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Synergism of Metabolite Action in Plant Responses to Stresses

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Abstract

A diversity of unfavorable environmental factors determines complex interactions between phytohormones and signal elements and also the formation and combined action of metabolites in plants. This permits the plant to overcome stresses and to realize its potential capacities. Synergism between plant chemical constituents during ontogeny was revealed in the case of their responses to various abiotic stressors, such as pathogens or pests, and also during competition between plants. Jasmonic, salicylic, and abscisic acids, ethylene, hydrogen peroxide, NO, antioxidants, defensive proteins, and enzymes can manifest synergistic plant responses to unfavorable factors.

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Abbreviations

HSR:

hypersensitivity response

ISR:

induced systemic resistance

SAR:

systemic acquired resistance

TMV:

tobacco mosaic virus

SA:

salicylic acid

SNP:

sodium nitroprusside

REFERENCES

  1. Tarchevsky, I.A., Signal’nye sistemy kletok rastenii (Signal Transduction Pathways in Plant Cells), Moscow: Nauka, 2002.

    Google Scholar 

  2. Sudha, G. and Ravichankar, G.A., Involvement and Interaction of Various Signaling Compounds on the Plant Metabolic Events during Defense Response: Resistance to Stress Factors, Formation of Secondary Metabolites and Their Molecular Aspects, Plant Cell, Tissue Organ Cult., 2002, vol. 71, pp. 181–212.

    Google Scholar 

  3. Samuilov, V.D., Oleskin, A.B., and Lagunova, E.M., Programmed Cell Death, http://phm.bio.msu.ru/edocs/samuilov-2.html

  4. Dmitriev, A.P., Signal Molecules for Plant Defense Responses to Biotic Stress, Fiziol. Rast. (Moscow), 2003, vol. 50, pp. 465–474 (Russ. J. Plant Physiol., Engl. Transl., 417–425).

    Google Scholar 

  5. Xiong, L., Schumaker, K.S., and Zhu, J.-K., Cell Signaling during Cold, Drought, and Salt Stress, Plant Cell, 2002, vol. 14,Suppl., S165–S183.

    Google Scholar 

  6. Dong, X., SA, JA, Ethylene, and Disease Resistance in Plants, Curr. Opin. Plant Biol., 1998, vol. 1, pp. 316–323.

    Article  PubMed  Google Scholar 

  7. Chen, W., Provart, N.J., Glazebrook, J., Katagiri, F., Chang, H.-S., Eulgem, Th., Mauch, F., Luan, Sh., Zou, G., Whitham, S.A., Budworth, P.R., Tao, Y., Xie, Zh., Chen, X., Lam, S., Kreps, J.A., Harper, J.F., Si-Ammour, A., Mauch-Mani, B., Heinlein, M., Kobayashi, K., Hohn, Th., Dangl, J.L., Wang, X., and Zhu, T., Expression Profile Matrix of Arabidopsis Transcription Factor Genes Suggests Their Putative Functions in Response to Environmental Stresses, Plant Cell, 2002, vol. 14, pp. 559–574.

    Article  PubMed  Google Scholar 

  8. Kreps, J.A., Wu, Y., Chang, H.-S., Zhu, T., and Harper, J.F., Transcriptome Changes for Arabidopsis in Response to Salt, Osmotic, and Cold Stress, Plant Physiol., 2002, vol. 130, pp. 2129–2141.

    Article  PubMed  Google Scholar 

  9. Ryabushkina, N.A., Analysis of Coordinated Response of Gene Expression in Plants under Stresses. Physiological View, Izv. MON RK, NAN RK. Ser. Biol. Med., 2004, no. 2(242), pp. 69–76.

    Google Scholar 

  10. Corning, P.A., The Synergism Hypothesis: On the Concept of Synergy and Its Role in the Evolution of Complex Systems, J. Soc. Evol. Syst., 1998, vol. 21, p. 33.

