Molecular and General Genetics MGG

, Volume 250, Issue 5, pp 547–557 | Cite as

Self-incompatibility (S) alleles of the rosaceae encode members of a distinct class of the T2/S ribonuclease superfamily

  • Hidenori Sassa
  • Takeshi Nishio
  • Yasuo Kowyama
  • Hisashi Hirano
  • Takato Koba
  • Hiroshi Ikehashi
Original Paper

Abstract

Stylar riboncleases (RNases) are associated with gametophytic self-incompatibility in two plant families, the Solanaceae and the Rosaceae. The self-incompatibility-associated RNases (S-RNases) of both the Solanaceae and the Rosaceae were recently reported to belong to the T2 RNase gene family, based on the presence of two well-conserved sequence motifs. Here, the cloning and characterization of S-RNase genes from two species of Rosaceae, apple (Malus × domestica) and Japanese pear (Pyrus serotina) is described and these sequences are compared with those of other T2-type RNases. The S-RNases of apple specifically accumulated in styles following maturation of the flower bud. Two cDNA clones for S-RNases from apple, and PCR clones encoding a further two apple S-RNases as well as two Japanese pear S-RNases were isolated and sequenced. The deduced amino acid sequences of the rosaceous S-RNases contained two conserved regions characteristic of the T2/S-type RNases. The sequences showed a high degree of diversity, with similarities ranging from 60.4% to 69.2%. Interestingly, some interspecific sequence similarities were higher than those within a species, possibly indicating that diversification of S-RNase alleles predated speciation in the Rosaceae. A phylogenetic tree of members of the T2/S-RNase superfamily in plants was obtained. The rosaceous S-RNases formed a new lineage in the tree that was distinct from those of the solanaceous S-RNases and the S-like RNases. The findings suggested that self-incompatibility mechanisms in Rosaceae and Solanaceae are similar but arose independently in the course of evolution.

