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Cellular Mechanisms for Pollen Tube Growth Inhibition in Gametophytic Self-incompatibility

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The Pollen Tube

Part of the book series: Plant Cell Monographs ((CELLMONO,volume 3))

Abstract

Self-incompatibility (SI) is a mechanism used by angiosperms to prevent self-fertilization. Here we review current knowledge of two different gametophytic SI systems at the cellular level, revealing different mechanisms that interfere with pollen tube growth. In the Solanaceae, Rosaceae, and Scrophulariaceae, SI is controlled by an interaction between a pistil component, S-RNase, and a pollen component, an F-box protein, SLF/SFB. While a variety of models focused on ubiquitylation have been explored, it is still unclear exactly how the S-RNase based system operates at the cellular level. In Papaver, entirely different S-proteins act as signalling ligands that trigger a Ca 2+-dependent signalling cascade that results in programmed cell death (PCD). Although the pollen S-receptor has not been identified in Papaver, the mechanisms involved in inhibiting incompatible pollen are better understood.

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References

  1. Anderson MA, Cornish EC, Mau S-L, Williams EG, Hoggart R, Atkinson A, Bonig I, Grego B, Simpson R, Roche PJ, Haley JD, Penschow JD, Niall HD, Tregear GW, Coughlan 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

    Article  CAS  Google Scholar 

  2. Atkinson AH, Heath RL, Simpson RJ, Clarke AE, Anderson MA (1993) Proteinase inhibitors in Nicotiana alata stigmas are derived from a precursor protein which is processed into five homologous inhibitors. Plant Cell 5:203–213

    Article  CAS  PubMed  Google Scholar 

  3. Brewbaker JL (1957) Pollen cytology and self-incompatibility systems in plants. J Hered 48:271–277

    Google Scholar 

  4. Chen SH, Chen S, Tokarev AA, Liu F, Jedd G, Segev N (2005) Ypt31/32 GTPases and their novel F-box effector protein Rcy1 regulate protein recycling. Mol Biol Cell 16:178–192

    Article  CAS  PubMed  Google Scholar 

  5. Cooperman BS, Baykov AA, Lahti R (1992) Evolutionary conservation of the active site of soluble inorganic pyrophosphatase. Trends Biochem Sci 17:262–266

    Article  CAS  PubMed  Google Scholar 

  6. Cruz-Garcia F, Hancock CN, Kim D, McClure B (2005) Stylar glycoproteins bind to S-RNasein vitro. Plant J 42:295–304

    Article  CAS  PubMed  Google Scholar 

  7. Danon A, Delorme V, Mailhac N, Gallois P (2000) Plant programmed cell death: a common way to die. Plant Physiol Biochem 38:647–655

    Article  CAS  Google Scholar 

  8. de Graaf BHJ, Cheung AY, Andreyeva T, Levasseur K, Kieliszewski M, Wu H-M (2005) Rab11 GTPase-Regulated Membrane Trafficking Is Crucial for Tip-Focused Pollen Tube Growth in Tobacco. Plant Cell 17:2564–2579

    Article  PubMed  Google Scholar 

  9. Esser C, Alberti S, Höhfeld J (2004) Cooperation of molecular chaperones with the ubiquitin/proteasome system. Biochim Biophys Acta 1695:171–188

    Article  CAS  PubMed  Google Scholar 

  10. Foote HCC, Ride JP, Franklin-Tong VE, Walker EA, Lawrence MJ, Franklin FCH (1994) Cloning and Expression of a Distinctive Class of Self-Incompatibility (S) Gene from Papaver rhoeas L. Proc Natl Acad Sci USA 91:2265–2269

    Article  CAS  PubMed  Google Scholar 

  11. Franklin-Tong VE, Hackett G, Hepler PK (1997) Ratio-imaging of Ca2+iin the self-incompatibility response in pollen tubes of Papaver rhoeas. Plant J 12:1375–1386

    Article  CAS  Google Scholar 

  12. Franklin-Tong VE, Holdaway-Clarke TL, Straatman KR, Kunkel JG, Hepler PK (2002) Involvement of extracellular calcium influx in the self-incompatibility response of Papaver rhoeas. Plant J 29:333–345

