S-RNases and sexual incompatibility: structure, functions, and evolutionary perspectives.

S-RNase-based gametophytic self-incompatibility appears to be the most phylogenetically widespread form of self-incompatibility found in the angiosperms, having been reported in the Solanaceae, Scrophulariaceae, and Rosaceae. This intraspecific breeding barrier is controlled by a single genetic locus termed S. Rejection of self-pollen has been shown to be mediated in the pistil by a highly polymorphic series of ribonucleases, but as yet the pollen component of this recognition system has not been identified. Here we review our present knowledge concerning the structure, functions, and evolution of S-RNases and the S-loci in which they reside. In addition we present two new phylogenetic analyses of S-RNases which suggest that (1). sequence variability between S-alleles is spread across the whole gene and is not as clustered as is generally believed and (2). there is evidence of recombination and/or diversifying selection in two distinct regions of S-RNases. The implications of these findings are discussed.

[1]  A. McCubbin,et al.  Identification of self-incompatibility (S-) locus linked pollen cDNA markers in Petunia inflata. , 2000, Genome.

[2]  A. McCubbin,et al.  Construction of a binary bacterial artificial chromosome library of Petunia inflata and the isolation of large genomic fragments linked to the self-incompatibility (S-) locus. , 2000, Genome.

[3]  H. Dickinson,et al.  Unilateral incompatibility within the brassicaceae: further evidence for the involvement of the self-incompatibility (S)-locus , 1993, Theoretical and Applied Genetics.

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

[5]  J. Brewbaker.  Biology of the Angiosperm Pollen grain , 1959 .

[6]  M. J. Lawrence.  Population Genetics of the Homomorphic Self-incompatibility Polymorphisms in Flowering Plants , 2000 .

[7]  M. Uyenoyama,et al.  On the origin of self-incompatibility haplotypes: transition through self-compatible intermediates. , 2001, Genetics.

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

[9]  T. Kao,et al.  Breakdown of self-incompatibility in a natural population of Petunia axillaris (Solanaceae) in Uruguay containing both self-incompatible and self-compatible plants , 1999, Sexual Plant Reproduction.

[10]  K. Fukui,et al.  Centromeric localization of an S-RNase gene in Petunia hybrida Vilm. , 1999, Theoretical and Applied Genetics.

[11]  Stephen J. Elledge,et al.  SKP1 Connects Cell Cycle Regulators to the Ubiquitin Proteolysis Machinery through a Novel Motif, the F-Box , 1996, Cell.

[12]  Hong Wang,et al.  A pollen tube growth stimulatory glycoprotein is deglycosylated by pollen tubes and displays a glycosylation gradient in the flower , 1995, Cell.

[13]  D. Mulcahy,et al.  Biotechnology and ecology of pollen : proceedings of the International Conference on the Biotechnology and Ecology of Pollen, 9-11 July 1985, University of Massachusetts, Amherst, MA, U.S.A. , 1986 .

[14]  M. Uyenoyama,et al.  Evolutionary Dynamics of Dual-Specificity Self-Incompatibility Alleles , 2000, Plant Cell.

[15]  A. E. Clarke,et al.  Inhibition of in Vitro Pollen Tube Growth by Isolated S-Glycoproteins of Nicotiana alata. , 1989, The Plant cell.

[16]  H. Willard,et al.  Physical and genetic mapping of the human X chromosome centromere: repression of recombination. , 1998, Genome research.

[17]  F. W. Martin.  The behavior of lycopersicon incompatibility alleles in an alien genetic milieu. , 1968, Genetics.

[18]  E. Coen,et al.  Origin of allelic diversity in antirrhinum S locus RNases. , 1996, The Plant cell.

[19]  C. Kunz,et al.  Phosphorylation of style S-RNases by Ca2+-dependent protein kinases from pollen tubes , 2004, Sexual Plant Reproduction.

[20]  C. N. Hancock,et al.  S-RNase complexes and pollen rejection. , 2003, Journal of experimental botany.

[21]  O. Maes,et al.  Production of an S RNase with Dual Specificity Suggests a Novel Hypothesis for the Generation of New S Alleles , 1999, Plant Cell.

