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Vinegar residue compost as a growth substrate enhances cucumber resistance against the Fusarium wilt pathogen Fusarium oxysporum by regulating physiological and biochemical responses

Abstract

Fusarium wilt caused by the fungus Fusarium oxysporum f. sp. cucumerinum (FOC) is the most severe soil-borne disease attacking cucumber. To assess the positive effects of vinegar residue substrate (VRS) on the growth and incidence of Fusarium wilt on cucumber, we determined the cucumber growth parameters, disease severity, defense-related enzyme and pathogenesis-related (PR) protein activities, and stress-related gene expression levels. In in vitro and pot experiments, we demonstrated the following results: (i) the VRS extract exhibited a higher biocontrol activity than that of peat against FOC, and significantly improved the growth inhibition of FOC, with values of 48.3 %; (ii) in response to a FOC challenge, antioxidant enzymes and the key enzymes of phenylpropanoid metabolic activities, as well as the PR protein activities in the roots of cucumber, were significantly increased. Moreover, the activities of these proteins were higher in VRS than in peat; (iii) the expression levels of stress-related genes (including glu, pal, and ethylene receptor) elicited responses to the pathogens inoculated in cucumber leaves; and (iv) the FOC treatment significantly inhibited the growth of cucumber seedlings. Moreover, all of the growth indices of plants grown in VRS were significantly higher than those grown in peat. These results offer a new strategy to control cucumber Fusarium wilt, by upregulating the activity levels of defense-related enzymes and PR proteins and adjusting gene expression levels. They also provide a theoretical basis for VRS applications.

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References

  1. Alabouvette C, Olivain C, Steinberg C (2006) Biological control of plant diseases: the European situation. European journal of plant pathology 114:329–341

  2. Beaudoin-Eagan LD, Thorpe TA (1985) Tyrosine and phenylalanine ammonia lyase activities during shoot initiation in tobacco callus cultures. Plant Physiology 78:438–441

  3. Bernal-Vicente A, Ros M, Tittarelli F, Intrigliolo F, Pascual J (2008) Citrus compost and its water extract for cultivation of melon plants in greenhouse nurseries. Evaluation of nutriactive and biocontrol effects. Bioresource technology 99:8722–8728

  4. Blaya J, López-Mondéjar R, Lloret E, Pascual JA, Ros M (2013) Changes induced by Trichoderma harzianum in suppressive compost controlling Fusarium wilt. Pesticide biochemistry and physiology 107:112–119

  5. Boller T, Gehri A, Mauch F, Vögeli U (1983) Chitinase in bean leaves: induction by ethylene, purification, properties, and possible function. Planta 157:22–31

  6. Borrero C, Trillas MI, Ordovás J, Tello JC, Avilés M (2004) Predictive factors for the suppression of Fusarium wilt of tomato in plant growth media. Phytopathology 94:1094–1101

  7. Borrero C, Infantes MJ, González E, Aviles M, Tello JC, Urrestarazu-Gavilan M (2005) Relation between suppressiveness to tomato Fusarium wilt and microbial populations in different growth media. Acta Horticulturae 697:425

  8. Borrero C, Trillas I, Avilés M (2009) Carnation Fusarium wilt suppression in four composts. European Journal of Plant Pathology 123:425–433

  9. Britton C, Mehley AC (1955) Assay of catalase and peroxidase. Method in enzymology 2:764–775

  10. Çakır B, Gül A, Yolageldi L, Özaktan H (2014) Response to Fusarium oxysporum f.sp. radicis-lycopersici in tomato roots involves regulation of SA- and ET-responsive gene expressions. European Journal of Plant Pathology 139:379–391

  11. Cheng F, Sun ZH, Zhao YG, Li SJ (2001) Analysis of physical and chemical properties of reed residue substrate. Journal of Nanjing Agricultural University 24:19–22 (in Chinese)

  12. Conrath U, Pieterse CM, Mauch-Mani B (2002) Priming in plant–pathogen interactions. Trends in plant science 7:210–216

  13. Craft CM, Nelson EB (1996) Microbial properties of composts that suppress damping-off and root rot of creeping bentgrass caused by Pythium graminicola. Applied and Environmental Microbiology 62:1550–1557

  14. Danon M, Zmora-Nahum S, Chen Y, Hadar Y (2007) Prolonged compost curing reduces suppression of Sclerotium rolfsii. Soil Biology and Biochemistry 39:1936–1946

  15. De Cal A, Pascual S, Larena I, Melgarejo P (1995) Biological control of Fusarium oxysporum f. sp. lycopersici. Plant pathology 44:909–917

