Skip to main content
Log in

The molecular biology of self-incompatibility systems in flowering plants

  • Published:
Plant Cell, Tissue and Organ Culture Aims and scope Submit manuscript

Abstract

Self-incompatibility is a common mechanism by which flowering plants can exert some control over the process of fertilization. Typically, the self-incompatibility response involves the recognition and rejection of self-incompatible pollen which leads to a block in self-fertilization and, as a consequence, promotes outcrossing. In recent years, considerable progress has been made in the molecular understanding of several self-incompatibility systems. Interestingly, a common mechanism for self-incompatibility is not employed by all flowering plants, but in fact quite diverse mechanisms have been recruited for the rejection of self-incompatible pollen. In this review, the recent advances in the self-incompatibility systems of the Solanaceae, Papaveraceae, and Brassicaceae will be described as well as some of the molecular work that is emerging for the Poaceae and the heteromorphic self-incompatibility systems.

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

  • Anderson MA, Cornish EC, Mau S-L, Willams EG, Hoggart R, Atkinson A, Bonig I, Grego B, Simpson R, Roche PJ, Haley JD, Penschow JD, Niall H, Tregar GW, Coghlan JP, Crawford RJ & Clarke AE (1986) Cloning of cDNA for a stylar glycoprotein associated with the expression of self-incompatibility in Nicotiana alata. Nature 321: 38–43

    Google Scholar 

  • Anthanasiou A & Shore JS (1997) Morph-specific proteins in pollen and styles of diystylous Turnera (Turneraceae). Genetics 146: 669–679

    Google Scholar 

  • Ai Y, Singh A, Coleman CE, Ioerger TR, Kheryr-Pour & Kao Th (1990) Self-incompatibility in Petunia inflata: isolation and characterization of cDNAs encoding three S-allele-associated proteins. Sex. Plant Reprod. 3: 130–138

    Google Scholar 

  • 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

    Google Scholar 

  • Barrett SCH & Curzan MB (1994) Incompatibility in heterostylous plants. In: Willams EG, Clarke AE & Knox (eds) Genetic Control of Self-incompatibility and Reproductive Development in Flowering Plants (pp. 189–219). Kluwer Academic Publishers, London

    Google Scholar 

  • Bateman AJ (1955) Self-incompatibility systems in angiosperms. III. Cruciferae. Heredity 9: 53–68

    Google Scholar 

  • Bauman U, Juttner J, Bian X & Langridge P (2000) Selfincompatibility in the grasses. Ann. Bot. 85: 203–209

    Google Scholar 

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

    Google Scholar 

  • Berdemeijer GMM & Bass J (1981) S-specific proteins in styles of self-incompatible Nicotiana alata. Theor. Appl. Genet. 59: 185–190

    Google Scholar 

  • Bower MS, Matis DD, Fernandes-Carvalho, Mazzurco M, Gu T, Rothstein SJ & Goring DR (1996) Two members of the thioredoxin-h family interacts with the kinase domain of a Brassica S locus receptor kinase. Plant Cell 8: 1641–1650

    Google Scholar 

  • Boyes DC & Nasrallah (1995) An anther-specific gene encoded by an S locus haplotype of Brassica produces complementary and differentially regulated transcripts. Plant Cell 7: 1283–1294

    Google Scholar 

  • Boyes DC, Nasrallah ME, Vrebalov J & Nasrallah JB (1997) The self-incompatibility (S) haplotypes of Brassica contain highly divergent and rearranged sequences of ancient origin. Plant Cell 9: 237–47

    Google Scholar 

  • Braun DM, Stone JM & Walker JC (1997) Interaction of the maize and Arabidopsis kinase interaction domains with a subset of receptor-like kinases: implications for transmembrane signaling in plants. Plant J. 12(1): 83–95

    Google Scholar 

  • Brewbaker JL & Natarajan AT (1960) Centric fragments and pollenpart mutations of incompatibility alleles in Petunia. Genetics 45: 699–704

    Google Scholar 

  • Broothaerts W, Vanvicckenroye P, Decock B, Van Damme J & Vendrig JC (1991) Petunia hybrida S-proteins: ribonuclease activity and the role of their glycan side chains in selfincompatibility. Sex. Plant Reprod. 4: 258–266

    Google Scholar 

  • Broothaerts WJ, Janssens GA, Proost P & Broekaert WF (1995) cDNA cloning and molecular analysis of two selfincompatibility alleles form apple. Plant Mol. Biol. 27: 499–511

    Google Scholar 

  • Cabrillac D, Delmore V, Garin J, Ruffio-Chable V, Giranton JL, Dumas C, Gaude T & Cock M (1999) The S15 haplotype in Brassica oleracea includes three S gene family members expressed in stigmas. Plant Cell 11: 971–986

    Google Scholar 

  • Cabrillac D, Cock JM, Dumas C & Gaude T (2001) The S-locus receptor kinase is inhibited by thioredoxins and activated by pollen coat proteins. Nature 410: 220–223

    Google Scholar 

  • Casselman AL, Vrebalov J, Conner JA, Singhal A, Giovannoni J, Nasrallah ME & Nasrallah JB (2000) Determining the physical limits of the Brassica S locus by recombinational analysis. Plant Cell 12: 23–33