[22]  Richard H. Glaven,et al.  S-related protein can be recombined with self-compatibility in interspecific derivatives ofLycopersicon , 1995, Biochemical Genetics.

[23]  H. Horiuchi,et al.  Primary structure of a base non-specific ribonuclease from Rhizopus niveus. , 1988, Journal of biochemistry.

[24]  W. Ruhland.  Encyclopedia of plant physiology. , 1958 .

[25]  R. Raines,et al.  RNS2: a senescence-associated RNase of Arabidopsis that diverged from the S-RNases before speciation. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[26]  M. Nasrallah,et al.  Self-incompatibility in the Brassicaceae: receptor-ligand signaling and cell-to-cell communication. , 2002, The Plant cell.

[27]  B. Beecher,et al.  Effects of RNases on rejection of pollen from Nicotiana tabacum and N. plumbaginifolia , 2001, Sexual Plant Reproduction.

[28]  A. Hughes,et al.  Evidence that intragenic recombination contributes to allelic diversity of the S-RNase gene at the self-incompatibility (S) locus in Petunia inflata. , 2001, Plant physiology.

[29]  B. Mou,et al.  A small asparagine-rich protein required for S-allele-specific pollen rejection in Nicotiana. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[30]  H. D. Niall,et al.  Cloning of cDNA for a stylar glycoprotein associated with expression of self-incompatibility in Nicotiana alata , 1986, Nature.

[31]  M. Tyers,et al.  The F-box: a new motif for ubiquitin dependent proteolysis in cell cycle regulation and signal transduction. , 1999, Progress in biophysics and molecular biology.

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

[33]  Carbohydrate moiety of the Petunia inflata S3 protein is not required for self-incompatibility interactions between pollen and pistil. , 1994, The Plant cell.

[34]  A. Geitmann,et al.  Signalling and the cytoskeleton of pollen tubes of Papaver rhoeas. , 2000 .

[35]  D. Mulcahy,et al.  Biotechnology and Ecology of Pollen , 1986, Springer New York.

[36]  K. K. Pandey.  EVOLUTION OF UNILATERAL INCOMPATIBILITY IN FLOWERING PLANTS: FURTHER EVIDENCE IN FAVOUR OF TWIN SPECIFICITIES CONTROLLING INTRA‐AND INTERSPECIFIC INCOMPATIBILITY , 1981 .

[37]  N. G. Hogenboom.  Incongruity: Non-Functioning of Intercellular and Intracellular Partner Relationships Through Non-Matching Information , 1984 .

[38]  T. Kao,et al.  The flanking regions of twoPetunia inflata S alleles are heterogeneous and contain repetitive sequences , 1992, Plant Molecular Biology.

[39]  Xi Wang,et al.  Use of Petunia inflata as a Model for the Study of Solanaceous Type Self-incompatibility , 2000 .

[40]  P. Dodds,et al.  A genetic map of the Nicotiana alata S locus that includes three pollen-expressed genes , 2000, Theoretical and Applied Genetics.

[41]  F. Franklin,et al.  Evidence for DNA fragmentation triggered in the self-incompatibility response in pollen of Papaver rhoeas. , 2000, The Plant journal : for cell and molecular biology.

[42]  V. Su,et al.  Genetic analysis of Nicotiana pollen-part mutants is consistent with the presence of an S-ribonuclease inhibitor at the S locus , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[43]  J. Deverna,et al.  Expression of unilateral incompatibility in pollen of Lycopersicon pennellii is determined by major loci on chromosomes 1, 6 and 10 , 1991, Theoretical and Applied Genetics.

[44]  B. Beecher,et al.  S RNase and Interspecific Pollen Rejection in the Genus Nicotiana: Multiple Pollen-Rejection Pathways Contribute to Unilateral Incompatibility between Self-Incompatible and Self-Compatible Species. , 1996, The Plant cell.

[45]  H. Hirano,et al.  Cloning and characterization of cDNAs encoding S-RNases from almond (Prunus dulcis): primary structural features and sequence diversity of the S-RNases in Rosaceae , 1998, Molecular and General Genetics MGG.

