Skip to main content
Log in

Expression of the gene encoding the PR-like protein PRms in germinating maize embryos

  • Published:
Molecular and General Genetics MGG Aims and scope Submit manuscript

Summary

The PRms protein is a pathogenesis-related (PR)-like protein whose mRNA accumulates during germination of maize seeds. Expression of the PRms gene is induced after infection of maize seeds with the fungus Fusarium moniliforme. To further our investigations on the expression of the PRms gene we examined the accumulation of PRms mRNA in different tissues of maize seedlings infected with E. moniliforme and studied the effect of fungal elicitors, the mycotoxin moniliformin, the hormone gibberellic acid, and specific chemical agents. Our results indicate that fungal infection, and treatment either with fungal elicitors or with moniliformin, a mycotoxin produced by F. monilforme, increase the steady-state level of PRms mRNA. PRms mRNA accumulation is also stimulated by the application of the hormone gibberellic acid or by treatment with silver nitrate, whereas acetylsalicylic acid has no effect. In situ RNA hybridization in isolated germinating embryo sections demonstrates that the PRms gene is expressed in the scutellum, particularly in a group of inner cells, and in the epithelium lying at the interface of the scutellum and the endosperm. The pattern of expression of the PRms gene closely resembles that found for hydrolytic enzymes, being confined to the scutellum and the aleurone layer of the germinating maize seed. Our results suggest that the PRms protein has a function during the normal process of seed germination that has become adapted to serve among the defence mechanisms induced in response to pathogens during maize seed germination.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ayers AR, Ebel J, Valent B, Albersheim P (1976) Host-pathogen interaction. X. Fractionation and biological activity of an elicitor isolated from the mycellial walls of Phytophtora megasperma var sojae. Plant Physiol 57:760–765

    Google Scholar 

  • Bellés JM, Conejero V (1989) Ethylene mediation of the viroid-like syndrome induced by Ag+ ions in Gynura aurantiaca DC plants. J Phytopathol 124:275–284

    Google Scholar 

  • Bellés JM, Granell A, Durdn-Vila N, Conejero V (1989) ACC synthesis as the activated stop responsible for the rise of ethylene production accompanying citrus exocortis viroid infection in tomato plants. J Phytopathol 125:198–208

    Google Scholar 

  • Bol JF, Linthorst HJM, Cornelissen BJC (1990) Plant-pathogenesis-related proteins induced by virus infection. Annu Rev Phytopathol 28:113–38

    Google Scholar 

  • Burmeister HR, Ciegler A, Vesonder RF (1979) Moniliformin, a metabolite of Fusarium moniliforme NRRL 6322: Purification and toxicity. Appl Environ Microbiol 37:11–13

    Google Scholar 

  • Camacho-Henriquez A, Sanger H-L (1984) Purification and partial characterization of the major “pathogenesis-related” tomato leaf protein P14 from potato spindle tuber viroid (PSTV)-infected tomato leaves. Arch Virol 81:263–284

    Google Scholar 

  • Casacuberta JM, Puigdoménech, P, San Segundo B (1991) A gene coding for a basic pathogenesis-related (PR-like) protein from Zea mays. Molecular cloning and induction by a fungus (Fusarium moniliforme) in germinating maize seeds. Plant Mol Biol 16:527–536

    Google Scholar 

  • Castresana C, de Carvalho F, Gheysen G, Habets M, Inzé D, Van Montagu M (1990) Tissue-specific and pathogen-induced regulation of a Nicotiana plumbaginifolia β-1,3-glucanase gene. Plant Cell 2:1131–1143

    Google Scholar 

  • Cline K, Wade M, Albersheim P (1978) Host-pathogen interactions XV. Fungal glucans which elicit phytoalexin accumulation in soybean also elicit the accumulation of phytoalexins in other plants. Plant Physiol 62:918–921

    Google Scholar 

  • Cole RJ, Kirksey JW, Cutler HG, Doupnik BL, Peckham JC (1973) Toxin from Fusarium moniliforme: effects on plants and animals. Science 179:1324–1326

    Google Scholar 

  • Conejero V, Granell A (1986) Stimulation of a viroid-like syndrome and the impairment of viroid infection in Gynura aurantiaca plants by treatment with silver ions. Physiol Mol Plant Pathol 29:317–323

    Google Scholar 

  • Cornelissen BJC, Hooft van Huijsduinjnen RAM, van Loon LC, Bol JF (1986) Molecular characterization of messenger RNAs for “pathogenesis-related” proteins 1 a, 1 b and c, induced by TMV infection of tobacco. EMBO J 5:37–40