    Google Scholar 

  • Clark AG & Kao T-H (1991) Excess nonsynonymous substitution at shared polymorphic sites among self-incompatibility alleles of Solanaceae. Proc. Natl. Acad. Sci. USA 88: 9823–9827

    Google Scholar 

  • Clark KR, Okuley JJ, Collins PD & Sims TL (1990) Sequence variability and developmental expression of S-alleles in selfincompatible and pseudo-self-compatible Petunia. Plant Cell 2: 815–826

    Google Scholar 

  • Cohen JJ (1993) Apoptosis. Immunol. Today 14: 126–130

    Google Scholar 

  • Conner HE (1979) Breeding systems in the grasses: a survey. NZ J. Bot. 17: 547–574

    Google Scholar 

  • Conner JA, Tantikanjana T, Stein JC, Kandasamy MK, Nasrallah JB & Nasrallah ME (1997) Transgene-induced silencing of S-locus genes and related genes in Brassica. Plant J. 11(4): 809–823

    Google Scholar 

  • Conner JA, Conner P, Nasrallah ME & Nasrallah JB (1998) Comparative mapping of the Brassica S locus region and its homeolog in Arabidopsis. Implications for the evolution of mating systems in the Brassicaceae. Plant Cell 10: 801–12

    Google Scholar 

  • 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

    Google Scholar 

  • Cui Y, Brugiere N, Jackman L, Bi YM and Rothstein SJ (1999) Structural and transcriptional comparative analysis of the S locus regions in two self-incompatible Brassica napus lines. Plant Cell 11: 2217–2231

    Google Scholar 

  • Cui Y, Bi Y-M, Brugiere N, Arnoldo M & Rothstein SJ (2000) The S locus glycoprotein and the S receptor kinase are sufficient for self-pollen rejection in Brassica. Proc. Natl. Acad. Sci. USA 97: 3713–3717

    Google Scholar 

  • Dearnaley JDW, Levina NN, Lew RR, Heath IB & Goring DR (1997) Interrelationships between cytoplasmic Ca2+ peaks, pollen hydration and plasma membrane conductances during compatible and incompatible pollinations of Brassica napus papillae. Plant Cell Physiol 38: 985–999

    Google Scholar 

  • Dearnaley JDW, Clark KM, Heath IB, Lew RR & Goring DR (1999) Compatible and self-incompatible pollinations of Brassica napus do not involve reorganization of the papillar cytoskeleton. New Phytol 141: 199–207

    Google Scholar 

  • Delmore V, Giranton J-L, Hatzfeld Y, Friry A, Heizmann P, Ariza MJ, Dumas C, Gaude T & Cock M (1995) Characterization of the S locus genes, SLG and SRK, of Brassica S3 haplotype: identification of a membrane localized protein encoded by the S locus receptor kinase gene. Plant J. 7(3): 429–440

    Google Scholar 

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

    Google Scholar 

  • Dodds PN, Bonig I, Du H, Rodin J, Anderson MA, Newbigin E & Clarke AE (1993) S-RNase gene of Nicotiana alata is expressed in developing pollen. Plant Cell 5: 1771–1782

    Google Scholar 

  • Dodds PN, Ferguson C, Clarke AE & Newbigin E (1999) Pollenexpressed S-RNases are not involved in self-incompatibility in Lycopersicon peruvianum. Sex. Plant Reprod. 12: 76–87

    Google Scholar 

  • Dorwick VPJ (1956) Heterostyly and homostyly in Primula obconica. Heredity 10: 219–236

    Google Scholar 

  • Doughty J, Hedderson F, McCubbin A & Dickinson H (1993) Interaction between a coating-borne peptide of the Brassica pollen grain and stigmatic S (self-incompatibility)-locus-specific glycoproteins. Proc. Natl. Acad. Sci. USA 90: 467–471

    Google Scholar 

  • Doughty J, Dixon S, Hiscock SJ, Willis AC, Parkin IAP & Dickinson HG (1998) PCP-A1, a defensin-like Brassica pollen coat protein that binds S locus glycoprotein, is the product of gametophytic gene expression. Plant Cell 10: 1333–1347

    Google Scholar 

  • Dowd PE, McCubbin AG, Wang X, Verica JA, Tsukamoto T, Ando T & Kao T-H (2000) Use of Petunia inflata as a model for the study of Solanaceous type self-incompatibility. Ann. Bot. 85: 87–93

    Google Scholar 

  • Dulberg R (1992) Floral polymorphism and their functional significance in the heterostylous syndrome. In: Barrett SCH (ed) Evolution and Function of Heterostyly, (pp 41–84). Springer, New York

    Google Scholar 

  • Dwyer KG, Balent Ma, Nasrallah JB & Nasrallah ME (1991) DNA sequences of self-incompatibility gene from Brassica campestris and B. oleracea: polymorphism predating speciation. Plant Mol. Biol. 16: 481–486

    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. Natl. Acad. Sci. USA 91: 2265–2269

    Google Scholar 

  • Franklin FCH, Atwal KK, Ride JP & Franklin-Tong VE (1994) Towards the elucidation of the mechanism of pollen tube inhibition during the self-incompatibility response in Papaver rhoeas. In: Scott RD & Stead AD (eds). Molecular & Cellular Aspects of Plant Reproduction, Cambridge University Press, Cambridge