    Google Scholar 

  11. Famintsin, A.S., O roli simbioza v evolyutsii organizmov (The Role of Symbiosis in Organism Evolution), Tr. Botan. Lab. Imperatorskoi Akad. Nauk, St. Petersburg, 1906, no. 9.

    Google Scholar 

  12. Kozo-Polyanskii, B., Novyi printsip biologii. Ocherk teorii simbiogeneza (New Principle in Biology. Theory of Symbiogenesis), Leningrad-Moscow: Putchina, 1924.

    Google Scholar 

  13. Wink, M., Evolution of Secondary Metabolites from an Ecological and Molecular Phylogenetic Perspective, Phytochemistry, 2003, vol. 64, pp. 3–19.

    Article  PubMed  Google Scholar 

  14. Telitchenko, M.M. and Ostroumov, S.A., Vvedenie v problemy biokhimicheskoi ekologii (Introduction to the Problem of Biochemical Ecology), Moscow: Nauka, 1990.

    Google Scholar 

  15. Croteau, R., Kutchan, T.M., and Lewis, N.G., Natural Products (Secondary Metabolites), Biochemistry and Molecular Biology of Plants, Buchanan, B., Gruissem, W., and Jones, R., Eds., Rockville (Maryland): Am. Soc. Plant Physiol., 2000, pp. 1250–1310.

    Google Scholar 

  16. Nelson, A.C. and Kursar, Th.A., Interactions among Defense Compounds: A Method for Analysis, Chemoecology, 1999, vol. 9, pp. 81–92.

    Article  Google Scholar 

  17. Trewavas, A., Signal Perception and Transduction, Biochemistry and Molecular Biology of Plants, Buchanan, B., Gruissem, W., and Jones, R., Eds., Rockville (Mary-land): Am. Soc. Plant Physiol., 2000, pp. 930–987.

    Google Scholar 

  18. Shulaev, V., Leon, J., and Raskin, I., Is Salicylic Acid a Translocated Signal of Systemic Acquired Resistance in Tobacco? Plant Cell, 1995, vol. 7, pp. 1691–1701.

    Article  PubMed  Google Scholar 

  19. Katz, V., Fuchs, A., and Conrath, U., Pretreatment with Salicylic Acid Primers Parsley Cells for Enhanced Ion Transport Following Elicitation, FEBS Lett., 2002, vol. 520, pp. 53–57.

    Article  PubMed  Google Scholar 

  20. Grayer, R.J. and Kokubun, T., Plant-Fungal Interactions: The Search for Phytoalexins and Other Antifungal Compound from Higher Plants, Phytochemistry, 2001, vol. 56, pp. 253–263.

    Article  PubMed  Google Scholar 

  21. Molina, A., Hunt, M.D., and Ryals, J.A., Impaired Fungicide Activity in Plants Blocked in Disease Resistance Signal Transduction, Plant Cell, 1998, vol. 10, pp. 1903–1914.

    Article  PubMed  Google Scholar 

  22. Siegrist, J., Orober, M., and Buchenauer, H., β-Aminobutyric Acid-Mediated Enhancement of Resistance in Tobacco to Tobacco Mosaic Virus Depends on the Accumulation of Salicylic Acid, Physiol. Mol. Plant Pathol., 2000, vol. 56, pp. 95–106.

    Article  Google Scholar 

  23. Lamb, Ch. and Dixon, R.A., The Oxidative Burst in Plant Disease Resistance, Annu. Rev. Plant Physiol. Plant Mol. Biol., 1997, vol. 48, pp. 251–275.

    Article  PubMed  Google Scholar 

  24. Qiao, J.J., Yuan, Y.J., Zhao, H., Wu, J.C., and Zeng, A.P., Apoptotic Cell Death in Suspension Cultures of Taxus Cuspidate Co-Treated with Salicylic Acid and Hydrogen Peroxide, Biotechnol. Lett., 2003, vol. 25, pp. 387–390.