    Google Scholar 

  • Darvill AG, Albersheim P (1984) Phytoalexins and their elicitors. A defense against microbial infection in plants. Annu Rev Plant Physiol 35:243–275

    Google Scholar 

  • de Tapia M, Bergman P, Awade A, Burkard G (1986) Analysis of acid extractable bean leaf proteins induced by mercuric chloride treatment and alfalfa mosaic virus infection. Partial purification and characterization. Plant Sci 45:167–177

    Google Scholar 

  • Fincher GB (1989) Molecular and cellular biology associated with endosperm mobilization in germinating cereal grains. Annu Rev Plant Physiol Mol Biol 40:305–346

    Google Scholar 

  • Fraser RSS (1981) Evidence for the occurrence of pathogenesisrelated proteins in leaves of healthy tobacco plants during flowering. Physiol Plant Pathol 19:69–76

    Google Scholar 

  • Gram NH (1982) The ultrastructure of germinating barley seeds. I. Changes in the scutellum and aleurone layer in Nordal barley. Carlsberg Res Commun 47:143–162

    Google Scholar 

  • ranell A, Bellés JM, Conejero V (1987) Induction of pathogenesis-related proteins in tomato by citrus exocortis viroid, silver ion and ethephon. Physiol Mol Plant Pathol 31:83–89

    Google Scholar 

  • Hammerton R, Ho T-HD (1986) Hormonal regulation of the development of protease and carboxypeptidase activities in barley aleurone layers. Plant Physiol 80:692–697

    Google Scholar 

  • Jamet E, Fritig B (1986) Purification and characterization of 8 of the pathogenesis-related proteins in tobacco leaves reacting hypersensitively to tobacco mosaic virus. Plant Mol Biol 6:69–80

    Google Scholar 

  • Kauffmann S, Legrand M, Geoffroy P, Fritig B (1987) Biological function of “pathogenesis-related” proteins: four PR proteins of tobacco have 1,3-a-glucanase activity. EMBO J 6:3209–3212

    Google Scholar 

  • Kombrink E, Schröder M, Hahlbrock K (1988) Several pathogenesis-related proteins in potato are 1,3-β-glucanases and chitinases. Proc Natl Acad Sci USA 85:782–786

    Google Scholar 

  • Langdale JA, Rothermel B, Nelson T (1988) Cellular pattern of photosynthetic gene expression in developing maize leaves. Genes Dev 2:106–115

    Google Scholar 

  • Legrand M, Kauffmann S, Geoffroy P, Fritig B (1987) Biological function of “pathogenesis-related” proteins: four tobacco pathogenesis-related proteins are chitinases. Proc Natl Acad Sci USA 84:6750–6754

    Google Scholar 

  • Logeman J, Schell J, Willmitzer L (1987) Improved method for the isolation of RNA from plant tissues. Anal Biochem 163:16–20

    Google Scholar 

  • Lotan T, Ori N, Fluhr N (1989) Pathogenesis-related proteins are developmentally regulated in tobacco flowers. Plant Cell 1: 881–887

    Google Scholar 

  • Lucas J, Camacho-Henriquez A, Lottspeich F, Henschen A, Sängei HL (1985) Amino acid sequence of the “pathogenesis-related” leaf protein P14 from viroid-infected tomato reveals a new type of structurally unfamilar proteins. EMBO J 4:2745–2749

    Google Scholar 

  • MacGregor AW, MacDonald FH, Mayer C, Daussant J (1984) Changes in levels of α-amylase components in barley tissues during germination and early seedling growth. Plant Physiol 75:203–206

    Google Scholar 

  • Malamy J, Carr JP, Klessig D, Raskin I (1990) Salicylic acid: A likely endogenous signal in the resistance response of tobacco to viral infection. Science 250:1002–1004

    Google Scholar 

  • Matsuoka M, Ohashi Y (1986) Induction of pathogenesis-related proteins in tobacco leaves. Plant Physiol 80:505–510

    Google Scholar 

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

    Google Scholar 

  • McFadden DI, Ahluwalia B, Clarke AE, Fincher GB (1988) Expression sites and developmental regulation of genes encoding (1-3, 1-4)-β-glucanases in germinated barley. Planta 173:500–508

