Plant Molecular Biology

, Volume 70, Issue 5, pp 499–509 | Cite as

Genetic features of a pollen-part mutation suggest an inhibitory role for the Antirrhinum pollen self-incompatibility determinant

  • Yongbiao Xue
  • Yijing Zhang
  • Qiuying Yang
  • Qun Li
  • Zhukuan Cheng
  • Hugh G. Dickinson


Self-incompatibility (SI), an important barrier to inbreeding in flowering plants, is controlled in many species by a single polymorphic S-locus. In the Solanaceae, two tightly linked S-locus genes, S-RNase and SLF (S-locus F-box)/SFB (S-haplotype-specific F-box), control SI expression in pistil and pollen, respectively. The pollen S-determinant appears to function to inhibit all but self S-RNase in the Solanaceae, but its genetic function in the closely-related Plantaginaceae remains equivocal. We have employed transposon mutagenesis in a member of the Plantaginaceae (Antirrhinum) to generate a pollen-part SI-breakdown mutant Pma1 (Pollen-part mutation in Antirrhinum1). Molecular genetic analyses showed that an extra telocentric chromosome containing AhSLF-S 1 is present in its self-compatible but not in its SI progeny. Furthermore, analysis of the effects of selection revealed positive selection acting on both SLFs and SFBs, but with a stronger purifying selection on SLFs. Taken together, our results suggest an inhibitor role of the pollen S in the Plantaginaceae (as represented by Antirrhinum), similar to that found in the Solanaceae. The implication of these findings is discussed in the context of S-locus evolution in flowering plants.


Self-incompatibility Antirrhinum SLF Pollen-part mutation S-RNase 



We thank Enrico Coen and Rosemary Carpenter for providing Antirrhinum plants and constant support and advice, Peter Walker for growing the plants and Ruth McGrath, Gwyneth Ingram and Richard Waites for their involvement in the mutagenesis work. This work was supported by the Ministry of Science and Technology of China (2007CB947603) to Y. Xue and the UK Biotechnology and Biological Sciences Research Council to H.D.

Supplementary material

11103_2009_9487_MOESM1_ESM.doc (7.7 mb)
Supplementary material 1 (DOC 7927 kb)