    Google Scholar 

  • Franklin-Tong VE, Lawrence MJ & Franklin FCH (1988) An in vitro bioassay for the stigmatic product of the selfincompatibility gene in Papaver rhoeas L. New Phytol. 110: 109–118

    Google Scholar 

  • Franklin-Tong VE, Lawrence MJ & Franklin FCH (1989) Characterization of a stigmatic component of from Papaver rhoeas L. which exhibits the specific activity of a self-incompatibility (S-) gene product. New Phytol. 112: 307–315

    Google Scholar 

  • Franklin-Tong VE, Lawrence MJ & Franklin FCH (1990) Selfincompatibility in Papaver rhoeas L.: inhibition of incompatible pollen is dependent upon pollen gene expression. New Phytol. 116: 319–324

    Google Scholar 

  • Franklin-Tong VE, Atwal KK, Howell EC, Lawrence MJ& Franklin FCH (1991) Self-incompatibility in Papaver rhoeas L.: There is no evidence for the involvement of stigmatic ribonuclease activity. Plant Cell Environ. 14: 423–429

    Google Scholar 

  • Franklin-Tong VE, Thorlby GJ, Lawrence MJ & Franklin FCH (1992) Recognition signals and pollen response in the incompatibility reaction in Papaver rhoeas. In: Mulcahy DL, Bergamini-Mulcahy G & Ottaviano, E (eds) Angiosperm Pollen and Ovules: Basic and Applied Aspects. Springer, New York

    Google Scholar 

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

    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(2): 299–307

    Google Scholar 

  • Franklin-Tong VE, Dorbak BK, Allan AC, Watkins PAC & Trewavas AJ (1996) Growth of pollen tubes of Papaver rhoeas is regulates by a slow moving calcium wave propagated by inositol 1,4,5–triphosphate. Plant Cell 8: 1305–1321

    Google Scholar 

  • Franklin-Tong VE, Hackett G & Hepler PK (1997) Ratio-imaging of Ca2+ in the self-incompatibility response in pollen tubes of Papaver rhoeas. Plant J. 12(6): 1375–1386

    Google Scholar 

  • Fukai E, Nishio T & Nasrallah ME (2001) Molecular genetic analysis of the candidate gene forMOD, a locus required for selfincompatibility in Brassica rapa. Mol. Genet. Genomics 265: 519–525.

    Google Scholar 

  • Galvin TL, Goring DR, Schafer U & Rothstein SJ ( 1994) Features of the extracellular domain on the S-locus receptor kinase from Brassica. Mol. Gen. Genet. 244: 630–637

    Google Scholar 

  • Gaude T, Friry A, Heizmann P, Mariac C, Rougier M, Fobis I & Dumas C (1993) Expression of a self-incompatibility gene in a self-compatibility line of Brassica oleracea. Plant Cell 5: 75–86

    Google Scholar 

  • Gaude T, Rougier M, Heizmann P, Ockendon DJ & Dumas C (1995) Expression of the SLG gene is not correlated with the self-incompatibility phenotype in the class II S haplotypes of Brassica oleracea. Plant Mol. Biol. 27: 1003–1014

    Google Scholar 

  • Geitmann A, Snowman BN, Emons AMC & 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: 1239–1251

    Google Scholar 

  • Giranton J-L, Ariza M-J, Dumas C, Cock JM & Gaude T (1995) The S-locus receptor kinase gene encodes a soluble glycoprotein corresponding to the SRK extracellular domain in Brassica oleracea. Plant J. 8: 101–108

    Google Scholar 

  • Giranton J-L, Dumas C, Cock M & Gaude T (2000) The integral membrane S-locus receptor kinase of Brassica has serine threonine kinase activity in a membranous environment and spontaneously forms oligomers in planta. Proc. Natl. Acad. Sci. USA 97: 3759–3764

    Google Scholar 

  • Golynskaya EL, Bashkirova & Tomchuk NN (1976) Phytoheamagglutinins of the pistil in Primula as possible proteins of generative incompatibility. Sov. Plant Physiol. 23: 169–176

    Google Scholar 

  • Golz JF, Su AE, Clarke AE & Newbigin E (1999) A molecular description of mutations affecting the pollen component of the Nicotiana alata S locus. Genetics 152: 1123–1135

    Google Scholar 

  • Golz JF, Clarke AE & Newbigin E (2000) Mutational approaches to the study of self-incompatibility: Revisting the pollen-part mutants. Ann. Bot. 85: 95–103

    Google Scholar 

  • Goring DR (2000) The search for the components of the selfincompatibility signaling pathway(s) in Brassica napus. Ann. Bot. 85: 171–179

    Google Scholar 

  • Goring DR & Rothstein SJ (1992) The S-locus kinase receptor gene in a self-incompatible Brassica napus line encodes a functional serine/threonine kinase. Plant Cell 4: 1273–1281

    Google Scholar 

  • Goring DR & Rothstein SJ (1996) S-locus receptor kinase genes and self-incompatibility in Brassica napus. In: Verma DPS (ed) Signal Transduction in Plant Growth and Development. (pp 217–230). Springer, New York

