Skip to main content
Log in

Pollen-expressed F-box gene family and mechanism of S-RNase-based gametophytic self-incompatibility (GSI) in Rosaceae

  • Review Article
  • Published:
Sexual Plant Reproduction Aims and scope Submit manuscript

Abstract

Many species of Rosaceae, Solanaceae, and Plantaginaceae exhibit S-RNase-based self-incompatibility (SI) in which pistil-part specificity is controlled by S locus-encoded ribonuclease (S-RNase). Although recent findings revealed that S locus-encoded F-box protein, SLF/SFB, determines pollen-part specificity, how these pistil- and pollen-part S locus products interact in vivo and elicit the SI reaction is largely unclear. Furthermore, genetic studies suggested that pollen S function can differ among species. In Solanaceae and the rosaceous subfamily Maloideae (e.g., apple and pear), the coexistence of two different pollen S alleles in a pollen breaks down SI of the pollen, a phenomenon known as competitive interaction. However, competitive interaction seems not to occur in the subfamily Prunoideae (e.g., cherry and almond) of Rosaceae. Furthermore, the effect of the deletion of pollen S seems to vary among taxa. This review focuses on the potential differences in pollen-part function between subfamilies of Rosaceae, Maloideae, and Prunoideae, and discusses implications for the mechanistic divergence of the S-RNase-based SI.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Cheng J, Han Z, Xu X, Li T (2006) Isolation and identification of the pollen-expressed polymorphic F-box genes linked to the S-locus in apple (Malus × domestica). Sex Plant Reprod 19:175–183

    Article  CAS  Google Scholar 

  • Crane MB, Lewis D (1942) Genetical studies in pears. III. Incompatibility and sterility. J Genet 43:31–44

    Article  Google Scholar 

  • de Nettancourt D (2001) Incompatibility and incongruity in wild and cultivated plants. Springer, Berlin

    Google Scholar 

  • Entani T, Iwano M, Shiba H, Che F-S, Isogai A, Takayama S (2003) Comparative analysis of the self-incompatibility (S-) locus region of Prunus mume: identification of a pollen-expressed F-box gene with allelic diversity. Genes Cells 8:203–213

    Article  PubMed  CAS  Google Scholar 

  • Franklin-Tong VE (2008) Self-incompatibility in flowering plants—evolution, diversity, and mechanisms. Springer, Berlin

    Book  Google Scholar 

  • Golz JF, Su V, Oh H-Y, Kusaba M, Newbigin E (2001) Genetic analysis of Nicotiana pollen-part mutants is consistent with the presence of an S-ribonuclease inhibitor at the S locus. Proc Natl Acad Sci USA 98:15372–15376

    Article  PubMed  CAS  Google Scholar 

  • Hauck NR, Ikeda K, Tao R, Iezzoni AF (2006a) The mutated S f-haplotype in sour cherry has an altered S haplotype-specific F-box protein gene. J Hered 97:514–520

    Article  PubMed  CAS  Google Scholar 

  • Hauck NR, Yamane H, Tao R, Iezzoni AF (2006b) Accumulation of nonfunctional S-haplotypes results in the breakdown of gametophytic self-incompatibility in tetraploid Prunus. Genetics 172:1191–1198

    Article  PubMed  Google Scholar 

  • Hua ZH, Kao T (2006) Identification and characterization of components of a putative Petunia S-locus F-box-containing E3 ligase complex involved in S-RNase-based self-incompatibility. Plant Cell 18:2531–2553

    Article  PubMed  CAS  Google Scholar 

  • Hua Z-H, Fields A, Kao T-h (2008) Biochemical models for S-RNase-based self-incompatibility. Mol Plant 1:575–585

    Article  PubMed  CAS  Google Scholar 

  • Huang S-X, Wu H-Q, Li Y-R, Wu J, Zhang S-J, Heng W, Zhang S-L (2008) Competitive interaction between two functional S-haplotypes confer self-compatibility on tetraploid Chinese cherry (Prunus pseudocerasus Lindlcv. Nanjing Chuisi). Plant Cell Rep 27:1075–1085

    Article  PubMed  CAS  Google Scholar 

  • Ikeda K, Ushijima K, Yamane H, Tao R, Hauck NR, Sebolt AM, Iezzoni A (2005) Linkage and physical distances between the S haplotype S-RNase and SFB in sweet cherry. Sex Plant Reprod 17:289–296

    Article  CAS  Google Scholar 

  • Kakui H, Tsuzuki T, Koba T, Sassa H (2007) Polymorphisms of SFBB and its use for S genotyping in Japanese pear (Pyrus pyrifolia). Plant Cell Rep 26:1619–1625

    Article  PubMed  CAS  Google Scholar 

  • Lai Z, Ma W, Han B, Liang L, Zhang Y, Hong G, Xue Y (2002) An F-box gene linked to the self-incompatibility (S) locus of Antirrhinum is expressed specifically in pollen and tapetum. Plant Mol Biol 50:29–42

    Article  PubMed  CAS  Google Scholar 

  • Lansari A, Iezzoni A (1990) A preliminary analysis of self-incompatibility in sour cherry. HortSci 25:1636–1638

    Google Scholar 

  • McClure B (2006) New views of S-RNase-based self-incompatibility. Curr Opin Plant Biol 9:639–646

    Article  PubMed  CAS  Google Scholar 

  • Newbigin E, Paape T, Kohn JR (2008) RNase-based self-incompatibility: puzzled by Pollen S. Plant Cell 20:2286–2292