    Article  CAS  PubMed  Google Scholar 

  13. Franklin-Tong VE, Ride JP, Franklin FCH (1995) Recombinant stigmatic self-incompatibility (S-) protein elicits a Ca2+transient in pollen of Papaver rhoeas. Plant J 8:299–307

    Article  CAS  Google Scholar 

  14. Franklin-Tong VE, Ride JP, Read ND, Trewavas AJ, Franklin FCH (1993) The self-incompatibility response in Papaver rhoeas is mediated by cytosolic free calcium. Plant J 4:163–177

    Article  CAS  Google Scholar 

  15. Gagne JM, Downes BP, Shiu S-h, Durski AM, Vierstra RD (2002) The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis. Proc Natl Acad Sci USA 99:11519–11524

    Article  CAS  PubMed  Google Scholar 

  16. Geitmann A (1999) Cell death of self-incompatible pollen tubes: necrosis or apoptosis? In: Cresti M, Cai G, Moscatelli A (eds) Fertilization in higher plants. Springer, Berlin, Heidelberg

    Google Scholar 

  17. Geitmann A, Franklin-Tong VE, Emons AC (2004) The self-incompatibility response in Papaver rhoeas pollen causes early and striking alterations to organelles. Cell Death Differ 11:812–822

    CAS  Google Scholar 

  18. Geitmann A, Hudak J, Vennigerholz F, Walles B (1995) Immunogold localization of pectin and callose in pollen grains and pollen tubes of Brugmansia suaveolens – implications for the self-incompatibility reaction. J Plant Physiol 147:225–235

    CAS  Google Scholar 

  19. Geitmann A, Snowman BN, Emons AC, Franklin-Tong VE (2000) Alterations in the Actin Cytoskeleton of Pollen Tubes Are Induced by the Self-Incompatibility Reaction in Papaver rhoeas. Plant Cell 12:1239–1252

    Article  CAS  PubMed  Google Scholar 

  20. Goldraij A, Kondo K, Lee CB, Hancock CN, Sivaguru M, Vasquez-Santana S, Kim S, Phillips TE, Cruz-Garcia F, McClure B (2006) Compartmentalization of S-RNase and HT-B degradation in self-incompatible Nicotiana. Nature (in press)

    Google Scholar 

  21. Hicke L, Dunn R (2003) Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Ann Rev Cell Dev Biol 19:141–172

    Article  CAS  Google Scholar 

  22. Huang S, Blanchoin L, Chaudhry F, Franklin-Tong VE, Staiger CJ (2004) A gelsolin-like protein from Papaver rhoeas Pollen (PrABP80) stimulates calcium-regulated severing and depolymerization of actin filaments. J Biol Chem 279:23364–23375

    Article  CAS  PubMed  Google Scholar 

  23. Huang S, Lee H-S, Karunanandaa B, Kao T-h (1994) Ribonuclease activity of Petunia inflata S proteins is essential for rejection of self-pollen. Plant Cell 6:1021–1028

    Article  CAS  PubMed  Google Scholar 

  24. Ida K, Norioka S, Yamamoto M, Kumasaka T, Yamashita E, Newbigin E, Clarke AE, Sakiyama F, Sato M (2001) The 1.55A resolution structure of Nicotiana alata S(F11)-RNase associated with gametophytic self-incompatibility. J Mol Biol 314:103–112

    Article  CAS  PubMed  Google Scholar 

  25. Igic B, Kohn JR (2001) Evolutionary relationships among self-incompatibility RNases. Proc Natl Acad Sci USA 98:13167–13171

    Article  CAS  PubMed  Google Scholar 

  26. 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

    Article  CAS  Google Scholar 

  27. Innes RW (2001) Mapping out the roles of MAP kinases in plant defense. Trends Plant Sci 6:392–394

    Article  CAS  PubMed  Google Scholar 

  28. Ioerger TR, Gohlke JR, Xu B, Kao T-h (1991) Primary structural features of the self-incompatibility protein in Solanaceae. Sex Plant Reprod 4:81–87