  16. Du NS, Shi L, Du LT, Yuan YH, Li B, Sang T, Sun J, Shu S, Guo SR (2015) Effect of vinegar residue compost amendments on cucumber growth and Fusarium wilt. Environmental Science and Pollution Research 22:19133–19141

  17. Giannopolitis CN, Ries SK (1977) Superoxide dismutases I. Occurrence in higher plants Plant physiology 59:309–314

  18. Graham MY, Weidner J, Wheeler K, Pelow MJ, Graham TL (2003) Induced expression of pathogenesis-related protein genes in soybean by wounding and the Phytophthora sojae cell wall glucan elicitor. Physiological and molecular plant pathology 63:141–149

  19. Guo SR (2003) Soilless culture. China Agriculture, Beijing (in Chinese)

  20. Gupta KJ, Mur LA, Brotman Y (2014) Trichoderma asperelloides suppresses nitric oxide generation elicited by Fusarium oxysporum in Arabidopsis roots. Molecular plant-microbe interactions 27:307–314

  21. Hadar Y (2011) Suppressive compost: when plant pathology met microbial ecology. Phytoparasitica 39:311–314

  22. Ham KS, Kauffmann S, Albersheim P, Darvill AG (1991) Host pathogen Interactions XXXIX. A soybean pathogenesis-related protein with b-1, 3-glucanase activity releases phytoalexin elicitor-active heat stable fragments from fungal walls. Mol. Plant-Microbe Interact 4:545–552

  23. Hoitink HAJ, Boehm MJ (1999) Biocontrol within the context of soil microbial communities: a substrate-dependent phenomenon. Annual review of phytopathology 37:427–446

  24. Hoitink HAJ, Schmitthenner AF, Herr LJ (1975) Composted bark for control of root rot in ornamentals. Ohio report on research and development in agriculture, home economics, and natural resources

  25. Huang S, Li R, Zhang Z, Li L, Gu X, Fan W, Lucas WJ, Wang X, Xie B, Ni P et al (2009) The genome of the cucumber, Cucumis sativus L. Nature Genetics 41:1275–1281

  26. Huang X, Shi D, Sun F, Lu H, Liu J, Wu W (2012) Efficacy of sludge and manure compost amendments against Fusarium wilt of cucumber. Environmental Science and Pollution Research 19:3895–3905

  27. Khan W, Prithiviraj B, Smith DL (2003) Chitosan and chitin oligomers increase phenylalanine ammonia-lyase and tyrosine ammonia-lyase activities in soybean leaves. Journal of plant physiology 160:859–863

  28. King SR, Davis AR, Liu W, Levi A (2008) Grafting for disease resistance. HortScience 43:1673–1676

  29. Kochba J, Lavee S, Spiegel-Roy P (1977) Differences in peroxidase activity and isoenzymes in embryogenic ane non-embryogenic ‘Shamouti’orange ovular callus lines. Plant and Cell Physiology 18:463–467

  30. Larkin RP, Fravel DR (1998) Efficacy of various fungal and bacterial biocontrol organisms for control of Fusarium wilt of tomato. Plant disease 82:1022–1028

  31. Li HS, Sun Q, Zhao SJ, Zhang WH (2000) Principles and techniques of plant physiological biochemical experiment. Higher Education, Beijing, pp 195–197

  32. Li YZ, Zheng XH, Tang HL, Zhu JW, Yang JM (2003) Increase of ß-1, 3-glucanase and chitinase activities in cotton callus cells treated by salicylic acid and toxin of Verticillium dahliae

  33. Liu CJ, Guo SR, Wang CY, Shu S, Liu SR, Cheng YJ (2010) Vinegar residue substrate as component of mixed substrate for pepper seedling growth. Acta Horticulturae Sinica 37:559–566 (in Chinese)

  34. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408

  35. Lumsden RD, Lewis JA, Millner PD (1983) Effect of composted sewage sludge on several soilborne pathogens and diseases. Phytopathology 73:1543–1548

  36. Medina E, Garcia V, Cuevas E (1990) Sclerophylly and oligotrophic environments: relationships between leaf structure, mineral nutrient content, and drought resistance in tropical rain forests of the upper Rio Negro region. Biotropica 51–64

  37. Nadeem SM, Ahmad M, Zahir ZA, Javaid A, Ashraf M (2014) The role of mycorrhizae and plant growth promoting rhizobacteria (PGPR) in improving crop productivity under stressful environments. Biotechnology advances 32:429–448

  38. Nakano Y, Asada K (1981) Hydrogen Peroxide is Scavenged by Ascorbate-specific Peroxidase in Spinach Chloroplasts. Plant and Cell Physiology 22:867–880

