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The rice pathogen-related protein 10 (JIOsPR10) is induced by abiotic and biotic stresses and exhibits ribonuclease activity

  • Biotic and Abiotic Stress
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An Erratum to this article was published on 03 September 2008

Abstract

We previously reported that rice blast fungus or jasmonic acid induced the expression of rice pathogenesis-related class 10 (JIOsPR10) proteins (Kim et al. 2003, 2004). However, no further studies have been carried out to examine the expression, localization, and enzymatic activity of this protein in either developmental tissues or in tissues under abiotic stress conditions. In this study, rice JIOsPR10 was examined by Western blot analysis, immunolocalization, and biochemical assays. Western blots revealed that the JIOsPR10 protein was expressed in developmental tissues, including in flower and root. The protein was also expressed under abiotic stresses, such as occurs during senescence and wounding. Using immunohistochemical techniques, we determined that expression of JIOsPR10 was localized to the palea of flower, in the exodermis, and inner part of the endodermis of the root. In senescencing tissues of leaf and coleoptiles, its expression was localized in vascular bundles. The RNase activity using JIOsPR10 recombinant protein was determined and abolished after treatment with DTT in a native in-gel assay. To test this, we created JIOsPR10 mutant proteins containing serine substitutions of amino acids C81S, C83S, or both and examined their RNase activities. The activity of the C83S mutant was decreased in the agarose gel assay compared to the wild type. Taken together, we hypothesize that the JIOsPR10 protein possesses RNase activity that is sensitive to DTT, suggesting the importance of the disulfide bonding between cysteine residues and that it might play a role in constitutive self-defense mechanisms in plants against biotic and abiotic stresses.

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References

  • Agrawal GK, Rakwal R, Yonekura M, Kubo A, Saji H (2002) Proteome analysis of differentially displayed proteins as a tool for investigating ozone stress in rice (Oryza sativa L.) seedlings. Proteomics 2:947–959

    Article  PubMed  CAS  Google Scholar 

  • Ansaldi M, Lepelletier M, Mejean V (1996) Site-specific mutagenesis by using an accurate recombinant polymerase chin reaction method. Anal Biochem 23:110–111

    Article  Google Scholar 

  • Bantignies B, Seguin J, Muzac I, Dedaldechamp F, Gulick P, Ibrahim R (2000) Direct evidence for ribonucleolytic activity of a PR-10-like protein from white lupin roots. Plant Mol Biol 42:871–881

    Article  PubMed  CAS  Google Scholar 

  • Barral DHP, Clark JA (1991) Proteins arising during the late stages of embryogenesis in Pisum sativum. Planta 184:14–23

    Google Scholar 

  • Breda C, Sallaud C, El-Turk J, Buffard D, de Kozak I, Esnault R, Kondorosi A (1996) Defense reaction in Medicago sativa: a gene encoding a class PR-10 protein is expressed in vascular bundles. Mol Plant Microbe Interact 9:713–719

    PubMed  CAS  Google Scholar 

  • Breiteneder H, Pettenburger K, Bito A, Valenta R, Kraft D, Rumpold H, Scheiner O, Breitenbach M (1989) The gene coding for the major birch pollen allergen Betv1, is highly homologous to a pea disease resistance response gene. EMBO J 8:1935–1938

    PubMed  CAS  Google Scholar 

  • Bruinsma J (1963) The quantitative analysis of chlorophylls a and b in plant extracts. Photochem Photobiol 2:241–249

    Article  CAS  Google Scholar 

  • Bufe A, Spangfort MD, Kahlert H, Schlaak M, Becker WM (1996) The major birch pollen allergen, bet V1, shows ribonuclease activity. Planta 199:413–415

    Article  PubMed  CAS  Google Scholar 

  • Chen Z, Ling J, Gallie DR (2004) RNase activity requires formation of disulfide bonds and is regulated by the redox state. Plant Mol Biol 55:83–96

    Article  PubMed  CAS  Google Scholar 

  • Constabel CP, Brisson N (1995) Stigma- and vascular-specific expression of the PR10a gene of potato: a novel pattern of expression of a pathogenesis-related gene. Mol Plant Microbe Interact 8:104–113

    CAS  Google Scholar 

  • Crowell DN, John ME, Russell D, Amasino RM (1992) Characterization of a stress-induced, developmentally regulated gene family from soybean. Plant Mol Biol 18:459–466