    Google Scholar 

  • Goring DR, Banks P, Beversdorf WD & Rothstein SJ (1992a) Use of the polymerase chain reaction to isolate an S-locus glycoprotein cDNA introgressed from Brassica campestris into B. napus ssp. oleifera. Mol. Gen. Genet. 234: 185–192

    Google Scholar 

  • Goring DR, Banks P, Fallis L, Basczynski L, Beversdorf WD & Rothstein SJ (1992b) Identification of an S-locus glycoprotein allele introgressed form B. napus ssp. rapifera to B. napus ssp. oleifera. Plant J. 2(6): 983–989

    Google Scholar 

  • Goring DR, Galvin TL, Schafer U & Rothstein SJ (1993) An S receptor kinase gene in self-compatible Brassica napus has a 1–bp deletion. Plant Cell 5: 531–539

    Google Scholar 

  • Gray JE, McClure BA, Bonig 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

    Google Scholar 

  • Gu T, Mazzurco M, Sulman W, Matias DD & Goring DR (1998) Binding of a novel arm repeat protein to the kinase domain of the S-locus receptor kinase. Proc. Natl. Acad. Sci. USA 95: 382–387

    Google Scholar 

  • Harbord RM, Napoli CA & Robbins TP (2000) Segregation distortion of T-DNA markers linked to the self-incompatibility (S) locus in Petunia hybrida. Genetics 154: 1323–1333

    Google Scholar 

  • Hatzfeld M (1999) The armadillo family of structural proteins. Int. Rev. Cytol. 186: 179–224

    Google Scholar 

  • Hayman DL & Richter J (1992) Mutations affecting selfincompatibility in Phalaris coerulescens. Heredity 68: 495–503

    Google Scholar 

  • Hearn MJ, Franklin FCH & Ride JP (1996) Identification of a membrane glycoprotein in pollen of Papaver rhoeas which binds stigmatic self-incompatibility (S-) proteins. Plant J. 9(4): 467–475

    Google Scholar 

  • Hinata K & Nishio T (1978) S-allele specificity of stigma proteins in Brassica oleracea and B. campestris. Heredity 41: 93–100

    Google Scholar 

  • Hiscock SJ, Doughty J, Willis AC & Dickinson HG (1995) A 7–kDa pollen coating borne peptide from Brassica napus interacts with the S-locus glycoprotein and S-locus-related glycoprotein. Planta 196: 367–374

    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

    Google Scholar 

  • Ikeda S, Nasrallah JB, Dixit R, Preiss S & Nasrallah ME (1997) An aquaporin-like gene required for the Brassica selfincompatibility response. Science 276: 1564–1566

    Google Scholar 

  • Ioerger TR, Clark AG & Kao T-H (1990) Polymorphism at the selfincompatibility locus in Solanaceae predates speciation. Proc. Natl. Acad. Sci. USA 87: 9732–9735

    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

    Google Scholar 

  • Ishimizu T, Miyagi M, Norioka S, Liu Y-H, Clarke AE & Sakiyamy F (1995) Identification of histidine 31 and cysteine 95 in the active site of self-incompatibility associated S6–RNase in Nicotiana alata. J. Biochem. 118: 1007–1013

    Google Scholar 

  • Ishimizu T, Norioka S, Kanai M, Clarke AE & Sakiyama F (1996) Location of cystiene and cysteine residues in S-ribonuclease associated with gametophytic self-incompatibility. Eur. J. Biochem. 242: 627–635

    Google Scholar 

  • Ishimizu T, Endo T, Yamaguchi-Kabata Y, Nakamura T, 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-RNases. FEBS Letter 440: 337–342

    Google Scholar 

  • Ishimizu T, Mitsukami Y, Shinkawa T, Natsuka S, Hase S, Miyagi, Sakiyama F & Norioka S (1999) Presence of asparagine-linked N-acetylglucosamine and chitobiose in Pyrus pyfifolia S-RNases associated with gametophytic self-incompatibility. Eur. J. Biochem. 263: 624–634

    Google Scholar 

  • Jordan ND, Kakeda K, Conner A, Ride JP, Franklin-Tong VE & Franklin FCH (1999) S-protein mutants indicate a functional role for SBP in the self-incompatibility reaction of Papaver rhoeas. Plant J. 20(1): 119–125

    Google Scholar 

  • Jordan ND, Ride JP, Rudd JJ, Davies EM, Franklin-Tong VE & Franklin FCH (2000a) Inhibition of self-incompatibility in Papaver rhoeas involves a complex series of cellular events. Ann. Bot. 85: 197–202

    Google Scholar 

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

    Google Scholar 

  • Kandasamy MK, Paolillo DJ, Faraday CD, Nasrallah JB & Nasrallah ME (1989) The S-locus glycoproteins of Brassica accumulate in the cell wall of developing stigma papillae. Dev. Biol. 134: 462–472

    Google Scholar 

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

    Google Scholar 

  • Kao T-H & McCubbin A (1996) How flowering plants discriminate between self and non-self pollen to prevent inbreeding. Proc. Natl. Acad. Sci. USA 93: 12059–12065

