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Induction of mRNA accumulation corresponding to a gene encoding a cell wall hydroxyproline-rich glycoprotein by fungal elicitors

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Abstract

The Hrgp (hydroxyproline-rich glycoprotein) gene codes in maize for one of the most abundant proteins of the cell wall. HRGPs may contribute to the structural support of the wall and they have also been involved in plant defense mechanisms. This second aspect has been tested for the Hrgp gene in maize where, in contrast with the situation in dicot species, the gene is encoded by a single-copy sequence. Hrgp mRNA accumulation is induced in maize suspension-cultured cells by elicitors, isolated either from maize pathogenic or non-pathogenic fungi. The induction of Hrgp mRNA accumulation by elicitor extracted from Fusarium moniliforme has been studied in detail. The level of induction depends on elicitor concentration and remains high until at least 24 h. Ethylene and protein phosphorylation appear to be involved in the transduction pathway of Hrgp gene activation by the F. moniliforme elicitor but not by 5 µM methyl jasmonate or 1 mM salycilic acid. Different compounds known to participate in plant stress responses such as ascorbic acid or reduced glutathione have also a positive effect on Hrgp mRNA accumulation.

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References

  1. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K: Current Protocols in Molecular Biology, vol. 2. John Wiley, New York. (1994).

    Google Scholar 

  2. Ayers AR, Ebel J, Valent B, Albersheim P: Host-pathogen interactions. IX. Quantitative assays of elicitor activity and characterization of the elicitor present in the extracellular medium of cultures of Phytophthora megasperma var. sojae. X. Fractionation and biological activity of an elicitor isolated from the mycelial walls of Phytophthora megasperma var. sojae. XI. Composition and structure of wall-release elicitor fractions. Plant Physiol 57: 751–774 (1976).

    Google Scholar 

  3. Benhamou N: Time-course study of the accumulation of hydroxiproline-rich glycoproteins in root cells of susceptible and resistant tomato plants infected by Fusarium oxysporum f.sp. radicis-lycopersici. Planta 184: 196–208 (1990).

    Google Scholar 

  4. Boudart G, Dechamp-Guillaume G, Lafitte C, Ricart G, Barthe J-P, Mazau D, Esquerré-Tugayé MT: Elicitors and suppressors of hydroxiproline-rich glycoprotein accumulation are solubilized from plant cell walls by endopolygalacturonase. Eur J Biochem 232: 449–457 (1995).

    PubMed  Google Scholar 

  5. Bronstein J, McGrath P: Hybridization with nonradioactive probes and detection by chemiluminescence. Nature 338: 599–600 (1989).

    PubMed  Google Scholar 

  6. Caelles C, Delseny M, Puigdomè nech P: The hydroxyprolinerich glycoprotein gene from Oryza sativa. Plant Mol Biol 18: 617–619 (1992).

    PubMed  Google Scholar 

  7. Carpita NC, Gibeaut DM: Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3: 1–30 (1993).

    PubMed  Google Scholar 

  8. Casacuberta JM, Puigdomè nech P, San Segundo B: A gene coding for a basic ‘pathogenesis-related’ (PR-like) protein PRms from Zea mays. Plant Mol Biol 16: 527–536 (1991).

    Article  PubMed  Google Scholar 

  9. Cassab GL, Lin JJ, Lin LS, Varner JE: Ethylene effect on extensin and peroxidase distribution in the subapical region of pea epicotyls. Plant Physiol 88: 522–524 (1988).

    Google Scholar 

  10. Cassab GI, Varner JE: Inmunocytolocalization of extensin in developing soybean seed coats by inmunogold-silver staining and by tissue printing on nitrocellulose paper. J Cell Biol 105: 2581–2588 (1987).

    Article  PubMed  Google Scholar 

  11. Cassab GI, Varner JE: Tissue printing on nitrocellulose paper: a new method for immunolocalization of proteins, localization of enzyme activities and anatomical analysis. Cell Biol Int Rep 13: 1147–1152 (1989).

    Google Scholar 

  12. Clarke JA, Lisker N, Lamport DTA, Ellingboe AH: Hydroxyproline enhancement as a primary event in the successful development of Erysiphe graminis in wheat. Plant Physiol 67: 188–189 (1981).

    Google Scholar 

  13. Cohen Y, Niderman T, Mosinger E, Fluhr R: Betaaminobutyric induces the accumulation of pathogenesisrelated proteins in tomato (Lycopersicon esculentum L.) plants and resistance to late blight infection caused by Phytophthora infestans. Plant Physiol 104: 59–66 (1994).

    PubMed  Google Scholar 

  14. Constabel CP, Bergey DR, Ryan CA: Systemin activates synthesis of wound-inducible tomato leaf polyphenol oxidase via the octadecanoid defense signaling pathway. Proc Natl Acad Sci USA 92: 407–411 (1995).