[46]  R. T. Hoopen,et al.  The self-incompatibility (S) locus in Petunia hybrida is located on chromosome III in a region, syntenic for the solanaceae , 1998 .

[47]  T. Kao,et al.  How flowering plants discriminate between self and non-self pollen to prevent inbreeding. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[48]  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.

[49]  L. K. Crowe,et al.  Unilateral interspecific incompatibility in flowering plants , 1958, Heredity.

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

[51]  J. P. Mascarenhas.  Molecular Mechanisms of Pollen Tube Growth and Differentiation. , 1993, The Plant cell.

[52]  B. Han,et al.  An F-box gene linked to the self-incompatibility (S) locus of Antirrhinum is expressed specifically in pollen and tapetum , 2002, Plant Molecular Biology.

[53]  D. Lewis.  Comparative incompatibility in angiosperms and fungi. , 1954, Advances in genetics.

[54]  W. Broothaerts,et al.  Self-incompatibility RNases from three plant families: homology or convergence? , 1997, American journal of botany.

[55]  R. Knox,et al.  Genetic control of self-incompatibility and reproductive development in flowering plants , 1994, Advances in Cellular and Molecular Biology of Plants.

[56]  G. D'alessio,et al.  Ribonucleases : structures and functions , 1997 .

[57]  Y. Kawata,et al.  Amino-acid sequence of ribonuclease T2 from Aspergillus oryzae. , 1988, European journal of biochemistry.

[58]  S. Tanksley,et al.  An interspecific backcross of Lycopersicon esculentum x L. hirsutum: linkage analysis and a QTL study of sexual compatibility factors and floral traits. , 1997, Genetics.

[59]  G. Ledyard Stebbins,et al.  Variation and Evolution in Plants , 1951 .

[60]  G. Copenhaver,et al.  Assaying genome-wide recombination and centromere functions with Arabidopsis tetrads. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[61]  M. Hirai,et al.  Cultivated tomato has defects in both S-RNase and HT genes required for stylar function of self-incompatibility. , 2002, The Plant journal : for cell and molecular biology.

[62]  Shihshieh Huang,et al.  Ribonuclease activity of Petunia inflata S proteins is essential for rejection of self-pollen. , 1994, The Plant cell.

[63]  T. Nishio,et al.  Style‐specific self‐compatible mutation caused by deletion of the S‐RNase gene in Japanese pear (Pyrus serotina) , 1997 .

[64]  M. Anderson,et al.  Loss of a histidine residue at the active site of S-locus ribonuclease is associated with self-compatibility in Lycopersicon peruvianum. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[65]  K. K. Pandey.  Phases in the S-gene expression, and S-allele interaction in the control of interspecific incompatibility , 1973, Heredity.

[66]  S. Y. Lee,et al.  The 5' flanking sequences of two S alleles in Lycopersicon peruvianum are highly heterologous but contain short blocks of homologous sequences. , 1995, Plant & cell physiology.

[67]  Richard D. Thompson,et al.  Sequence variability and gene structure at the self-incompatibility locus of Solanum tuberosum , 1991, Molecular and General Genetics MGG.

[68]  E. Newbigin,et al.  The S-locus of Nicotiana alata: genomic organization and sequence analysis of two S-RNase alleles , 1995, Plant Molecular Biology.

[69]  Boris Igic,et al.  Evolutionary relationships among self-incompatibility RNases , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[70]  T. Ioerger,et al.  Primary structural features of the self-incompatibility protein in solanaceae , 1991, Sexual Plant Reproduction.

[71]  T. Shinkawa,et al.  Primary structural features of rosaceous S-RNases associated with gametophytic self-incompatibility , 1998, Plant Molecular Biology.

[72]  P. Ebert,et al.  Style self-incompatibility gene products of Nicotlana alata are ribonucleases , 1989, Nature.

[73]  Anuradha Singh,et al.  Characterization of Ribonuclease Activity of Three S-Allele-Associated Proteins of Petunia inflata. , 1991, Plant physiology.

[74]  F. W. Martin.  The Genetic Control of Unilateral Incompatibility between Two Tomato Species. , 1967, Genetics.