  39. Nelson N (1944) A photometric adaptation of the Somogyi method for the determination of glucose. J biol Chem 153:375–380

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

  41. Pareek SS, Ravi I, Sharma V (2013) Induction of β-1,3-glucanase and chitinase in Vigna aconitifolia inoculated with Macrophomina phaseolina. Journal of Plant Interactions 9:434–439

  42. Peltier AJ, Grau CR (2008) The influence of light on relationships between sclerotinia stem rot of soybean in field and controlled environments. Plant Disease 92:1510–1514

  43. Pugliese M, Gullino M, Garibaldi A, Benetti A (2014) Use of compost from different origins to control soilborne pathogens in potted vegetables. VIII International Symposium on Chemical and Non-Chemical Soil and Substrate Disinfestation 1044:145–148

  44. Qiu Z, Guo J, Zhu A, Zhang L, Zhang M (2014) Exogenous jasmonic acid can enhance tolerance of wheat seedlings to salt stress. Ecotoxicol Environ Saf 104:202–208

  45. Roe NE, Stoffella PJ, Graetz D (1997) Composts from various municipal solid waste feedstocks affect vegetable crops. II. Growth, yields, and fruit quality. Journal of the American Society for Horticultural Science 122:433–437

  46. Somogyi M (1952) Notes on sugar determination. Journal of biological chemistry 195:19–23

  47. Song XX, Shu S, Guo SR, Zhang Y, Hu R (2013) Effects of vinegar residue mixed substrates on growth and yield of mini-cucumber. Journal of Changjiang Vegetables 10:30–34, in Chinese

  48. Stall RE, Hall CB (1984) Chlorosis and ethylene production in pepper leaves infected by Xanthomonas campestris pv. vesicatoria. Phytopathology 74:373–375

  49. Szczech MM (1999) Suppressiveness of vermicompost against Fusarium wilt of tomato. Journal of Phytopathology 147:155–161

  50. Ting ASY, Chai JY (2015) Chitinase and β-1,3-glucanase activities of Trichoderma harzianum in response towards pathogenic and non-pathogenic isolates: Early indications of compatibility in consortium. Biocatalysis and Agricultural Biotechnology 4:109–113

  51. Tsuge S, Ochiai H, Inoue Y, Oku T, Tsuno K, Kaku H, Kubo Y (2004) Involvement of phosphoglucose isomerase in pathogenicity of Xanthomonas oryzae pv. oryzae. Phytopathology 94:478–483

  52. Vavrina CS, Ozores-Hampton M, Armbrester K, Pena M (1996) Spent mushroom compost and biological amendments as an alternative to soilless media. Southwest Florida Research and Education Center Report-Veg 96

  53. Wei G, Kloepper JW, Tuzun S (1991) Induction of systemic resistance of cucumber to Colletotrichum orbiculare by select strains of plant growth-promoting rhizobacteria. Phytopathology 81:1508–1512

  54. Xue D, Huang X (2013) The impact of sewage sludge compost on tree peony growth and soil microbiological, and biochemical properties. Chemosphere 93:583–589

  55. Zhang S, Reddy MS, Kokalis-Burelle N, Wells LW, Nightengale SP, Kloepper JW (2001) Lack of induced systemic resistance in peanut to late leaf spot disease by plant growth-promoting rhizobacteria and chemical elicitors. Plant Disease 85:879–884

  56. Zhang Y, Sun J, Guo SR (2012) Effects of vinegar residue mixed substrates on growth and photosynthesis of tomato seedlings. Journal of Jiangsu Agricultural Science 40:149–151 (in Chinese)

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Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (Grant Nos. 31401919, 31471869, and 31272209), the China Earmarked Fund for Modern Agro-industry Technology Research System (CARS-25-C-03), and the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD). This study was also sponsored by the Research Fund for the Doctoral Program of Higher Education (20130097120015).

Author information

Correspondence to Shirong Guo.

Additional information

Lu Shi and Nanshan Du should be considered cofirst authors.

Lu Shi and Nanshan Du contributed equally to this work.

Responsible editor: Philippe Garrigues

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Shi, L., Du, N., Yuan, Y. et al. Vinegar residue compost as a growth substrate enhances cucumber resistance against the Fusarium wilt pathogen Fusarium oxysporum by regulating physiological and biochemical responses. Environ Sci Pollut Res 23, 18277–18287 (2016). https://doi.org/10.1007/s11356-016-6798-7

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Keywords

  • Vinegar residue substrate
  • Cucumber
  • Fusarium wilt
  • Growth suppressive effect
  • Defense-related enzyme
  • Gene expression