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Identification of a non-S RNase, a possible ancestral form of S-RNases, in Prunus

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Abstract

This study identifies and characterizes a basic non-S RNase in the styles with stigmas of sweet cherry ( Prunus avium L.), a member of the Rosaceae subfamily Amygdaloideae, which has an RNase-based gametophytic self-incompatibility system. Internal sequences of putative non-S RNases (RNase PA1 and PA2) were determined, and a cDNA for PA1 was obtained. The deduced amino acid sequence of PA1 contained two conserved sequence motifs essential for T2/S-type RNase activity. PA1 shows 20–30% sequence identity to S-RNases of Rosaceae, Solanaceae and Scrophulariaceae, and non-S RNases of higher plants. Transcription of the PA1 gene was specific to the styles with stigmas, and the gene was not expressed in other tissues. Although PA1 resembles RNase X2, a non-S RNase from Petunia inflata, the placement of PA1 and RNase X2 in the phylogenetic tree was quite different. Placement of PA1 was also distinct from that of rosaceous S-RNases, while RNase X2 was incorporated in the clade of S-RNases from the Solanaceae. The sole intron in the PA1 gene is located at a position equivalent to that of the second intron of amygdaloid S-RNase genes, and that of the only intron in most other S-RNase genes. Genomic Southern analysis revealed the presence of sequences homologous to PA1 in all of the other four Prunus species tested, suggesting that PA1 has an important physiological function. The significance of the discovery of PA1 is discussed in terms of the origin and evolution of S-RNases and self-incompatibility in Rosaceae.

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References

  • Ai Y, Singh A, Coleman CE, Ioerger TR, Kheyr-Pour A, Kao T-H (1990) Self-incompatibility in Petunia inflata: isolation and characterization of cDNAs encoding three S-allele-associated proteins. Sex Plant Reprod 3:130–138

    Google Scholar 

  • Bariola PA, Green PJ (1997) Plant ribonucleases. In: D'Alessio G, Riordan JF (eds) Ribonucleases: structures and functions. Academic Press, New York, pp 163–190

    Google Scholar 

  • Bariola PA, Howard CJ, Taylor CB, Verburg MT, Haglan VD, Green PJ (1994) The Arabidopsis ribonuclease gene RNS1 is tightly controlled in response to phosphate limitation. Plant J 6:673–685

    CAS  PubMed  Google Scholar 

  • Bošković R, Tobutt KR (1996) Correlation of stylar ribonuclease zymograms with incompatibility alleles in sweet cherry. Euphytica 90:245–250

    Google Scholar 

  • Bošković R, Russell K, Tobutt KR (1997) Inheritance of stylar ribonucleases in cherry progenies, and reassignment of incompatibility alleles to two incompatibility groups. Euphytica 95:221–228

    Article  Google Scholar 

  • Broothaerts W, Janssens GA, Proost P, Broekaert WF (1995) cDNA cloning and molecular analysis of two self-incompatibility alleles from apple. Plant Mol Biol 27:499–511

    CAS  PubMed  Google Scholar 

  • Burgos L, Perez-Tornero O, Ballester J, Olmos E (1998) Detection and inheritance of stylar ribonucleases associated with incompatibility alleles in apricot. Sex Plant Reprod 11:153–158

    CAS  Google Scholar 

  • Certal AC, Almeida, RB, Bošković R, Oliveira MM, Feijó JA (2002) Structural and molecular analyses of self-incompatibility in almond ( Prunus dulcis). Sex Plant Reprod 15:13–20

    CAS  Google Scholar 

  • Dodds PN, Clark AE, Newbigin E (1996) Molecular characterization of an S-like RNase of Nicotiana alata that is induced by phosphate starvation. Plant Mol Biol 31:227–238

    CAS  PubMed  Google Scholar 

  • Galiana E, Bonnet P, Conrod S, Keller H, Panabieres F, Ponchet M, Poupet A, Ricci P (1997) RNase activity prevents the growth of a fungal pathogen in tobacco leaves and increases upon induction of systemic acquired resistance with elicitin. Plant Physiol 115:1557–1567

    Article  CAS  Google Scholar 

  • Golz JF, Clarke AE, Newbigin E, Anderson M (1998) A relic S-RNase is expressed in the styles of self-compatible Nicotiana sylvestris. Plant J 16:591–599

    Article  CAS  Google Scholar 

  • Hauck NR, Iezzoni AF, Yamane H, Tao R (2001) Revisiting the S -allele nomenclature in sweet cherry ( Prunus avium L) using RFLP profiles. J Amer Soc Hort Sci 127:654–660