    Google Scholar 

  • Karunanandaa B, Haung S & Kao T-H (1994) Carbohydrate moiety of the Petunia inflata S3–protein is not required for selfincompatibility interactions between pollen and pistil. Plant Cell 6: 1933–1940

    Google Scholar 

  • Kawata Y, Sakiyama F & Tamaoki H (1988) Amino acid sequence of ribonuclease T2 from Aspergillus oryzae. Eur. J. Biochem. 176: 683–697

    Google Scholar 

  • Khosravi D (2000) Putative incompatibility proteins in distylous Tunera species: Immunoblot and immunocytochemistry analyses. MSc Thesis, York University, Toronto, Canada

    Google Scholar 

  • Kuafmann H, Salamini F & Thompson RD (1991) Sequence variability and gene structure at the self-incompatibility locus of Solanum tuberosum. Mol. Gen. Genet. 226: 457–466

    Google Scholar 

  • Kunz C, Chang A, Faure J-D, Clarke AE, Polya G & Anderson MA (1996) Phosphorylation of style S-RNase by Ca2+-dependent protein kinase from pollen tubes. Sex. Plant Reprod. 9: 25–34

    Google Scholar 

  • Kurihara H, Mitsui Y, Ohgi K, Irie M, Mizuno H & Nakamura KT (1992) Crystal and molecular structure of RNase RH, a new class of microbial ribonuclease from Rhizopus niveus. FEBS Letter 306: 189–192

    Google Scholar 

  • Kurup S, Ride JP, Jordan N, Fletcher G, Franklin-Tong VE & Franklin FCH (1998) Identification and cloning of related selfincompatibility S-genes in Papaver rhoeas and Papaver nudicaule. Sex. Plant Reprod. 11: 192–198

    Google Scholar 

  • Kusaba M & Nishio T (1999) Comparative analysis of S haplotypes with very similar SLG alleles in Brassica rapa and Brassica oleracea. Plant J. 17(1): 83–91

    Google Scholar 

  • Kusaba M, Nishio T, Satta Y, Hinata K & Ockendon D (1997) Striking sequence similarity in inter-and intra-specific comparison of class I SLG alleles from Brassica oleracea and Brassica campestris: implications for the evolution and recognition mechanism. Proc. Natl. Acad. Sci. USA 94: 7673–7678

    Google Scholar 

  • Langridge P, Bauman U & Juntter J (1999) Revisiting and revising the self-incompatibility genetics of Phalaris coerulescens. Plant Cell 11: 1826

    Google Scholar 

  • Lawrence MJ, Afazal M & Kenrick J (1978) The genetic control of self-incompatibility in Papaver rhoeas. Heredity 40: 239–285

    Google Scholar 

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

    Google Scholar 

  • Letham DLD, Blissard GW & Nasrallah JB (1999) Production and characterization of the Brassica oleracea self-incompatibility locus glycoprotein and receptor kinase in a baculovirus infected insect cell culture system. Sex. Plant Reprod. 12: 179–187

    Google Scholar 

  • Lewis D & Jones DA (1992) The genetics of heterostyly. In: Barrett SCH (ed) Evolution and Function of Heterostyly (pp 129–154). Springer, New York

    Google Scholar 

  • Li J-H, 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: 956–964

    Google Scholar 

  • Li X, Nield J, Hayman D & Langridge P (1994) Cloning a putative self-incompatibility gene from the pollen of the grass Phalaris coerulescens. Plant Cell 6: 1923–1932

    Google Scholar 

  • Li X, Nield J, Hayman D & Langridge P (1995) Thioredoxin activity in the C terminus of Phalaris coerulescens S protein. Plant J. 8(1): 133–138

    Google Scholar 

  • Li X, Nield J, Hayman D & Langridge P (1996) A fertile mutant of Phalaris coerulescens produces an S protein with reduced thioredoxin activity. Plant J. 10(3): 505–513

    Google Scholar 

  • Li X, Paech N, Nield J, Hayman D & Langridge P (1997) Selfincompatibility in the grasses: evolutionary relationships of the S gene from Phalaris coerulescens to homologous sequences in other grasses. Plant Mol. Biol. 34: 223–232

    Google Scholar 

  • Lundqvist A (1956) Self-incompatibility in rye. I. Genetic control in the diploid. Hereditas 42: 293–348

    Google Scholar 

  • Lush WM & Clarke AE (1997) Observations of pollen tube growth in Nicotiana alata and their implications for mechanism of selfincompatibility. Sex. Plant Reprod. 10: 27–35

    Google Scholar 

  • Luu D-T, Marty-Mazars D, Trick M, Dumas C & Heizmann P (1999) Pollen-stigma adhesion in Brassica involves SLG and SLR1 glycoproteins. Plant Cell 11: 251–262

    Google Scholar 

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

    Google Scholar 

  • Martin FW (1968) The behavior of Lycopersicon incompatibility alleles in an alien genetic milieu. Genetics 60: 101–109

    Google Scholar 

  • Mather K (1943) Specific differences in Petunia. I. Incompatibility. J. Genet. 45: 215–235

