Molecular Biology Of S-Rnase-Based Self-Incompatibility

  • Y. Zhang
  • Y. Xue

Abstract

Many Flowering Plants Have Developed Self-Incompatibility (Si) Systems To Avoid Inbreeding And To Promote Out-Crossing. Among The Various Si Systems, Gametophytic Si (Gsi) In The Solanaceae, Plantaginaceae And Rosaceae Is Believed To Be The Most Common Type, In Which The Specificity Of Si Response Is Controlled By A Single Polymorphic Locus, Termed The Self-Incompatibility S-Locus. It Has Been Shown That This Locus Is Organised In A Haplotype Fashion Carrying At Least Two Genes Determining The Self And Non-Self Pollen Recognition Specificity: S-Rnase (S-Ribonucleases) Expressed In Pistil (Pistil S) And Slf (S-Locus F-Box)/Sfb(Shaplotype- Specific F-Box) Genes In Pollen (Pollen S). In This Chapter, We Present And Discuss The Current Knowledge About Molecular Biology Of S-Rnase-Based Self-Incompatibility.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Anderson MA, Cornish EC, Mau SL, Williams EG, Hogart R, Atkinson A, Bonig I, Grego B, Simpson R, Roche PJ, Haley JD, Penshow JD, Niall HD, Tregear GW, Coghlan JP, Crawford RJ, Clarke AE (1986) Cloning of cDNA for a stylar glycoprotein associated with expression of self-incompatibility in Nicotiana alata. Nature 321:38-44CrossRefGoogle Scholar
  2. Anderson MA, McFadden GI, Bernatzky R, Atkinson A, Orpin T, Dedman H, Tregear G, Fernley R, Clarke AE (1989) Sequence variability of three alleles of the self-incompatibility gene of Nicotiana alata. Plant Cell 1:483-491CrossRefPubMedGoogle Scholar
  3. Bredemeijer GMM, Blaas J (1981) S-Specific proteins in styles of self-incompatible Nicotiana alata. Theor Appl Genet 59:185-190CrossRefGoogle Scholar
  4. Brewbaker JL, Natarajan AT (1960) Centric fragments and pollen-part mutation of self-incompatibility alleles in Petunia. Genetics 45:699-704PubMedGoogle Scholar
  5. 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 19:175-183CrossRefGoogle Scholar
  6. Cornish EC, Pettitt JM, Bonig I, Clarke AE (1987) Developmentally controlled expression of a gene associated with self-incompatibility in Nicotiana alata. Nature 326:99-102.CrossRefGoogle Scholar
  7. Cruz-Garcia F, Hancock CN, McClure BA (2003) S-RNase complexes and pollen rejection. J Exp Bot 54:123-130CrossRefPubMedGoogle Scholar
  8. Cruz-Garcia F, Hancock CN, Kim D, McClure BA (2005) Stylar glycoproteins bind to S-RNase in vitro. Plant J 42:295-304CrossRefPubMedGoogle Scholar
  9. de Nettancourt D (2001) Incompatibility and incongruity in wild and cultivated plants, 2 edn. Springer, Berlin Heidelberg New YorkGoogle Scholar
  10. Dodds PN, Clarke AE, Newbigin E (1996) A molecular perspective on pollination in flowering plants. Cell 85:141-144CrossRefPubMedGoogle Scholar
  11. Dowd PE, McCubbin AG, Wang X, Verica JA, Tsukamoto T, Andos T, Kao T-H (2000) Use of Petunia inflata as a model for the study of solanaceous type self-incompatibility. Ann Bot 85 (Suppl A):87-93CrossRefGoogle Scholar
  12. Entani T, Iwano M, Shiba H, Che FS, 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. Gene Cell 8:203-213CrossRefGoogle Scholar
  13. Franklin-Tong VE, Franklin FCH (2003) Gametophytic self-incompatibility inhibits pollen tube growth using different mechanisms. Trends Plant Sci 8:598-605CrossRefPubMedGoogle Scholar