    Google Scholar 

  • Hauck NR, Yamane H, Tao R, Iezzoni AF (2002) Self-compatibility and incompatibility in tetraploid sour cherry ( Prunus cerasus L.). Sex Plant Reprod 15:39–46

    CAS  Google Scholar 

  • Hellman U, Wernstedt C, Gonez J, Heldin CH (1995) Improvement of "in-gel" digestion procedure for the micropreparation of internal protein fragments for amino acid sequencing. Anal Biochem 224:451–455

    Article  CAS  Google Scholar 

  • Hugot K, Ponchet M, Marais A, Ricci P, Galiana E (2002) A tobacco S-like RNase inhibits hyphal elongation of plant pathogens. Mol Plant-Microbe Interact 15:243–250

    CAS  Google Scholar 

  • Ide H, Kimura M, Arai M, Funatsu G (1991) The complete amino acid sequence of ribonuclease from the seeds of bitter gourd. FEBS Lett 284:161–164

    Article  CAS  Google Scholar 

  • Igic B, Kohn JR (2001) Evolutionary relationships among self-incompatibility RNases. Proc Natl Acad Sci USA 98:13167–13171

    Article  CAS  PubMed  Google Scholar 

  • Ishimizu T, Shinkawa T, Sakiyama F, Norioka S (1998) Primary structural features of rosaceous S-RNases associated with gametophytic self-incompatibility. Plant Mol Biol 37:931–941

    CAS  PubMed  Google Scholar 

  • Kariu T, Sano K, Shimokawa H, Itoh R, Yamasaki N, Kimura M (1998) Isolation and characterization of a wound-inducible ribonuclease from Nicotiana glutinosa leaves. Biosci Biotechnol Biochem 62:1144–1151

    CAS  Google Scholar 

  • Kaufmann H, Salamini F, Thompson RD (1991) Sequence variability and gene structure at the self-incompatibility locus of Solanum tuberosum. Mol Gen Genet 226:457–466

    CAS  Google Scholar 

  • Köck M, Löffler A, Abel S, Glund K (1995) cDNA structure and regulatory properties of a family of starvation-induced ribonucleases from tomato. Plant Mol Biol 27:477–485

    PubMed  Google Scholar 

  • Kuroda S, Norioka S, Mitta M, Kato I, Sakiyama F (1994) Primary structure of a novel stylar RNase unassociated with self-incompatibility in tobacco plant, Nicotiana alata. J Protein Chem 13:438–439

    Google Scholar 

  • LeBrasseur ND, MacIntosh GC, Perez-Amador MA, Saitoh M, Green PJ (2002) Local and systemic wound-induction of RNase and nuclease activities in Arabidopsis: RNS1 as a marker for a JA-independent systemic signaling pathway. Plant J 29:393–403

    Article  CAS  Google Scholar 

  • Lee H-S, Singh A, Kao T-H (1992) RNase X2, a pistil-specific ribonuclease from Petunia inflata, shares sequence similarity with Solanaceae S proteins. Plant Mol Biol 20:1131–1141

    CAS  PubMed  Google Scholar 

  • Lee H-S, Huang S, Kao T-H (1994) S proteins control rejection of incompatible pollen in Petunia inflate. Nature 367:560–563

    CAS  PubMed  Google Scholar 

  • Lermann K, Hause B, Altmann D, Kock M (2001) Tomato ribonuclease LX with the functional endoplasmic reticulum retention motif HDEF is expressed during programmed cell death processes, including xylem differentiation, germination, and senescence. Plant Physiol 127:436–449

    Article  Google Scholar 

  • Lers A, Khalchitski A, Lomaniec E, Burd S, Green PJ (1998) Senescence-induced RNases in tomato. Plant Mol Biol 36:439–449

    Article  CAS  Google Scholar 

  • Loffler A, Glund K, Irie M (1993) Amino acid sequence of an intracellular, phosphate-starvation-induced ribonuclease from cultured tomato ( Lycopersicon esculentum) cells. Eur J Biochem 214:627–633

    CAS  Google Scholar 

  • Ma R-C, Oliveira MM (2000) The RNase PD2 gene of almond ( Prunus dulcis) represents an evolutionarily distinct class of S-like RNase genes. Mol Gen Genet 263:925–933

    Article  CAS  Google Scholar 

  • Ma R-C, Oliveira MM (2001) Molecular cloning of the self-incompatibility genes S1 and S3 from almond (Prunus dulcis cv. Ferragnes). Sex Plant Reprod 14:163–167

    CAS  Google Scholar 

  • Ma R-C, Oliveira MM (2002) Evolutionary analyses of S-RNase genes from Rosaceae species. Mol Genet Genomics 267:71–78

