les cultivars de peˆcher et repre´sente 58,3 % de toutes les obtentions examine´es. De meˆme, on a ...

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“…Therefore, isoplethy may not be observed if S-alleles are commonly linked with recessive deleterious alleles. This effect is expected to be more pronounced in species where recombination is suppressed in a large region around the S-locus, as thought for Maloideae (Sassa et al, 2007). Nevertheless, in Prunus the S-locus seems to encompass at most three genes (Entani et More data are needed from natural populations of other polyploid self-incompatible species to establish the generality of the observation made for P. spinosa, regarding specificities frequencies distribution.…”

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confidence: 94%

Inferences on the number and frequency of S-pollen gene (SFB) specificities in the polyploid Prunus spinosa

et al. 2008

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In flowering plants, self-incompatibility is a genetic mechanism that prevents self-fertilization. In gametophytic selfincompatibility (GSI), pollen specificity is encoded by the haploid genotype of the pollen tube. In GSI, specificities are maintained by frequency-dependent selection, and for diploid species, at equilibrium, equal specificity frequencies (isoplethy) are expected. This prediction has been tested in diploid, but never in polyploid self-incompatible species. For the latter, there is no theoretical expectation regarding isoplethy. Here, we report the first empirical study on specificity frequencies in a natural population of a polyploid self-incompatible species, Prunus spinosa. A total of 32 SFB (the pollen S gene) putative specificities are observed in a large sample from a natural population. Although P. spinosa is polyploid, the number of specificities found is similar to that reported for other diploid Rosaceae species. Unequal specificity frequencies are observed.

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S Locus F-Box Brothers: Multiple and Pollen-Specific F-Box Genes WithSHaplotype-Specific Polymorphisms in Apple and Japanese Pear

Cited by 162 publications

References 47 publications

Gene duplication and genetic exchange drive the evolution of S-RNase-based self-incompatibility in Petunia

Gene duplication and genetic exchange drive the evolution of S-RNase-based self-incompatibility in Petunia

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

Inferences on the number and frequency of S-pollen gene (SFB) specificities in the polyploid Prunus spinosa

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