  14. Goldraij A, Kondo K, Lee CB, Hancock CN, Sivaguru M, Vazquez-Santana S, Kim S, Phillips TE, Cruz-Garcia F, McClure BA (2006) Compartmentalization of S-RNase and HT-B degradation in self-incompatible Nicotiana. Nature 439:805-810CrossRefPubMedGoogle Scholar
  15. Golz JF, Su V, Clarke AE, Newbigin E (1999) A molecular description of mutations affecting the pollen component of the Nicotiana alata S-locus. Genetics 152:1123-1135PubMedGoogle Scholar
  16. Golz JF, Oh HY, Su V, 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 98:15372-15376CrossRefPubMedGoogle Scholar
  17. Hancock CN, Kent L, McClure BA (2005) The stylar 120 kDa glycoprotein is required for S-specific pollen rejection in Nicotiana. Plant J 43:716-723CrossRefPubMedGoogle Scholar
  18. Hauck NR, Ikeda K, Tao R, Iezzoni AF (2006a) The mutated S1 -haplotype in sour cherry has an altered S-haplotype-specific F-box protein gene. J Hered 97:514-520CrossRefGoogle Scholar
  19. 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 172:1191-1198CrossRefGoogle Scholar
  20. Hua Z, Kao T-H (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 18:2531-2553CrossRefPubMedGoogle Scholar
  21. Huang J, Zhao L, Yang Q, Xue Y (2006) AhSSK1, a novel SKP1-like protein that interacts with the S-locus F-box protein SLF. Plant J 46:780-793CrossRefPubMedGoogle Scholar
  22. Huang S, Lee HS, Karunanandaa B, Kao T-H (1994) Ribonuclease activity of Petunia inflata S-proteins is essential for rejection of self-pollen. Plant Cell 6:1021-1028CrossRefPubMedGoogle Scholar
  23. Ida K, Norioka S, Yamamoto M, Kumasaka T, Yamashita E, Newbigin E, Clarke AE, Sakiyama F, Sato M (2001) The 1.55 Å resolution structure of Nicotiana alata SF 11 -RNase associated with gametophytic self-incompatibility. J Mol Biol 314:103-112CrossRefPubMedGoogle Scholar
  24. Igic B, Kohn JR (2001) Evolutionary relationships among self-incompatibility RNases. Proc Natl Acad Sci USA 98:13167-13171CrossRefPubMedGoogle Scholar
  25. Ikeda K, Igic B, Ushijima K, Yamane H, Hauck NR, Nakano R, Sassa H, Iezzoni AF, Kohn JR, Tao R (2004) Primary structural features of the S-haplotype-specific F-box protein, SFB, in Prunus. Sex Plant Reprod 16:235-243CrossRefGoogle Scholar
  26. Ioerger TR, Gohlke JR, Xu B, Kao T-H (1991) Primary structural features of the self-incompatibility protein in Solanaceae. Sex Plant Reprod 4:81-87CrossRefGoogle Scholar
  27. Ishimizu T, Shinkawa T, Sakiyama F, Norioka S (1998) Primary structural features of rosaceous S-RNases associated with gametophytic self-incompatibility. Plant Mol Biol 37:931-941CrossRefPubMedGoogle Scholar
  28. Kao T-H, McCubbin AG (1996) How flowering plants discriminate between self and non-self pollen to prevent inbreeding. Proc Natl Acad Sci USA 93:12059-12065CrossRefPubMedGoogle Scholar
  29. Kao T-H, Tsukamoto T (2004) The molecular and genetic bases of S-RNase-based self-incompatibility. Plant Cell 16(Suppl):S72-S83CrossRefPubMedGoogle Scholar
  30. Karunanandaa B, Huang S, Kao T-H (1994) Carbohydrate moiety of the Petunia inflata S3 pro-tein is not required for self-incompatibility interactions between pollen and pistil. Plant Cell 6:1933-1940CrossRefPubMedGoogle Scholar
  31. Kawata Y, Sakiyama F, Tamaoki H (1988) Amino-acid sequence of ribonuclease T2 from Aspergillus oryzae. Eur J Biochem 176:683-697CrossRefPubMedGoogle Scholar
  32. Kerscher O, Felberbaum R, Hochstrasser M (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 22:159-180CrossRefPubMedGoogle Scholar