    Article  PubMed  CAS  Google Scholar 

  • Dixon RA, Lamb CJ (1990) Molecular communication in interactions between plants and microbial pathogens. Annu Rev Plant Physiol Plant Mol Biol 41:339–367

    Article  CAS  Google Scholar 

  • Dubos C, Plomion C (2001) Drought differentially affects expression of a PR-10 protein in needles of maritime pine (Pinus pinaster Ait.) seedlings. J Exp Bot 52:1143–1144

    Article  PubMed  CAS  Google Scholar 

  • Hajduch M, Rakwal R, Agrawal GK, Yonekura M, Pretova A (2001) High-resolution two-dimensional electrophoresis separation of proteins from metal-stressed rice (Oryza sativa L.) leaves: drastic reductions/fragmentation of ribulose-1,5-bisphosphate carboxylase/oxygenase and induction of stress-related proteins. Electrophoresis 22:2824–2831

    Article  PubMed  CAS  Google Scholar 

  • Hashimoto M, Kisseleva L, Sawa S, Furukawa T, Komatsu S, Koshiba T (2004) A novel rice PR10 protein, RSJIOsPR10, specifically induced in roots by biotic and abiotic stresses, possibly via the jasmonic acid signaling pathway. Plant Cell Physiol 45:550–559

    Article  PubMed  CAS  Google Scholar 

  • Huang JC, Chang FC, Wang CS (1997) Characterization of a lily tapetal transcript that shares sequence similarity with a class of intracellular pathogenesis-related (IPR) proteins. Plant Mol Biol 34:681–686

    Article  PubMed  CAS  Google Scholar 

  • Jwa N-S, Agrawal GK, Rakwal R, Park CH, Agrawal VP (2001) Molecular cloning and characterization of a novel Jasmonate inducible pathogenesis-related class 10 protein gene, JIOsPR10, from rice (Oryza sativa L.) seedling leaves. Biochem Biophys Res Commun 286:973–983

    Article  PubMed  CAS  Google Scholar 

  • Kav NNV, Srivastava S, Goonewardene L, Blade SF (2004) Proteome-level changes in the roots of Pisum sativum L. in response to salinity. Ann Appl Biol 145:217–230

    Article  CAS  Google Scholar 

  • Kawai M, Uchimiya H (2000) Coleoptiles senescence in rice (Oryza sativa L). Ann Bot 86:405–414

    Article  CAS  Google Scholar 

  • Kim ST, Cho KS, Jang YS, Kang KY (2001) Two-dimensional electrophoretic analysis of rice proteins by polyethylene glycol fractionation for protein arrays. Electrophoresis 22:2103–2109

    Article  PubMed  CAS  Google Scholar 

  • Kim ST, Cho KS, Yu S, Kim SG, Hong JC, Han C, Bae DW, Nam MH, Kang KY (2003) Proteomic analysis of differentially expressed proteins induced by rice blast fungus and elicitor in suspension-cultured rice cells. Proteomics 3:2368–2378

    Article  PubMed  CAS  Google Scholar 

  • Kim ST, Kim SG, Hwang DH, Kang SY, Kim HJ, Lee BH, Lee JJ, Kang KY (2004) Proteomic analysis of pathogen-responsive proteins from rice leaves induced by rice blast fungus, Magnaporthe grisea. Proteomics 4:3569–3578

    Article  PubMed  CAS  Google Scholar 

  • Lee MW, Qi M, Yang Y (2001) A novel jasmonic acid-inducible rice myb gene associates with fungal infection and host cell death. Mol Plant Microbe Interact 14:527–535

    Article  PubMed  CAS  Google Scholar 

  • Lehmann K, Hause B, Altmann D, Köck 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  PubMed  CAS  Google Scholar 

  • Lo SC, Hipskind JD, Nicholson RL (1999) cDNA cloning of a sorghum pathogenesis-related protein (PR-10) and differential expression of defense-related genes following inoculation with Cochliobolus heterostrophus or Colletotrichum sublineolum. Mol Plant Microbe Interact 12:479–489

    Article  PubMed  CAS  Google Scholar 

  • McGee JD, Hamer JE, Hodges TK (2001) Characterization of a PR-10 pathogenesis-related gene family induced in rice during infection with Magnaporthe grisea. Mol Plant Microbe Interact 14:877–886

