High doses of melatonin confer abiotic stress tolerance to phytopathogenic fungi grown in vitro

Melatonin enhances phytopathogenic fungal growth

  • Andrew Pio Madigan Department of Animal, Plant and Soil Sciences, La Trobe University, AgriBio, Centre for AgriBiosciences, La Trobe University, Bundoora, VIC 3086, Australia and Department of Physiology, Anatomy and Microbiology, La Trobe University, Bundoora, VIC 3086, Australia
  • Christopher Harris Department of Animal, Plant and Soil Sciences, La Trobe University, AgriBio, Centre for AgriBiosciences, La Trobe University, Bundoora, VIC 3086, Australia
  • Frank Bedon Department of Animal, Plant and Soil Sciences, La Trobe University, AgriBio, Centre for AgriBiosciences, La Trobe University, Bundoora, VIC 3086, Australia
  • Ashley E Franks Department of Physiology, Anatomy and Microbiology, La Trobe University, Bundoora, VIC 3086, Australia and Centre for Future Landscapes, La Trobe, University, Bundoora, VIC 3086, Australia
  • Kim M Plummer Department of Animal, Plant and Soil Sciences, La Trobe University, AgriBio, Centre for AgriBiosciences, La Trobe University, Bundoora, VIC 3086, Australia
Keywords: Melatonin, plant pathogen, abiotic stress, ethanol, cold, antioxidant, reactive oxygen species (ROS)

Abstract

Melatonin is a secondary metabolite produced in all domains of life. Exogenous melatonin triggers defence mechanisms in plants that enhance abiotic stress tolerance. However, knowledge regarding the role of melatonin as a signal or an antioxidant in microbes is lacking. We investigated the in vitro growth responses of three phytopathogenic fungi, Sclerotinia sclerotiorum, Botrytis cinerea and Fusarium oxysporum f.sp. vasinfectum, to abiotic stress (2.5% ethanol with/without cold priming) under varying concentrations of melatonin. Melatonin at high concentrations (1000 – 2000 µM) partially restored fungal growth under stress, compared to controls, suggesting a role for melatonin in alleviating the impacts of stress exposure. Understanding how melatonin impacts fungal growth during stress conditions will be important for future applications using melatonin as a tool for crop protection.


