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Compost enhances plant resistance against the bacterial wilt pathogen Ralstonia solanacearum via up-regulation of ascorbate-glutathione redox cycle

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Abstract

The interactions between the pathogen Ralstonia solanacearum and potato Solanum tuberosum plants were studied to investigate the reactive oxygen species metabolic system and ascorbate (ASC)-glutathione (GSH) redox cycle in response to compost application. Single potato eyepieces were germinated and grown in pots containing sandy soil with or without compost at a rate of 7.5 g kg−1 soil. Non-compost- and compost-treated plants (CTP) were inoculated with R. solanacearum 25 days after planting and then analyzed after 10 days, unless otherwise stated. The present results revealed that pathogen infection caused a remarkable decrease in plant growth related parameters and productivity and an increase in disease incidence. However, under these conditions compost had substantially improved plant growth and decreased disease incidence and bacterial population. R. solanacearum resulted in significant enhancement in the activities of NADPH oxidase, lipoxygenase, the production rate of superoxide and hydroxyl radicals, levels of hydrogen peroxide, membrane lipid peroxidation, and protein oxidation indicating the induction of oxidative stress in potato roots. However, the pathogen-mediated enhancement in indices of oxidative stress was considerably decreased by compost application, which enhanced the activities of ascorbate peroxidase (APX, EC 1.11.1.11), monodehydroascorbate reductase (MDHAR, EC 1.6.5.4), dehydroascorbate reductase (DHAR, EC 1.8.5.1) and glutathione reductase (GR, EC 1.6.4.2) in infected potato plants, implying a better ROS-scavenging activity. Data also indicated that there were general increases in ASC and GSH content in infected compost treated plants, but non-compost treated ones significantly had lower levels of such redox metabolites. In addition, significantly higher ratios of ASC/DHA (dehydroascorbate) and GSH/GSSG (glutathione disulphide) were generally found in CTP than in non-compost treated-ones. The obtained results suggest that compost provides effective protection against the Ralstonia bacterial pathogen via up-regulation of the capacity of the ASC-GSH cycle and modulation of the cellular redox status, thereby eliminating ROS damage and sustaining membrane stability.

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References

  • Aldahmani, J. H., Abbasi, P. A., Sahin, F., Hoitink, H. A. J., & Miller, S. A. (2005). Reduction of bacterial leaf spot severity on radish, lettuce, and tomato plants grown in compost-amended potting mixes. Canadian Journal of Plant Pathology, 27, 186–193.

    Article  Google Scholar 

  • Amaya-Carpio, L., Davies, F. T., Jr., Fox, T., & He, C. (2009). Arbuscular mycorrhizal fungi and organic fertilizer influence photosynthesis, root phosphatase activity, nutrition, and growth of Ipomoea carnea ssp. fistulosa. Phtosynthetica, 47, 1–10.

    Article  CAS  Google Scholar 

  • Antolín, M. C., Muro, I., & Sánchez-Díaz, M. (2010). Application of sewage sludge improves growth, photosynthesis and antioxidant activities of nodulated alfalfa plants under drought conditions. Environmental and Experimental Botany, 68, 75–82.

    Article  Google Scholar 

  • Asada, K. (1999). The water-water cycle in chloroplasts: scavenging of active oxygens and dissipation of excess photons. Annual Review of Plant Physiology & Plant Molecular Biology, 50, 601–639.

    Article  CAS  Google Scholar 

  • Bastida, F., Kandeler, E., Moreno, J. L., Ros, M., Garcia, C., & Hernandez, T. (2008). Application of fresh and composted organic wastes modifies structure, size and activity of soil microbial community under semiarid climate. Applied Soil Ecology, 40, 318–329.

    Article  Google Scholar 

  • Bonanomi, G., Antignani, V., Pane, C., & Scala, F. (2007). Suppression of soilborne fungal diseases with organic amendments. Journal of Plant Pathology, 89, 311–340.

    Google Scholar 

  • Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254.

    Article  PubMed  CAS  Google Scholar 

  • Brash, A. R. (1999). Lipoxygenases: occurrence, functions, catalysis, and acquisition of substrate. Journal of Biological Chemistry, 274, 23679–23682.

    Article  PubMed  CAS  Google Scholar 

  • Cakmak, I., & Marschner, H. (1988). Zinc-dependent changes in electron-spin-resonance signals, NADPH oxidase and plasma-membrane permeability in cotton roots. Physiologia Plantarum, 73, 182–186.