    CAS  Google Scholar 

  • Matton DP, Mau SL, Okamoto S, Clarke AE, Newbigin E (1995) The S -locus of Nicotiana alata: genomic organization and sequence analysis of two S-RNase alleles. Plant Mol Biol 28:847–858

    CAS  PubMed  Google Scholar 

  • McClure BA, Haring v, Ebert PR, Andeson MA, Simpson RF, Sakiyama F, Clarke AE (1989) Style self-incompatibility gene products of Nicotiana alata are ribonucleases. Nature 342:955–957

    CAS  PubMed  Google Scholar 

  • McCubbin AG, Kao T-H (2000) Molecular recognition and response in pollen and pistil interactions. Ann Rev Cell Dev Biol 16:333–364

    Article  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    CAS  Google Scholar 

  • Murfett J, Atherton TL, Mou B, Gasser CS, McClure BA (1994) S-RNase expressed in transgenic Nicotiana causes S -allele-specific pollen rejection. Nature 367:563–566

    CAS  PubMed  Google Scholar 

  • Murfett J, Strabala TJ, Zurek DM, Mou B, Beecher B, McClure BA. (1996) 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. Plant Cell 8:943–958

    Article  CAS  Google Scholar 

  • Norioka N, Norioka S, Ohnishi Y, Ishimizu T, Oneyama C, Nakanishi T, Sakiyama F (1996) 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

    CAS  PubMed  Google Scholar 

  • Qi X, Luu DT, Yang Q, Maes O, Matton DP, Morse D, Cappadocia M (2001) Genotype-dependent differences in S12-RNase expression lead to sporadic self-compatibility. Plant Mol Biol 45:295–305

    Article  CAS  Google Scholar 

  • Richman AD, Broothaerts W, Kohn JR (1997) Self-incompatibility RNases from three plant families: homology or convergence? Amer J Bot 84:912–917

    CAS  Google Scholar 

  • Royo J, Kowyama Y, Clarke AE (1994) Cloning and nucleotide sequence of two S-RNases from Lycopersicon peruvianum (L.) Mill. Plant Physiol 105:751–752

    Article  CAS  Google Scholar 

  • Sassa H, Hirano H, Ikehashi H (1992) Self-incompatibility-related RNases in styles of Japanese pear ( Pyrus serotina Rehd). Plant Cell Physiol 33:811–814

    CAS  Google Scholar 

  • 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 241:17–25

    CAS  PubMed  Google Scholar 

  • Sassa H, Nishio T, Kowyama Y, Hirano H, Koba T, Ikehashi H (1996) Self-incompatibility ( S) alleles of the Rosaceae encode members of a distinct class of the T2/S ribonucleases superfamily. Mol Gen Genet 250:547–557

    Article  CAS  PubMed  Google Scholar 

  • Sonneveld T, Robbins TP, Bošković R, Tobutt KR (2001) Cloning of six cherry self-incompatibility alleles and development of allele-specific PCR detection. Theor Appl Genet 102:1046–1055

    CAS  Google Scholar 

  • Stockinger EF, Mulinix CA, Long CM, Brettin TS, Iezzoni AF (1996) A linkage map of sweet cherry based on RAPD analysis of a microspore-derived callus culture population. J Hered 87:214–218

    CAS  PubMed  Google Scholar 

  • Swofford DL (2001) PAUP*: Phylogenetic analysis using parsimony (*and other methods) Version 4. Sinauer, Sunderland, Mass.

  • Tamura M, Ushijima K, Sassa H, Hirano H, Tao R, Gradziel TM, Dandekar AM (2000) Identification of self-incompatibility genotypes of almond by allele specific PCR analysis. Theor Appl Genet 101:344–349

    Article  CAS  Google Scholar 

  • Tao R, Yamane H, Sassa H, Mori H, Gradziel TM, Dadekar AM, Sugiura A (1997) Identification of stylar RNases associated with gametophytic self-incompatibility in almond ( Prunus dulcis). Plant Cell Physiol 38:304–311

    CAS  PubMed  Google Scholar 

  • Tao R, Yamane H, Sugiura A (1999a) Cloning and nucleotide sequences of cDNAs encoding S1- and S4-RNases (Accession Nos. AB028153 and AB028154) from sweet cherry ( Prunus avium L.). (PGR99-121). Plant Physiol 120:1207

    Google Scholar 

  • Tao R, Yamane H, Sugiura A (1999b) Cloning of genomic DNA sequences encoding S1, S3, S4, and S6-RNases (Accession Nos. AB03185, AB03186, AB03187 and AB03188) from sweet cherry ( Prunus avium L.). (PGR99-166). Plant Physiol 121:1057

    Article  Google Scholar 

  • Tao R, Yamane H, Sugiura A, Murayama H, Sassa H, Mori H (1999c) Molecular typing of S -alleles through identification, characterization and cDNA cloning for S-RNases in sweet cherry. J Amer Soc Hort Sci 124:224–233

    CAS  Google Scholar 

  • Tao R, Habu T, Namba A, Yamane H, Fuyuhiro Y, Iwamoto K, Sugiura A (2002) Inheritance of S f-RNase in Japanese apricot ( Prunus mume) and its relation to self-incompatibility. Theor Appl Genet 105:222–228.