  33. Kondo K, Yamamoto M, Itahashi R, Sato T, Egashira H, Hattori T, Kowyama Y (2002a) Insights into the evolution of self-compatibility in Lycopersicon from a study of stylar factors. Plant J 30:143-153CrossRefGoogle Scholar
  34. Kondo K, Yamamoto M, Matton DP, Sato T, Hirai M, Norioka S, Hattori T, Kowyama Y (2002b) Cultivated tomato has defects in both S-RNase and HT genes required for stylar function of self-incompatibility. Plant J 29:627-636CrossRefGoogle Scholar
  35. 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 50:29-42CrossRefPubMedGoogle Scholar
  36. Lee HS, Huang S, Kao T-H (1994) S proteins control rejection of incompatible pollen in Petunia inflata. Nature 367:560-563CrossRefPubMedGoogle Scholar
  37. Lewis D (1943) Physiology of incompatibility on plants. III. Autopolyploids. J Genet 45:171-185CrossRefGoogle Scholar
  38. Li JH, Nass N, Kusaba M, Dodds PN, Treloar N, Clarke AE, Newbigin E (2000) A genetic map of the Nicotiana alata S-locus that includes three pollen-expressed genes. Theor Appl Genet 100:956-964CrossRefGoogle Scholar
  39. Lind JL, Bacic A, Clarke AE, Anderson MA (1994) A style-specific hydroxyproline-rich glyco-protein with properties of both extensins and arabinogalactan proteins. Plant J 6:491-502CrossRefPubMedGoogle Scholar
  40. Lind JL, Bönig I, Clarke AE, Anderson MA (1996) A style-specific 120 kDa glycoprotein enters pollen tubes of Nicotiana alata in vivo. Sex Plant Reprod 9:75-86CrossRefGoogle Scholar
  41. Lush WM, Clarke AE (1997) Observations of pollen tube growth in Nicotiana alata and their implications for the mechanism of self-incompatibility. Sex Plant Reprod 10:27-35CrossRefGoogle Scholar
  42. Luu DT, Qin X, Morse D, Cappadocia M (2000) S-RNase uptake by compatible pollen tubes in gametophytic self-incompatibility. Nature 407:649-651CrossRefPubMedGoogle Scholar
  43. Luu DT, Qin X, Laublin G, Yang Q, Morse D, Cappadocia M (2001) Rejection of S-heteroallelic pollen by a dual-specific S-RNase in Solanum chacoense predicts a multimeric SI pollen component. Genetics 159:329-335PubMedGoogle Scholar
  44. Mable BK (2004) Polyploidy and self-incompatibility: Is there an association? New Phytol 162:803-811CrossRefGoogle Scholar
  45. Matsuura T, Sakai H, Unno M, Ida K, Sato M, Sakiyama F, Norioka S (2001) Crystal structure at 1.5-Å resolution of Pyrus pyrifolia pistil ribonuclease responsible for gametophytic self-incompatibility. J Biol Chem 276:45261-45269CrossRefPubMedGoogle Scholar
  46. Matton DP, Maes O, Laublin G, Xike Q, Bertrand C, Morse D, Cappadocia M (1997) Hypervari-able domains of self-incompatibility RNases mediate allele-specific pollen recognition. Plant Cell 9:1757-1766CrossRefPubMedGoogle Scholar
  47. Matton DP, Luu DT, Xike Q, Laublin G, O’Brien M, Maes O, Morse D, Cappadocia M (1999) Production of an S-RNase with dual specificity suggests a novel hypothesis for the generation of new S alleles. Plant Cell 11:2087-2097CrossRefPubMedGoogle Scholar
  48. McClure BA (2004) S-RNase and SLF determine S-haplotype-specific pollen recognition and rejection. Plant Cell 16:2840-2847CrossRefPubMedGoogle Scholar
  49. McClure BA (2006) New views of S-RNase-based self-incompatibility. Curr Opin Plant Biol 9:639-946CrossRefPubMedGoogle Scholar
