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Apple S locus region represents a large cluster of related, polymorphic and pollen-specific F-box genes

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Abstract

Gametophytic self-incompatibility (GSI) of Rosaceae, Solanaceae and Plantaginaceae is controlled by a complex S locus that encodes separate proteins for pistil and pollen specificities, extracellular ribonucleases (S-RNases) and F-box proteins SFB/SLF, respectively. SFB/SLFs of Prunus (subfamily Prunoideae of Rosaceae), Solanaceae and Plantaginaceae are single copy in each S haplotype, while recently identified pollen S candidates SFBBs of subfamily Maloideae of Rosaceae, apple and Japanese pear, are multiple; two and three related SFBBs were isolated from each S haplotype of apple and Japanese pear, respectively. Here, we show that apple (Malus × domestica) SFBBs constitute a gene family that is much larger than initially thought. Twenty additional SFBB-like genes/alleles were isolated by screening of a BAC library derived from S 3 S 9 genotype, and tentatively named MdFBX1-20. All but one MdFBX showed S haplotype-specific polymorphisms. All the polymorphic MdFBXs were completely linked to S-RNase in 239 segregants. In addition, FISH revealed that the monomorphic gene MdFBX11 is also located near S-RNase, and the S locus is located in a subtelomeric region of a chromosome and is not close to the centromere. All MdFBXs were specifically expressed in pollen, except for a pseudogene MdFBX4 that showed no expression in any organs analyzed. Phylogenetic analysis revealed that the closest relatives of most MdFBXs were from a different S haplotype, suggesting that proliferation of MdSFBB/FBXs predates diversification of the S haplotypes.

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Abbreviations

GSI:

Gametophytic self-incompatibility

SFBB :

S locus F-box brothers

S-RNase:

S-ribonuclease

BAC:

Bacterial artificial chromosome

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Acknowledgments

We thank Dr. K. Abe of National Institute of Fruit Tree Science for plant materials, Dr. K. Ushijima of Okayama University for comments, and M. Miyamoto for technical help. This work was supported by the Grants-in-Aid for Scientific Research (B, 20380003) from the Ministry of Education, Science, Sports and Culture of Japan. H.K and S.W. were supported by JSPS Research Fellowship for Young Scientists and JSPS Postdoctoral Fellowship for Foreign Researchers, respectively.

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Correspondence to Hidenori Sassa.

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Sequence data from this article have been deposited with DDBJ/EMBL/GenBank Data Libraries under accession nos. AB539844 (MdFBX1), AB539845 (MdFBX2), AB539846 (MdFBX3), AB539847 (MdFBX4), AB539848 (MdFBX5), AB539849 (MdFBX6), AB539850 (MdFBX7), AB539851 (MdFBX8), AB539852 (MdFBX9), AB539853 (MdFBX10), AB539854 (MdFBX11), AB539855 (MdFBX12), AB539856 (MdFBX13), AB539857 (MdFBX14), AB539858 (MdFBX15), AB539859 (MdFBX16), AB539860 (MdFBX17), AB539861 (MdFBX18), AB539862 (MdFBX19), AB539863 (MdFBX20).

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Minamikawa, M., Kakui, H., Wang, S. et al. Apple S locus region represents a large cluster of related, polymorphic and pollen-specific F-box genes. Plant Mol Biol 74, 143–154 (2010). https://doi.org/10.1007/s11103-010-9662-z

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