    Google Scholar 

  • Memelink J, Hoge JHC, Schilperoort RA (1987) Cytokinin stress changes the developmental regulation of several defence-related genes in tobacco. EMBO J 6:3579–3583

    Google Scholar 

  • Metraux JP, Signer H, Ryals J, Ward E, Wyss-Benz M, Gaudin J, Raschdorf K, Schmid E, Blum W, Inverardi B (1990) Increase in salicylic acid at the onset of systemic acquired resistance in cucumber. Science 250:1004–1006

    Google Scholar 

  • Mundy J, Brandt A, Fincher GB (1985) Messenger RNAs from the scutellum and aleurone of germinating barley encode (1-3, 1-4)-β-d-glucanase, a-amylase and carboxypeptidase. Plant Physiol 79:867–871

    Google Scholar 

  • Nasser W, deTapia M, Kauffmann S, Montasser-Kouhsari S, Burkard G (1988) Identification and characterization of maize pathogenesis-related proteins. Four maize PR proteins are chitinases. Plant Mol Biol 11:529–538

    Google Scholar 

  • Neale AD, Wahleithner JA, Lund M, Bonnet HT, Kelly A, Meeks-Wagner DR, Peacoc WJ, Dennis ES (1990) Chitinase, β-1,3-glucanase, osmotin and extensin are expressed in tobacco explants during flower formation. Plant Cell 2:673–684

    Google Scholar 

  • Ohshima M, Itoh H, Matsuoka M, Murakami T, Ohashi Y (1990) Analysis of stress-induced or salicylic acid-induced expression of the pathogenesis-related 1 a protein gene in transgenic tobacco. Plant Cell 2:95–106

    Google Scholar 

  • Payne G, Middlesteadt W, Desai N, Willians S, Dincher S, Carnes M, Ryals J (1989) Isolation and sequence of a genomic clone encoding the basic form of pathogenesis-related protein 1 from Nicotiana tabacum. Plant Mol Biol 12:595–596

    Google Scholar 

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

    Google Scholar 

  • Somssich IE, Schmelzer E, Bollmann J, Hahlbrock K (1986) Rapid activation by fungal elicitors of genes encoding “pathogenesisrelated” proteins in cultured parsley cells. Proc Natl Acad Sci USA 83:2427–2430

    Google Scholar 

  • Stuart IM, Loi L, Fincher GB (1986) Development of (1-3, 1-4)-β-d-glucan endohydrolase isoenzymes in isolated scutella and aleurone layers of barley (Hordeum vulgare). Plant Physiol 80:310–314

    Google Scholar 

  • Thiel PG, Gelderblom WCA, Marasas PE, Nelson PE, Wilson TM (1986) Natural ocurrence of moniliformin and Fusarium C in corn screenings known to be hepatocarcinogenic in rats. J Agric Food Chem 34:773–775

    Google Scholar 

  • Toppan A, Esquerré-Tugayé MT (1984) Cell surfaces in plant-microorganisms interactions IV. Fungal glycopeptides which elicit the synthesis of ethylene in plants. Plant Physiol 75:1133–1138

    Google Scholar 

  • Van de Rhee MD, van Kan JAL, Gonzalez-Jaen MT, Bol JF (1990) Analysis of regulatory elements involved in the induction of two tobacco genes by salicylate treatment and virus infection. Plant Cell 2:357–366

    Google Scholar 

  • Van Loon LC (1972) Pathogenese en symptoomexpressie in viruszieke tabak. Een onderzoek naar veranderingen in oplobare eiwitten. Ph.D. thesis, Agricultural University, Wageningen

    Google Scholar 

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

    Google Scholar 

  • Van Loon LC (1985) Pathogenesis-related proteins. Plant Mol Biol 4:111–116

    Google Scholar 

  • Vera P, Conejero V (1988) Pathogenesis-related proteins of tomato. P69 as an alkaline endoproteinase. Plant Physiol 87:58–63

    Google Scholar 

  • Vera P, Hernandez Yago J, Conejero V (1988) Immunocytochemical localization of the major “pathogenesis-related” (PR) protein of tomato plants. Plant Sci 55:223–230

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by A. Kondorosi

Rights and permissions

Reprints and permissions

About this article

Cite this article

Casacuberta, J.M., Raventós, D., Puigdoménech, P. et al. Expression of the gene encoding the PR-like protein PRms in germinating maize embryos. Molec. Gen. Genet. 234, 97–104 (1992). https://doi.org/10.1007/BF00272350

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00272350

Key words

Navigation