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Plant Biol (Stuttg) 2004; 6(6): 664-672
DOI: 10.1055/s-2004-830351
Research Paper

Georg Thieme Verlag Stuttgart KG · New York

Inhibition of Phosphoinositide-Specific Phospholipase C Results in the Induction of Pathogenesis-Related Genes in Soybean

W-M. Chou[*] 1 , 2 , T. Shigaki[*] 1 , 3 , C. Dammann1 , 4 , Y-Q. Liu1 , 5 , M. K. Bhattacharyya1 , 6
  • 1Plant Biology Division, The Samuel Roberts Noble Foundation, P.O. Box 2180, Ardmore, Oklahoma 73402, USA
  • 2Present address: National Huwei University of Science and Technology, 64 Wenhua Road, Huwei, Yunlin 63208, Taiwan, Republic of China
  • 3Present address: Plant Physiology Laboratories, Children's Nutrition Research Center, Baylor College of Medicine, 1100 Bates St., Houston, TX 77030, USA
  • 4Present address: BASF Plant Science, 26 Davis Drive, P.O. Box 13528, Research Triangle Park, NC 27709-3528, USA
  • 5Present address: Environmental Sciences Division, Oak Ridge National Laboratory, Building 1505, MS 6038, Oak Ridge, TN 37831, USA
  • 6Present address: Department of Agronomy, G303 Agronomy Hall, Iowa State University, Ames, IA 50011-1010, USA
Further Information

Publication History

Received: March 23, 2004

Accepted: September 1, 2004

Publication Date:
29 November 2004 (online)

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Abstract

The inositol 1,4,5-trisphosphate (IP3) content is decreased in soybean cells following infection with Pseudomonas syringae pv. glycinea (Psg). In this investigation, a differential display approach was applied to isolate soybean genes that are transcriptionally up-regulated by the inhibition of phosphoinositide-specific phospholipase C (PI-PLC) activity and to study if the transcription of those genes is altered following Psg infection. Four genes, transcriptionally activated following treatment with the PI-PLC-specific inhibitor U-73122, were cloned. Three of the four genes were induced following infection with Psg. The transcripts of a hydrolase homologue (GmHy) were induced in the incompatible but not compatible soybean-Psg interaction. The transcripts of a putative ascorbate oxidase gene (GmAO) were induced in both compatible and incompatible interactions. GmHy and GmAO may represent new classes of pathogenesis-related genes. In addition to these two novel genes, homologues of PR-10 and polygalacturonase inhibitor protein (GmPR10 and GmPGIP, respectively) were identified. These two genes have previously been reported as pathogenesis-related. Transcripts of GmPR-10, but not GmPGIP, were induced in both compatible and incompatible soybean-Psg interactions. Induction of these genes, except for GmPGIP, following inhibition of PI-PLC by either the U-73122 treatment or bacterial infection suggests that PI-PLC may negatively regulate the expression of defence genes.