    Article  Google Scholar 

  • Taylor CB, Bariola PA, Del Cardayre SB, Raines RT, Green PJ (1993) RNS2: a senescence-associated RNase of Arabidopsis that diverged from the S-RNase before speciation. Proc Natl Acad Sci USA 90:5118–5122

    CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    CAS  PubMed  Google Scholar 

  • Ushijima K, Sassa H, Tao R, Yamane H, Dandekar AM, Gradziel TM, Hirano H (1998) Cloning and characterization of cDNAs encoding S-RNases in almond ( Prunus dulcis): primary structural features and sequence diversity of the S-RNases in Rosaceae. Mol Gen Genet 260:261–268

    CAS  PubMed  Google Scholar 

  • Van Nerum I, Certal AC, Oliveira MM, Keulemans J, Broothaerts W (2000) PD1, an S-like RNase from a self-incompatible cultivar of almond. Plant Cell Reports 19:1108–1114

    Article  Google Scholar 

  • Von Heijne G (1986) A new method for predicting signal sequence cleavage site. Nucleic Acids Res 14:4683–3690

    PubMed  Google Scholar 

  • Wiersma PA, Wu Z, Zhou L, Hampson C, Kappel F (2001) Identification of new self-incompatibility alleles in sweet cherry ( Prunus avium L.) and clarification of incompatibility groups by PCR and sequencing analysis. Theor Appl Genet 102:700–708

    Article  CAS  Google Scholar 

  • Xue Y, Carpenter R, Dickinson HG, Coen ES (1996) Origin of allelic diversity in Antirrhinum S locus RNases. Plant Cell 8:805–814

    CAS  PubMed  Google Scholar 

  • Yaegaki H, Shimada T, Moriguchi T, Hayama H, Haji T, Yamaguchi M (2001) Molecular characterization of S-RNase genes and S -genotypes in the Japanese apricot ( Prunus mume Sieb. et Zucc.). Sex Plant Reprod 13:251–257

    Google Scholar 

  • Yamane H, Tao R, Sugiura A (1999) Identification and cDNA cloning for S-RNases in self-incompatible Japanese plum ( Prunus salicina Lindl. cv. Sordum). Plant Biotech 16:389–396

    CAS  Google Scholar 

  • Yamane H, Murayama H, Tao R, Sugiura A (2000) Determining the S -genotypes of several sweet cherry cultivars based on PCR-RFLP analysis. J Hort Sci Biotech 75:562–567

    CAS  Google Scholar 

  • Yamane H, Tao R, Sugiura A, Hauck NR, Iezzoni AF (2001) Identification and characterization of S-RNases in tetraploid sour cherry ( Prunus cerasus). J Amer Soc Hort Sci 126:661–667

    CAS  Google Scholar 

  • Ye Z-H, Droste DL (1996) Isolation and characterization of cDNAs encoding xylogenesis-associated and wounding-induced ribonucleases in Zinnia elegans. Plant Mol Biol 30:697–709

    CAS  Google Scholar 

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Acknowledgements

This work was supported in part by Grants in Aid 13460014 for scientific research (B) to R. Tao, and 14760017 for Young Scientists (B) to H. Yamane, from the Japan Society for the Promotion of Science. We thank A. F. Iezzoni and J. Soejima for providing the plant material. We gratefully acknowledge H. Sassa and K. Ushijima for helpful discussion and J. R. Kohn for critical reviews

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  1. Laboratory of Pomology, Graduate School of Agriculture, Kyoto University, 606-8502, Kyoto, Japan

    H. Yamane, R. Tao & A. Sugiura

  2. Graduate School of Bioagricultural Science, Nagoya University, 464-8601, Nagoya, Japan

    H. Mori

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  1. H. Yamane
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  2. R. Tao
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  3. H. Mori
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  4. A. Sugiura
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Correspondence to R. Tao.

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Communicated by R. Hagemann

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Yamane, H., Tao, R., Mori, H. et al. Identification of a non-S RNase, a possible ancestral form of S-RNases, in Prunus . Mol Gen Genomics 269, 90–100 (2003). https://doi.org/10.1007/s00438-003-0815-5

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