How far are we from unravelling self-incompatibility in grasses?

The genetic and physiological mechanisms involved in limiting self-fertilization in angiosperms, referred to as self-incompatibility (SI), have significant effects on population structure and have potential diversification and evolutionary consequences. Up to now, details of the underlying genetic control and physiological basis of SI have been elucidated in two different gametophytic SI (GSI) systems, the S-RNase SI and the Papaver SI systems, and the sporophytic SI (SSI) system (Brassica). In the grass family (Poaceae), which contains all the cereal and major forage crops, SI has been known for half a century to be controlled gametophytically by two multiallelic and independent loci, S and Z. But still none of the gene products for S and Z is known and only limited information on related biochemical responses is available. Here we compare current knowledge of grass SI with that of other well-characterized SI systems and speculate about the relationship between SSI and grass SI. Additionally, we discuss comparative mapping as a tool for the further investigation of grass SI.

[1]  J. Richter,et al.  Poly(A) elongation during Xenopus oocyte maturation is required for translational recruitment and is mediated by a short sequence element. , 1989, Genes & development.

[2]  R. Mullen,et al.  ARC1 Is an E3 Ubiquitin Ligase and Promotes the Ubiquitination of Proteins during the Rejection of Self-Incompatible Brassica Pollen Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.009845. , 2003, The Plant Cell Online.

[3]  B. Kemp,et al.  S cysteine-rich (SCR) binding domain analysis of the Brassica self-incompatibility S-locus receptor kinase. , 2007, The New phytologist.

[4]  T. Nishio,et al.  Genomic organization of the S core region and the S flanking regions of a class-II S haplotype in Brassica rapa , 2003, Molecular Genetics and Genomics.

[5]  A. Lundqvist STUDIES ON SELF‐STERILITY IN RYE, SECALE CEREALE L , 2010 .

[6]  P. Bedinger The remarkable biology of pollen. , 1992, The Plant cell.

[7]  P. Langridge,et al.  Self-incompatibility in the grasses: evolutionary relationship of the S gene from Phalaris coerulescens to homologous sequences in other grasses , 1997, Plant Molecular Biology.

[8]  J. Gray,et al.  Self-incompatibility in Nicotiana alata involves degradation of pollen rRNA , 1990, Nature.

[9]  T. Nishio,et al.  Comparison of the Genome Structure of the Self-Incompatibility (S) Locus in Interspecific Pairs of S Haplotypes , 2006, Genetics.

[10]  M. Laurin,et al.  Molecular analysis of the stylar-expressed Solanum chacoense small asparagine-rich protein family related to the HT modifier of gametophytic self-incompatibility in Nicotiana. , 2002, The Plant journal : for cell and molecular biology.

[11]  J. Heslop-Harrison Genetics and physiology of angiosperm incompatibility systems , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[12]  A. Iezzoni,et al.  Accumulation of Nonfunctional S-Haplotypes Results in the Breakdown of Gametophytic Self-Incompatibility in Tetraploid Prunus , 2006, Genetics.

[13]  A. Isogai,et al.  Comparative analysis of the self‐incompatibility (S‐) locus region of Prunus mume: identification of a pollen‐expressed F‐box gene with allelic diversity , 2003, Genes to cells : devoted to molecular & cellular mechanisms.

[14]  F. C. H. Franklin,et al.  Gametophytic self-incompatibility inhibits pollen tube growth using different mechanisms. , 2003, Trends in plant science.

[15]  T. Nishio,et al.  The S receptor kinase gene determines dominance relationships in stigma expression of self-incompatibility in Brassica. , 2001, The Plant journal : for cell and molecular biology.

[16]  Z. Grieg,et al.  A linkage map of meadow fescue (Festuca pratensis Huds.) and comparative mapping with other Poaceae species , 2003, Theoretical and Applied Genetics.

[17]  K. Shivanna,et al.  The receptive surface of the angiosperm stigma , 1977 .

[18]  J. Nasrallah,et al.  Recognition and rejection of self in plant reproduction. , 2002, Science.