    PubMed  Google Scholar 

  15. Corbin DR, Sauer N, Lamb CJ: Differential regulation of a hydroxyproline-rich glycoprotein gene family in wounded and infected plants. Mol Cell Biol 7: 4337–4344 (1987).

    PubMed  Google Scholar 

  16. Cordero MJ, Raventó s D, San Segundo B: Expression of a maize proteinase inhibitor gene is induced in response to wounding and fungal infection. Systemic wound response of monocot gene. Plant J 6:141 (1994).

    Article  PubMed  Google Scholar 

  17. Darvill AG, Albersheim P: Phytoalexins and their elicitors: a defense against microbial infection in plants. Annu Rev Plant Physiol 35: 243–298 (1984).

    Google Scholar 

  18. Davis D, Merida J, Legendre L, Low PS, Heinstein P: Independent elicitation of the oxidative burst and phytoalexin formation in cultured plant cells. Phytochemistry 32: 607–611 (1993).

    Google Scholar 

  19. Ecker JR, Davis RW: Plant defense genes are regulated by ethylene. Proc Natl Acad Sci USA 84: 5202–5206 (1987).

    Google Scholar 

  20. Edwards R, Blount JW, Dixon RA: Glutatione and elicitation on the phytoalexin response in legume cell cultures. Planta 184: 403–409 (1991).

    Google Scholar 

  21. Esquerré-Tugayé MT, Lamport DTA: Cell surfaces in plantmicroorganism interactions. II. Evidence for the accumulation of hydroxyproline-rich glycoprotein in the cell wall of diseased plants as a defense mechanism. Plant Physiol 64: 320–326 (1979).

    Google Scholar 

  22. Esquerré-Tugayé MT, Bottin A, Rickauer M, Sancan JP, Fournier J, Pouenat ML: Ethylene in early signalling phenomena at the plant-microorganism interface. In: Pech JC et al. (eds) Cellular and Molecular Aspects of the Plant Hormone Ethylene, pp. 217–222 (1993).

  23. Felix G, Grosskopf DG, Regenass M, Boller T: Rapid changes of protein phosphorylation are involved in transduction of the elicitor signal in plant cells. Proc Natl Acad Sci USA 88: 8831–8834 (1991).

    PubMed  Google Scholar 

  24. Grantz AA, Brummell DA, Bennett AB: Ascorbate free radical reductase mRNA levels are induced by wounding. Plant Physiol 108: 411–418 (1995).

    PubMed  Google Scholar 

  25. Green R, Fluhr R: UV-B-Induced PR-1 accumulation is mediated by active oxygen species. Plant Cell 7: 203–212 (1995).

    PubMed  Google Scholar 

  26. Grosskopf DG, Felix G, Boller T: K-252a inhibits the response of tomato cells to fungal elicitors in vivo and their microsomal protein kinase in vitro. FEBS Lett 275: 177–180 (1990).

    PubMed  Google Scholar 

  27. Hancock K, Tang VCW: India ink staining of protein on nitrocellulose paper. Anal Biochem 133: 157–162 (1983).

    PubMed  Google Scholar 

  28. Hood KR, Baasiri RA, Fritz SE, Hood EE: Biochemical and tissue print analysis of hydroxyproline-rich glycoproteins in cell walls of sporophytic maize tissues. Plant Physiol. 96: 1214–1219 (1991).

    Google Scholar 

  29. Iiyama K, Lam TB-T, Stone BA: Covalent cross-links in the cell wall. Plant Physiol 104: 315–320 (1994).

    PubMed  Google Scholar 

  30. Johnston A, Booth C (eds) Plant Pathologist=s Pocketbook, 2nd ed., p. 111. The Cambrian News, Aberystwyth, Wales. (1983).

    Google Scholar 

  31. Keller B, Lamb CJ: Specific expression of a novel cell wall hydroxyproline-rich glycoprotein gene in lateral root initiation. Genes Devel 3: 1639–1646 (1989).

    PubMed  Google Scholar 

  32. Kieliszewski MJ, Leykam JF, Lamport DTA: Structure of the threonine-rich extension from Zea mays. Plant Physiol 92: 316–326 (1990).

    Google Scholar 

  33. Lamport DTA: The protein component of primary cell walls. Adv Bot Res 2:151–218 (1965).

    Google Scholar 

  34. Leach JE, Cantrell MA, Sequeira L: A hydroxyproline-rich bacterial agglutin from potato: extraction, purification and characterisation. Plant Physiol 70: 1353–1358 (1982).

    Google Scholar 

  35. Lotan T, Fluhr R: Xylanase, a novel elicitor of pathogenesisrelated proteins in tobacco, uses a non-ethylene pathway for induction. Plant Physiol 93: 811–817 (1990).