    Google Scholar 

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

    Google Scholar 

  • 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: 2087–97

    Google Scholar 

  • Mazzurco M, Sulaman W, Elina H, Cock JM & Goring DR (2001) Further analysis of the interactions between the Brassica S receptor kinase and three interacting proteins (ARC1, THL1 and THL2) in the yeast two-hybrid system. Plant Mol. Biol. 45: 365–376

    Google Scholar 

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

    Google Scholar 

  • McClure BA, Gray JE, Anderson MA & Clarke AE (1990) Selfincompatibility in Nicotiana alata involves degradation of pollen rRNA. Nature 347: 757–760

    Google Scholar 

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

    Google Scholar 

  • McClure BA, Garcia-Cruz F, Beecher B & Sulaman W (2000) Factors affecting Inter-and Intra-specific pollen rejection in Nicotiana. Ann. Bot. 85: 113–123

    Google Scholar 

  • McCubbin AG, Chung Y-Y & Kao T-h (1997) A mutant S3–RNase of Petunia inflata lacking RNase activity has an allele-specific dominant negative effect on self-incompatibility interactions. Plant Cell 9: 85–95

    Google Scholar 

  • Murrett J, Atherton TL, Mou B, Gasser CS& McClure BA (1994) SRNase expressed in transgenic Nicotiana causes S-allele-specific pollen rejection. Nature 367: 563–566

    Google Scholar 

  • Nasrallah JB (1997) Signal perception and response in the interactions of self-incompatibility in Brassica. Essay Biochem. 32: 143–160

    Google Scholar 

  • Nasrallah JB, Kao T-h, Goldberg ML & Nasrallah ME (1985) A cDNA encoding an S-locus-specific glycoprotein from Brassica oleracea. Nature 318: 263–267

    Google Scholar 

  • Nasrallah JB, Nishio T & Nasrallah ME (1991) The selfincompatibility genes of Brassica. Annu. Rev. Plant Physiol. Plant Mol. Biol. 42: 393–422

    Google Scholar 

  • Nasrallah JB, Rundle SJ & Nasrallah ME (1994) Genetic evidence for the requirement for the Brassica S-locus receptor kinase gene in the self-incompatibility response. Plant J. 5(3): 373–384

    Google Scholar 

  • Nasrallah ME & Wallace DH (1967) Immunogenetics of selfincompatibility in Brassica oleracea. Heredity 22: 519–527

    Google Scholar 

  • Nasrallah ME, Wallace DH & Savo RM (1972) Genotype-proteinphenotype relationships in self-incompatibility of Brassica. Genet. Res. 20: 151–160

    Google Scholar 

  • Nasrallah ME, Kandasamy MK & Nasrallah JB (1992) A genetically defined trans-acting locus regulates S-locus function in Brassica. Plant J. 2: 497–506

    Google Scholar 

  • Okazaki K, Kusaba M, Ockendon DJ & Nisho T (1999) Characterization of tester lines in Brassica oleracea: polymorphism of restriction fragment length of SLG homologues and isoelectric points of S-locus glycoproteins. Theor. Appl. Genet. 98: 1329–1334

    Google Scholar 

  • Oxley D & Bacic A (1996) Disulphide bonding in a stylar selfincompatibility ribonuclease of Nicotiana alata. Eur. J. Biochem. 242: 75–80

    Google Scholar 

  • Oxley D, Munro SL, Craik DJ & Bacic (1996) Structure of Nglycans on the S3–and S6–allele stylar self-incompatibility ribonucleases of Nicotiana alata. Glycobiology 6: 611–618

    Google Scholar 

  • Parry S, Newbigin E, Currie G, Bacic A & Oxley (1997) Identi-fication of active-site histidine residues of a self-incompatibility ribonuclease from a wild tomato. Plant Physiol. 115: 142–1429

    Google Scholar 

  • Parry S, Newbigin E, Craik D, Nakamura KT, Bacic A & Oxley D (1998) Structural analysis and molecular model of a selfincompatibility RNase from wild tomato. Plant Physiol. 116: 463–469

    Google Scholar 

  • Pastuglia M, Ruffio-Chable V, Delmore V, Gaude T, Dumas C & Cock JM (1997) A functional S locus anther is not required for the self-incompatibility response in Brassica oleracea. Plant Cell 9: 2065–2076

    Google Scholar 

  • Ride JP, Davies EM, Franklin FCH & Marshall DF (1999) Analysis of Arabidopsis genome sequence reveals a large new gene family in plants. Plant Mol. Biol. 39: 927–932

    Google Scholar 

  • Robbins TP, Harbord RM, Sonneveld T & Clarke K (2000) The molecular genetics of self-incompatibility in Petunia hybrida. Ann. Bot. 85: 105–112

    Google Scholar 

  • Royo J, Kunz C, Kowyama Y, Anderson M, Clarke AE & Newbigin E (1994) Loss of a histidine residue at the active site of S-locus ribonuclease is associated with self-incompatibility in Lycopersicon peruvianum. Proc. Natl. Acad. Sci. USA 91: 6511–6514

    Google Scholar 

  • Rudd JJ, Franklin FCH, Lord JM & Franklin-Tong V (1996) Increased phosphorylation of a 26 kD pollen protein induced by the self-incompatibility response in Papaver rhoeas. Plant Cell. 8: 713–724