    Article  PubMed  CAS  Google Scholar 

  • Okada K, Tonaka N, Moriya Y, Norioka N, Sawamura Y, Matsumoto T, Nakanishi T, Takasaki-Yasuda T (2008) Deletion of a 236 kb region around S 4-RNase in a stylar-part mutant S sm4 -haplotype of Japanese pear. Plant Mol Biol 66:389–400

    Article  PubMed  CAS  Google Scholar 

  • Qiao H, Wang H, Zhao L, Zhou J, Lai Z, Zhang Y, Robbins TP, Xue Y (2004) The F-box protein AhSLF-S2 controls the pollen function of S-RNase-based self-incompatibility. Plant Cell 16:2307–2322

    Article  PubMed  CAS  Google Scholar 

  • Saito T, Sato Y, Sawamura Y, Shoda M, Kotobuki K (2002) Studies on breeding of self-compatibility in Japanese pear. 2. Characteristic of pollen of the S 4sm gene originated from ‘Osanjisseiki’. J Jpn Soc Hort Sci 71(suppl 2):123 (in japanese)

    Google Scholar 

  • Sassa H, Hirano H, Nishino T, Koba T (1997) Style-specific self-compatible mutation caused by deletion of the S-RNase gene in Japanese pear (Pyrus serotina). Plant J 12:223–227

    Article  CAS  Google Scholar 

  • Sassa H, Kakui H, Miyamoto M, Suzuki Y, Hanada T, Ushijima K, Kusaba M, Hirano H, Koba T (2007) S locus F-box brothers: multiple and pollen-specific F-box genes with S haplotype-specific polymorphisms in apple and pear. Genetics 175:1869–1881

    Article  PubMed  CAS  Google Scholar 

  • Sato Y, Kurihara A, Abe K, Ogata T, Kajiura I, Kotobuki K, Machida Y (1988) Studies on the mode of inheritance of self-compatibility in Japanese pear. J Jpn Soc Hort Sci 57(suppl 2):76–77 (in japanese)

    Google Scholar 

  • Sijacic P, Wang X, Skirpan AL, Wang Y, Dowd PE, McCubbin AG, Huang S, Kao TH (2004) Identification of the pollen determinant of S-RNase-mediated self-incompatibility. Nature 429:302–305

    Article  PubMed  CAS  Google Scholar 

  • Sonneveld T, Tobutt KR, Vaughan SP, Robbins T (2005) Loss of pollen-S function in two self-compatible selections of Prunus avium is associated with deletion/mutation of an S haplotype-specific F-box gene. Plant Cell 17:37–51

    Article  PubMed  CAS  Google Scholar 

  • Tsukamoto T, Hauck NR, Tao R, Jiang N, Iezzoni AF (2006) Molecular characterization of three non-functional S-haplotypes in sour cherry (Prunus cerasus). Plant Mol Biol 62:325–479

    Article  CAS  Google Scholar 

  • Ushijima K, Sassa H, Dandekar AM, Gradziel TM, Tao R, Hirano H (2003) Structural and transcriptional analysis of the self-incompatibility locus of almond: identification of a pollen-expressed F-box gene with haplotype-specific polymorphism. Plant Cell 15:771–781

    Article  PubMed  CAS  Google Scholar 

  • Ushijima K, Yamane H, Watari A, Kakehi E, Ikeda K, Hauck NR, Iezzoni A, Tao R (2004) The S haplotype-specific F-box protein gene, SFB, is defective in self-compatible haplotypes of Prunus avium and P. mume. Plant J 39:573–586

    Article  PubMed  CAS  Google Scholar 

  • Vieira J, Fonseca NA, Vieira CP (2009) RNase-based gametophytic self-incompatibility evolution: questioning the hypothesis of multiple independent recruitments of the S-pollen gene. J Mol Evol 69:32–41

    Article  PubMed  CAS  Google Scholar 

  • Wheeler D, Newbigin E (2008) Expression of 10 S-class SLF-like genes in Nicotiana alata pollen and its implications for understanding the pollen factor of the S locus. Genetics 177:2171–2180

    Article  CAS  Google Scholar 

  • Xue Y, Zhang Y, Yang Q, Li Q, Cheng Z, Dickinson HG (2009) Genetic features of a pollen-part mutation suggest an inhibitory role for the Antirrhinum pollen self-incompatibility determinant. Plant Mol Biol 70:499–509

    Article  PubMed  CAS  Google Scholar 

  • Yamane H, Tao R (2009) Molecular basis of self-(in)compatibility and current status of S-genotyping in rosaceous fruit trees. J Jpn Soc Hort Sci 78:137–157

    Article  CAS  Google Scholar 

  • Yamane H, Ikeda K, Ushijima K, Sassa H, Tao R (2003) A pollen-expressed gene for a novel protein with an F-box motif that is very tightly linked to a gene for S-RNase in two species of cherry, Prunus cerasus and P. avium. Plant Cell Physiol 44:764–769

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Koichiro Ushijima for critical reading of the manuscript. Research in the authors’ laboratory is supported in part by the Grants-in-Aid for Scientific Research (B, 20380003) from the Ministry of Education, Science, Sports and Culture of Japan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hidenori Sassa.

Additional information

Communicated by Scott Russell.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sassa, H., Kakui, H. & Minamikawa, M. Pollen-expressed F-box gene family and mechanism of S-RNase-based gametophytic self-incompatibility (GSI) in Rosaceae. Sex Plant Reprod 23, 39–43 (2010). https://doi.org/10.1007/s00497-009-0111-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00497-009-0111-6

Keywords

Navigation