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The S-LOCUS CYSTEINE-RICH PROTEIN (SCR): A Small Peptide with A High Impact on the Evolution of Flowering Plants

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Plant Signaling Peptides

Part of the book series: Signaling and Communication in Plants ((SIGCOMM,volume 16))

Abstract

Self-incompatibility (SI) is an archetypal cell-to-cell communication system in which self-pollen is rejected to prevent inbreeding. In crucifers (or Brassicaceae family), the pollen SI determinant is a small peptide, the S-LOCUS CYSTEINE-RICH PROTEIN (SCR, also known as SP11). During self-pollination, SCR binds to the extracellular domain of its cognate stigmatic receptor, the S-LOCUS RECEPTOR KINASE (SRK). This initiates a signaling cascade leading to self-pollen inhibition. The genes encoding both SI determinants are tightly linked in a multiallelic genomic region defined as the S-locus. Among S alleles, SCR shows extreme variability, and few residues in the protein have been reported to be critical for its specificity. In a heterozygous situation, SCR alleles display complex dominance relationships based on the silencing of certain SCR genes. This chapter provides a summary of the role of SCR in SI, the relationships between SCR alleles, and the role SCR loss played in the model plant Arabidopsis thaliana.

IFL and RI contributed equally to this work

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References

  • Bechsgaard J, Bataillon T, Schierup MH (2004) Uneven segregation of sporophytic self-incompatibility alleles in Arabidopsis lyrata. J Evol Biol 17:554–561

    Article  PubMed  CAS  Google Scholar 

  • Boggs NA, Dwyer KG, Nasrallah ME, Nasrallah JB (2009a) In vivo detection of residues required for ligand-selective activation of the S-locus receptor in Arabidopsis. Curr Biol 19:786–791

    Article  PubMed  CAS  Google Scholar 

  • Boggs NA, Nasrallah JB, Nasrallah ME (2009b) Independent S-locus mutations caused self-fertility in Arabidopsis thaliana. PLoS Genet 5:e1000426

    Article  PubMed  Google Scholar 

  • Boyes DC, Nasrallah JB (1993) Physical linkage of the SLG and SRK genes at the self-incompatibility locus of Brassica oleracea. Mol Gen Genet 236:369–373

    Article  PubMed  CAS  Google Scholar 

  • Busch JW, Schoen DJ (2008) The evolution of self-incompatibility when mates are limiting. Trends Plant Sci 13:128–136

    Article  PubMed  CAS  Google Scholar 

  • Cabrillac D, Delorme V, Garin J, Ruffio-Chable V, Giranton JL, Dumas C, Gaude T, Cock JM (1999) The S 15 self-incompatibility haplotype in Brassica oleracea includes three S gene family members expressed in stigmas. Plant Cell 11:971–986

    PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Chookajorn T, Kachroo A, Ripoll DR, Clark AG, Nasrallah JB (2004) Specificity determinants and diversification of the Brassica self-incompatibility pollen ligand. Proc Natl Acad Sci USA 101:911–917

    Article  PubMed  CAS  Google Scholar 

  • de Nettancourt D (2001) Incompatibility and incongruity in wild and cultivated species. Springer-Verlag, Berlin

    Google Scholar 

  • Finnegan EJ, Liang D, Wang MB (2011) Self-incompatibility: Smi silences through a novel sRNA pathway. Trends Plant Sci 16:238–241

    Article  PubMed  CAS  Google Scholar 

  • Fujimoto R, Sugimura T, Fukai E, Nishio T (2006) Suppression of gene expression of a recessive SP11/SCR allele by an untranscribed SP11/SCR allele in Brassica self-incompatibility. Plant Mol Biol 61:577–587

    Article  PubMed  CAS  Google Scholar 

  • Gaude T, Fobis-Loisy I, Miege C (2006) Control of fertilization by self-incompatibility mechanisms. In: Jordan B (ed) The molecular biology and biotechnology of flowering. CAB International, Wallingford, CT, pp 269–297

    Chapter  Google Scholar 

  • Giranton JL, Ariza MJ, Dumas C, Cock JM, Gaude T (1995) The S locus receptor kinase gene encodes a soluble glycoprotein corresponding to the SKR extracellular domain in Brassica oleracea. Plant J 8:827–834

    Article  PubMed  CAS  Google Scholar 

  • Giranton JL, Dumas C, Cock JM, 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