[75]  M. J. Lawrence,et al.  Cell and Molecular Biology of Self-Incompatibility in Flowering Plants , 1995 .

[76]  T. Nishio,et al.  Self-incompatibility (S) alleles of the rosaceae encode members of a distinct class of the T2/S ribonuclease superfamily , 2005, Molecular and General Genetics MGG.

[77]  O. Maes,et al.  Hypervariable Domains of Self-Incompatibility RNases Mediate Allele-Specific Pollen Recognition. , 1997, The Plant cell.

[78]  P. Dodds,et al.  Pollen-expressed S-RNases are not involved in self-incompatibility in Lycopersicon peruvianum , 1999, Sexual Plant Reproduction.

[79]  D. Luu,et al.  S-RNase uptake by compatible pollen tubes in gametophytic self-incompatibility , 2000, Nature.

[80]  A. Cheung,et al.  A pollen tube growth-promoting arabinogalactan protein from nicotiana alata is similar to the tobacco TTS protein. , 2000, The Plant journal : for cell and molecular biology.

[81]  B. Beecher,et al.  Exchanging sequence domains between S-RNases from Nicotiana alata disrupts pollen recognition. , 1997, The Plant journal : for cell and molecular biology.

[82]  Professor Dreux de Nettancourt.  Incompatibility and Incongruity in Wild and Cultivated Plants , 2000, Springer Berlin Heidelberg.

[83]  A. Kheyr-Pour,et al.  A New S-Allele and Specific S-Proteins Associated with Two S-Alleles in Nicotiana Alata , 1986 .

[84]  M. Anderson,et al.  A relic S-RNase is expressed in the styles of self-compatible Nicotiana sylvestris. , 1998, The Plant journal : for cell and molecular biology.

[85]  M. Mutschler,et al.  Interspecific crossing barriers in Lycopersicon and their relationship to self-incompatibility , 1994 .

[86]  M. Anderson,et al.  Self-incompatibility: a self-recognition system in plants. , 1990, Science.

[87]  H. Hirano,et al.  Characterization of the S-locus region of almond (Prunus dulcis): analysis of a somaclonal mutant and a cosmid contig for an S haplotype. , 2001, Genetics.

[88]  T. Kao,et al.  S-alleles are retained and expressed in a self-compatible cultivar of Petunia hybrida , 1991, Molecular and General Genetics MGG.

[89]  E. Yamashita,et al.  The 1.55 A resolution structure of Nicotiana alata S(F11)-RNase associated with gametophytic self-incompatibility. , 2001, Journal of molecular biology.

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

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

[92]  J. Golz,et al.  A molecular description of mutations affecting the pollen component of the Nicotiana alata S locus. , 1999, Genetics.

[93]  P. Green,et al.  The Ribonucleases of Higher Plants , 1994 .

[94]  T. Kao,et al.  Sequence of an S-protein of Lycopersicon peruvianum and comparison with other solanaceous S-proteins , 1992, Sexual Plant Reproduction.

[95]  R. Thompson,et al.  The S locus of flowering plants: when self-rejection is self-interest. , 1992, Trends in genetics : TIG.

[96]  T. Kao,et al.  Are the Hypervariable Regions of S RNases Sufficient for Allele-Specific Recognition of Pollen? , 1998, Plant Cell.

[97]  D. Luu,et al.  Rejection of S-heteroallelic pollen by a dual-specific s-RNase in Solanum chacoense predicts a multimeric SI pollen component. , 2001, Genetics.

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

[99]  T. L. Sims,et al.  Identification of a S-ribonuclease-binding protein in Petunia hybrida , 2001, Plant Molecular Biology.

[100]  C. Napoli,et al.  Segregation distortion of T-DNA markers linked to the self-incompatibility (S) locus in Petunia hybrida. , 2000, Genetics.

[101]  Anuradha Singh,et al.  RNase X2, a pistil-specific ribonuclease from Petunia inflata, shares sequence similarity with solanaceous S proteins , 1992, Plant Molecular Biology.

[102]  D. Charlesworth,et al.  Molecular variation at the self-incompatibility locus in natural populations of the genera Antirrhinum and Misopates , 2002, Heredity.