    Article  PubMed  Google Scholar 

  25. Garcia-Mata, C. and Lamattina, L., Nitric Oxide and Abscisic Acid Cross Talk in Guard Cells, Plant Physiol., 2002, vol. 128, pp. 790–792.

    Article  PubMed  Google Scholar 

  26. Neill, S.J., Desican, R., Clarke, A., Hurst, R.D., and Hancock, J.T., Hydrogen Peroxide and Nitric Oxide as Signaling Molecules in Plants, J. Exp. Bot., 2002, vol. 53, pp. 1237–1247.

    Article  PubMed  Google Scholar 

  27. Delledonne, M., Xia, Y., Dixon, R.A., and Lamb, C., Nitric Oxide Functions as a Signal in Plant Disease Resistance, Nature, 1998, vol. 394, pp. 585–588.

    Article  PubMed  Google Scholar 

  28. Van Wees, S.C.M., de Swart, E.A.M., van Pelt, J.A., van Loon, L.C., and Pieterse, C.M.J., Enhancement of Induced Disease Resistance by Simultaneous Activation of Salicylate-and Jasmonate-Dependent Defense Pathways in Arabidopsis thaliana, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 8711–8716.

    Article  PubMed  Google Scholar 

  29. Pieterse, C.M.J., van Wees, S.C.M., van Pelt, J.A., Knoester, M., Laan, R., Gerrits, H., Weisbeek, P.J., and van Loon, L.C., A Novel Signaling Pathway Controlling Induced Systemic Resistance in Arabidopsis, Plant Cell, 1998, vol. 10, pp. 1571–1580.

    Article  PubMed  Google Scholar 

  30. Penninckx, I.A.M., Thomma, B.P.H.J., Buchala, A., Metraux, J.-P., and Broekaert, W.F., Concominant Activation of Jasmonate and Ethylene Response Pathways Is Required for Induction of a Plant Defensin Gene in Arabidopsis, Plant Cell, 1998, vol. 10, pp. 2103–2113.

    Article  PubMed  Google Scholar 

  31. Smirnoff, N., Plant Resistance to Environmental Stress, Curr. Opin. Biotechnol., 1998, vol. 9, pp. 214–219.

    Article  PubMed  Google Scholar 

  32. Hasegawa, P.M., Bressan, R.A., Zhu, J.K., and Bohnert, H.J., Plant Cellular and Molecular Responses to High Salinity, Annu. Rev. Plant Physiol. Plant Mol. Biol., 2000, vol. 51, pp. 463–499.

    Article  PubMed  Google Scholar 

  33. Taylor, C.B., Defense Responses in Plants and Animals — More of the Same, Plant Cell, 1998, vol. 10, pp. 873–876.

    Article  PubMed  Google Scholar 

  34. Kirakosyan, A., Seymour, E., Kaufman, P.B., Warber, S., Bolling, S., and Chang, S.C., Antioxidant Capacity of Polyphenolic Extracts from Leaves of Crataegus laevigata and Crataegus monogyna (Hawthorn) Subjected to Drought and Cold Stress, J. Agric. Food Chem., 2003, vol. 51, pp. 3973–3976.

    Article  PubMed  Google Scholar 

  35. Kiddle, G., Pastori, G.M., Bernard, S., Pignocchi, C., Antoniw, J., Verrier, P.J., and Foyer, C.H., Effects of Leaf Ascorbate Content on Defense and Photosynthesis Gene Expression in Arabidopsis thaliana, Antioxid. Redox. Signal., 2003, vol. 5, pp. 23–32.

    Article  PubMed  Google Scholar 

  36. Hu, C., Zawistowski, J., Ling, W., and Kitts, D.D., Black Rice (Oryza sativa L. indica) Pigmented Fraction Suppresses both Reactive Oxygen Species and Nitric Oxide in Chemical and Biological Model Systems, J. Agric. Food Chem., 2003, vol. 27, pp. 5271–5277.