Key words

Differential display - IP3 - PI-PLC - PR genes - soybean - U-73122

References

  • 1 Ashcroft F. M.. Exciting times for PIP2.  Science. (1998);  282 1059-1060
    CrossrefPubMedGoogle Scholar
  • 2 Ausubel F. M., Brent R., Kingston R. E., Moore D. D., Seidman J. G., Smith J. A., Struhl K.. Current Protocols in Molecular Biology. New York; Greene Publishing Associates/Wiley Interscience (1998)
    Google Scholar
  • 3 Bantignies B., Seguin J., Muzac I., Dedaldechamp F., Gulick P.. Direct evidence for ribonucleolytic activity of a PR-10-like protein from white lupin roots.  Plant Molecular Biology. (2000);  42 871-881
    CrossrefPubMedGoogle Scholar
  • 4 Berridge M. J.. Inositol trisphosphate and calcium signalling.  Nature. (1993);  361 315-325
    CrossrefPubMedGoogle Scholar
  • 5 Bleasdale J. E., Thakur N. R., Gremban R. S., Bundy G. L., Fitzpatrick F. A., Smith R. J., Bunting S.. Selective inhibition of receptor-coupled phospholipase C-dependent processes in human platelets and polymorphonuclear neutrophils.  Journal of Pharmacology and Experimental Therapeutics. (1990);  255 756-768
    PubMedGoogle Scholar
  • 6 Buchanan S. G. S., Gay N. J.. Structural and functional diversity in the leucine-rich repeat family of proteins.  Progress in Biophysics and Molecular Biology. (1996);  65 1-44
    PubMedGoogle Scholar
  • 7 Chevalier C., Bourgeois E., Pradet A., Raymond P.. Molecular cloning and characterization of six cDNAs expressed during glucose starvation in excised maize (Zea mays L.) root tips.  Plant Molecular Biology. (1995);  28 473-485
    CrossrefPubMedGoogle Scholar
  • 8 Cockcroft S., Thomas M. H.. Inositol-lipid-specific phospholipase C isozymes and their differential regulation by receptors.  Biochemical Journal. (1992);  288 1-14
    PubMedGoogle Scholar
  • 9 Crowell D. N., John M. E., Russell D., Amasino R. M.. Characterization of a stress-induced, developmentally regulated gene family from soybean.  Plant Molecular Biology. (1992);  18 459-466
    CrossrefPubMedGoogle Scholar
  • 10 Davies C., Robinson S. P.. Differential screening indicates a dramatic change in mRNA profiles during grape berry ripening. Cloning and characterization of cDNAs encoding putative cell wall and stress response proteins.  Plant Physiology. (2000);  122 803-812
    CrossrefPubMedGoogle Scholar
  • 11 De Camilli P., Takei K.. Molecular mechanisms in synaptic vesicle endocytosis and recycling.  Neuron. (1996);  16 481-486
    CrossrefPubMedGoogle Scholar
  • 12 De Lorenzo G., Ferrari S.. Polygalacturonase-inhibiting proteins in defense against phytopathogenic fungi.  Current Opinion in Plant Biology. (2002);  5 295-299
    CrossrefPubMedGoogle Scholar
  • 13 den Hartog M., Musgrave A., Munnik T.. Nod factor-induced phosphatidic acid and diacylglycerol pyrophosphate formation: a role for phospholipase C and D in root hair deformation.  Plant Journal. (2001);  25 55-65
    CrossrefPubMedGoogle Scholar
  • 14 Diallinas G., Pateraki I., Sanmartin M., Scossa A., Stilianou E., Panopoulos N. J., Kanellis A. K.. Melon ascorbate oxidase: cloning of a multigene family, induction during fruit development and repression by wounding.  Plant Molecular Biology. (1997);  34 759-770
    CrossrefPubMedGoogle Scholar
  • 15 Engstrom E. M., Ehrhardt D. W., Mitra R. M., Long S. R.. Pharmacological analysis of Nod factor-induced calcium spiking in Medicago truncatula. Evidence for the requirement of type II calcium pumps and phosphoinositide signaling.  Plant Physiology. (2002);  128 1390-1401
    CrossrefPubMedGoogle Scholar
  • 16 Favaron F., D'Ovidio R., Porceddu E., Alghisi P.. Purification and molecular characterization of a soybean polygalacturonase-inhibiting protein.  Planta. (1994);  195 80-87
    PubMedGoogle Scholar
  • 17 Feng J.-F., Rhee S. G., Im M.-J.. Evidence that phospholipase δ1 is the effector in the Gh (Transglutaminase II)-mediated signaling.  Journal of Biological Chemistry. (1996);  271 16451-16454