    Google Scholar 

  • Rundle SJ, Nasrallah ME & Nasrallah JB (1993) Effects of inhibitors of protein serine/threonine phosphatases on pollination in Brassica. Plant Physiol. 103: 1165–1171

    Google Scholar 

  • Saba-El-Leil M, 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: 571–583

    Google Scholar 

  • Sassa H, Hirano H & Ikehashi H (1993) Identification and characterization of stylar glycoproteins associated with selfincompatibility genes of Japanese pear Pyrus serontina Rehd. Mol. Gen. Genet. 241(1–2): 17–25

    Google Scholar 

  • Sassa H, Hirano H & Ikehashi H (1994) Identification of selfincompatibility-related glycoproteins in styles of apple (Malus × domestica). Theor. Appl. Genet. 89: 201–205

    Google Scholar 

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

    Google Scholar 

  • Schopfer CR, Nasrallah ME & Nasrallah JB (1999) The male determinant of self-incompatibility in Brassica. Science 286: 1697–1700

    Google Scholar 

  • Scutt CP, Fordham-Skelton AP & Cory RRD (1993) Okadaic acid causes breakdown of self-incompatibility in Brassica oleracea: Evidence for the involvement of protein phosphatases in the incompatibility response. Sex. Plant Reprod. 6: 282–285

    Google Scholar 

  • Shiba H, Hinata K, Suzuki A & Isogai (1995) Breakdown of selfincompatibility in Brassica by the antisense RNA of the SLG gene. Proc. Jpn. Acad. 71: 81–83

    Google Scholar 

  • Silva NF, Stone SL, Christie LN, Sulaman W, Nazarian KAP, Burnett LA, Arnoldo M, Rothstein SJ & Goring DR (2001) Expression of the S receptor kinase in self-compatible Brassica napus cv. Westar leads to the allele-specific rejection of self-114 incompatible Brassica napus pollen. Mol. Genet. Genomics 265: 522–559

    Google Scholar 

  • Sims TL (1993) Genetic regulation of self-incompatibility. Crit. Rev. Plant Sci. 12: 129–167

    Google Scholar 

  • Stahl RJ, Arnoldo M, Glavin T, Goring DR & Rothstein SJ (1998) The self-incompatibility phenotype in Brassica is altered by the transformation of a mutant S locus receptor kinase. Plant Cell 10: 209–218

    Google Scholar 

  • Stanchev BS, Doughty J, Scutt CP, Dickinson H & Croy RRD (1996) Cloning of PCP1, a member of a family of pollen coat protein (PCP) genes from Brassica oleracea encoding novel cysteine-rich proteins involved in pollen-stigma interactions. Plant J. 10(2): 303–313

    Google Scholar 

  • Stein JC & Nasrallah JB (1993) A plant receptor-like gene, the S-locus receptor kinase of Brassica oleracea L., encodes a functional serine/threonine kinase. Plant Physiol 101: 1103–1106

    Google Scholar 

  • Stein JC, Howlett B, Boyes DC, Nashrallah ME & Nasrallah JB (1991) Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc. Natl. Acad. Sci. USA 88: 8816–8820

    Google Scholar 

  • Stein JC, Dixit R, Nasrallah ME & Nasrallah JB (1996) SRK, the stigma-specific S locus receptor kinase of Brassica, is targeted to the plasma membrane in transgenic tobacco. Plant Cell 8: 429–445

    Google Scholar 

  • Stone SL, Arnoldo M & Goring DR (1999) A breakdown of Brassica self-incompatibility in ARC1 antisense transgenic plants. Science 286: 1729–1731

    Google Scholar 

  • Sulaman W, Arnoldo M, Yu K, Tulsieram L, Rothstein S & Goring DR (1997) Loss of callose in the stigmas papillae does not affect the Brassica self-incompatibility phenotype. Planta 203: 327–331

    Google Scholar 

  • Suzuki G, Kai N, Hirose T, Fukui K, Takayama S, Isogai A, Watanabe M & Hinata K (1999) Genomic organization of the S locus: identification of genes in SLG/SRK region of S(9) haplotype of Brassica campestris (syn. Rapa). Genetics 153(1): 391–400

    Google Scholar 

  • Takasaki T, Hatakeyama K, Watanabe M, Toriyama K, Isogai A & Hinata K (1999) Introduction of SLG (S locus glycoprotein) alters the phenotype of endogenous S haplotype, but confers no new S haplotype specificity in Brassica rapa L. Plant Mol Biol. 40: 659–668

    Google Scholar 

  • Takasaki T, Hatakeyama K, Suzuki G, Watanabe M, Isogai A & Hinata K (2000) The S receptor kinase determines selfincompatibility inBrassica stigma. Nature 403: 913–916

    Google Scholar 

  • Takayama S, Isogai A, Tsukamoto C, Ueda Y, Hinata K, Okazaki K & Suzuki A (1987) Sequences of S-glycoproteins, products of the Brassica campestris self-incompatibility locus. Nature 326: 102–105

    Google Scholar 

  • Takayama S, Shiba H, Iwano M, Shimosato H, Che FS, Kai N, Watanabe M, Suzuki G, Hinata K & Isogai A (2000a) The pollen determinant of self-incompatibility in Brassica campestris. Proc. Natl. Acad. Sci. 97: 1920–1925