    Article  Google Scholar 

  37. Gyorgy, P. and Tomarelly, R.M., Further Observations on Physiological Antioxidants, J. Biol. Chem., 1944, vol. 154, pp. 317–324.

    Google Scholar 

  38. Jayasinghe, C., Gotoh, N., Aoki, T., and Wada, S., Phenolics Composition and Antioxidant Activity of Sweet Basil (Ocimum basilicum L.), J. Agric. Food Chem., 2003, vol. 51, pp. 4442–4449.

    Article  PubMed  Google Scholar 

  39. Hara, M., Terashima, S., Fukaya, T., and Kuboi, T., Enchancement of Cold Tolerance and Inhibition of Lipid Peroxidation by Citrus Dehydrin in Transgenic Tobacco, Planta, 2003, vol. 217, pp. 290–298.

    PubMed  Google Scholar 

  40. Roberts, W.G. and Gordon, M.H., Determination of the Total Antioxidant Activity of Fruits and Vegetables by a Liposome Assay, J. Agric. Food Chem., 2003, vol. 51, pp. 1486–1493.

    Article  PubMed  Google Scholar 

  41. Rice-Evans, C.A., Miller, N.J., and Paganga, G., Antioxidant Properties of Phenolic Compounds, Trends Plant Sci., 1997, vol. 2, pp. 152–159.

    Article  Google Scholar 

  42. Kayano, S., Kikuzaki, H., Fukutsuka, N., Mitani, T., and Nakatani, N., Antioxidant Activity of Prune (Prunus domestica L.), J. Agric. Food Chem., 2002, vol. 50, pp. 3708–3712.

    Article  PubMed  Google Scholar 

  43. Stermitz, F.R., Lorenz, P., Tamara, J.N., Zenewicz, L.A., and Lewis, K., Synergy in the Medicinal Plant: Antimicrobial Action of Berberine Potentiared by 5′-Metthoxyhydrocarpin, a Multidrug Pump Inhibitor, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, pp. 1433–1437.

    Article  PubMed  Google Scholar 

  44. Smith, D.B., Roddick, J.G., and Jones, L.J., Synergism between the Potato Glycoalkaloids α-Chaconine and α-Solanine in Inhibition of Snail Feeding, Phytochemistry, 2001, vol. 57, pp. 229–234.

    Article  PubMed  Google Scholar 

  45. Edris, A.E. and Farrag, E.S., Antifungal Activity of Peppermint and Sweet Basil Essential Oils and Their Major Aroma Constituents on Some Plant Pathogenic Fungi from the Vapor Phase, Nahrung, 2003, vol. 47, pp. 117–121.

    Article  PubMed  Google Scholar 

  46. Hummelbrunner, L.A. and Isman, M.B., Acute, Sublethal, Antifeedant, and Synergistic Effects of Monoterpenoid Essential Oil Compounds on the Tobacco Cutworm Spodoptera litura (Lep., Noctuidae), J. Agric. Food Chem., 2001, vol. 49, pp. 715–720.

    Article  PubMed  Google Scholar 

  47. Plant Physiology, Salisbury R.C.W. and Delmont, F.B., Eds., California: Wadsworth Publ., 1992.

    Google Scholar 

  48. Chou, Ch.-H., Roles of Allelopathy in Plant Biodiversity and Sustainable Agriculture, CRS J. Crit. Rev. Plant Sci., 1999, vol. 18, pp. 609–636.

    Article  Google Scholar 

  49. Bais, H.P., Vepachedu, R., Gilroy, S., Callaway, R.M., and Vivanco, J.M., Allelopathy and Exotic Plant Invasion: From Molecules and Genes to Species Interactions, Science, 2003, vol. 301, pp. 1377–1380.

    Article  PubMed  Google Scholar 

  50. Reigosa, M.J., Sanchez-Moreiras, A., and Gonzalez, L., Ecophysiological Approach in Allelopathy, CRS J. Crit. Rev. Plant Sci., 1999, vol. 18, pp. 577–608.