  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 321:38–44. doi: 10.1038/321038a0 CrossRefGoogle Scholar
  2. Brewbaker JL, Natarajan AT (1960) Centric fragments and pollen-part mutation of self-incompatibility alleles in Petunia. Genetics 45:699–704PubMedGoogle Scholar
  3. Brieger FG (1935) The inheritance of self-sterility and the peloric flower shape in Antirrhinum. Genetica 17:385–408. doi: 10.1007/BF01508186 CrossRefGoogle Scholar
  4. Burton TL, Husband BC (2000) Fitness differences among diploids, tetraploids, and their triploid progeny in Chamerion angustifolium: mechanisms of inviability and implications for polyploid evolution. Evol Int J Org Evol 54:1182–1191Google Scholar
  5. Carpenter R, Martin C, Coen ES (1987) Comparison of genetic behavior of the transposable element Tam3 at two unlinked pigment loci in Antirrhinum majus. Mol Gen Genet 207:82–89. doi: 10.1007/BF00331494 CrossRefGoogle Scholar
  6. de Nettancourt D (2001) Incompatibility and incongruity in wild and cultivated plants. Springer, HeidelbergGoogle Scholar
  7. Dodds PN, Clarke AE, Newbigin E (1996) A molecular perspective on pollination in flowering plants. Cell 85:141–144. doi: 10.1016/S0092-8674(00)81090-9 PubMedCrossRefGoogle Scholar
  8. Entani T, Takayama S, Iwano M, Shiba H, Che FS, Isogai A (1999) Relationship between polyploidy and pollen self-incompatibility phenotype in Petunia hybrida Vilm. Biosci Biotechnol Biochem 63:1882–1888. doi: 10.1271/bbb.63.1882 PubMedCrossRefGoogle Scholar
  9. 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. Genes Cells 8:203–213. doi: 10.1046/j.1365-2443.2003.00626.x PubMedCrossRefGoogle Scholar
  10. Franklin-Tong VE, Franklin FCH (2003) Gametophytic self-incompatibility inhibits pollen tube growth using different mechanisms. Trends Plant Sci 8:598–605. doi: 10.1016/j.tplants.2003.10.008 PubMedCrossRefGoogle Scholar
  11. 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 439:805–810PubMedCrossRefGoogle Scholar
  12. 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
  13. 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 98:15372–15376. doi: 10.1073/pnas.261571598 PubMedCrossRefGoogle Scholar
  14. Hauck N, Yamane H, Tao R, Iezzoni A (2002) Self-compatibility and incompatibility in tetraploid sour cherry (Prunus cerasus L.). Sex Plant Reprod 15:39–46. doi: 10.1007/s00497-002-0136-6 CrossRefGoogle Scholar
  15. Hauck NR, Ikeda K, Tao R, Iezzoni AF (2006a) The mutated S 1-haplotype in sour cherry has an altered S-haplotype-specific F-box protein gene. J Hered 97:514–520. doi: 10.1093/jhered/esl029 PubMedCrossRefGoogle Scholar
  16. 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. doi: 10.1534/genetics.105.049395 PubMedCrossRefGoogle Scholar
  17. Hicke L, Dunn R (2003) Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cell Dev Biol 19:141–172. doi: 10.1146/annurev.cellbio.19.110701.154617 PubMedCrossRefGoogle Scholar
  18. 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 18:2531–2553. doi: 10.1105/tpc.106.041061 PubMedCrossRefGoogle Scholar
  19. Hua Z, Kao T-H (2008) Identification of major lysine residues of S(3)-RNase of Petunia inflata involved in ubiquitin-26S proteasome-mediated degradation in vitro. Plant J 54:1094–1104. doi: 10.1111/j.1365-313X.2008.03487.x PubMedCrossRefGoogle Scholar
  20. Hua Z, Meng X, Kao TH (2007) Comparison of Petunia inflata S-Locus F-Box Protein (Pi SLF) with Pi SLF like proteins reveals its unique function in S-RNase based self-incompatibility. Plant Cell 19:3593–3609. doi: 10.1105/tpc.107.055426 PubMedCrossRefGoogle 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 46:780–793. doi: 10.1111/j.1365-313X.2006.02735.x PubMedCrossRefGoogle Scholar
  22. 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 16:235–243. doi: 10.1007/s00497-003-0200-x CrossRefGoogle Scholar
  23. Kao T-H, McCubbin AG (1996) How flowering plants discriminate between self and non-self pollen to prevent inbreeding. Proc Natl Acad Sci USA 93:12059–12065. doi: 10.1073/pnas.93.22.12059 PubMedCrossRefGoogle Scholar
