RNAi-Based Biofungicides as a Promising Next-Generation Strategy for Controlling Devastating Gray Mold Diseases
Abstract
:1. Introduction
2. RNAi: Biosynthesis and Actions
3. Small Interfering RNA (siRNA) Regulate the Virulence of B. cinerea
4. Plant siRNA Induce Immune Responses to Counteract B. cinerea Infections
5. RNAi-Based Biofungicides and Spray-Induced Gene Silencing (SIGS) for Controlling B. cinerea
6. Conclusions and Future Perspectives
Author Contributions
Funding
Conflicts of Interest
References
- Petrasch, S.; Knapp, S.J.; van Kan, J.A.L.; Blanco-Ulate, B. Grey mould of strawberry, a devastating disease caused by the ubiquitous necrotrophic fungal pathogen Botrytis cinerea. Mol. Plant Pathol. 2019, 20, 877–892. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dean, R.; van Kan, J.A.; Pretorius, Z.A.; Hammond-Kosack, K.E.; Di Pietro, A.; Spanu, P.D.; Rudd, J.J.; Dickman, M.; Kahmann, R.; Ellis, J.; et al. The Top 10 fungal pathogens in molecular plant pathology. Mol. Plant Pathol. 2012, 13, 414–430. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Weiberg, A.; Wang, M.; Lin, F.M.; Zhao, H.; Zhang, Z.; Kaloshian, I.; Huang, H.D.; Jin, H. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 2013, 342, 118–123. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Veloso, J.; van Kan, J.A.L. Many shades of grey in Botrytis-host plant interactions. Trends Plant Sci. 2018, 23, 613–622. [Google Scholar] [CrossRef]
- Pedras, M.S.; Hossain, S.; Snitynsky, R.B. Detoxification of cruciferous phytoalexins in Botrytis cinerea: Spontaneous dimerization of a camalexin metabolite. Phytochemistry 2011, 72, 199–206. [Google Scholar] [CrossRef]
- Villa-Rojas, R.; Sosa-Morales, M.E.; Lopez-Malo, A.; Tang, J. Thermal inactivation of Botrytis cinerea conidia in synthetic medium and strawberry puree. Int. J. Food Microbiol. 2012, 155, 269–272. [Google Scholar] [CrossRef]
- Malhat, F.M.; Haggag, M.N.; Loutfy, N.M.; Osman, M.A.; Ahmed, M.T. Residues of organochlorine and synthetic pyrethroid pesticides in honey, an indicator of ambient environment, a pilot study. Chemosphere 2015, 120, 457–461. [Google Scholar] [CrossRef]
- Oliveira, B.R.; Penetra, A.; Cardoso, V.V.; Benoliel, M.J.; Barreto Crespo, M.T.; Samson, R.A.; Pereira, V.J. Biodegradation of pesticides using fungi species found in the aquatic environment. Environ. Sci. Pollut. R. 2015, 22, 11781–11791. [Google Scholar] [CrossRef]
- Tomenson, J.A.; Matthews, G.A. Causes and types of health effects during the use of crop protection chemicals: Data from a survey of over 6300 smallholder applicators in 24 different countries. Int. Arch. Occup. Environ. Health 2009, 82, 935–949. [Google Scholar] [CrossRef] [Green Version]
- Rupp, S.; Weber, R.W.S.; Rieger, D.; Detzel, P.; Hahn, M. Spread of Botrytis cinerea strains with multiple fungicide resistance in german horticulture. Front. Microbiol. 2017, 7, 2075. [Google Scholar] [CrossRef] [Green Version]