    Article  Google Scholar 

  51. Hu, F. and Kong, C., Allelopathy of Ageranum conyzoides: 4. Effects of Meteorological Conditions on Allelopathy of Ageranum conyzoides, Ying Yong Sheng Tai Xue Bao, 2002, vol. 13, pp. 76–80.

    Google Scholar 

  52. Kato, T., Saito, N., Kashimura, K., Shinohara, M., Kurahashi, T., and Taniguchi, K., Germination and Growth Inhibitors from Wheat (Triticum aestivum L.) Husks, J. Agric. Food Chem., 2002, vol. 50, pp. 6307–6312.

    Article  PubMed  Google Scholar 

  53. Fujita, K.-I. and Kubo, I., Synergism of Polygodial and Trans-Cinnamic Acid on Inhibition of Root Elongation in Lettuce Growth Bioassays, J. Chem. Ecol., 2003, vol. 29, pp. 2253–2262.

    Article  PubMed  Google Scholar 

  54. Estabrook, E.M. and Yoder, J.I., Plant-Plant Communications: Rhizosphere Signaling between Parasitic Angiosperms and Their Hosts, Plant Physiol., 1998, vol. 116, pp. 1–7.

    Article  Google Scholar 

  55. Terras, F.R.G., Schoofs, H.M.E., Thevissen, O.R.W., Vanderleyden, J., Cammue, B.P.A., and Brorkaert, W.F., Synergistic Enhancement of the Antifungal Activity of Wheat and Barley Thionins by Radish and Oilseed Rape 2S Albumins and Barley Trypsin Inhibitors, Plant Physiol., 1993, vol. 103, pp. 1311–1319.

    PubMed  Google Scholar 

  56. Herrera-Estrella, A. and Chet, I., Chitinases in Biological Control, EXS, 1999, vol. 87, pp. 171–184.

    PubMed  Google Scholar 

  57. Bolar, J.P., Norelli, J.I., Harman, G.E., Brown, S.K., and Aldwinchkle, H.S., Synergistic Activity of Endochitinase and Exochitinase from Trichoderma atroviride (T. harzianum) against the Pathogenic Fungus (Venturia inaequalis) in Transgenic Apple Plants, Transgen. Res., 2001, vol. 10, pp. 533–543.

    Article  Google Scholar 

  58. Lorito, M., Peterbauer, C., Hayes, C.K., and Harman, G.E., Synergic Interaction between Fungal Cell Wall Degrading Enzymes and Different Antifungal Compounds Enhances Inhibition of Spore Germination, Microbiology, 1994, vol. 140, pp. 623–629.

    PubMed  Google Scholar 

  59. Karasuda, S., Tanaka, S., Kajihara, H., Yamamoto, Y., and Koga, D., Plant Chitinase as a Possible Biocontrol Agent for Use Instead of Chemical Fungicides, BioSci. Biotechnol. Biochem., 2003, vol. 67, pp. 221–224.

    Article  PubMed  Google Scholar 

  60. Boller, T., Ethylene and the Regulation of Antifungal Hydrolases in Plants, Oxford Survey Plant Mol. Cell Biol., 1988, vol. 5, pp. 145–174.

    Google Scholar 

  61. Sela-Buurlage, M.B., Ponstein, A.S., Bres-Vloemans, S.A., Melchers, L.S., van den Elsen, P., and Cornelissen, B., Only Specific Tobacco (Nicotiana tabacum) Chitinases and β-1,3-Glucanases Exhibit Antifungal Activity, Plant Physiol., 1993, vol. 101, pp. 857–863.

    PubMed  Google Scholar 

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Translated from Fiziologiya Rastenii, Vol. 52, No. 4, 2005, pp. 614–621.

Original Russian Text Copyright © 2005 by Ryabushkina.

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Ryabushkina, N.A. Synergism of Metabolite Action in Plant Responses to Stresses. Russ J Plant Physiol 52, 547–552 (2005). https://doi.org/10.1007/s11183-005-0081-y

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