    CrossrefPubMedGoogle Scholar
  • 18 Gamas P., Niebel de C. F., Lescure N., Cullimore J.. Use of a subtractive hybridization approach to identify new Medicago truncatula genes induced during root nodule development.  Molecular Plant-Microbe Interactions. (1996);  9 233-242
    PubMedGoogle Scholar
  • 19 Hammond-Kosack K. E., Parker J. E.. Deciphering plant-pathogen communication: fresh perspectives for molecular resistance breeding.  Current Opinion in Biotechnology. (2003);  14 177-193
    CrossrefPubMedGoogle Scholar
  • 20 Hermsmeier D., Hart J. K., Byzova M., Rodermel S. R., Baum T. J.. Changes in mRNA abundance within Heterodera schachtii-infected roots of Arabidopsis thaliana. .  Molecular Plant-Microbe Interactions. (2000);  13 309-315
    PubMedGoogle Scholar
  • 21 Hirayama T., Ohto C., Mizoguchi T., Shinozaki K.. A gene encoding a phosphatidylinositol-specific phospholipase C induced by dehydration and salt stress in Arabidopsis thaliana. .  Proceedings of the National Academy of Sciences of the USA. (1995);  92 3903-3907
    PubMedGoogle Scholar
  • 22 Jia Y., Mcadams S. A., Bryan G. T., Hershey H. P., Valent B.. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance.  EMBO Journal. (2000);  19 4004-4014
    CrossrefPubMedGoogle Scholar
  • 23 Kamada Y., Muto S.. Stimulation by fungal elicitor of inositol phospholipid turnover in tobacco suspension culture cells.  Plant and Cell Physiology. (1994);  35 397-404
    PubMedGoogle Scholar
  • 24 Kato N., Esaka M.. cDNA cloning and gene expression of ascorbate oxidase in tobacco.  Plant Molecular Biology. (1996);  30 833-837
    CrossrefPubMedGoogle Scholar
  • 25 Kato N., Esaka M.. Expansion of transgenic tobacco protoplasts expressing pumpkin ascorbate oxidase is more rapid than that of wide-type protoplasts.  Planta. (2000);  210 1018-1022
    CrossrefPubMedGoogle Scholar
  • 26 Keen N. T., Buzzell R. I.. New disease resistance genes in soybean against Pseudomonas syringae pv. glycinea: Evidence that one of them interacts with a bacterial elicitor.  Theoretical and Applied Genetics. (1991);  81 133-138
    PubMedGoogle Scholar
  • 27 Kisu Y., Harada Y., Goto M., Esaka M.. Cloning of the pumpkin ascorbate oxidase gene and analysis of a cis-acting region involved in induction by auxin.  Plant and Cell Physiology. (1997);  38 631-637
    PubMedGoogle Scholar
  • 28 Koonin E. V., Tatusov R. L.. Computer analysis of bacterial haloacid dehalogenases defines a large superfamily of hydrolases with diverse specificity.  Journal of Molecular Biology. (1994);  244 125-132
    CrossrefPubMedGoogle Scholar
  • 29 Kopka J., Pical C., Gray J. E., Müller-Röber B.. Molecular and enzymatic characterization of three phosphoinositide-specific phospholipase C isoforms from potato.  Plant Physiology. (1998);  116 239-250
    CrossrefPubMedGoogle Scholar
  • 30 Leckie F., Mattei B., Capodicasa C., Hemmings A., Nuss L., Aracri B., Lorenzo G. D., Cervone F.. The specificity of polygalacturonase-inhibiting protein (PGIP): a single amino acid substitution in the solvent-exposed β-strand/β-turn region of the leucine-rich repeats (LRRs) confers a new recognition capability.  EMBO Journal. (1999);  18 2352-2363
    CrossrefPubMedGoogle Scholar
  • 31 Lee Y., Choi Y. B., Suh S., Lee J., Assmann S. M., Joe C. O., Kelleher J. F., Crain R. C.. Abscisic acid-induced phosphoinositide turnover in guard cell protoplasts of Vicia faba. .  Plant Physiology. (1996);  110 987-996
    PubMedGoogle Scholar
  • 32 Legendre L., Yueh Y. G., Crain R., Haddock N., Heinstein P. F., Low P. S.. Phospholipase C activation during elicitation of the oxidative burst in cultured plant cells.  Journal of Biological Chemistry. (1993);  268 24559-24563
    PubMedGoogle Scholar