  50. McClure BA, Franklin-Tong VE (2006) Gametophytic self-incompatibility: Understanding the cellular mechanisms involved in “self ” pollen tube inhibition. Planta 224:233-245CrossRefPubMedGoogle Scholar
  51. McClure BA, Haring V, Ebert PR, Anderson MA, Simpson RJ, Sakiyama F, Clarke AE (1989) Style self-incompatibility gene products of Nicotiana alata are ribonucleases. Nature 342:955-957CrossRefPubMedGoogle Scholar
  52. McClure BA, Gray JE, Anderson MA, Clarke AE (1990) Self-incompatibility in Nicotiana alata involves degradation of pollen rRNA. Nature 347:757-760CrossRefGoogle Scholar
  53. McClure BA, Mou B, Canevascini S, Bernatzky R (1999) A small asparagine-rich protein required for S-allele-specific pollen rejection in Nicotiana. Proc Natl Acad Sci USA 96:13548-13553CrossRefPubMedGoogle Scholar
  54. McClure BA, Cruz-Garcia F, Beecher BS, Sulaman W (2000) Factors affecting inter- and intra-specific pollen rejection in Nicotiana. Ann Bot 85:113-123CrossRefGoogle Scholar
  55. McCubbin AG, Kao T-H (2000) Molecular recognition and response in pollen and pistil interac-tions. Annu Rev Cell Dev Biol 16:333-364CrossRefPubMedGoogle Scholar
  56. McCubbin AG, Wang X, Kao T-H (2000) Identification of self-incompatibility S-locus linked pollen cDNA markers in Petunia inflata. Genome 43:619-627CrossRefPubMedGoogle Scholar
  57. Murfett J, Atherton TL, Mou B, Gasser CS, McClure BA (1994) S-RNase expressed in transgenic Nicotiana causes S-allele-specific pollen rejection. Nature 367:563-566CrossRefPubMedGoogle Scholar
  58. Nasrallah JB (2005) Recognition and rejection of self in plant self-incompatibility: Comparisons to animal histocompatibility. Trends Immunol 26:412-418CrossRefPubMedGoogle Scholar
  59. O’Brien M, Kapfer C, Major G, Laurin M, Bertrand C, Kondo K, Kowyama Y, Matton DP (2002) Molecular analysis of the stylar-expressed Solanum chacoense small asparagine-rich protein family related to the HT modifier of gametophytic self-incompatibility in Nicotiana. Plant J 32:985-996CrossRefPubMedGoogle Scholar
  60. O’Brien M, Major G, Chantha S-C, Matton DP (2004) Isolation of S-RNase binding proteins from Solanum chacoense:identification of an SBP1 (RING finger protein) ortholog. Sex Plant Reprod 17:81-87CrossRefGoogle Scholar
  61. Olmstead RG, de Pamphilis CW, Wolfe AD, Young ND, Elisons WJ, Reeves PA (2001) Disintegration of the Scrophulariaceae. Am J Bot 88:348-361CrossRefPubMedGoogle Scholar
  62. Oxley D, Munro SL, Craik DJ, Bacic A (1996) Structure of N-glycans on the S3 - and S6 -allele stylar self-incompatibility ribonucleases of Nicotiana alata. Glycobiology 6:611-618CrossRefPubMedGoogle Scholar
  63. Petroski MD, Deshaies RJ (2005) Function and regulation of cullin-RING ubiquitin ligases. Nat Rev Mol Cell Biol 6:9-20CrossRefPubMedGoogle Scholar
  64. Qiao H, Wang F, Zhao L, Zhou J, Lai Z, Zhang Y, Robbins TP, Xue Y (2004a) The F-box pro-tein AhSLF-S2 controls the pollen function of S-RNase-based self-incompatibility. Plant Cell 16:2307-2322CrossRefGoogle Scholar
  65. Qiao H, Wang H, Zhao L, Zhou J, Huang J, Zhang Y, Xue Y (2004b) The F-box protein AhSLF-S2 physically interacts with S-RNases that may be inhibited by the ubiquitin/26S pro-teasome pathway of protein degradation during compatible pollination in Antirrhinum. Plant Cell 16:582-595CrossRefGoogle Scholar
  66. Roalson EH, McCubbin AG (2003) S-RNases and sexual incompatibility: Structure, functions, and evolutionary perspectives. Mol Phylogenet Evol 29:490-506CrossRefPubMedGoogle Scholar
