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Gametophytic self-incompatibility: understanding the cellular mechanisms involved in “self” pollen tube inhibition

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Abstract

Self-incompatibility (SI) prevents the production of “self” seed and inbreeding by providing a recognition and rejection system for “self,” or genetically identical, pollen. Studies of gametophytic SI (GSI) species at a molecular level have identified two completely different S-genes and SI mechanisms. One GSI mechanism, which is found in the Solanaceae, Rosaceae and Scrophulariaceae, has S-RNase as the pistil S-component and an F-box protein as the pollen S-component. However, non-S-locus factors are also required. In an incompatible situation, the S-RNases degrade pollen RNA, thereby preventing pollen tube growth. Here, in the light of recent evidence, we examine alternative models for how compatible pollen escapes this cytotoxic activity. The other GSI mechanism, so far found only in the Papaveraceae, has a small secreted peptide, the S-protein, as its pistil S-component. The pollen S-component remains elusive, but it is thought to be a transmembrane receptor, as interaction of the S-protein with incompatible pollen triggers a signaling network, resulting in rapid actin depolymerization and pollen tube inhibition and programmed cell death (PCD). Here, we present an overview of what is currently known about the mechanisms involved in regulating pollen tube inhibition in these two GSI systems.

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Abbreviations

SI:

Self-incompatibility

GSI:

Gametophytic self-incompatibility

[Ca2+]i :

Intracellular cytosolic free calcium concentration

ECM:

Extracellular matrix

ABP:

Actin binding protein

MAPK:

Mitogen activated protein kinase

PCD:

Programmed cell death

PARP:

Poly (ADP-ribose) polymerase

cyt c:

Cytochrome c

S-RNase:

S-locus ribonuclease

SLF/SFB:

S-locus F-box

 120K:

120 kDa glycoprotein

SC:

Self-compatible

References

  • Ai Y, Kron E, Kao T-H (1991) S-alleles are retained and expressed in a self-compatible cultivar of Petunia hybrida. Mol Gen Genet 230:353–358

    Article  PubMed  CAS  Google Scholar 

  • Anderson MA, Cornish EC, Mau S-L, Williams EG, Hoggart R, Atkinson A, Bönig 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 

  • Anderson M, McFadden G, Bernatzky R, Atkinson A, Orpin T, Dedman H, Tregear G, Fernley R, AE Clark (1989) Sequence variability of three alleles of the self-incompatibility gene of Nicotiana alata. Plant Cell 1:483–491

    Article  PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • Balk J, Leaver CJ, McCabe PF (1999) Translocation of cytochrome c from the mitochondria to the cytosol occurs during heat-induced programmed cell death in cucumber plants. FEBS Lett 463:151–154

    Article  PubMed  CAS  Google Scholar 

  • Bernatzky R, Glaven RH, Rivers BA (1995) S-related protein can be recombined with self-compatibility in interspecific derivatives of Lycopersicon. Biochem Genet 33:215–225

    Article  PubMed  CAS  Google Scholar 

  • Bredemeijer GMM, Blaas J (1981) S-Specific proteins in styles of self-incompatible Nicotiana alata. Theor Appl Genet 59:185–190

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Cheung AY, Wu H-M (2001) Pollen-tube guidance-right on target. Science 293:1441–1442

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Danon A, Rotari VI, Gordon A, Mailhac N, Gallois P (2004) Ultraviolet-C overexposure induces programmed cell death in Arabidopsis, which is mediated by caspase-like activities and which can be suppressed by caspase inhibitors, p35 and defender against apoptotic death. J Biol Chem 279:779–787

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Feijó JA, Sainhas J, Holdaway-Clarke TL, Cordeiro MS, Kunkel JG, Hepler PK (2001) Cellular oscillations and the regulation of growth: the pollen tube paradigm. BioEssays 23:86–94

    Article  PubMed  Google Scholar 

  • 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 Nat Acad Sci USA 91:2265–2269

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

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

    Article  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • Fu Y, Wu G, Yang Z (2001) Rop GTPase-dependent dynamics of tip-localized F-actin control tip growth in pollen tubes. J Cell Biol 152:1019–1032

    Article  PubMed  CAS  Google Scholar 

  • Galan J-M, Wiederkehr A, Seol JH, Haguenauer-Tsapis R, Deshaies RJ, Riezman H, Peter M (2001) Skp1p and the F-box protein Rcy1p form a non-SCF complex involved in recycling of the SNARE Snc1p in yeast. Mol Cell Biol 21:3105–3117

    Article  PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • Goldraij A, Kondo K, Lee CB, Hancock CN, Sivaguru M, Vazquez-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 439:805–810

    Article  PubMed  CAS  Google Scholar 

  • 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 152:1123–1135

    PubMed  CAS  Google Scholar 

  • Golz JF, Oh H-Y, 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 Nat Acad Sci USA 98:15372–15376

    Article  PubMed  CAS  Google Scholar 

  • 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  CAS  Google Scholar 

  • Gray JE, McClure BA, Bönig I, Anderson MA, Clarke AE (1991) Action of the style product of the self-incompatibility gene of Nicotiana alata (S-RNase) on in vitro-grown pollen tubes. Plant Cell 3:271–283

    Article  PubMed  CAS  Google Scholar 

  • Greenberg JT, Yao N (2004) The role and regulation of programmed cell death in plant-pathogen interactions. Cell Microbiol 6:201–211

    Article  PubMed  CAS  Google Scholar 

  • Hancock CN, Kent L, BA McClure (2005) The 120 kDa glycoprotein is required for S-specific pollen rejection in Nicotiana. Plant J 43:716–723