- Fernández-Ortuño, D.; Grabke, A.; Li, X.; Schnabel, G. Independent emergence of resistance to seven chemical classes of fungicides in Botrytis cinerea. Phytopathology 2015, 105, 424–432. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Qi, T.; Guo, J.; Peng, H.; Liu, P.; Kang, Z.; Guo, J. Host-induced gene silencing: A powerful strategy to control diseases of wheat and barley. Int. J. Mol. Sci. 2019, 20, 206. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, M.; Thomas, N.; Jin, H. Cross-kingdom RNA trafficking and environmental RNAi for powerful innovative pre- and post-harvest plant protection. Curr. Opin. Plant Biol. 2017, 38, 133–141. [Google Scholar] [CrossRef] [PubMed]
- Wang, M.; Weiberg, A.; Lin, F.M.; Thomma, B.P.H.J.; Huang, H.D.; Jin, H. Bidirectional cross-kingdom RNAi and fungal uptake of external RNAs confer plant protection. Nat. Plants 2016, 2, 16151. [Google Scholar] [CrossRef]
- Xiong, F.; Liu, M.; Zhuo, F.; Yin, H.; Deng, K.; Feng, S.; Liu, Y.; Luo, X.; Feng, L.; Zhang, S.; et al. Host-induced gene silencing of BcTOR in Botrytis cinerea enhances plant resistance to grey mould. Mol. Plant Pathol. 2019, 20, 1722–1739. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Machado, A.K.; Brown, N.A.; Urban, M.; Kanyuka, K.; Hammond-Kosack, K.E. RNAi as an emerging approach to control Fusarium head blight disease and mycotoxin contamination in cereals. Pest Manag. Sci. 2018, 74, 790–799. [Google Scholar] [CrossRef] [Green Version]
- Koch, A.; Biedenkopf, D.; Furch, A.; Weber, L.; Rossbach, O.; Abdellatef, E.; Linicus, L.; Johannsmeier, J.; Jelonek, L.; Goesmann, A.; et al. An RNAi-based control of Fusarium graminearum infections through spraying of long dsRNAs involves a plant passage and is controlled by the fungal silencing machinery. PLoS Pathog. 2016, 12, e1005901. [Google Scholar] [CrossRef]
- Song, X.S.; Gu, K.X.; Duan, X.X.; Xiao, X.M.; Hou, Y.P.; Duan, Y.B.; Wang, J.X.; Yu, N.; Zhou, M.G. Secondary amplification of siRNA machinery limits the application of spray-induced gene silencing. Mol. Plant Pathol. 2018, 19, 2543–2560. [Google Scholar] [CrossRef] [Green Version]
- Mcloughlin, A.G.; Wytinck, N.; Walker, P.L.; Girard, I.J.; Rashid, K.Y.; De Kievit, T.; Fernando, W.G.D.; Whyard, S.; Belmonte, M.F. Identification and application of exogenous dsRNA confers plant protection against Sclerotinia sclerotiorum and Botrytis cinerea. Sci. Rep. 2018, 8, 7320. [Google Scholar] [CrossRef]
- Mcloughlin, A.G.; Walker, P.L.; Wytinck, N.; Sullivan, D.S.; Whyard, S.; Belmonte, M.F. Developing new RNA interference technologies to control fungal pathogens. Can. J. Plant Pathol. 2018, 40, 325–335. [Google Scholar] [CrossRef]
- Kandasamy, S.K.; Fukunaga, R. Phosphate-binding pocket in Dicer-2 PAZ domain for high-fidelity siRNA production. Proc. Natl. Acad. Sci. USA 2016, 113, 14031–14036. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dang, Y.; Yang, Q.; Xue, Z.; Liu, Y. RNA interference in fungi: Pathways, functions, and applications. Eukaryot. Cell 2011, 10, 1148–1155. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Voinnet, O. Origin, biogenesis, and activity of plant microRNAs. Cell 2009, 136, 669–687. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dalakouras, A.; Wassenegger, M.; Dadami, E.; Ganopoulos, I.; Pappas, M.L.; Papadopoulou, K. Genetically modified organism-free RNA interference: Exogenous application of RNA molecules in plants. Plant Physiol. 2020, 182, 38–50. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chan, S.W.; Zilberman, D.; Xie, Z.; Johansen, L.K.; Carrington, J.C.; Jacobsen, S.E. RNA silencing genes control de novo DNA methylation. Science 2004, 303, 1336. [Google Scholar] [CrossRef]