    Google Scholar 

  36. Ludevid MD, Ruiz-Avila L, Vallés MP, Stiefel V, Torrent M, Torné JM, Puigdomè nech P: Expression of genes for cell-wall proteins in dividing and wounded tissues of Zea mays L. Planta 180: 524–529 (1990).

    Google Scholar 

  37. Mazau D, Esquerré-Tugayé MT: Hydroxyproline-rich glycoprotein accumulation in the cell walls of plants infected by various pathogens. Plant Physiol 80: 540–546 (1986).

    Google Scholar 

  38. McMullen M, Hunter B, Phillips RL, Rubenstein I: The structure of the maize ribosomal DNA spacer region. Nucl Acids Res 14: 4953–4968 (1986).

    PubMed  Google Scholar 

  39. Mellon JE, Helgeson JP: Interaction of a hydroxyproline-rich glycoprotein from tobacco callus with potential pathogens. Plant Physiol 70: 401–405 (1982).

    Google Scholar 

  40. Memelink J, Swords KMM, de Kan RJ, Schilperoort RA, Hoge JHC, Staehelin: Structure and regulation of tobacco extensin. Plant J 4: 1011–1022 (1993).

    Article  PubMed  Google Scholar 

  41. Menossi M: Estudio de la expresió n del gen Hrgp de una proteína de la pared celular del maíz en células transformadas mediante bombardeo con microproyectiles. Ph D thesis, Barcelona University, Spain (1995).

    Google Scholar 

  42. Menossi M, Martinez-Izquierdo JA, Puidomè nech P: Promoter tissue specific activity and ethylene control of the gene coding for the maize hydroxyproline-rich glycoprotein in maize cells transformed by particle bombardment. Plant Sci 125: 189–200 (1997).

    Google Scholar 

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

    Google Scholar 

  44. Murillo I, Cavallarin L, San Segundo B: The maize Pathogenesis-related Prms protein localizes to plasmodesmata in maize radicles. Plant Cell 9: 145–156 (1997).

    PubMed  Google Scholar 

  45. Parmentier Y, Durr A, Marbach J, Hirsinger C, Criqui M-C, Fleck J, Jamet E: A novel wound-inducible extensine gene is expressed early in newly isolated protoplasts of Nicotiana sylvestris. Plant Mol Biol 29: 279–292 (1995).

    PubMed  Google Scholar 

  46. Peñ a-Cortés H, Albrecht T, Prat S, Weller EW, Willmitzer L: Aspirin prevents wound-induced gene expression in tomato leaves by blocking jasmonic acid biosynthesis. Planta 191: 123 (1993).

    Article  Google Scholar 

  47. Phillips G, Chauvet M, Chaboute ME, Ehling M, Gigot C: Genomic organization and nucleotide sequences of two corn histone H4 genes. Gene 42: 225–229 (1986).

    Article  PubMed  Google Scholar 

  48. Raventó s D, Jensen AB, Rask M-B, Casacuberta JM, Mundy J, San Segundo B: A 20 bp cis-acting element is both necessary and sufficient to mediate elicitor response of a maize PRms gene. Plant J 7: 147–155 (1995).

    Article  PubMed  Google Scholar 

  49. Raz R, José M, Moya A, Martínez-Izquierdo JA, Puigdomè nech P: Different mechanisms generating sequence variability are revealed in distinct regions of the hydroxyprolinerich glycoprotein gene from maize and related species. Mol Gen Genet 233: 252–259 (1992).

    PubMed  Google Scholar 

  50. Raz V, Flurh R: Calcium requirement for ethylene-dependent responses. Plant Cell 4: 1123–1130 (1992).

    Article  PubMed  Google Scholar 

  51. Raz V, Flurh R: Ethylene signal is transduced via protein phosphorylation events in plants. Plant Cell 5: 523–530 (1993).

    Article  PubMed  Google Scholar 

  52. Ruiz-Avila L, Burgess SR, Stiefel V, Ludevid MD, Puigdomè nech P: Accumulation of the cell wall Hrgp mRNA is an early event in maize embryo cell differentiation. Proc Natl Acad Sci USA 89: 2414–2418 (1992).

    PubMed  Google Scholar 

  53. Sauer N, Corbin DR, Keller B, Lamb CJ: Cloning and characterisation of a wound specific hydroxyproline-rich glycol-protein in Phaseolus vulgaris. Plant Cell Envir 13: 257–266 (1990).

    Google Scholar 

  54. Showalter AM, Bell JN, Cramer CL, Bailey JA, Varner JE: Accumulation of hydroxyproline-rich glycoprotein mRNA in response to fungal elicitor and infection. Proc Natl Acad Sci USA 82: 6551–6555 (1985).