Key words

Self-incompatibility Rosaceae Ribonuclease Style Gene genealogy 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ai Y, Singh A, Coleman CE, Ioerger TR, Kheyr-Pour A, Kao T-H (1990) Self-incompatibility inPetunia inflata: isolation and characterization of cDNAs encoding three S-allele-associated proteins. Sex Plant Reprod 3: 130–138Google Scholar
  2. Anderson MA, Cornish EC, Mau S-L, Williams EG, Hoggart R, Atkinson A, Bönig I, Grego B, Simpson R, Roche PJ, Haley JD, Penschow JD, Niall HD, Tregear GW, Coghlan JP, Crawford RJ, Clarke AE (1986) Cloning of cDNA for a stylar glycoprotein associated with expression of self-incompatibility inNicotiana alata. Nature 321: 38–44Google Scholar
  3. Anderson MA, McFadden GI, Bernatzky R, Atkinson A, Orpin T, Dedman H, Tregear G, Fernley R, Clarke AE (1989) Sequence variability of three alleles of the self-incompatibility gene ofNicotiana alata. Plant Cell 1:483–491Google Scholar
  4. Bariola PA, Howard CJ, Taylor CB, Verburg MT, Jaglan VD, Green PJ (1994) TheArabidopsis thaliana ribonuclease geneRNS1 is tightly controlled in response to phosphate limitation. Plant J 6:673–685Google Scholar
  5. Breathnach R, Chambon P (1981) Organization and expression of eucaryotic split genes conding for proteins. Ann Rev Biochem 50:349–383Google Scholar
  6. Broothaerts W, Janssens GA, Proost P, Broekaert WF (1995) cDNA cloning and molecular analysis of two self-incompatibility alleles from apple. Plant Mol Biol 27:499–511Google Scholar
  7. Chase MW, Soltis DE, Olmstead RG, Morgan D, Les DH, Mishler BD, Duvall MR, Price RA, Hills HG, Qiu Y-L, Kron KA, Rettig JH, Conti E, Palmer JD, Manhart JR, Systma KJ, Michaels HJ, Kress WJ, Karol KG, Clake WD, Hedren M, Gaul BS, Jansen RK, Kim K-J, Wimpee CF, Smith JF, Furnier GR, Strauss SH, Xiang Q-Y, Plunkett GM, Soltis PS, Swensen SM, Williams SE, Gadek PA, Quinn CJ, Eguiarte LE, Golenberg E, Learn Jr. GH, Graham SW, Barrett SCH, Dayanandan S, Albert VA (1993) Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid generbcL. Ann Missouri Bot Gard 80:528–580Google Scholar
  8. Clark KR, Okuley JJ, Collins PD, Sims TL (1990) Sequence variability and developmental expression ofS-alleles in self-incompatible and pseudo-self-compatible Petunia. Plant Cell 2:815–826Google Scholar
  9. Dellaporta SL, Wood J, Hicks JB (1983) A plant DNA minipreparation: version II. Plant Mol Bio Rep 1:19–21Google Scholar
  10. De Nettancourt D (1977) Incompatibility in angiosperms. Springer-Verlag BerlinGoogle Scholar
  11. De Vries S, Hoge H, Bisseling T (1988) Isolation of total and polysomal RNA from plant tissues. In: Glevin SB, Schilperoot RA, Verma DPS (eds) Plant Molecular Biology Manual. Kluwer Academic Publishers, Dordrecht, pp 1–13Google Scholar
  12. 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 fromPapaver rhoeas L. Proc Natl Acad Sci USA 91:2265–2269Google Scholar
  13. Hirano H, Watanabe T (1990) Microsequencing of proteins electroblotted onto immobilizing matrices from polyacrylamide gel electrophoresis: Application to an insoluble protein. Electrophoresis 11:573–580Google Scholar
  14. Horiuchi H, Yanai K, Takagi M, Yano K, Wakabayashi E, Sanda A, Mine S, Ohgi K, Irie M (1988) Primary structure of a base nonspecific ribonuclease fromRhizopus niveus. J Biochem 103:408–418Google Scholar
  15. Huang S, Lee H-S, Karunanandaa B, Kao T-H (1994) Ribonuclease activity ofPetunia inflata S proteins is essentianl for rejection of self-pollen. Plant Cell 6:1021–1028Google Scholar
  16. Ide H, Kimura M, Arai M, Funatsu G (1991) The complete amino acid sequence of ribonuclease from the seeds of bitter gourd (Momordica charantia). FEBS Lett 284:161–164Google Scholar
  17. Inada Y, Watanabe H, Ohgi K, Irie M (1991) Isolation, characterization, and primary structure of a base non-specific and adenylic acid preferential ribonuclease with higher specific activity fromTrichoderma viride. J Biochem 110:896–904Google Scholar
  18. Ioerger TR, Clark AG, Kao T-H (1990) Polymorphism at the self-incompatibility locus in Solanaceae predates speciation. Proc Natl Acad Sci USA 87:9732–9735Google Scholar
  19. Ioerger TR, Gohlke JR, Xu B, Kao T-H (1991) Primary structural features of the self-incompatibility protein in solanaceae. Sex Plant Reprod 4:81–87Google Scholar
  20. Jost W, Bak H, Glund K, Terpstra P, Beintema JJ (1991) Amino acid sequence of an extracellular, phosphate-starvation-induced ribonuclease from cultured tomato (Lycopersicon esculentum) cells. Eur J Biochem 198:1–6Google Scholar
  21. Kao T-H, Huang S (1994) Gametophytic self-incompatibility: a mechanism for self/nonself discrimination during sexual reproduction. Plant Physiol 105:461–466Google Scholar
  22. Kaufmann H, Salamini F, Thompson RD (1991) Sequence variability and gene structure at the self-incompatibility locus ofSolanum tuberosum. Mol Gen Genet 226:457–466Google Scholar
  23. Kawata Y, Sakiyama F, Tamaoki H (1988) Amino-acid sequence of ribonuclease T2 fromAspergillus oryzae. Eur J Biochem 176:683–697Google Scholar