  • 33 Lopez I., Mak E. C., Ding S., Hamm H. E., Lomasney J. W.. A novel bifunctional phospholipase C that is regulated by Gα12 and stimulates the Ras/mitogen-activated protein kinase pathway.  Journal of Biological Chemistry. (2001);  276 2758-2765
    CrossrefPubMedGoogle Scholar
  • 34 Moiseyev G. P., Fedoreyeva L. I., Zhuravlev Y. N., Yasnetskaya E., Jekel P. A., Beintema J. J.. Primary structures of two ribonucleases from ginseng calluses. New members of the PR-10 family of intracellular pathogenesis-related plant proteins.  FEBS Letters. (1997);  407 207-210
    CrossrefPubMedGoogle Scholar
  • 35 Morse M. J., Crain R. C., Coté G. G., Satter R. L.. Light-stimulated inositol phospholipid turnover in Samanea saman pulvini. Increased levels of diacylglycerol.  Plant Physiology. (1989);  89 724-727
    PubMedGoogle Scholar
  • 36 Morse M. J., Crain R. C., Satter R. L.. Light-stimulated inositol phospholipid turnover in Samanea saman leaf pulvini.  Proceedings of the National Academy of Sciences of the USA. (1987);  84 7075-7078
    PubMedGoogle Scholar
  • 37 Munnik T.. Phosphatidic acid: an emerging plant lipid second messenger.  Trends in Plant Science. (2001);  6 227-233
    CrossrefPubMedGoogle Scholar
  • 38 Munnik T., Irvine R. F., Musgrave A.. Phospholipid signalling in plants.  Biochimica et Biophysica Acta. (1998);  1389 222-272
    PubMedGoogle Scholar
  • 39 Murashige T., Skoog F.. A revised medium for rapid growth and bioassays with tobacco tissue cultures.  Physiologia Plantarum. (1962);  15 473-497
    PubMedGoogle Scholar
  • 40 Ohkawa J., Okada N., Shinmyo A., Takano M.. Primary structure of cucumber (Cucumis sativus) ascorbate oxidase deduced from cDNA sequence: homology with blue copper proteins and tissue-specific expression.  Proceedings of the National Academy of Sciences of the USA. (1989);  86 1239-1243
    PubMedGoogle Scholar
  • 41 Ortega X., Petrez L. M.. Participation of the phosphoinositide metabolism in the hypersensitive response of Citrus limon against Alternaria alternata. .  Biological Research. (2001);  34 43-50
    PubMedGoogle Scholar
  • 43 Perera I. Y., Heilmann I., Boss W. F.. Transient and sustained increases in inositol 1,4,5-trisphosphate precede the differential growth response in gravistimulated maize pulvini.  Proceedings of the National Academy of Sciences of the USA. (1999);  96 5838-5843
    CrossrefPubMedGoogle Scholar
  • 44 Perera I. Y., Heilmann I., Chang S. C., Boss W. F., Kaufman P. B.. A role for inositol 1, 4, 5-trisphosphate in gravitropic signaling and the retention of cold-perceived gravistimulation of oat shoot pulvini.  Plant Physiology. (2001);  125 1499-1507
    CrossrefPubMedGoogle Scholar
  • 45 Pignocchi C., Foyer C. H.. Apoplastic ascorbate metabolism and its role in the regulation of cell signalling.  Current Opinion in Plant Biology. (2003);  6 379-389
    CrossrefPubMedGoogle Scholar
  • 46 Pingret J. L., Journet E. P., Barker D. G.. Rhizobium Nod factor signaling. Evidence for a G protein-mediated transduction mechanism.  Plant Cell. (1998);  10 659-671
    CrossrefPubMedGoogle Scholar
  • 47 Potters G., Horemans N., Caubergs R. J., Asard H.. Ascorbate and dehydroascorbate influence cell cycle progression in a tobacco cell suspension.  Plant Physiology. (2000);  124 17-20
    CrossrefPubMedGoogle Scholar
  • 48 Rhee S. G., Choi K. D.. Regulation of inositol phospolipid-specific phospholipase C isozymes.  Journal of Biological Chemistry. (1992);  267 12393-12396
    PubMedGoogle Scholar
  • 49 Rudd J. J., Franklin-Tong V. E.. Unravelling response-specificity in Ca2+ signalling pathways in plant cells.  New Phytologist. (2001);  151 7-33
    CrossrefPubMedGoogle Scholar
  • 50 Saunders C. M., Larman M. G., Parrington J., Cox L. J., Royse J., Blayney L. M., Swann K., Lai F. A.. PLCζ: a sperm-specific trigger of Ca2+ oscillations in eggs and embryo development.  Development. (2002);  129 3533-3544
    PubMedGoogle Scholar
