Plant Molecular Biology

, Volume 37, Issue 6, pp 931–941 | Cite as

Primary structural features of rosaceous S-RNases associated with gametophytic self-incompatibility

  • Takeshi Ishimizu
  • Toyohide Shinkawa
  • Fumio Sakiyama
  • Shigemi Norioka
Article

Abstract

We isolated cDNA clones encoding five S-RNases (S1-,S3- , S5-, S6-, S7-RNases) from pistils of Pyrus pyrifolia (Japanese pear), a member of the Rosaceae. Their amino acid sequences were aligned with those of other rosaceous S-RNases sequenced so far. A total of 76 conserved amino acid residues were stretched throughout the sequence, but were absent from the 51–66 region which was designated the hypervariable (HV) region. The phylogenetic tree of rosaceous S-RNases showed that S-RNase polymorphism predated the divergence of Pyrus and Malus. Pairwise comparison of these S-RNases detected two highly homologous pairs, P. pyrifolia S1- and S4-RNases (90.0%) and P. pyrifolia S3- and S5-RNases (95.5%). The positions of amino acid substitutions between S1- and S4-RNases were spread over the entire region, but in the pair of S3- and S5-RNases, amino acid substitutions were found in the 21–90 region including the HV region. The substitutions in this restricted region appear to be sufficient to discriminate between S3 and S5 pollen and to trigger the self-incompatible reaction.