    Article  PubMed  CAS  Google Scholar 

  • Goring DR, Glavin 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

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ivanov R, Gaude T (2009a) Brassica self-incompatibility: a glimpse below the surface. Plant Signal Behav 4:996–998

    Article  PubMed  CAS  Google Scholar 

  • Ivanov R, Gaude T (2009b) Endocytosis and endosomal regulation of the S-receptor kinase during the self-incompatibility response in Brassica oleracea. Plant Cell 21:2107–2117

    Article  PubMed  CAS  Google Scholar 

  • Ivanov R, Fobis-Loisy I, Gaude T (2010) When no means no: guide to Brassicaceae self-incompatibility. Trends Plant Sci 15:387–394

    Article  PubMed  CAS  Google Scholar 

  • Iwano M, Shiba H, Funato M, Shimosato H, Takayama S, Isogai A (2003) Immunohistochemical studies on translocation of pollen S-haplotype determinant in self-incompatibility of Brassica rapa. Plant Cell Physiol 44:428–436

    Article  PubMed  CAS  Google Scholar 

  • Kachroo A, Schopfer CR, Nasrallah ME, Nasrallah JB (2001) Allele-specific receptor-ligand interactions in Brassica self-incompatibility. Science 293:1824–1826

    Article  PubMed  CAS  Google Scholar 

  • Kakita M, Murase K, Iwano M, Matsumoto T, Watanabe M, Shiba H, Isogai A, Takayama S (2007) Two distinct forms of M-locus protein kinase localize to the plasma membrane and interact directly with S-locus receptor kinase to transduce self-incompatibility signaling in Brassica rapa. Plant Cell 19:3961–3973

    Article  PubMed  CAS  Google Scholar 

  • Kakizaki T, Takada Y, Ito A, Suzuki G, Shiba H, Takayama S, Isogai A, Watanabe M (2003) Linear dominance relationship among four class-II S haplotypes in pollen is determined by the expression of SP11 in Brassica self-incompatibility. Plant Cell Physiol 44:70–75

    Article  PubMed  CAS  Google Scholar 

  • Kemp BP, Doughty J (2007) S cysteine-rich (SCR) binding domain analysis of the Brassica self-incompatibility S-locus receptor kinase. New Phytol 175:619–629

    Article  PubMed  CAS  Google Scholar 

  • Kuntal BK, Aparoy P, Reddanna P (2010) EasyModeller: a graphical interface to MODELLER. BMC Res Notes 3:226

    Article  PubMed  Google Scholar 

  • Kusaba M, Dwyer K, Hendershot J, Vrebalov J, Nasrallah JB, Nasrallah ME (2001) Self-incompatibility in the genus Arabidopsis: characterization of the S locus in the outcrossing A. lyrata and its autogamous relative A. thaliana. Plant Cell 13:627–643

    PubMed  CAS  Google Scholar 

  • Kusaba M, Tung CW, Nasrallah ME, Nasrallah JB (2002) Monoallelic expression and dominance interactions in anthers of self-incompatible Arabidopsis lyrata. Plant Physiol 128:17–20

    Article  PubMed  CAS  Google Scholar 

  • Liu P, Sherman-Broyles S, Nasrallah ME, Nasrallah JB (2007) A cryptic modifier causing transient self-incompatibility in Arabidopsis thaliana. Curr Biol 17:734–740

    Article  PubMed  CAS  Google Scholar 

  • Mable BK, Schierup MH, Charlesworth D (2003) Estimating the number, frequency, and dominance of S-alleles in a natural population of Arabidopsis lyrata (Brassicaceae) with sporophytic control of self-incompatibility. Heredity 90:422–431

    Article  PubMed  CAS  Google Scholar 

  • Mishima M, Takayama S, Sasaki K, Jee JG, Kojima C, Isogai A, Shirakawa M (2003) Structure of the male determinant factor for Brassica self-incompatibility. J Biol Chem 278:36389–36395

    Article  PubMed  CAS  Google Scholar 

  • Naithani S, Chookajorn T, Ripoll DR, Nasrallah JB (2007) Structural modules for receptor dimerization in the S-locus receptor kinase extracellular domain. Proc Natl Acad Sci USA 104:12211–12216

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Nasrallah JB, Nishio T, Nasrallah ME (1991) The self-incompatibility genes of Brassica: expression and use in genetic ablation of floral tissues. Annu Rev Plant Physiol Plant Mol Biol 42:393–422