    Article  CAS  Google Scholar 

  • Crecchio, C., Curci, M., Mininni, R., Ricciuti, P., & Ruggiero, P. (2001). Short term effects of municipal solid waste compost amendments on soil carbon and nitrogen content, some enzyme activities and genetic diversity. Biology and Fertility of Soils, 34, 311–318.

    Article  CAS  Google Scholar 

  • Duong, T. T. T., Verma, S. L., Penfold, C., & Marschner, P. (2013). Nutrient release from composts into the surrounding soil. Geoderma, 195–196, 42–47.

    Article  Google Scholar 

  • Ederli, M., Leuschen, M. P., Eirefaey, H., Hamada, F. M., & Rojas, P. (1996). The antioxidant properties of zinc and metallothionein. Neurochemistry International, 29, 159–166.

    Article  Google Scholar 

  • Elstner, F. F., & Heupel, C. (1976). Inhibition of nitrite formation from hydroxylammonium chloride: a simple assay for superoxide dismutase. Analytical Biochemistry, 70, 616–620.

    Article  PubMed  CAS  Google Scholar 

  • Ferraras, L., Gomez, E., Toresani, S., Firpo, I., & Rotondo, R. (2006). Effect of organic amendments on some physical, chemical and biological properties in a horticultural soil. Bioresource Technology, 97, 635–640.

    Article  Google Scholar 

  • Flores-Cruz, Z., & Allen, C. (2009). Ralstonia solanacearum encounters an oxidative environment during tomato infection. Molecular Plant - Microbe Interactions, 22, 773–782.

    Article  PubMed  CAS  Google Scholar 

  • Fotopoulos, V., Ziogas, V., Tanou, G., & Molassiotis, A. (2010). Involvement of AsA/DHA and GSH/GSSG ratios in gene and protein expression and in the activation of defence mechanisms under abiotic stress conditions. In N. A. Anjum, M. T. Chan, & S. Umar (Eds.), Ascorbate-glutathione pathway and stress tolerance in plants (pp. 265–302). Dordrecht: Springer.

    Chapter  Google Scholar 

  • Foyer, C. H., & Noctor, G. (2009). Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxidants and Redox Signaling, 11, 861–905.

    Article  PubMed  CAS  Google Scholar 

  • Foyer, C. H., & Noctor, G. (2011). Ascorbate and glutathione: the heart of the redox Hub. Plant Physiology, 155, 2–18.

    Article  PubMed  CAS  Google Scholar 

  • Foyer, C. H., Trebst, A., & Noctor, G. (2008). Signaling and integration of defense functions of tocopherol, ascorbate and glutathione. In B. Demmig-Adams, W. W. Adams III, A. K. Mattoo (Eds.), Photoprotection, photoinhibition, gene regulation, and environment (pp. 241–268). Dordrecht, The Netherlands: Springer Science + Business Media B.V.

  • French, E., Gutarra, L., Aley, P., & Elphinstone, J. (1995). Culture media for Pseudomonas solanacearum isolation, identification and maintenance. Fitopatologia, 30, 126–130.

    Google Scholar 

  • Fuchs, J. G., Baier, U., Berner, A., Mayer, J., Tamm, L., & Schleiss, K. (2006). Potential of different composts to improve soil fertility and plant health. In E. Kraft, W. Bidlingmaier, M. de Bertoldi, L. F. Diaz, J. Barth (Eds.), Biological waste management: From local to global (pp 507–518). Proceedings of the International Conference ORBIT 2006, chapter Part 2.

  • Fujiwara, K., Aoyama, C., Takano, M., & Shinohara, M. (2012). Suppression of Ralstonia solanacearum bacterial wilt disease by an organic hydroponic system. Journal of General Plant Pathology, 78, 217–220.

    Article  Google Scholar 

  • Hayward, A. C. (1991). Biological and epidemiology of bacterial wilt caused by Pseudomonas solanacearum. Annual Review of Phytopatholog, 29, 65–87.

    Article  CAS  Google Scholar 

  • Hayward, A. C. (2000). Ralstonia solanacearum. In J. Lederberg (Ed.), Encyclopedia of microbiology Vol. 4 (pp. 32–42). San Diego: Academic.

    Google Scholar 

  • Heath, R. L., & Packer, L. (1968). Photoperoxidation in isolated chloroplasts I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics, 125, 189–198.