amino acid sequencing cDNA Rosaceae S-allele specificity self-incompatibility S-RNase 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Banno K, Kumashiro K, Tateishi S, Takamizawa M, Kimura Y, Tokuhisa T, Tamura F, Tanabe K: Breeding of intergeneric hybrids between Japanese pear and the apple. (In Japanese). J Jpn Soc Hort Sci 62 (Suppl 1): 138–139 (1993).Google Scholar
  2. 2.
    Broothaerts W, Janssens GA, Proost P, Broekaert WF: cDNA cloning and molecular analysis of two self-incompatibility alleles from apple. Plant Mol Biol 27: 499–511(1995).PubMedGoogle Scholar
  3. 3.
    Challice JS: Rosaceae chemotaxonomy and the origins of the Pomoidae. Bot J Linn Soc 69: 239–259 (1974).Google Scholar
  4. 4.
    Crestfield AM, Moore S, Stein WH: The preparation and enzymatic hydrolysis of reduced and S-carboxymethylated proteins. J Biol Chem 238: 622–627 (1963).PubMedGoogle Scholar
  5. 5.
    de Nettancourt, D. Incompatibility in Angiosperms. Springer-Verlag, Berlin (1977).Google Scholar
  6. 6.
    Dodds PN, Clarke AE, Newbigin E: A molecular perspective on pollination in flowering plants. Cell 85: 141–144 (1996).PubMedGoogle Scholar
  7. 7.
    Ioerger TR, Clark AG, Kao T-h: Polymorphism at the selfincompatibility locus in Solanaceae predates speciation. Proc Natl Acd Sci USA 87: 9732–9735 (1990).Google Scholar
  8. 8.
    Ioerger TR, Gohlke JR, Xu B, Kao T-h: Primary structural features of the self-incompatibility protein in Solanaceae. Sex Plant Reprod 4: 81–87 (1991).CrossRefGoogle Scholar
  9. 9.
    Ishimizu T, Sato Y, Saito T, Yoshimura Y, Norioka S, Nakanishi T, Sakiyama F: Identification and partial amino acid sequences of seven S-RNases associated with selfincompatibility of the Japanese pear, Pyrus pyriforia Nakai. J Biochem 120: 326–334 (1996).PubMedGoogle Scholar
  10. 10.
    Ishimizu T, Norioka S, Kanai M, Clarke AE, Sakiyama F: Location of cysteine and cystine residues in S-ribonucleases associated with gametophytic self-incompatibility. Eur J Biochem 242: 627–635 (1996).PubMedGoogle Scholar
  11. 11.
    Ishimizu T, Norioka S, Nakanishi T, Sakiyama F: S-genotype of Japanese pear ‘Hosui’. J Jpn Soc Hort Sci, in press (1998).Google Scholar
  12. 12.
    Janssens GA, Goderis IJ, Broekaert WF, Broothaerts W: A molecular method for S-allele identification in apple based on allele-specific PCR. Theor Appl Genet 91: 691–698 (1995).Google Scholar
  13. 13.
    Kao T-h, McCubbin AG: How flowering plants discriminate between self and non-self pollen to prevent inbreeding. Proc Natl Acad Sci USA 93: 12059–12065 (1996).PubMedGoogle Scholar
  14. 14.
    Kawata Y, Sakiyama F, Hayashi F, Kyogoku Y: Identification of two essential histidine residues of ribonuclease T2 from Aspergillus oryzae. Eur J Biochem 187: 255–262 (1989).Google Scholar
  15. 15.
    Lee HS, Huang S, Kao T-h: S proteins control rejection of incompatible pollen in Petunia inflata. Nature 367, 560–563 (1994).CrossRefPubMedGoogle Scholar
  16. 16.
    Machida Y, Sato Y, Kozaki I, Seike K: S-genotype of several cultivars of Japanese pear and the question of the parents of ‘Hosui’. (In Japanese.) J Jpn Soc Hort Sci 51 (Suppl 2), 58–59 (1982).Google Scholar
  17. 17.
    Matsushita M, Watanabe M, Yamakawa S, Takayama S, Isogai A, Hinata K: The SLGs corresponding to the same S24-haplotype are perfectly conserved in three different selfincompatible Brassica campestris L.. Genes Genet Syst 71: 255–258 (1996).PubMedGoogle Scholar
  18. 18.
    Matton DP, Maes O, Laublin G, Xike Q, Bertrand C, Morse D, Cappadocia M: Hypervariable domains of self-incompatibility RNases mediate allele-specific pollen recognition. Plant Cell 9: 1757–1766 (1997).PubMedGoogle Scholar
  19. 19.
    McCubbin AG, Chung Y-Y, Kao T-h: 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 (1997).PubMedGoogle Scholar
  20. 20.
    Morgan DR, Soltis DE, Robertson KR: Systematic and evolutionary implications of rbcL sequence variation in Rosaceae. Am J Bot 81: 890–903 (1994)Google Scholar
  21. 21.
    Murfett J, Atherton TL, Beiquan M, Gasser CS, McClure BA: S-RNase expressed in transgenic Nicotiana causes S-allelespecific pollen rejection. Nature 367: 563–566 (1994).CrossRefPubMedGoogle Scholar
  22. 22.
    Norioka N, Ohnishi Y, Norioka S, Ishimizu T, Nakanishi T, Sakiyama F: Nucleotide sequences of cDNAs encoding S2-and S4-RNases (D49527 and D49528 for EMBL) from Japanese pear (Pyrus pyrifolia Nakai) (PGR95–020). Plant Physiol 108: 1343 (1995).Google Scholar