[19]  J. Richter,et al.  Mutations affecting self-incompatibility in Phalaris coerulescens Desf. (Poaceae) , 1992, Heredity.

[20]  H. Dickinson,et al.  PCP-A1, a Defensin-like Brassica Pollen Coat Protein That Binds the S Locus Glycoprotein, Is the Product of Gametophytic Gene Expression , 1998, Plant Cell.

[21]  T. Nishio,et al.  Characterization of Brassica S‐haplotypes lacking S‐locus glycoprotein 1 , 2000, FEBS letters.

[22]  B. Beecher,et al.  Factors Affecting Inter- and Intra-specific Pollen Rejection in Nicotiana , 2000 .

[23]  G. Wricke,et al.  Linkage between the incompatibility locus Z and a β-glucosidase locus in rye , 1989 .

[24]  M. J. Lawrence,et al.  Self-incompatibility in ryegrass , 1979, Heredity.

[25]  P. Langridge,et al.  Cloning a putative self-incompatibility gene from the pollen of the grass Phalaris coerulescens. , 1994, The Plant cell.

[26]  M. D. Hayward,et al.  The genetic control of self-compatibility in an inbred line of Lolium perenne L , 1991, Heredity.

[27]  T. Nishio,et al.  Effects of Recombination on Hitchhiking Diversity in the Brassica Self-incompatibility Locus Complex , 2007, Genetics.

[28]  A. Isogai,et al.  Characterization of the SP11/SCR High-Affinity Binding Site Involved in Self/Nonself Recognition in Brassica Self-Incompatibility , 2007, The Plant Cell Online.

[29]  M. J. Lawrence,et al.  Self-incompatibility in ryegrass , 1979, Heredity.

[30]  F. Franklin,et al.  The molecular and genetic basis of pollen-pistil interactions. , 2001, The New phytologist.

[31]  H. Hirano,et al.  S Locus F-Box Brothers: Multiple and Pollen-Specific F-Box Genes With S Haplotype-Specific Polymorphisms in Apple and Japanese Pear , 2007, Genetics.

[32]  Mervyn O. Humphreys,et al.  Comparison and integration of genetic maps generated from F2 and BC1‐type mapping populations in perennial ryegrass , 2002 .

[33]  P. Wehling,et al.  Approaching the self-incompatibility locus Z in rye (Secale cereale L.) via comparative genetics , 2005, Theoretical and Applied Genetics.

[34]  P. Wehling,et al.  Phosphorylation of pollen proteins in relation to self-incompatibility in rye (Secale cereale L.) , 1994, Sexual Plant Reproduction.

[35]  J. Heslop-Harrison,et al.  THE POLLEN‐STIGMA INTERACTION IN THE GRASSES. 2. POLLEN‐TUBE PENETRATION AND THE STIGMA RESPONSE IN SECALE , 1981 .

[36]  H. Dickinson,et al.  Pollination in species with dry stigmas: the nature of the early stigmatic response and the pathway taken by pollen tubes. , 1992, The New phytologist.

[37]  D. Ripoll,et al.  Structural modules for receptor dimerization in the S-locus receptor kinase extracellular domain , 2007, Proceedings of the National Academy of Sciences.

[38]  D. de Nettancourt,et al.  Incompatibility in angiosperms , 1977, Sexual Plant Reproduction.

[39]  F. Franklin,et al.  Gametophytic self-incompatibility inPapaver rhoeas L. , 1992, Sexual Plant Reproduction.

[40]  J. Heslop-Harrison,et al.  Pollen-wall proteins: the fate of intine-held antigens on the stigma in compatible and incompatible pollinations of Phalaris tuberosa L. , 1971, Journal of cell science.

[41]  L. Bohs,et al.  Historical inferences from the self‐incompatibility locus , 2003 .

[42]  A. Lundqvist The complex S‐gene system for control of self‐incompatibility in the buttercup genus Ranunculus , 2008 .