  24. Kao T-H, Tsukamoto T (2004) The molecular and genetic bases of S-RNase-based self-incompatibility. Plant Cell 16(Suppl):S72–S83. doi: 10.1105/tpc.016154 CrossRefGoogle Scholar
  25. 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. doi: 10.1023/A:1016050018779 PubMedCrossRefGoogle Scholar
  26. Lee HS, Huang S, Kao T-H (1994) S proteins control rejection of incompatible pollen in Petunia inflata. Nature 367:560–563. doi: 10.1038/367560a0 PubMedCrossRefGoogle Scholar
  27. Livermore JR, Johnstone FE (1940) The effect of chromosome doubling on the crossability of Solanum chacoense, S. jamesii and S. bulbocastanum with S. tuberosum. Am Potato J 17:170–173. doi: 10.1007/BF02892035 CrossRefGoogle Scholar
  28. Luo D, Carpenter R, Vincent C, Copsey L, Coen E (1996) Origin of floral asymmetry in Antirrhinum. Nature 383:794–799. doi: 10.1038/383794a0 PubMedCrossRefGoogle Scholar
  29. Luu DT, Qin X, Morse D, Cappadocia M (2000) S-RNase uptake by compatible pollen tubes in gametophytic self-incompatibility. Nature 407:649–651. doi: 10.1038/35036623 PubMedCrossRefGoogle Scholar
  30. Mable BK (2004) Polyploidy and self-incompatibility: is there an association? New Phytol 162:803–811. doi: 10.1111/j.1469-8137.2004.01055.x CrossRefGoogle Scholar
  31. Martin FW (1959) Staining and observing pollen tubes in the style by means of fluorescence. Stain Technol 34:125–128PubMedGoogle Scholar
  32. McClure BA (2006) New views of S-RNase-based self-incompatibility. Curr Opin Plant Biol 9:639–646. doi: 10.1016/j.pbi.2006.09.004 PubMedCrossRefGoogle Scholar
  33. McClure BA, Franklin-Tong VE (2006) Gametophytic self-incompatibility: understanding the cellular mechanisms involved in “self” pollen tube inhibition. Planta 224:233–245. doi: 10.1007/s00425-006-0284-2 PubMedCrossRefGoogle Scholar
  34. McClure BA, Gray JE, Anderson MA, Clarke AE (1990) Self-incompatibility in Nicotiana alata involves degradation of pollen rRNA. Nature 347:757–760. doi: 10.1038/347757a0 CrossRefGoogle Scholar
  35. Mukhopadhyay D, Riezman H (2007) Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 315:201–205. doi: 10.1126/science.1127085 PubMedCrossRefGoogle Scholar
  36. Murfett J, Atherton TL, Mou B, Gasser CS, McClure BA (1994) S-RNase expressed in transgenic Nicotiana causes S-allele-specific pollen rejection. Nature 367:563–566. doi: 10.1038/367563a0 PubMedCrossRefGoogle Scholar
  37. Newbigin E, Uyenoyama MK (2005) The evolutionary dynamics of self-incompatibility systems. Trends Genet 21:500–505. doi: 10.1016/j.tig.2005.07.003 PubMedCrossRefGoogle Scholar
  38. Newbigin E, Paape T, Kohn JR (2008) RNase-based self-incompatibility: puzzled by pollen S. Plant Cell 20:2286–2292. doi: 10.1105/tpc.108.060327 PubMedCrossRefGoogle Scholar
  39. Pandy KK (1965) Centric chromosome fragments and pollen-part mutation of the incompatibility gene in Nicotiana alata. Nature 206:792–795. doi: 10.1038/206792a0 CrossRefGoogle Scholar
  40. Pickart CM (2001) Mechanisms underlying ubiquitination. Annu Rev Biochem 70:503–533. doi: 10.1146/annurev.biochem.70.1.503 PubMedCrossRefGoogle Scholar
  41. Qiao H, Wang F, Zhao L, Zhou J, Lai Z, Zhang Y, Robbins TP, Xue Y (2004a) The F-box protein AhSLF-S2 controls the pollen function of S-RNase-based self-incompatibility. Plant Cell 16:2307–2322. doi: 10.1105/tpc.104.024919 PubMedCrossRefGoogle Scholar
  42. 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 proteasome pathway of protein degradation during compatible pollination in Antirrhinum. Plant Cell 16:582–595. doi: 10.1105/tpc.017673 PubMedCrossRefGoogle Scholar
  43. 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 175:1869–1881. doi: 10.1534/genetics.106.068858 PubMedCrossRefGoogle Scholar
  44. 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 429:302–305. doi: 10.1038/nature02523 PubMedCrossRefGoogle Scholar
  45. 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 17:37–51. doi: 10.1105/tpc.104.026963 PubMedCrossRefGoogle Scholar
  46. Stout AB, Chandler C (1941) Change from self-incompatibility to self-compatibility accompanying change from diploidy to tetraploidy. Science 94:118. doi: 10.1126/science.94.2431.118 PubMedCrossRefGoogle Scholar