References

1. Gonzalez-Fernandez R, Jorrin-Novo JV (2012) Contribution of proteomics to the study of plant pathogenic fungi. J. Proteome Res. 11: 3-16.
2. Michielse CB, Rep M (2009) Pathogen profile update: Fusarium oxysporum. Mol. Plant Pathol. 10: 311-324.
3. Boland GJ, Hall R (1994) Index of plant hosts of Sclerotinia sclerotiorum. Canadian J. Plant Pathol. 16: 93-108.
4. AbuQamar S, Moustafa K, Tran LSP (2017) Mechanisms and strategies of plant defense against Botrytis cinerea. Crit. Rev. in Biotechnol. 37: 262-274.
5. Dean R, Van Kan JAL, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, et al. (2012) The Top 10 fungal pathogens in molecular plant pathology. Mol. Plant Pathol. 13: 414-430.
6. Hardeland R (1999) Melatonin and 5-methoxytryptamine in non-metazoans. Reprod. Nutr. Dev. 39: 399-408.
7. Reiter RJ, Mayo JC, Tan DX, Sainz RM, Alatorre-Jimenez M, Qin L (2016) Melatonin as an antioxidant: under promises but over delivers. J. Pineal Res. 61: 253-278.
8. Manchester LC, Poeggeler B, Alvares FL, Ogden GB, Reiter RJ (1995) Melatonin immunoreactivity in the photosynthetic prokaryote Rhodospirillum rubrum: implications for an ancient antioxidant system. Cell. Mol. Biol. Res. 41: 391-395.
9. Tan DX, Zheng XD, Kong J, Manchester LC, Hardeland R, et al. (2014) Fundamental issues related to the origin of melatonin and melatonin isomers during evolution: relation to their biological functions. Int. J. Mol. Sci. 15: 15858-15890.
10. Muszyńska B, Sułkowska-Ziaja K. (2012) Analysis of indole compounds in edible Basidiomycota species after thermal processing. Food Chem. 132: 455-459.
11. Arnao MB, Hernández-Ruiz J (2019) Melatonin: a new plant hormone and/or a plant master regulator? Trends Plant Sci. 24:38-48.
12. Hu XH, Wang MH, Tan T, Li JR, Yang H, et al. (2007) Genetic dissection of ethanol tolerance in the budding yeast Saccharomyces cerevisiae. Genetics 175: 1479-1487.
13. Ma M, Liu ZL (2010) Mechanisms of ethanol tolerance in Saccharomyces cerevisiae. Appl. Microbiol. Biot. 87: 829-845.
14. Ding F, Liu B, Zhang S (2017) Exogenous melatonin ameliorates cold-induced damage in tomato plants. Sci. Hortic. 219: 264-271.
15. Debnath B, Islam W, Li M, Sun Y, Lu X, et al. (2019) Melatonin mediates enhancement of stress tolerance in plants. Int. J. Mol. Sci. 20: 1040.
16. Liu T, Zhao F, Liu Z, Zuo Y, Hou J, Wang Y (2016) Identification of melatonin in Trichoderma spp. and detection of melatonin content under controlled-stress growth conditions from T. asperellum. J. Basic Microbiol. 56: 838-843.
17. Liang HJ, Lu XM, Zhu ZQ, Zhu FX (2016) Effect of organic solvent on fungicide toxicity to Sclerotinia sclerotiorum and Botrytis cinerea. Eur. J. Plant Pathol. 146: 1-9.
18. Zhang S, Liu S, Zhang J, Reiter RJ, Wang Y, et al. (2018) Synergistic anti-oomycete effect of melatonin with a biofungicide against oomycetic black shank disease. J. Pineal Res. 65: e12492.
19. Wang HX, Liu F, Ng TB (2001) Examination of pineal indoles and 6-methoxy-2-benzoxazolinone for antioxidant and antimicrobial effects. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 130: 379-388.
20. Arnao MB, Hernández-Ruiz J (2015) Functions of melatonin in plants: a review. J. Pineal Res. 59: 133-150.
21. Asiimwe T, Krause K, Schlunk I, Kothe E (2012) Modulation of ethanol stress tolerance by aldehyde dehydrogenase in the mycorrhizal fungus Tricholoma vaccinum. Mycorrhiza. 22: 471-484.
22. Sakaki T, Zähringer U, Warnecke DC, Fahl A, Knogge W, Heinz E (2001) Sterol glycosides and cerebrosides accumulate in Pichia pastoris, Rhynchosporium secalis and other fungi under normal conditions or under heat shock and ethanol stress. Yeast 18: 679-695.
23. Yogabaanu U, Weber JFF, Convey P, Rizman-Idid M, Alias SA (2017) Antimicrobial properties and the influence of temperature on secondary metabolite production in cold environment soil fungi. Polar Sci. 14: 60-67.
24. Duarte AWF, dos Santos JA, Vianna MV, Vieira JMF, Mallagutti VH, et al. (2017) Cold-adapted enzymes produced by fungi from terrestrial and marine Antarctic environments. Crit. Rev. Biotechnol. 38: 1-20.
25. Godinho VM, Furbino LE, Santiago IF, Pellizzari FM, Yokoya NS, et al. (2013) Diversity and bioprospecting of fungal communities associated with endemic and cold-adapted macroalgae in Antarctica. ISME J. 7: 1434-1451.
26. Pérez-Gallardo RV, Briones LS, Díaz-Pérez AL, Gutiérrez S, Rodríguez-Zavala JS, Campos-García J (2013) Reactive oxygen species production induced by ethanol in Saccharomyces cerevisiae increases because of a dysfunctional mitochondrial iron-sulfur cluster assembly system. FEMS Yeast Res. 13: 804-819.
27. Kostadinova N, Vassilev S, Spasova B, Angelova M (2011) Cold stress in Antarctic fungi targets enzymes of the glycolytic pathway and tricarboxylic acid cycle. Biotechnol. Biotechnol. Equip. 25: 50-57.
28. Zhang N, Sun Q, Zhang H, Cao Y, Weeda S, et al. (2015) Roles of melatonin in abiotic stress resistance in plants. J. Exp. Bot. 66: 647-656.
29. Vázquez J, Grillitsch K, Daum G, Mas A, Torija MJ, Beltran G (2018) Melatonin minimizes the impact of oxidative stress induced by hydrogen peroxide in Saccharomyces and Non-conventional yeast. Front. Microbiol. 9: 1933.
30. Yin L, Wang P, Li M, Ke X, Li C, et al. (2013) Exogenous melatonin improves Malus resistance to Marssonina apple blotch. J. Pineal Res. 54: 426-434.
31. Wei W, Li QT, Chu YN, Reiter RJ, Yu XM, et al. (2015) Melatonin enhances plant growth and abiotic stress tolerance in soybean plants. J. Exp. Bot. 66: 695-707.
32. Cui G, Zhao X, Liu S, Sun F, Zhang C, Xi Y. (2017) Beneficial effects of melatonin in overcoming drought stress in wheat seedlings. Plant Physiol. Bioch. 118: 138-149.
33. Zhang YP, Yang SJ, Chen YY (2017) Effects of melatonin on photosynthetic performance and antioxidants in melon during cold and recovery. Biol. Plantarum. 61: 571-578.
34. Moustafa-Farag M, Almoneafy A, Mahmoud A, Elkelish A, Arnao MB (2019) Melatonin and its protective role against abiotic stress impacts in plants. Biomolecules 10: E54.
35. Du Fall LA, Solomon PS (2013) The necrotrophic effector SnToxA induces the synthesis of a novel phytoalexin in wheat. New Phytol. 200: 185-200.
36. Madigan AP, Harris C, Bedon F, Franks AF, Plummer KM (2019) Bacterial and fungal communities are diferentially modifidied by melatonin in agricultural soils under abiotic stress. Front. Microbio. 10: 2616.
Published
2020-06-01
How to Cite
[1]
Madigan, A., Harris, C., Bedon, F., Franks, A. and Plummer, K. 2020. High doses of melatonin confer abiotic stress tolerance to phytopathogenic fungi grown in vitro. Melatonin Research. 3, 2 (Jun. 2020), 187-193. DOI:https://doi.org/https://doi.org/10.32794/mr11250056.
Section
Short Communication