  67. Royo J, Kunz C, Kowyama Y, Anderson MA, Clarke AE, Newbigin E (1994) Loss of a histi-dine residue at the active site of S-locus ribonuclease is associated with self-compatibility in Lycopersicon peruvianum. Proc Natl Acad Sci USA 91:6511-6514CrossRefPubMedGoogle Scholar
  68. Saba-el-Leil MK, Rivard S, Morse D, Cappadocia M (1994) The S11 and S13 self incompatibility alleles in Solanum chacoense Bitt. are remarkably similar. Plant Mol Biol 24:571-583CrossRefPubMedGoogle Scholar
  69. Sassa H, Nishio T, Kowyama Y, Hirano H, Koba T, Ikehashi H (1996) Self-incompatibility (S) alleles of the rosaceae encode members of a distinct class of the T2 /S ribonuclease superfamily. Mol Gen Genet 250:547-557PubMedGoogle Scholar
  70. Sassa H, Hirano H, Nishio T, Koba T (1997) Style-specific self-compatible mutation caused by deletion of the S-RNase gene in Japanese pear (Pyrus serotina). Plant J 12:223-227CrossRefGoogle Scholar
  71. 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 Japanese pear. Genetics 175:1869-1881CrossRefPubMedGoogle Scholar
  72. Sijacic P, Wang X, Skirpan AL, Wang Y, Dowd PE, McCubbin AG, Huang S, Kao T-H (2004) Identification of the pollen determinant of S-RNase-mediated self-incompatibility. Nature 429:302-305CrossRefPubMedGoogle Scholar
  73. Sims TL (2005) Pollen recognition and rejection in different self-incompatibility systems. Recent Res Dev Plant Mol Biol 2:31-62Google Scholar
  74. Sims TL, Ordanic M (2001) Identification of a S-ribonuclease-binding protein in Petunia hybrida. Plant Mol Biol 47:771-783CrossRefPubMedGoogle Scholar
  75. Singh A, Ai Y, Kao T-H (1991) Characterization of ribonuclease activity of three S-Allele-associated proteins of Petunia inflata. Plant Physiol 96:61-68CrossRefPubMedGoogle Scholar
  76. Sonneveld T, Tobutt KR, Vaughan SP, Robbins TP (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 17:37-51CrossRefPubMedGoogle Scholar
  77. Surbanovski N, Tobutt KR, Konstantinovic M, Maksimovic V, Sargent DJ, Stevanovic V, Boškovià ę R (2007) Self-incompatibility of Prunus tenella and evidence that reproductively isolated species of Prunus have different SFB alleles coupled with an identical S-RNase allele. Plant J 50:723-734CrossRefPubMedGoogle Scholar
  78. Takayama S, Isogai A (2005) Self-incompatibility in plants. Annu Rev Plant Biol 56:467-489CrossRefPubMedGoogle Scholar
  79. Thompson RD, Uhrig H, Hermsen JGT, Salamini F, Kaufmann H (1991) Investigation of a self-compatible mutation in Solanum tuberosum clones inhibiting S-allele activity in pollen differentially. Mol Gen Genet 226:283-288CrossRefPubMedGoogle Scholar
  80. Tsai DS, Lee HS, Post LC, Kreiling KM, Kao T-H (1992) Sequence of an S-protein of Lycop-ersicon peruvianum and comparison with other solanaceous S-proteins. Sex Plant Reprod 5:256-263CrossRefGoogle Scholar
  81. Tsukamoto T, Ando T, Watanabe H, Marchesi E, Kao T-H (2005) Duplication of the S-locus F-box gene is associated with breakdown of pollen function in an S-haplotype identified in a natural population of self-incompatible Petunia axillaris. Plant Mol Biol 57:141-153CrossRefPubMedGoogle Scholar
  82. 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 62:371-383CrossRefPubMedGoogle Scholar