    Article  PubMed  CAS  Google Scholar 

  • Haring V, Gray JE, McClure B, Anderson MA, Clarke A (1990) Self-Incompatibility: A Self-Recognition System in Plants. Science 250:937–941

    Article  PubMed  CAS  Google Scholar 

  • Higashiyama T, Yabe S, Sasaki N, Nishimura Y, Miyagishima S, Kuroiwa H, Kuroiwa T (2001) Pollen tube attraction by the synergid cell. Science 293:1480–1483

    Article  PubMed  CAS  Google Scholar 

  • Hiscock SJ, McInnis SM (2003) Pollen recognition and rejection during the sporophytic self-incompatibility response: Brassica and beyond. Trends Plant Sci 8:606–613

    Article  PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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 

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

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • Jahnen W, Batterham MP, Clarke AE, Moritz RL, Simpson RJ (1989) Identification, isolation, and N-terminal sequencing of style glycoproteins associated with self-incompatibility in Nicotiana alata. Plant Cell 1:493–499

    Article  PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • 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 

  • Kornberg A (1962) On the metabolic significance of phosphorolytic and pyrophosphorolytic reactions. Academic, New York pp 251–264

    Google Scholar 

  • Kuriyama H, Fukuda H (2002) Developmental programmed cell death in plants. Curr Opin Plant Biol 5:568–573

    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 

  • Lam E, del Pozo O (2000) Caspase-like proteases involvement in the control of plant cell death. Plant Mol Biol 44:417–428

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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 

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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Malho R, Read ND, Pais MS, Trewavas AJ (1994) Role of cytosolic-free calcium in the reorientation of ppollen- tube growth. Plant J 5:331–341

    Article  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • McClure BA (2004) S-RNase and SLF determine S-haplotype-specific pollen recognition and rejection. Plant Cell 16:2840–2847

    Article  PubMed  CAS  Google Scholar 

  • McClure BA, Haring V, Ebert PR, Anderson MA, Simpson RJ, Sakiyama F, Clarke A (1989) Style self-incompatibility gene products of Nicotiana alata are ribonucleases. Nature 342:955–957

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • de Nettancourt D (1977) Incompatibility in angiosperms. Springer, Berlin Heidelberg New York

    Google Scholar 

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

    Google Scholar 

  • 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 asparagine-rich protein family related to the HT modifier of gametophytic self-incompatibility in Nicotiana. Plant J 32:1–12

    Article  Google Scholar 

  • Pierson ES, Miller DD, Callaham DA, van Aken J, Hackett G, Hepler PK (1996) Tip-localized calcium entry fluctuates during pollen tube growth. Dev Biol 174:160–73

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • Samaj J, Ovecka M, Hlavacka A, Lecourieux F, Meskiene I, Lichtscheidl I, Lenart P, Salaj J, Volkmann D, Bogre L, Baluska F, Hirt H (2002) Involvement of the mitogen-activated protein kinase SIMK in regulation of root hair tip growth. EMBO J 21:3296–3306

    Article  PubMed  CAS  Google Scholar 

  • Sanchez AM, Bosch M, Bots M, Nieuwland J, Feron R, Mariani C (2004) Pistil factors controlling pollination. Plant Cell 16:98–106

    Article  Google Scholar 

  • Schaller A (2004) A cut above the rest: the regulatory function of plant proteases. Planta 220:183–197

    Article  PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Swanson R, Edlund AF, Preuss D (2004) Species specificity in pollen-pistil interactions. Ann Rev of Genet 38:793–818

    Article  CAS  Google Scholar 

  • Swidzinski JA, Sweetlove LJ, Leaver CJ (2002) A custom microarray analysis of gene expression during programmed cell death in Arabidopsis thaliana. Plant J 30:431–446

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Tsukamoto T, Ando T, Kokubun H, Watanabe H, Sato T, Masada M, Marchesi E, Kao T-h (2003) Breakdown of self-incompatibility in a natural population of Petunia axillaris caused by a modifier locus that suppresses the expression of an S-RNase gene. Sex Plant Reprod 15:255–263

    CAS  Google Scholar 

  • 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-compatible Petunia axillaris. Plant Mol Biol 57:141–153

    Article  PubMed  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 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  PubMed  CAS  Google Scholar 

  • Walles B, Han SP (1998) Ribosomes in incompatible pollen tubes in the Solanaceae. Physiol Plant 103:461–465

    Article  CAS  Google Scholar 

  • Woltering EJ, van der Bent A, Hoeberichts FA (2002) Do plant caspases exist? Plant Physiol 130:1764–1769

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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  PubMed  CAS  Google Scholar 

  • Zhang S, Liu Y (2001) Activation of salicylic acid-induced protein kinase, a mitogen-activated protein kinase, induces multiple defense responses in tobacco. Plant Cell 13:1877–1889

    Article  PubMed  CAS  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. We thank Melody Kroll for manuscript assistance.

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  1. Department of Biochemistry, 105 Christopher S. Bond Life Sciences Center, 1201 E. Rollins St., Columbia, MO, 65211-7310, USA

    Bruce A. McClure

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

    Vernonica Franklin-Tong

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  1. Bruce A. McClure
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  2. Vernonica Franklin-Tong
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Correspondence to Vernonica Franklin-Tong.

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McClure, B.A., Franklin-Tong, V. Gametophytic self-incompatibility: understanding the cellular mechanisms involved in “self” pollen tube inhibition. Planta 224, 233–245 (2006). https://doi.org/10.1007/s00425-006-0284-2

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