    Google Scholar 

  • Takayama S, Shiba H, Iwano M, Asano K, Minoru H, Che F-S, Watanabe M, Hinata K & Isogai A (2000b) Isolation and characterization of pollen coat proteins of Brassica campestris that interact with S locus-related glycoprotein 1 involved in pollenstigma interactions. Proc. Natl. Acad. Sci. USA 97: 3765–3770

    Google Scholar 

  • Tantikanjana T, Nasharallah ME, Stein JC, Chen C-H & Nasrallah JB (1993) An alternative transcript of the S locus glycoprotein gene in a class II pollen-recessive self-incompatibility haplotype of Brassica oleracea encodes a membrane-anchored protein. Plant Cell 5: 657–666

    Google Scholar 

  • Thomas RD & Kirch HH (1992) The S-locus of flowering plants: when self-rejection is of self-interest. Trends Genet. 8(11): 381–387

    Google Scholar 

  • Thomas KF & Taylor JP (1966) Non-linear dominance relationships between S-alleles. Heredity 21: 345–362

    Google Scholar 

  • Thorogood D & Hayward DM (1991) The genetic control of selfincompatibility in an inbreed line of Lolium perenne L. Heredity 67: 175–181

    Google Scholar 

  • Toriyama K, Stein JC, Nasrallah ME & Nasrallah JB (1991) Transforming of Brassica oleracea with an S-locus gene from B. campestris changes the self-incompatibility phenotype. Theor. Appl. Genet. 81: 769–776

    Google Scholar 

  • Tsai D-S, Lee H-S, Post LC, Kreiling KM & Kao T-H (1992) Sequence of an S-protein of Lycopersicon pervianum and comparison with other solanaceous S-proteins. Sex. Plant Reprod. 5: 256–263

    Google Scholar 

  • Verica JA, McCubbin AG & Kao T-h (1998) Are the hypervariable regions of S RNases sufficient for allele-specific rejection of pollen? Plant Cell. 10: 314–316

    Google Scholar 

  • Walker EA, Ride Jp, Kurup S, Franklin-Tong VE, Lawrence MJ & Franklin FCH (1996) Molecular analysis of two functional homologues of the S3 allele of the Papaver rhoeas selfincompatibility gene isolated from different populations. Plant Mol. Biol. 30: 983–994

    Google Scholar 

  • Watanabe M, Ito A, Takada Y, Ninomiya C, Kakizaki T, Takahata Y, Hatakeyama K, Hinata K, Suzuki G, Takasaki T, Satta Y, Shiba H, Takayama S & Isogai A (2000) Highly divergent sequences of the pollen self-incompatibility (S) gene in class-I S haplotypes of Brassica campestris (syn. rapa) L. FEBS Lett. 473: 139–144

    Google Scholar 

  • Watson L (1990) The grass family, Poaceae. In: Chapman GP (ed) Reproduction Versatility in the Grasses. Cambridge University Press, Cambridge

    Google Scholar 

  • Wheling P, Hacuf B & Wricke G (1994) Phosphorylation of pollen proteins in relation to self-incompatibility in rye (Secale cereale). Sex. Plant Reprod. 7: 67–75

    Google Scholar 

  • Wong KC, Watanabe M & Hinata K (1994) Protein profiles in pin and thrum floral organs of distylous Averrhoa carambola L. Sex. Plant Reprod. 7: 107–115

    Google Scholar 

  • Woodward JR, Bacic A, Jahnen W & Clarke AE (1989) N-linked glycan chains on S-allele-associated glycoproteins from Nicotiana alata. Plant Cell 1: 511–514

    Google Scholar 

  • Woodward JR, Craik D, Dell A, Khoo KK-H, Munro SLA, Clarke AE & Bacic A (1992) Structural analysis of the N-glycan chains from a stylar glycoprotein associated with the expression of selfincompatibility in Nicotiana alata. Glycobiology 2(3): 241–250

    Google Scholar 

  • Xu B, Mu J, Nevins DL, Grun P & Kao T-H (1990) Cloning and sequencing of cDNAs encoding two self-incompatibility associated proteins in Solanum chacoense. Mol. Gen. Genet. 224: 341–346

    Google Scholar 

  • Xue Y, Carpenter R, Dickinson HG & Coen ES (1996) Origin of allelic diversity in Antirrhinum S locus RNases. Plant Cell. 8: 805–814

    Google Scholar 

  • Yu K, Schafer U, Glavin TL, Goring DR & Rothstein SJ (1996) Molecular characterization of the S locus in two self-incompatible Brassica napus lines. Plant Cell 8: 2369–80

    Google Scholar 

  • Zurek DM, Mou B, Beecher B & McClure BA (1997) Exchanging sequence domains between S-RNases from Nicotiana alata disrupts pollen recognition. Plant J. 11(4): 797–808

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Stone, S.L., Goring, D.R. The molecular biology of self-incompatibility systems in flowering plants. Plant Cell, Tissue and Organ Culture 67, 93–114 (2001). https://doi.org/10.1023/A:1011980210048

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1011980210048

Navigation