    Article  Google Scholar 

  29. Ishimizu T, Endo T, Yamaguchi-Kabata Y, Nakamura KT, Sakiyama F, Norioka S (1998) Identification of regions in which positive selection may operate in S-RNase of Rosaceae: Implication for S-allele-specific recognition sites in S-RNase. FEBS Lett 440:337–342

    Article  CAS  PubMed  Google Scholar 

  30. Jordan ND, Franklin FCH, Franklin-Tong VE (2000) Evidence for DNA fragmentation triggered in the self-incompatibility response in pollen of Papaver rhoeas. Plant J 23:471–479

    Article  CAS  PubMed  Google Scholar 

  31. Kakeda K, Jordan ND, Conner A, Ride JP, Franklin-Tong VE, Franklin FCH (1998) Identification of residues in a hydrophilic loop of the Papaver rhoeas S protein that play a crucial role in recognition of incompatible pollen. Plant Cell 10:1723–1731

    Article  CAS  PubMed  Google Scholar 

  32. Kao T-h, Tsukamoto T (2004) The molecular and genetic bases of S-RNase-based self-incompatibility. Plant Cell 16:72–83

    Article  Google Scholar 

  33. Katzmann D, Sarkar S, Chu T, Audhya A, Emr SD (2004) Multivesicular body sorting: ubiquitin ligase Rsp5 is required for the modification and sorting of carboxypeptidase S. Mol Biol Cell 15:468–480

    Article  CAS  PubMed  Google Scholar 

  34. Kipreos ET, Pagano M (2000) The F-box protein family. Gen Biol 2000 1:3002.3001–3002.3007

    Google 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 50:29–42

    Article  CAS  PubMed  Google Scholar 

  36. Lee H-S, Huang S, Kao T-h (1994) S proteins control rejection of incompatible pollen in Petunia inflata. Nature 367:560–563

    Article  CAS  PubMed  Google Scholar 

  37. 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 9:75–86

    Article  Google Scholar 

  38. Luu D-t, 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 159:329–335

    CAS  Google Scholar 

  39. Luu D-T, Qin X, Morse D, Cappadocia M (2000) S-RNase uptake by compatible pollen tubes in gametophytic self-incompatibility. Nature 407:649–651

    Article  CAS  PubMed  Google Scholar 

  40. Matton DP, Maes O, Laublin G, Xike Q, Bertrand C, Morse D, Cappadocia M (1997) Hypervariable domains of self-incompatibility RNases mediate allele-specific pollen recognition. Plant Cell 9:1757–1766

    Article  CAS  PubMed  Google Scholar 

  41. Matton DP, Nass N, Clarke AE, Newbigin E (1994) Self-Incompatibility: How plants avoid ilegitimate offspring. Proc Natl Acad Sci USA 91:1992–1997

    Article  CAS  PubMed  Google Scholar 

  42. McClure BA, Cruz-Garcia F, Beecher BS, Sulaman W (2000) Factors affecting inter- and intra-specific pollen rejection in Nicotiana. Ann Bot 85:113–123

    Article  Google Scholar 

  43. McClure BA, Gray JE, Anderson MA, Clarke AE (1990) Self-incompatibility in Nicotiana alata involves degradation of pollen rRNA. Nature 347:757–760

    Article  CAS  Google Scholar 

  44. 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 342:955–957

    Article  CAS  PubMed  Google Scholar 

  45. McClure BA, Mou B, Canevascini S, Bernatzky R (1999) A small asparagine-rich protein required for S-allele-specific pollen rejection in Nicotiana. Proc Nat Acad Sci USA 96:13548–13553

    Article  CAS  PubMed  Google Scholar 

  46. 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

    Article  CAS  PubMed  Google Scholar 

  47. 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 32:1–12

    Article  Google Scholar 

  48. Qiao H, Wang F, 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  CAS  PubMed  Google Scholar 

  49. Qiao H, Wang H, Zhao L, Zhou J, Huang J, Zhang Y, Xue Y (2004a) 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

    Google Scholar 

  50. Rudd JJ, Franklin FCH, Lord JM, Franklin-Tong VE (1996) Increased Phosphorylation of a 26-kD Pollen Protein Is Induced by the Self-Incompatibility Response in Papaver rhoeas. Plant Cell 8:713–724