[43]  K. K. Pandey Origin of complementary incompatibility systems in flowering plants , 1977, Theoretical and Applied Genetics.

[44]  Shihshieh Huang,et al.  Identification of the pollen determinant of S-RNase-mediated self-incompatibility , 2004, Nature.

[45]  J. Heslop-Harrison Pollen-Stigma Interaction and Cross-Incompatibility in the Grasses , 1982, Science.

[46]  D. Goring,et al.  Binding of an arm repeat protein to the kinase domain of the S-locus receptor kinase. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[47]  P. Awadalla,et al.  Identification and characterization of a polymorphic receptor kinase gene linked to the self-incompatibility locus of Arabidopsis lyrata. , 2001, Genetics.

[48]  H. Connor Breeding systems in the grasses: a survey , 1979 .

[49]  V. Franklin-Tong,et al.  Gametophytic self-incompatibility: understanding the cellular mechanisms involved in “self” pollen tube inhibition , 2006, Planta.

[50]  M. Nasrallah,et al.  The male determinant of self-incompatibility in Brassica. , 1999, Science.

[51]  G. Ledyard Stebbins,et al.  Flowering Plants: Evolution Above the Species Level , 1975 .

[52]  Shihshieh Huang,et al.  S proteins control rejection of incompatible pollen in Petunia inflata , 1994, Nature.

[53]  J. Heslop-Harrison,et al.  THE POLLEN‐STIGMA INTERACTION IN THE GRASSES: 4. AN INTERPRETATION OF THE SELF‐INCOMPATIBILITY RESPONSE , 1982 .

[54]  J. Heslop-Harrison Pollen-stigma interaction in grasses: a brief review , 1979 .

[55]  S. Good-Avila,et al.  Macrophylogenetic analyses of the gain and loss of self-incompatibility in the Asteraceae. , 2007, The New phytologist.

[56]  A. Isogai,et al.  Direct ligand–receptor complex interaction controls Brassica self-incompatibility , 2001, Nature.

[57]  D. Hayman The Genetical Control of Incompatibility in Phalaris Coerulescens Desf. , 1956 .

[58]  X. Vekemans,et al.  INVITED REVIEW: Plant self‐incompatibility in natural populations: a critical assessment of recent theoretical and empirical advances , 2004, Molecular ecology.

[59]  W. M. Lush,et al.  Observations of pollen tube growth in Nicotiana alata and their implications for the mechanism of self-incompatibility , 1997, Sexual Plant Reproduction.

[60]  Charles Darwin,et al.  The Effects of Cross and Self Fertilisation in the Vegetable Kingdom , 1972 .

[61]  M. Herrero,et al.  Pollen tube growth following compatible and incompatible intraspecific pollinations in Petunia hybrida , 1980, Planta.

[62]  S. McInnis,et al.  Pollen recognition and rejection during the sporophytic self-incompatibility response: Brassica and beyond. , 2003, Trends in plant science.

[63]  J. Rudd,et al.  Self-incompatibility in Papaver targets soluble inorganic pyrophosphatases in pollen , 2006, Nature.

[64]  Zhenhai Han,et al.  Isolation and identification of the pollen-expressed polymorphic F-box genes linked to the S-locus in apple (Malus × domestica) , 2006, Sexual Plant Reproduction.

[65]  Akira Isogai,et al.  The S receptor kinase determines self-incompatibility in Brassica stigma , 2000, Nature.

[66]  S. Hiscock,et al.  The different mechanisms of sporophytic self-incompatibility. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[67]  A. Voylokov,et al.  Genetic studies of self-fertility in rye (Secale cereale L.). 2. The search for isozyme marker genes linked to self-incompatibility loci , 1993, Theoretical and Applied Genetics.

[68]  J. Vrebalov,et al.  Determining the Physical Limits of the Brassica S Locus by Recombinational Analysis , 2000, Plant Cell.

[69]  C. Dumas,et al.  The S-locus receptor kinase is inhibited by thioredoxins and activated by pollen coat proteins , 2001, Nature.