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Nasrallah ME, Liu P, Nasrallah JB (2002) Generation of self-incompatible Arabidopsis thaliana by transfer of two S locus genes from A. lyrata. Science 297:247–249

    Article  PubMed  CAS  Google Scholar 

  • Nasrallah ME, Liu P, Sherman-Broyles S, Boggs NA, Nasrallah JB (2004) Natural variation in expression of self-incompatibility in Arabidopsis thaliana: implications for the evolution of selfing. Proc Natl Acad Sci USA 101:16070–16074

    Article  PubMed  CAS  Google Scholar 

  • Nishio T, Kusaba M (2000) Sequence Diversity of SLG and SRK in Brassica oleracea L. Ann Bot 85:141–146

    Article  CAS  Google Scholar 

  • Ockendon DJ (1975) Dominance relationships between S-alleles in the stigmas of Brussels sprouts (Brassica oleracea var. gemmifera). Euphytica 24:165–172

    Article  Google Scholar 

  • Okazaki K, Kusaba M, Ockendon DJ, Nishio T (1999) Characterization of S 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

    Article  CAS  Google Scholar 

  • Prigoda NL, Nassuth A, Mable BK (2005) Phenotypic and genotypic expression of self-incompatibility haplotypes in Arabidopsis lyrata suggests unique origin of alleles in different dominance classes. Mol Biol Evol 22:1609–1620

    Article  PubMed  CAS  Google Scholar 

  • Ruffio-Chable V, Gaude T (2001) S-haplotype polymorphism in Brassica oleracea. Acta Hortic 546:257–261

    CAS  Google Scholar 

  • Sali A, Blundell TL (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234:779–815

    Article  PubMed  CAS  Google Scholar 

  • Samuel MA, Mudgil Y, Salt JN, Delmas F, Ramachandran S, Chilelli A, Goring DR (2008) Interactions between the S-domain receptor kinases and AtPUB-ARM E3 ubiquitin ligases suggest a conserved signaling pathway in Arabidopsis. Plant Physiol 147:2084–2095

    Article  PubMed  CAS  Google Scholar 

  • Samuel MA, Chong YT, Haasen KE, Aldea-Brydges MG, Stone SL, Goring DR (2009) Cellular pathways regulating responses to compatible and self-incompatible pollen in Brassica and Arabidopsis stigmas intersect at Exo70A1, a putative component of the exocyst complex. Plant Cell 21:2655–2671

    Article  PubMed  CAS  Google Scholar 

  • Sarker RH, Elleman CJ, Dickinson HG (1988) Control of pollen hydration in Brassica requires continued protein synthesis, and glycosylation is necessary for intraspecific incompatibility. Proc Natl Acad Sci USA 85:4340–4344

    Article  PubMed  CAS  Google Scholar 

  • Sato Y, Okamoto S, Nishio T (2004) Diversification and alteration of recognition specificity of the pollen ligand SP11/SCR in self-incompatibility of Brassica and Raphanus. Plant Cell 16:3230–3241

    Article  PubMed  CAS  Google Scholar 

  • Schierup MH, Mable BK, Awadalla P, Charlesworth D (2001) Identification and characterization of a polymorphic receptor kinase gene linked to the self-incompatibility locus of Arabidopsis lyrata. Genetics 158:387–399

    PubMed  CAS  Google Scholar 

  • Schopfer CR, Nasrallah JB (2000) Self-incompatibility. Prospects for a novel putative peptide-signaling molecule. Plant Physiol 124:935–940

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Sherman-Broyles S, Boggs N, Farkas A, Liu P, Vrebalov J, Nasrallah ME, Nasrallah JB (2007) S locus genes and the evolution of self-fertility in Arabidopsis thaliana. Plant Cell 19:94–106

    Article  PubMed  CAS  Google Scholar 

  • Shiba H, Takayama S, Iwano M, Shimosato H, Funato M, Nakagawa T, Che FS, Suzuki G, Watanabe M, Hinata K, Isogai A (2001) A pollen coat protein, SP11/SCR, determines the pollen S-specificity in the self-incompatibility of Brassica species. Plant Physiol 125:2095–2103

    Article  PubMed  CAS  Google Scholar 

  • Shiba H, Iwano M, Entani T, Ishimoto K, Shimosato H, Che FS, Satta Y, Ito A, Takada Y, Watanabe M, Isogai A, Takayama S (2002) The dominance of alleles controlling self-incompatibility in Brassica pollen is regulated at the RNA level. Plant Cell 14:491–504