    Article  PubMed  CAS  Google Scholar 

  • Hiddink, G. A., van Bruggen, A. H. C., Termorshuizen, A. J., Raajjmakers, J. M., & Semenov, A. V. (2005). Effect of organic management of soils on suppressiveness to Gaeumannomyces graminis var. tritici and its antagonist, Pseudomonas fluorescens. European Journal of Plant Pathology, 113, 417–435.

    Article  Google Scholar 

  • Hissin, P. J., & Hilf, R. (1976). A fluorometric method for determination of oxidized and reduced glutathione in tissues. Analalytical Biochemistry, 74, 214–226.

    Article  CAS  Google Scholar 

  • Hodges, D. M., Andrews, C. J., Johnson, D. A., & Hamilton, R. I. (1996). Antioxidant compound responses to chilling stress in differentially sensitive inbred maize 23 lines. Physiologia Plantarum, 98, 685–692.

    Article  CAS  Google Scholar 

  • Hoitink, H. A. J., & Krause, M. S. (2001). Systemic resistance induced in plants against diseases by composts. In Orbit and spanish waste club (ed) Proceedings of ORBIT 2001, May 9–12, Sevilla, Spain, pp 143–146.

  • Jindo, K., Martim, S. A., Navarro, E. C., Pérez-Alfocea, F., Hernandez, T., Garcia, C., et al. (2012). Root growth promotion by humic acids from composted and non-composted urban organic wastes. Plant and Soil, 353, 209–220.

    Article  CAS  Google Scholar 

  • Joshi, D., Hooda, K. S., Bhatt, J. C., Mina, B. L., & Gupta, H. S. (2009). Suppressive effects of composts on soil-borne and foliar diseases of French bean in the field in the western Indian Himalayas. Crop Protection, 28, 608–615.

    Article  Google Scholar 

  • Kavroulakis, N., Ehaliotis, C., Ntougias, S., Zervakis, G. I., & Papadopou, K. K. (2005). Local and systemic resistance against fungal pathogens of tomato plants elicited by a compost derived from agricultural residues. Physiological and Molecular Plant Pathology, 66, 163–174.

    Article  Google Scholar 

  • Kempe, J., & Sequeira, L. (1983). Biological control of bacterial wilt of potatoes: attempts to induce resistance by treating tubes with bacteria. Plant Disease, 67, 499–501.

    Article  Google Scholar 

  • Kiddle, G., Pastori, G. M., Bernard, S., Pignocch, C., Antoniw, J., Verrier, P. J., et al. (2003). Effects of leaf ascorbate content on defence and photosynthesis gene expression in Arabidopsis thaliana. Antioxiants and Redox Signalling, 5, 3–32.

    Article  Google Scholar 

  • Kim, K. D., Nemec, S., & Musson, G. (1997). Effects of composts and soil amendments on soil microflora and Phytophthora root and crown rot of bell pepper. Crop Protection, 16, 165–172.

    Article  Google Scholar 

  • Krivosheeva, A., Tao, D. L., Ottander, C., Wingsle, G., Dube, S. L., & Öquist, G. (1996). Cold acclimation and photoinhibition of photosynthesis in Scots pine. Planta, 200, 296–305.

    Article  CAS  Google Scholar 

  • Larchevêque, M., Ballini, C., Baldy, V., Korboulewsky, N., Ormeño, E., Nicolas, et al. (2010). Restoration of a Mediterranean postfire shrubland: plant functional responses to organic soil amendment. Restoration Ecology, 18, 729–741.

    Article  Google Scholar 

  • Latowski, D., Surówka, E., & Strzałka, K. (2010). Regulatory role of components of ascorbate-glutathione pathway in plant stress tolerance. In N. A. Anjum et al. (Eds.), Ascorbate-glutathione pathway and stress tolerance in plants. Dordrecht, The Netherlands: Springer Science+Business Media B.V.

  • Lutts, S., Kinet, J. M., & Bouharmont, J. (1996). NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Annals of Botany, 78, 389–398.

    Article  CAS  Google Scholar 

  • Mandal, S., Das, R. K., & Mishra, S. (2011). Differential occurrence of oxidative burst and antioxidative mechanism in compatible and incompatible interactions of Solanum lycopersicum and Ralstonia solanacearum. Plant Physiology and Biochemistry, 49, 117–123.