    Article  PubMed  CAS  Google Scholar 

  • Midoh N, Iwata M (1996) Cloning and characterization of a probenazole-inducible gene for an intracellular pathogenesis-related protein in rice. Plant Cell Physiol 37:9–18

    PubMed  CAS  Google Scholar 

  • Moiseyev GP, Fedoreyeva LI, Zhuravlev YN, Yasnetslaya E, Jekel PA, Beintema JJ (1997) Primary structures of two ribonucleases from ginseng calluses new members of the PR-10 family of intracellular pathogenesis-related plant proteins. FEBS Lett 407:207–210

    Article  PubMed  CAS  Google Scholar 

  • Moons A, Prinsen E, Bauw G, Van Montagu M (1997) Antagonistic effects of abscisic acid and jasmonates on salt stress-inducible transcripts in rice roots. Plant Cell 9:2243–2259

    Article  PubMed  CAS  Google Scholar 

  • Mylona P, Moerman M, Yang W-C, Gloudemans T, Van De Kerckhove J, van Kammen A, Bisseling T, Franssen HJ (1994) The root epidermis-specific pea gene RH2 is homologous to a pathogenesis-related gene. Plant Mol Biol 26:39–50

    Article  PubMed  CAS  Google Scholar 

  • Muramoto Y, Watanabe A, Nakamura T, Takabe T (1999) Enhanced expression of a nuclease gene in leaves of barley plants under salt stress. Gene 234:315–321

    Article  PubMed  CAS  Google Scholar 

  • Park CJ, Kim KJ, Shin R, Park JM, Shin YC, Paek KH (2004) Pathogenesis-related protein 10 isolated from hot pepper functions as a ribonuclease in an antiviral pathway. Plant J 37:186–198

    PubMed  CAS  Google Scholar 

  • Pinto MP, Ricardo CP (1995) Lupinus albus L. pathogenesis-related proteins that show similarity to PR-10 proteins. Plant Physiol 109:1345–1351

    Article  PubMed  CAS  Google Scholar 

  • Pnueli L, Hallak-Herr E, Rozenberg M, Cohen M, Goloubinoff P, Kaplan A et al (2002) Molecular and biochemical mechanisms associated with dormancy and drought tolerance in the desert legume Retama raetam. Plant J 31:319–330

    Article  PubMed  CAS  Google Scholar 

  • Poupard P, Strullu DG, Simoneau P (1998) Two members of the Bet v 1 gene family encoding birch pathogenesis-related proteins display different patterns of root expression and wound-inducibility. Aust J Plant Physiol 25:459–464

    Article  CAS  Google Scholar 

  • Rakwal R, Agrawal GK, Yonekura M (1999) Separation of proteins from stressed rice (Oryza sativa L.) leaf tissues by two-dimensional polyacrylamide gel electrophoresis: induction of pathogenesis-related and cellular protectant proteins by jasmonic acid, UV irradiation and copper chloride. Electrophoresis 20:3472–3478

    Article  PubMed  CAS  Google Scholar 

  • Rakwal R, Agrawal GK, Tamogami S, Yonekura M, Agrawal VP, Iwahashi H (2003) Novel insight into kinetin-inducible stress responses in rice seedlings. Plant Physiol Biochem 41:453–457

    Article  CAS  Google Scholar 

  • Sikorski MM, Biesiadka J, Kasperska AE, Kopcinska J, Lotocka B, Golinowski W, Legockia AB (1999) Expression of genes encoding PR10 class pathogenesis-related proteins is inhibited in yellow lupine root nodules. Plant Sci 149:125–137

    Article  CAS  Google Scholar 

  • Srivastava S, Fristensky B, Kav NNV (2004) Constitutive expression of a PR 10 protein enhances the germination of Brassica napus under saline conditions. Plant Cell Physiol 45:1320–1324

    Article  PubMed  CAS  Google Scholar 

  • Steiner-Lange S, Fischer A, Boettcher A, Rouhara I, Liedgens H, Schmelzer E, Knogge W (2003) Differential defense reactions in leaf tissues of barley in response to infection by Rhynchosporium secalis and to treatment with a fungal avirulence gene product. Mol Plant Microbe Interact 16:893–902