    Article  PubMed  CAS  Google Scholar 

  • Shiba H, Kakizaki T, Iwano M, Tarutani Y, Watanabe M, Isogai A, Takayama S (2006) Dominance relationships between self-incompatibility alleles controlled by DNA methylation. Nat Genet 38:297–299

    Article  PubMed  CAS  Google Scholar 

  • Shimosato H, Yokota N, Shiba H, Iwano M, Entani T, Che FS, Watanabe M, Isogai A, Takayama S (2007) Characterization of the SP11/SCR high-affinity binding site involved in self/non self recognition in Brassica self-incompatibility. Plant Cell 19:107–117

    Article  PubMed  CAS  Google Scholar 

  • Stein JC, Howlett B, Boyes DC, Nasrallah 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

    Article  PubMed  CAS  Google Scholar 

  • Stephenson AG, Doughty J, Dixon S, Elleman C, Hiscock S, Dickinson HG (1997) The male determinant of self-incompatibility in Brassica oleracea is located in the pollen coating. Plant J 12:1351–1359

    Article  CAS  Google Scholar 

  • Stone SL, Anderson EM, Mullen RT, Goring DR (2003) ARC1 is an E3 ubiquitin ligase and promotes the ubiquitination of proteins during the rejection of self-incompatible Brassica pollen. Plant Cell 15:885–898

    Article  PubMed  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Takasaki T, Hatakeyama K, Suzuki G, Watanabe M, Isogai A, Hinata K (2000) The S receptor kinase determines self-incompatibility in Brassica stigma. Nature 403:913–916

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Takayama S, Shimosato H, Shiba H, Funato M, Che FS, Watanabe M, Iwano M, Isogai A (2001) Direct ligand-receptor complex interaction controls Brassica self-incompatibility. Nature 413:534–538

    Article  PubMed  CAS  Google Scholar 

  • Tang C, Toomajian C, Sherman-Broyles S, Plagnol V, Guo YL, Hu TT, Clark RM, Nasrallah JB, Weigel D, Nordborg M (2007) The evolution of selfing in Arabidopsis thaliana. Science 317:1070–1072

    Article  PubMed  CAS  Google Scholar 

  • Tarutani Y, Shiba H, Iwano M, Kakizaki T, Suzuki G, Watanabe M, Isogai A, Takayama S (2010) Trans-acting small RNA determines dominance relationships in Brassica self-incompatibility. Nature 466:983–986

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Tsuchimatsu T, Suwabe K, Shimizu-Inatsugi R, Isokawa S, Pavlidis P, Stadler T, Suzuki G, Takayama S, Watanabe M, Shimizu KK (2010) Evolution of self-compatibility in Arabidopsis by a mutation in the male specificity gene. Nature 464:1342–1346

    Article  PubMed  CAS  Google Scholar 

  • Uyenoyama MK (2000) Evolutionary dynamics of self-incompatibility alleles in Brassica. Genetics 156:351–359

    PubMed  CAS  Google Scholar 

  • Vanoosthuyse V, Miege C, Dumas C, Cock JM (2001) Two large Arabidopsis thaliana gene families are homologous to the Brassica gene superfamily that encodes pollen coat proteins and the male component of the self-incompatibility response. Plant Mol Biol 46:17–34

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Centre National de la Recherche Scientifique, Institut National de la Recherche Agronomique, Université Claude Bernard Lyon I, Ecole Normale Supérieure de Lyon, Lyon, France

    Isabelle Fobis-Loisy & Thierry Gaude

  2. Department of Plant Biology, Saarland University, Campus A 2.4, 66123, Saarbruecken, Germany

    Rumen Ivanov

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  1. Isabelle Fobis-Loisy
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  2. Rumen Ivanov
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  3. Thierry Gaude
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Correspondence to Thierry Gaude .

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  1. , Monash Institute of Pharmaceutical Scien, Monash University, Royal Parade 381, Parkville, 3052, Australia

    Helen R. Irving

  2. , Division of Chemistry, Life Science and, 4700 King Abdullah University of Science, Thuwal, 23955-6900, Saudi Arabia

    Christoph Gehring

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Fobis-Loisy, I., Ivanov, R., Gaude, T. (2012). The S-LOCUS CYSTEINE-RICH PROTEIN (SCR): A Small Peptide with A High Impact on the Evolution of Flowering Plants. In: Irving, H., Gehring, C. (eds) Plant Signaling Peptides. Signaling and Communication in Plants, vol 16. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-27603-3_5

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