  • 51 Shi J., Gonzales R. A., Bhattacharyya M. K.. Characterization of a plasma membrane-associated phosphoinositide-specific phospholipase C from soybean.  Plant Journal. (1995);  8 381-390
    CrossrefPubMedGoogle Scholar
  • 52 Shigaki T., Bhattacharyya M. K.. Decreased inositol 1,4,5-trisphophate content in pathogen-challenged soybean cells.  Molecular Plant-Microbe Interactions. (2000);  13 563-567
    PubMedGoogle Scholar
  • 53 Shigaki T., Bhattacharyya M. K.. Nutrients induce an increase in inositol 1,4,5-trisphosphate in soybean cells: implication for the involvement of phosphoinositide-specific phospholipase C in DNA synthesis.  Plant Biology. (2002);  4 53-61
    Article in Thieme ConnectPubMedGoogle Scholar
  • 54 Smith R. J., Sam L. M., Justen J. M., Bundy G. L., Bala G. A., Bleasdale J. E.. Receptor-coupled signal transduction in human polymorphonuclear neutrophils: effects of a novel inhibitor of phospholipase C-dependent processes on cell responsiveness.  Journal of Pharmacology and Experimental Therapeutics. (1990);  253 688-697
    PubMedGoogle Scholar
  • 55 Song C., Hu C.-D., Masago M., Kariyai K., Yamawaki-Kataoka Y., Shibatohge M., Wu D., Satoh T., Kataoka T.. Regulation of a novel human phospolipase C, PLCε, through membrane targeting by Ras.  Journal of Biological Chemistry. (2001);  276 2752-2757
    CrossrefPubMedGoogle Scholar
  • 56 Staxén I., Pical C., Montgomery L. T., Gray J. E., Hetherington A. M., McAinsh M. R.. Abscisic acid induces oscillations in guard-cell cytosolic free calcium that involve phosphoinositide-specific phospholipase C.  Proceedings of the National Academy of Sciences of the USA. (1999);  96 1779-1784
    CrossrefPubMedGoogle Scholar
  • 57 Takahashi S., Katagiri T., Hirayama T., Yamaguchi-Shinozaki K., Shinozaki K.. Hyperosmotic stress induces a rapid and transient increase in inositol 1,4,5-trisphosphate independent of abscisic acid in Arabidopsis cell culture.  Plant and Cell Physiology. (2001);  42 214-222
    CrossrefPubMedGoogle Scholar
  • 58 Tao Y., Xie Z., Chen W., Glazebrook J., Chang H. S., Han B., Zhu T., Zou G., Katagiri F.. Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. .  The Plant Cell. (2003);  15 317-330
    PubMedGoogle Scholar
  • 59 Thompson J. D., Higgins D. G., Gibson T. J.. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific-gap penalties and weight matrix choice.  Nucleic Acids Research. (1994);  22 4673-4680
    CrossrefPubMedGoogle Scholar
  • 60 Toyoda K., Shiraishi T., Yamada T., Ichinose Y., Oku H.. Rapid changes in polyphosphoinositide metabolism in pea in response to fungal signals.  Plant and Cell Physiology. (1993);  34 729-735
    PubMedGoogle Scholar
  • 61 Toyoda K., Shiraishi T., Yoshioka H., Yamada T., Ichinose Y., Oku H.. Regulation of polyphosphoinositide metabolism in pea plasma membranes by elicitor and suppressor from a pea pathogen, Mycosphaerella pinodes. .  Plant and Cell Physiology. (1992);  33 445-452
    PubMedGoogle Scholar
  • 62 van Loon L. C., Pierpoint W. S., Boller T., Conejero V.. Recommendation for naming plant pathogenesis-related proteins.  Plant Molecular Biology Reporter. (1994);  12 245-264
    PubMedGoogle Scholar
  • 63 Walton T. J., Cooke C. J., Newton R. P., Smith C. J.. Evidence that generation of inositol 1,4,5-trisphosphate and hydrolysis of phosphatidylinositol 4,5-bisphosphate are rapid responses following addition of fungal elicitor which induces phytoalexin synthesis in Lucerne (Medicago sativa) suspension culture cells.  Cellular Signalling. (1993);  5 345-356
    CrossrefPubMedGoogle Scholar
  • 64 Zhang X. G., Cote G. G., Grain R. C.. Involvement of phosphoinositide turnover in tracheary element differentiation in Zinnia elegans L. cells.  Planta. (2002);  215 312-318
    CrossrefPubMedGoogle Scholar

1 * Authors who contributed equally

M. K. Bhattacharyya

Department of Agronomy
G303 Agronomy Hall
Iowa State University

Ames, IA 50011-1010

USA

Email: mbhattac@iastate.edu

Editor: C. M. J. Pieterse