  24. Kheyr-Pour A, Bintrim SB, Ioerger TR, Remy R, Hammond SA, Kao T-H (1990) Sequence diversity of pistil S-proteins associated with gametophytic self-incompatibility inNicotiana alata. Sex Plant Reprod 3:88–97Google Scholar
  25. Kowyama Y, Shimano N, Kawase T (1980) Genetic analysis of incompatibility in the diploidIpomoea species closely related to the sweet potato. Theor Appl Genet 58:149–155Google Scholar
  26. Kowyama Y, Takahasi H, Muraoka T, Tani T, Hara K, Shiotani I (1994) Number, frequency and dominance relationships ofS-alleles in diploidIpomoea trifida. Heredity 73:275–283Google Scholar
  27. Lee H-S, Singh A, Kao T-H (1992) RNase X2, a pistil-specific ribonuclease fromPetunia inflata, shares sequence similarity with solanaceous S proteins. Plant Mol Biol 20:1131–1141Google Scholar
  28. Lee H-S, Huang S, Kao T-H (1994) S proteins control rejection of incompatible pollen inPetunia inflata. Nature 367:560–563Google Scholar
  29. Li X, Nield J, Hayman D, Langridge P (1994) Cloning a putative self-incompatibility gene from the pollen of the grassPhalaris coerulescens. Plant Cell 6:1923–1932Google Scholar
  30. Lipman DJ, Pearson WR (1985) Rapid and sensitive protein similarity searches. Science 227:1435–1441Google Scholar
  31. Löffler A, Glund K, Irie M (1993) Amino acid sequence of an intracellular, phosphate-starvation-induced ribonuclease from cultured tomato (Lycopersicon esculentum). Eur J Biochem 214:627–633Google Scholar
  32. Matton DP, Nass N, Clarke AE, Newbigin E (1994) Self-incompatibility: how plants avoid illegitimate offspring. Proc Natl Acad Sci USA 91:1992–1997Google Scholar
  33. McClure BA, Haring V, Ebert PR, Anderson MA, Simpson RJ, Sakiyama F, Clarke AE (1989) Style self-incompatibility gene products ofNicotiana alata are ribonucleases. Nature 342:955–957Google Scholar
  34. Murfett J, Atherton TL, Mou B, Gasser CS, McClure BA (1994)S-RNase expressed in transgenicNicotiana causesS-allele-specific pollen rejection. Nature 367:563–566Google Scholar
  35. Newbigin E, Anderson MA, Clarke AE (1993) Gametophytic self-incompatibility systems. Plant Cell 5:1315–1324Google Scholar
  36. Royo J, Kowyama Y, Clarke AE (1994a) Cloning and nucleotide sequences of two S-RNases fromLycopersicon peruvianum. Plant Physiol 105:751–752Google Scholar
  37. Royo J, Kuntz C, Kowyama Y, Anderson M, Clarke AE (1994b) Loss of a histidine residue at the active site ofS-locus ribonuc-lease is associated with self-compatibility inLycopersicon peruvianum. Proc Natl Acad Sci USA 91:6511–6514Google Scholar
  38. Rubin RW, Warren RW (1977) Quantitation of microgram amounts of protein in SDS-mercaptoethanol-Tris electrophoresis sample buffer. Anal Biochem 83:773–777Google Scholar
  39. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New YorkGoogle Scholar
  40. Sassa H, Hirano H, Ikehashi H (1992) Self-incompatibility-related RNases in styles of Japanese pear (Pyrus serotina Rehd.). Plant Cell Physiol 33:811–814Google Scholar
  41. Sassa H, Hirano H, Ikehashi H (1993) Identification and characterization of stylar glycoproteins associated with self-incompatibility genes of Japanese pear,Pyrus serotina Rehd. Mol Gen Genet 241:17–25Google Scholar
  42. Sassa H, Mase N, Hirano H, Ikehashi H (1994) Identification of self-incompatibility-related glycoproteins in styles of apple (Malus × domestica). Theor Appl Genet 89:201–205Google Scholar
  43. Singh A, Ai Y, Kao T-H (1991) Characterization of ribonuclease activity of three S-allele-associated proteins ofPetunia inflata. Plant Physiol 96:61–68Google Scholar
  44. Taylor CB, Bariola PA, del Cardayre SB, Raines RT, Green PJ (1993) RNS2: a senescence-associated RNase ofArabidopsis that diverged from the S-RNases before speciation. Proc Natl Acad Sci USA 90:5118–5122Google Scholar
  45. Tsai D-S, Lee H-S, Post LC, Kreiling KM, Kao T-H (1992) Sequence of an S-protein ofLycopersicon peruvianum and comparison with other solanaceous S-proteins. Sex Plant Reprod 5:256–263Google Scholar
  46. Watanabe H, Naitoh A, Suyama Y, Inokuchi N, Shimada H, Koyama T, Ohgi K, Irie M (1990) Primary structure of a base non-specific and adenylic acid preferential ribunuclease fromAspergillus saitoi. J Biochem 108:303–310Google Scholar
  47. Whitehouse HLK (1950) Multiple-allelomorph incompatibility of pollen and style in the evolution of the angiosperms. Ann Bot New Ser 54:198–216Google Scholar
  48. Xu B, Mu J, Nevins DL, Grun P, Kao T-H (1990) Cloning and sequencing of cDNAs encoding two self-incompatibility associated proteins inSolanum chacoense. Mol Gen Genet 224:341–346Google Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • Hidenori Sassa
    • 1
  • Takeshi Nishio
    • 2
  • Yasuo Kowyama
    • 3
  • Hisashi Hirano
    • 4
  • Takato Koba
    • 1
  • Hiroshi Ikehashi
    • 1
  1. 1.Faculty of HorticultureChiba UniversityMatsudo, ChibaJapan
  2. 2.Institute of Radiation Breeding, NIAR, MAFFIbarakiJapan
  3. 3.Faculty of BioresourcesMie UniversityTsu, MieJapan
  4. 4.Department of Molecular BiologyNational Institute of Agrobiological ResourcesIbarakiJapan
  5. 5.Faculty of AgricultureKyoto UniversityKyotoJapan
  6. 6.Kihara Institute for Biological ResearchYokohama City UniversityYokohamaJapan

Personalised recommendations