  47. Stout AB, Chandler C (1942) Hereditary transmission of induced tetraploidy and compatibility in fertilization. Science 96:257–258. doi: 10.1126/science.96.2489.257-a PubMedCrossRefGoogle Scholar
  48. Straub J (1941) Breakdown of self-incompatibility by polyploidization. (Die Beseitigung der Selbststerilitat durch Polyploidisierung). Ber Dtsch Bot Ges 59:296–304Google Scholar
  49. Takayama S, Isogai A (2005) Self-incompatibility in plants. Annu Rev Plant Biol 56:467–489. doi: 10.1146/annurev.arplant.56.032604.144249 PubMedCrossRefGoogle Scholar
  50. 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 62:371–383. doi: 10.1007/s11103-006-9026-x PubMedCrossRefGoogle Scholar
  51. Ushijima K, Sassa H, Tamura M, Kusaba M, Tao R, Gradziel TM, Dandekar AM, Hirano H (2001) Characterization of the S-locus region of almond (Prunus dulcis): analysis of a somaclonal mutant and a cosmid contig for an S haplotype. Genetics 158:379–386PubMedGoogle Scholar
  52. 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. doi: 10.1105/tpc.009290 PubMedCrossRefGoogle Scholar
  53. 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 39:573–586. doi: 10.1111/j.1365-313X.2004.02154.x PubMedCrossRefGoogle Scholar
  54. Uyenoyama MK, Zhang Y, Newbigin E (2001) On the origin of self-incompatibility haplotypes: transition through self-compatible intermediates. Genetics 157:1805–1817PubMedGoogle Scholar
  55. Vaughan SP, Russell K, Sargent DJ, Tobutt KR (2006) Isolation of S-locus F-box alleles in Prunus avium and their application in a novel method to determine self-incompatibility genotype. Theor Appl Genet 112:856–866. doi: 10.1007/s00122-005-0187-9 PubMedCrossRefGoogle Scholar
  56. 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 142:629–641. doi: 10.1104/pp.106.083865 PubMedCrossRefGoogle Scholar
  57. Wang Y, Tsukamoto T, Yi KW, Wang X, Huang S, McCubbin AG, Kao T-H (2004) Chromosome walking in the Petunia inflata self-incompatibility (S-) locus and gene identification in an 881-kb contig containing S 2-RNase. Plant Mol Biol 54:727–742. doi: 10.1023/B:PLAN.0000040901.98982.82 PubMedCrossRefGoogle Scholar
  58. Wheeler D, Newbigin E (2007) Expression of 10 S-class SLF-like genes in Nicotiana alata pollen and its implications for under-standing the pollen factor of the S locus. Genetics 177:2171–2180. doi: 10.1534/genetics.107.076885 PubMedCrossRefGoogle Scholar
  59. Wright S (1939) The distribution of self-sterility alleles in populations. Genetics 24:538–552PubMedGoogle Scholar
  60. Xue Y (2000) Establishment of the self-incompatibility (S) locus-directed transposon tagging system in Antirrhinum. Acta Bot Sin 42:408–415Google Scholar
  61. Xue Y, Carpenter R, Dickinson HG, Coen ES (1996) Origin of allelic diversity in Antirrhinum S locus RNases. Plant Cell 8:805–814PubMedCrossRefGoogle Scholar
  62. Yang Q, Zhang D, Li Q, Cheng Z, Xue Y (2007) Heterochromatic and genetic features are consistent with recombination suppression of the self-incompatibility locus in Antirrhinum. Plant J 51:140–151. doi: 10.1111/j.1365-313X.2007.03127.x PubMedCrossRefGoogle Scholar
  63. Zhang J, Nielsen R, Yang Z (2005) Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol Biol Evol 22:2472–2479. doi: 10.1093/molbev/msi237 PubMedCrossRefGoogle Scholar
  64. 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 16:165–177. doi: 10.1007/s00497-003-0185-5 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Yongbiao Xue
    • 1
  • Yijing Zhang
    • 1
    • 4
  • Qiuying Yang
    • 1
    • 4
  • Qun Li
    • 1
  • Zhukuan Cheng
    • 2
  • Hugh G. Dickinson
    • 3
  1. 1.Laboratory of Molecular and Developmental Biology, Institute of Genetics and Developmental BiologyChinese Academy of Sciences and National Center for Plant Gene ResearchChaoyang District, BeijingChina
  2. 2.The State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental BiologyChinese Academy of Sciences and National Center for Plant Gene ResearchBeijingChina
  3. 3.Department of Plant SciencesUniversity of OxfordOxfordUK
  4. 4.Graduate University of Chinese Academy of SciencesBeijingChina

Personalised recommendations