[70]  J. Heslop-Harrison,et al.  THE POLLEN‐STIGMA INTERACTION IN THE GRASSES. 3. FEATURES OF THE SELF‐INCOMPATIBILITY RESPONSE , 1982 .

[71]  W. Kaiser,et al.  Self-incompatibility in ryegrass 12. Genotyping and mapping the S and Z loci of Lolium perenne L , 2002, Heredity.

[72]  V. Korzun,et al.  Mapping of three self-fertility mutations in rye (Secale cereale L.) using RFLP, isozyme and morphological markers , 1998, Theoretical and Applied Genetics.

[73]  A. Isogai,et al.  The pollen determinant of self-incompatibility in Brassica campestris. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[74]  G. Jung,et al.  Chromosomal rearrangements differentiating the ryegrass genome from the Triticeae, oat, and rice genomes using common heterologous RFLP probes , 2005, Theoretical and Applied Genetics.

[75]  P. Langridge,et al.  Self-incompatibility in the Grasses , 2000 .

[76]  K. Holsinger,et al.  S-RNase-mediated gametophytic self-incompatibility is ancestral in eudicots. , 2002, Molecular biology and evolution.

[77]  H. Hirano,et al.  Structural and Transcriptional Analysis of the Self-Incompatibility Locus of Almond Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.009290.: Identification of a Pollen-Expressed F-Box Gene with Haplotype-Specific Polymorphism , 2003, The Plant Cell Online.

[78]  M. Nasrallah,et al.  Allele-Specific Receptor-Ligand Interactions in Brassica Self-Incompatibility , 2001, Science.

[79]  Monoallelic expression and dominance interactions in anthers of self-incompatible Arabidopsis lyrata. , 2002, Plant physiology.

[80]  O. Anderson Morphology and Systematics , 1983 .

[81]  F. Franklin,et al.  Identification of a membrane glycoprotein in pollen of Papaver rhoeas which binds stigmatic self‐incompatibility (S‐) proteins , 1996 .

[82]  S. Wright,et al.  The Distribution of Self-Sterility Alleles in Populations. , 1939, Genetics.

[83]  Y. Satta,et al.  The Dominance of Alleles Controlling Self-Incompatibility in Brassica Pollen Is Regulated at the RNA Level Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010378. , 2002, The Plant Cell Online.

[84]  S. Rothstein,et al.  Two members of the thioredoxin-h family interact with the kinase domain of a Brassica S locus receptor kinase. , 1996, The Plant cell.

[85]  M. D. Hayward,et al.  Identification and mode of action of self-compatibility loci in Lolium perenne L. , 2005, Heredity.

[86]  B. Mou,et al.  S-RNase expressed in transgenic Nicotiana causes S-allele-specific pollen rejection , 1994, Nature.

[87]  P. Langridge,et al.  Thioredoxin activity in the C terminus of Phalaris S protein. , 1995, The Plant journal : for cell and molecular biology.

[88]  K. Larsen,et al.  Complex self‐incompatibility systems in Ranunculus acris L. and Beta vulgaris L. , 2009 .

[89]  C. N. Hancock,et al.  The stylar 120 kDa glycoprotein is required for S-specific pollen rejection in Nicotiana. , 2005, The Plant journal : for cell and molecular biology.

[90]  Ulla Østerbye Self‐incompatibility in Ranunculus acris L. , 2008 .

[91]  J. S. Heslop-Harrison,et al.  AN INTERPRETATION OF THE HYDRODYNAMICS OF POLLEN , 1979 .

[92]  L. Bohs,et al.  Ancient polymorphism reveals unidirectional breeding system shifts , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[93]  Toshihiko Yamada,et al.  An enhanced molecular marker based genetic map of perennial ryegrass (Lolium perenne) reveals comparative relationships with other Poaceae genomes. , 2002, Genome.

[94]  P. Langridge,et al.  High-resolution mapping of the S and Z loci of Phalaris coerulescens. , 2004, Genome.