  23. 23.
    Norioka N, Norioka S, Ohnishi Y, Ishimizu T, Oneyama C, Nakanishi T, Sakiyama F: Molecular cloning and nucleotide sequences of cDNAs encoding S-allele specific stylar RNases in a self-incompatible cultivar and its self-compatible mutant of Japanese pear, Pyrus pyrifolia Nakai. J Biochem 120: 335–345 (1996).PubMedGoogle Scholar
  24. 24.
    Rich A, Nordheim A, Wang A H-j: The chemistry and biology of left-handed Z-DNA. Annu Rev Biochem 53: 791–846 (1984).PubMedGoogle Scholar
  25. 25.
    Richman AD, Broothaerts W, Kohn JR: Self-incompatibility RNases from three plant families: homology or convergence? Am J Bot 84: 912–917 (1997).Google Scholar
  26. 26.
    Saba-El-Leil MK, Rivard S, Morse D, Cappadocia M: The S11 and S13 self incompatibility alleles in Solanum chacoense Bit. are remarkably similar. Plant Mol Biol 24: 571–583 (1994).CrossRefPubMedGoogle Scholar
  27. 27.
    Saitou N, Nei M: The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425 (1987).PubMedGoogle Scholar
  28. 28.
    Sassa H, Hirano H, Ikehashi H: Identification and characterization of stylar glycoproteins associated with selfincompatibility genes of Japanese pear, Pyrus serotina Rehd. Mol Gen Genet 241: 17–25 (1993).CrossRefPubMedGoogle Scholar
  29. 29.
    Sassa H, Nishio T, Kowyama Y, Hirano H, Koba T, Ikehashi H: Self-incompatibility (S) alleles of the Rosaceae encode members of a distinct class of the T2/S ribonuclease superfamily. Mol Gen Genet 250: 547–557 (1996).PubMedGoogle Scholar
  30. 30.
    Sassa H, Hirano H: Nucleotide sequence of a cDNA encoding S5-RNase (Accession No. D88282) from Japanese pear (Pyrus serotina) (PGR97–007). Plant Physiol 113: 306 (1997).Google Scholar
  31. 31.
    Sato Y: Breeding of self-compatible Japanese pear. In: Hayashi T et al. (eds) Techniques on Gene Diagnosis and Breeding in Fruit Trees, pp. 241–247. FTRS/Japan, Tokyo (1993)Google Scholar
  32. 32.
    Shimura I, Ito Y, Seike K: Intergeneric hybrid between Japanese pear and quince. (In Japanese, English abstract). J Jpn Soc Hort Sci 52: 243–249 (1983).Google Scholar
  33. 33.
    Tao R, Yamane H, Sassa H, Mori H, Gradziel TM, Dandekar AM, Sugiura A: Identification of stylar RNases associated with gametophytic self-incompatibility in almond (Prunus dulicis). Plant Cell Physiol 38: 304–311 (1997).PubMedGoogle Scholar
  34. 34.
    Terami H, Torikata H, Shimazu Y: Analysis of the sterilityfactors existing in varieties of the Japanese pear (Pyrus serotina Rehd. var. culta Rehd.). (In Japanese, English abstract). Stud Hort Inst Kyoto Imp Univ 3: 267–271 (1946).Google Scholar
  35. 35.
    Tomimoto Y, Nakazaki T, Ikehashi H, Ueno H, Hayashi R: Analysis of self incompatibility-related riblnucleases (SRNases) in two species of pears, Pyrus communis and P. ussuriensis. Scient Hort 66: 159–167 (1997).Google Scholar
  36. 36.
    Tsai DS, Lee HS, Post LC, Kreiling KM, Kao T-h: Sequence of an S-protein of Lycopersicon peruvianum and comparison with other solanaceous S-proteins. Sex Plant Reprod 5: 256–263 (1992).CrossRefGoogle Scholar
  37. 37.
    von Heijne G: A new method for predicting signal sequence cleavage site. Nucl Acids Res 14: 4683–4690 (1986).PubMedGoogle Scholar
  38. 38.
    Walker EA, Ride JP, Kurup S, Franklin-Tong VE, Lawrence MJ, Franklin FCH: 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 (1996).PubMedGoogle Scholar
  39. 39.
    Watson MEE: Compilation of published signal sequences. Nucl Acids Res 12: 5145–5164 (1984).PubMedGoogle Scholar
  40. 40.
    Westwood MN, Lombard, PB, Bjornstad HO: Pear on ‘Winter Banana’ interstem with M. 26 apple rootstock as a compatible combination. HortScience 24: 765–767 (1989).Google Scholar
  41. 41.
    Xue Y, Carpenter R, Dickinson HG, Coen ES: Origin of allelic diversity in antirrhinum S locus RNases. Plant Cell 8: 805–814 (1996).PubMedGoogle Scholar
  42. 42.
    Zurek DM, Mou B, Beecher B, McClure B: Exchanging sequence domains between S-RNases from Nicotiana alata disrupts pollen recognition. Plant J 11: 797–808 (1997).PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 1998

Authors and Affiliations

  • Takeshi Ishimizu
    • 1
  • Toyohide Shinkawa
    • 1
  • Fumio Sakiyama
    • 1
  • Shigemi Norioka
    • 1
  1. 1.Division of Protein Chemistry, Institute for Protein ResearchOsaka UniversitySuita, OsakaJapan

Personalised recommendations