    Article  PubMed  CAS  Google Scholar 

  • Swoboda I, Hoffmann-Sommergrube K, O’Riordain G, Scheiner O, Heberle-Bors E, Vicente O (1996) Bet V1 proteins, the major birch pollen allergens and members of a family of conserved pathogenesis-related proteins, show ribonuclease activity in vitro. Physiol Plant 96:433–438

    Article  CAS  Google Scholar 

  • Tanaka N, Che F-S, Watanabe N, Fujiwara S, Takayama S, Isogai A (2003) Flagellin from an incompatible strain of Acidovorax avenae mediates H2O2 generation accompanying hypersensitive cell death and expression of PAL, Cht-1, and PBZ1, but not of LOX in rice. Mol Plant Microbe Interact 16:422–428

    Article  PubMed  CAS  Google Scholar 

  • Ukaji N, Kuwabara C, Takezawa D, Arakawa K, Fujikawa S (2004) Accumulation of pathogenesis-related (PR) 10/Bet v 1 protein homologues in mulberry (Morus bombycis Koidz.) tree during winter. Plant Cell Environ 27:1112–1121

    Article  CAS  Google Scholar 

  • Utriainen M, Kokko H, Auriola S, Sarrazin O, Kärenlampi S (1998) PR-10 protein is induced by copper stress in roots and leaves of a Cu/Zn tolerant clone of birch, Betula pendula. Plant Cell Environ 21:821–828

    Article  CAS  Google Scholar 

  • Van Loon LC, Van Strien EA (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55:85–97

    Article  Google Scholar 

  • Walter MH, Liu JW, Wünn J, Hess D (1996) Bean ribonuclease-like pathogenesis-related protein genes (Ypr10) display complex patterns of developmental, dark-induced and exogenous-stimulus-dependent expression. Eur J Biochem 239:281–293

    Article  PubMed  CAS  Google Scholar 

  • Warner SAJ, Scott R, Draper J (1992) Characterization of wound-induced transcript from the monocot asparagus that share similarity with a class of intracellular pathogenesis-related (PR) proteins. Plant Mol Biol 19:555–561

    Article  PubMed  CAS  Google Scholar 

  • Warner SAJ, Scott R, Draper J (1993) Isolation of an asparagus intracellular PR gene (AoPR1) wound-responsive promoter by the inverse polymerase chain reaction and its characterization in transgenic tobacco. Plant J 3:191–201

    Article  PubMed  CAS  Google Scholar 

  • Wilson CM (1975) Plant nucleases. Annu Rev Plant Physiol 26:187–208

    Article  CAS  Google Scholar 

  • Wisniewski M, Bassett C, Arora R (2004) Distribution and partial characterization of seasonally expressed proteins in different aged shoots and roots of ‘Loring’ peach (Prunus persica). Tree Physiol 24:339–345

    PubMed  CAS  Google Scholar 

  • Yen Y, Green PJ (1991) Identification and properties of the major ribonucleases of Arabidopsis thaliana. Plant Physiol 97:1487–1493

    Article  PubMed  CAS  Google Scholar 

  • Yin Z, Chen J, Zeng L, Goh M, Leung H, Khush GS, Wang GL (2000) Characterizing rice lesion mimic mutants and identifying a mutant with broad-spectrum resistance to rice blast and bacterial blight. Mol Plant Microbe Interact 13:869–876

    Article  PubMed  CAS  Google Scholar 

  • Zhou X-J, Lu S, Xu Y-H, Wang J-W, Chen X-Y (2002) A cotton cDNA (GaPR-10) encoding a pathogenesis-related 10 protein with in vitro ribonuclease activity. Plant Sci 162:629–636

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Hee Jong Ko, Seoul National University for kindly providing us with the lesion mimic mutants. This work was supported by ARPC, by a grant from KOSEF/MOST to the Environmental Biotechnology National Core Research Center and to National Research Laboratory on plant intercellular trafficking and by scholarships from the Brain Korea 21 Program.

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Correspondence to Kyu Young Kang.

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Communicated by H. Judelson.

An erratum to this article can be found at http://dx.doi.org/10.1007/s00299-008-0600-3

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Kim, S.T., Yu, S., Kang, Y.H. et al. The rice pathogen-related protein 10 (JIOsPR10) is induced by abiotic and biotic stresses and exhibits ribonuclease activity. Plant Cell Rep 27, 593–603 (2008). https://doi.org/10.1007/s00299-007-0485-6

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