    Google Scholar 

  55. Showalter, AM: Structure and function of plant cell wall proteins. Plant Cell 5: 9–23 (1993).

    Article  PubMed  Google Scholar 

  56. Stiefel V, Pérez-Grau L, Albericio F, Giralt E, Ruiz-Avila L, Ludevid MD, Puigdomè nech P: Molecular cloning of cDNAs encoding a putative cell wall protein from Zea mays and immunological identification of related polypetides. Plant Mol Biol 11: 483–493 (1988).

    Google Scholar 

  57. Stiefel V, Ruiz-Avila L, Raz R, Valles MP, Gomez J, Pages M, Martínez-Izquierdo JA, Ludevid MD, Langdale JA, Nelson T, Puigdomè nech P: Expression of a maize cell wall hydroxyproline-rich glycoprotein gene in early leaf and root vascular differentiation. Plant Cell 2: 785–793 (1990).

    Article  PubMed  Google Scholar 

  58. Tagu D, Walker N, Ruiz-Avila L, Burgess S, Martínez-Izquierdo JA, Leguay J-J, Netter P, Puigdomè nech P: Regulation of the maize Hrgp gene expression and wounding. mRNA accumulation and qualitative expression analysis of the promoter by microprojectile bombardment. Plant Mol Biol 20: 529–538 (1992).

    PubMed  Google Scholar 

  59. Tierney ML, Weichert J, Pluymers D: Analysis of the expression of extensin and p33-related cell wall proteins in carrot and soybean. Mol Gen Genet 88: 61–68 (1988).

    Google Scholar 

  60. Tire C, De Rycke R, De Loose M, Inze D, Van Montagu M, Engler G: Extensin gene expression is induced by mechanical stimuli leading to local cell wall strengthening in Nicotiana plumbaginifolia. Planta 195: 175–181 (1994).

    PubMed  Google Scholar 

  61. Toppan A, Roby D, Esquerré-Tugayé MT: Cell surfaces in plant-microorganism interaction. III. In vivo effect of ethylene on hydroxyproline-rich accumulation in the cell wall disease plants. Plant Physiol 70: 82–86 (1982).

    Google Scholar 

  62. Toppan A, Esquerre-Tugayé M-T: Cell surfaces in plantmicroorganism interaction. V. Fungal glycopeptides which elicit the synthesis of ethylene in plants. Plant Physiol 75: 1133–1138 (1984).

    Google Scholar 

  63. van Etten CH, Miller RW, Earle FR, Wolff IA: Hydroxyproline content of seed meals and distribution of the aminoacid in kernel, seed coat, and pericarp. J Agric Food Chem 9: 433–435 (1961).

    Google Scholar 

  64. van Loon LC: The induction of pathogenesis-related proteins by pathogens and specific chemicals. Neth J Plant Path 89: 265–273 (1983).

    Google Scholar 

  65. White RF: Acetylsalicylic acid (aspirin) induces resistance to tobacco mosaic virus in tobacco. Virology 99: 410–412 (1979).

    Article  Google Scholar 

  66. Wilson LG, Fry JC: Extensin: a major cell wall glycoprotein. Plant Cell Environ 9: 239–260 (1986).

    Google Scholar 

  67. Wingate VPM, Lawton MA, Lamb CJ: Glutathione causes a massive and selective induction of plant defense genes. Plant Physiol 87: 206–210 (1988).

    Google Scholar 

  68. Wycoof Kl, Powell PA, Gonzales RA, Corbin DR, Lamb C, Dixon, RA: Stress activation of a bean hydroxyproline-rich glycoprotein promoter is superimposed on a pattern of tissuespecific developmental expression. Plant Physiol 109: 41–52 (1995).

    Article  PubMed  Google Scholar 

  69. Ye Z-H., Song Y-R, Marcus A, Varner JE: Comparative localization of three classes of cell wall proteins. Plant J 1: 175–183 (1991).

    PubMed  Google Scholar 

  70. Ye Z-H, Varner JE: Tissue-specific expression of cell wall proteins in developing soybean tissues. Plant Cell 3: 23–37 (1991).

    Article  PubMed  Google Scholar 

  71. Zarembinski TI, Theologis A: Ethylene biosynthesis and action: a case of conservation. Plant Mol Biol 26: 1579–1597 (1994).

    PubMed  Google Scholar 

  72. Zhang S, Mehdy MC: Binding of a 50-kD protein to a U-rich sequence in an mRNA encoding a proline-rich protein that is destabilized by a fungal elicitor. Plant Cell 6: 135–145 (1994).

    PubMed  Google Scholar 

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García-Muniz, N., Martínez-Izquierdo, J.A. & Puigdomènech, P. Induction of mRNA accumulation corresponding to a gene encoding a cell wall hydroxyproline-rich glycoprotein by fungal elicitors. Plant Mol Biol 38, 623–632 (1998). https://doi.org/10.1023/A:1006056000957

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