    Article  CAS  PubMed  Google Scholar 

  51. Rudd JJ, Osman K, Franklin FCH, Franklin-Tong VE (2003) Activation of a putative MAP kinase in pollen is stimulated by the self-incompatibility (SI) response. FEBS Lett 547:223–227

    Article  CAS  PubMed  Google Scholar 

  52. Sage TL, Bertin RI, Williams EG (1994) Ovarian and other late-acting self-incompatibility systems. Kluwer Academic Publishers, Dordrecht

    Google Scholar 

  53. Sijacic P, Wang X, Skirpan A, Wang Y, Dowd P, McCubbin A, Huang S, Kao T-h (2004) Identification of the pollen determinant of S-RNase-mediated self-incompatibility. Nature 429:302–305

    Article  CAS  PubMed  Google Scholar 

  54. Sims TL, Ordanic M (2001) Identification of a S-ribonuclease binding protein in Petunia hybrida. Plant Mol Biol 47:771–783

    Article  CAS  PubMed  Google Scholar 

  55. Snowman BN, Kovar DR, Shevchenko G, Franklin-Tong VE, Staiger CJ (2002) Signal-Mediated Depolymerization of Actin in Pollen during the Self-Incompatibility Response. Plant Cell 14:2613–2626

    Article  CAS  PubMed  Google Scholar 

  56. Staiger CJ (2000) Signaling to the actin cytoskeleton in plants. Ann Rev Plant Physiol Plant Mol Biol 51:257–288

    Article  CAS  Google Scholar 

  57. Takayama S, Isogai A (2005) Self-incompatibility in plants. Annu Rev Plant Biol 56:467–489

    Article  CAS  PubMed  Google Scholar 

  58. Thomas SG, Franklin-Tong VE (2004) Self-incompatibility triggers programmed cell death in Papaver pollen. Nature 429:305–309

    Article  CAS  PubMed  Google Scholar 

  59. 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  CAS  PubMed  Google Scholar 

  60. 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

    Article  CAS  PubMed  Google Scholar 

  61. van Doorn WG, Woltering EJ (2005) Many ways to exit? Cell death categories in plants. Trends Plant Sci 10:117–122

    PubMed  Google Scholar 

  62. Willems AR, Schwab M, Tyers M (2004) A hitchhiker's guide to the cullin ubiquitin ligases: SCF and its kin. Biochim Biophys Acta 1695:133–170

    Article  CAS  PubMed  Google Scholar 

  63. Yang KY, Liu Y, Zhang S (2001) Activation of a mitogen-activated protein kinase pathway is involved in disease resistance in tobacco. Proc Natl Acad Sci USA 98:741–746

    Article  CAS  PubMed  Google Scholar 

  64. Yao N, Eisfelder BJ, Marvin J, Greenberg JT (2004) The mitochondrion – an organelle commonly involved in programmed cell death in Arabidopsis thaliana. Plant J 40:596–610

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

Research in the lab of VEF-T is supported by Biotechnology and Biological Sciences Research Council (BBSRC). Research in the lab of BAM is supported by U. S. National Science Foundation grant 03-15647.

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Authors and Affiliations

  1. School of Biosciences, University of Birmingham, Edgbaston, B15 2TT, Birmingham, UK

    Barend H. J. de Graaf & Noni (V. E.) Franklin-Tong

  2. Division of Biological Sciences, University of Missouri–Columbia, 105 Tucker Hall, 65211-7310, Columbia, MO, USA

    Chris Lee

  3. Department of Biochemistry, University of Missouri–Columbia, 105 Life Sciences Center, 65211-7310, Columbia, MO, USA

    Chris Lee & Bruce A. McClure

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  1. Barend H. J. de Graaf
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  2. Chris Lee
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  3. Bruce A. McClure
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  4. Noni (V. E.) Franklin-Tong
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Correspondence to Noni (V. E.) Franklin-Tong .

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Rui Malhó

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de Graaf, B.H.J., Lee, C., McClure, B.A., Franklin-Tong, N.(. Cellular Mechanisms for Pollen Tube Growth Inhibition in Gametophytic Self-incompatibility. In: Malhó, R. (eds) The Pollen Tube. Plant Cell Monographs, vol 3. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7089_050

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