  83. Ushijima K, Sassa H, Tao R, Yamane H, Dandekar AM, Gradziel TM, Hirano H (1998) Cloning and characterization of cDNAs encoding S-RNases from almond (Prunus dulcis): Primary structural features and sequence diversity of the S-RNases in Rosaceae. Mol Gen Genet 260:261-268CrossRefPubMedGoogle Scholar
  84. 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 15:771-781CrossRefPubMedGoogle Scholar
  85. Ushijima K, Yamane H, Watari A, Kakehi E, Ikeda K, Hauck NR, Iezzoni AF, 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 39:573-586CrossRefPubMedGoogle Scholar
  86. Verica JA, McCubbin AG, Kao T-H (1998) Are the hypervariable regions of S RNases sufficient for allele-specific recognition of pollen? Plant Cell 10:314-317CrossRefPubMedGoogle Scholar
  87. Vilanova S, Badenes ML, Burgos L, Martinez-Calvo J, Llacer G, Romero C (2006) Self-compatibility of two apricot selections is associated with two pollen-part mutations of different nature. Plant Physiol 142:629-641CrossRefPubMedGoogle Scholar
  88. Wang H, Xue Y (2005) Subcellular localization of the S-locus F-box protein AhSLF-S2 in pollen and pollen tubes of self-incompatible Antirrhinum. J Integr Plant Biol 47:76-83Google Scholar
  89. Wang L, Dong L, Zhang Y, Zhang Y, Wu W, Deng X, Xue Y (2004a) Genome-wide analysis of S-Locus F-box-like genes in Arabidopsis thaliana. Plant Mol Biol 56:929-945CrossRefGoogle Scholar
  90. Wang Y, Wang X, Skirpan AL, Kao T-H (2003) S-RNase-mediated self-incompatibility. J Exp Bot 54:115-122CrossRefPubMedGoogle Scholar
  91. Wang Y, Tsukamoto T, Yi KW, Wang X, Huang S, McCubbin AG, Kao T-H (2004b) Chromosome walking in the Petunia inflata self-incompatibility S-locus and gene identification in an 881-kb contig containing S2 -RNase. Plant Mol Biol 54:727-742CrossRefGoogle Scholar
  92. Woodward JR, Bacic A, Jahnen W, Clarke AE (1989) N-linked glycan chains on S-allele-associated glycoproteins from Nicotiana alata. Plant Cell 1:511-514CrossRefPubMedGoogle Scholar
  93. Woodward JR, Craik D, Dell A, Khoo KH, Munro SLA, Clarke AE, Bacic A (1992) Structural analysis of the N-linked glycan chains from a stylar glycoprotein associated with expression of self-incompatibility in Nicotiana alata. Glycobiology 2:241-250CrossRefPubMedGoogle Scholar
  94. Xue Y, Carpenter R, Dickinson HG, Coen ES (1996) Origin of allelic diversity in Antirrhinum S-locus RNases. Plant Cell 8:805-814CrossRefPubMedGoogle Scholar
  95. Yamane H, Ikeda K, Ushijima K, Sassa H, Tao R (2003a) 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 44:764-769CrossRefGoogle Scholar
  96. Yamane H, Ushijima K, Sassa H, Tao R (2003b) The use of the S-haplotype-specific F-box protein gene, SFB, as a molecular marker for S-haplotypes and self-compatibility in Japanese apricot (Prunus mume). Theor Appl Genet 107:1357-1361CrossRefGoogle Scholar
  97. Zhou J, Wang F, Ma W, Zhang Y, Han B, Xue Y (2003) Structural and transcriptional analysis of S-locus F-box (SLF) genes in Antirrhinum. Sex Plant Reprod 16:165-177CrossRefGoogle Scholar
  98. Zurek DM, Mou B, Beecher B, McClure BA (1997) Exchanging sequence domains between S-RNases from Nicotiana alata disrupts pollen recognition. Plant J 11:797-808CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2008

Authors and Affiliations

  • Y. Zhang
    • 1
  • Y. Xue
    • 1
  1. 1.Institute of Genetics and Developmental BiologyChinese Academy of Sciences and National Centre for Plant Gene ResearchChina

Personalised recommendations