    Article  PubMed  CAS  Google Scholar 

  • Martínez, J. P., & Araya, H. (2010). Ascorbate-glutathione cycle: Enzymatic and non-enzymatic integrated mechanisms and its biomolecular regulation. In: Anjum, N. A., et al. (Eds.), Ascorbate-glutathione pathway and stress tolerance in plants (pp. 303–322). Dordrecht, The Netherlands: Springer Science+Business Media B.V.

  • Minz, D., Green, S. J., Ofek, M., & Hadar, Y. (2010). Compost microbial populations and interactions with Plants. Insam H. et al. (Eds.), Microbes at work (pp 232–251). Heidelberg: Springer-Verlag Berlin Heidelberg.

  • Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends Plant Science, 7, 405–410.

    Article  CAS  Google Scholar 

  • Mittler, R., Vanderauwera, S., Gollery, M., & Van Breusegem, F. (2004). Reactive oxygen gene network of plants. Trends in Plant Science, 9, 490–498.

    Article  PubMed  CAS  Google Scholar 

  • Mittova, V., Volokita, M., Guy, M., & Tal, M. (2000). Activities of SOD and the ascorbate-glutathione cycle enzymes in subcellular compartments in leaves and roots of the cultivated tomato and its wild salt-tolerant relative Lycopersicon pennellii. Physiologia Plantarum, 110, 42–51.

    Article  CAS  Google Scholar 

  • Moller, I. M. (2001). Plant mitochondria and oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. Annual Review of Plant Physiology and Plant Molecular Biology, 52, 561–591.

    Article  PubMed  CAS  Google Scholar 

  • Montalba, R., Arriagada, C., Alvear, M., & Zúñiga, G. E. (2010). Effects of conventional and organic nitrogen fertilizers on soil microbial activity, mycorrhizal colonization, leaf antioxidant content, and Fusarium wilt in highbush blueberry (Vaccinium corymbosum L.). Scientia Horticulturae, 125, 775–778.

    Article  Google Scholar 

  • Mylavarapu, R. S., & Zinati, G. M. (2009). Improvement of soil properties using compost for optimum parsley production in sandy soils. Scientia Horticulturae, 120, 426–430.

    Article  Google Scholar 

  • Nakano, Y., & Asada, K. (1981). Hydrogen peroxide is scavenged by ascorbate specific peroxidase in spinch chloroplasts. Plant and Cell Physiology, 22, 679–690.

    Google Scholar 

  • Noble, R., & Coventry, E. (2005). Suppression of soil-borne plant diseases with composts: a review. Biocontrol Science and Technology, 15, 3–20.

    Article  Google Scholar 

  • Noctor, G., & Foyer, C. H. (1998). Ascorbate and glutathione: keeping active oxygen under control. Annual Review of Plant Physiology and Plant Molecular Biology, 49, 249–279.

    Article  PubMed  CAS  Google Scholar 

  • Ntougias, S., Papadopoulou, K. K., Zervakis, G. I., Kavroulakis, N., & Ehaliotis, C. (2008). Suppression of soil borne pathogens of tomato by composts derived from agro-industrial waste abundant in Mediterranean regions. Biology and Fertility of Soils, 44, 1081–1090.

    Article  Google Scholar 

  • Patterson, B. D., Macrae, E. A., & Ferguson, I. B. (1984). Estimation of hydrogen peroxide in plants extracts using titanium (IV). Annual Review of Biochemistry, 139, 487–492.

    Article  CAS  Google Scholar 

  • Reddy, P. S., Kumar, T. C., Reddy, M. N., Sarada, C., & Reddanna, P. (2000). Differential formation of octadecadienoic acid and octadecatrienoic acid products in control and injured/infected potato tubers. Biochimica et Biophysica Acta, 1483, 294–300.

    Article  PubMed  CAS  Google Scholar 

  • Reymond, P., & Farmer, E. E. (1998). Jasmonate and salicylate as global signals for defence gene expression. Current Opinion in Plant Biology, 1, 404–411.

    Article  PubMed  CAS  Google Scholar 

  • Reznick, A. Z., & Packer, L. (1994). Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods in Enzymology, 233, 357–363.

    Article  PubMed  CAS  Google Scholar 

  • Sang, M. K., & Kim, K. D. (2011). Biocontrol activity and primed systemic resistance by compost water extracts against anthracnoses of pepper and cucumber. Phytopathology, 101, 732–740.

    Article  PubMed  CAS  Google Scholar 

  • Schell, M. A. (2000). Control of virulence and pathogenicity genes of Ralstonia solanacearum by an elaborate sensory network. Annual Review of Phytopathology, 38, 263–292.

    Article  PubMed  CAS  Google Scholar 

  • Sečenji, M., Hideg, É., Bebes, A., & Gyrgyey, J. (2010). Transcriptional differences in gene families of the ascorbate-glutathione cycle in wheat during mild water deficit. Plant Cell Reports, 29, 37–50.

    Article  PubMed  Google Scholar 

  • Suárez-Estrella, F., Vargas-García, C., Lópeza, M. J., Capel, C., & Moreno, J. (2007). Antagonistic activity of bacteria and fungi from horticultural compost against Fusarium oxysporum f. sp. melonis. Crop Protection, 26, 46–53.

    Article  Google Scholar 

  • Tejada, M., Garcia, C., Gonzalez, J.L., & Hernandez, M.T. (2006). Use of organic amendment as a strategy for saline soil remediation: influence on the physical, chemical and biological properties of soil. Soil Biology & Biochemistry, 38, 1413–1421.

    Google Scholar 

  • Tejada, M., Hernandez, M. T., & Garcia, C. (2009). Soil restoration using composted plant residues: effects on soil properties. Soil and Tillage Research, 102(1), 109–117.

    Article  Google Scholar 

  • Temorshuizen, A. J., Van Rijn, E., Van der Gaag, D. J., Alabouvette, C., Chen, Y., Lgerlof, J., et al. (2006). Suppressiveness of 18 composts against 17 pathosystems: variability in pathogen response. Soil Biology & Biochemistry, 38, 2461–2477.

    Article  Google Scholar 

  • Tilston, E. L., Pitt, D., & Groenhof, A. C. (2002). Composted recycled organic matter suppresses soil-borne diseases of field crops. New Phytologist, 154, 731–740.

    Article  CAS  Google Scholar 

  • Von Tiedemann, A. (1997). Evidence for a primary role of active oxygen species in induction of host cell death during infection of bean leaves with Botrytis cinerea. Physiological and Molecular Plant Pathology, 50, 151–166.

    Article  CAS  Google Scholar 

  • Walker, D. J., & Bernal, M. P. (2008). The effects of olive mill waste compost and poultry manure on the availability and plant uptake of nutrients in a highly saline soil. Bioresource Technology, 99, 396–403.

    Article  PubMed  CAS  Google Scholar 

  • Walters, D., Walsh, D., Newton, A., & Lyon, G. (2005). Induced resistance for plant disease control: maximizing the efficacy of resistance elicitors. Phytopathology, 95, 1368–1373.

    Article  PubMed  CAS  Google Scholar 

  • Wang, S. Y., Chi-Tsun, C., Sciarappa, W., Wang, C. Y., & Camp, M. J. (2008). Fruit quality, antioxidant capacity, and flavonoid content of organically and conventionally grown blueberries. Journal of Agricultural and Food Chemistry, 56, 5788–5794.

    Article  PubMed  CAS  Google Scholar 

  • Welke, S. E. (2004). The effect of compost extract on the yield of strawberries and the severity of Botrytis cinerea. Journal of Sustainable Agriculture, 25, 57–68.

    Article  Google Scholar 

  • Yogev, A., Raviv, M., Hadar, Y., Cohen, R., Wolf, S., Gil, L., et al. (2010). Induced resistance as a putative component of compost suppressiveness. Biological Control, 54, 46–51.

    Article  Google Scholar 

  • Zhang, W., Dick, W. A., & Hoitink, H. A. J. (1996). Compost-induced systemic acquired resistance in cucumber to Pythium root rot and anthracnose. Phytopathology, 86, 1066–1070.

    Article  Google Scholar 

  • Zucconi, F., Pera, A., Forte, M., & Debertoldi, M. (1981). Evaluating toxicity of immature compost. Biocycle, 22, 54–57.

    Google Scholar 

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Acknowledgments

This work was supported by the Department of the Environmental Affairs and Community Services, Suez Canal Univ. # 127/2008.

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  1. Botany Department, Faculty of Agriculture, Suez Canal University, Ismailia, 41522, Egypt

    Sahar A. Youssef & Kamel A. H. Tartoura

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Youssef, S.A., Tartoura, K.A.H. Compost enhances plant resistance against the bacterial wilt pathogen Ralstonia solanacearum via up-regulation of ascorbate-glutathione redox cycle. Eur J Plant Pathol 137, 821–834 (2013). https://doi.org/10.1007/s10658-013-0291-7

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