- Weiberg, A.; Jin, H. Small RNAs—The secret agents in the plant–pathogen interactions. Curr. Opin. Plant Biol. 2015, 26, 87–94. [Google Scholar] [CrossRef] [Green Version]
- Mandadi, K.K.; Karen-Beth, G.; Scholthof, K.B.G. Plant immune responses against viruses: How does a virus cause disease? Plant Cell 2013, 25, 1489–1505. [Google Scholar] [CrossRef] [Green Version]
- Zhang, X.; Dai, Y.; Xiong, Y.; DeFraia, C.; Li, J.; Dong, X.; Mou, Z. Overexpression of Arabidopsis MAP kinase kinase leads to activation of plant basal and systemic acquired resistance. Plant J. 2007, 52, 1066–1079. [Google Scholar] [CrossRef]
- Lang, J.; Genot, B.; Hirt, H.; Colcombet, J. Constitutive activity of the Arabidopsis MAP Kinase 3 confers resistance to Pseudomonas syringae and drives robust immune responses. Plant Signal. Behav. 2017, 12, e1356533. [Google Scholar] [CrossRef]
- Genenncher, B.; Wirthmueller, L.; Roth, C.; Klenke, M.; Ma, L.; Sharon, A.; Wiermer, M. Nucleoporin-regulated MAP kinase signaling in immunity to a necrotrophic fungal pathogen. Plant Physiol. 2016, 172, 1293–1305. [Google Scholar] [CrossRef] [Green Version]
- Islam, M.T.; Lee, B.R.; Park, S.H.; La, V.H.; Bae, D.W.; Kim, T.H. Cultivar variation in hormonal balance is a significant determinant of disease susceptibility to Xanthomonas campestris pv. campestris in Brassica napus. Front. Plant Sci. 2017, 8, 2121. [Google Scholar] [CrossRef] [Green Version]
- Finiti, I.; Leyva, M.O.; Vicedo, B.; Gómez-pastor, R.; López-cruz, J.; Garcíaagustín, P.; Real, M.D.; González-Boschet, C. Hexanoic acid protects tomato plants against Botrytis cinerea by priming defense responses and reducing oxidative stress. Mol. Plant Pathol. 2014, 15, 550–562. [Google Scholar] [CrossRef]
- van Kan, J.A.L. Licensed to kill: The lifestyle of a necrotrophic plant pathogen. Trends. Plant Sci. 2006, 11, 247–253. [Google Scholar] [CrossRef]
- Brutus, A.; Sicilia, F.; Macone, A.; Cervone, F.; De Lorenzo, G. A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc. Natl. Acad. Sci. USA 2010, 107, 9452–9457. [Google Scholar] [CrossRef] [Green Version]
- Ferrari, S.; Savatin, D.V.; Sicilia, F.; Gramegna, G.; Cervone, F.; De Lorenzo, G. Oligogalacturonides: Plant damage-associated molecular patterns and regulators of growth and development. Front. Plant Sci. 2013, 4, 49. [Google Scholar] [CrossRef] [Green Version]
- Wang, M.; Weiberg, A.; Dellota, E.; Yamane, D.; Jin, H. Botrytis small RNA Bc-siR37 suppresses plant defense genes by cross-kingdom RNAi. RNA Biol. 2017, 14, 421–428. [Google Scholar] [CrossRef] [Green Version]
- Kim, K.C.; Fan, B.; Chen, Z. Pathogen-induced Arabidopsis WRKY7 is a transcriptional repressor and enhances plant susceptibility to Pseudomonas syringae. Plant Physiol. 2006, 142, 1180–1192. [Google Scholar] [CrossRef] [Green Version]
- Jiang, Y.; Liang, G.; Yang, S.; Yu, D. Arabidopsis WRKY57 functions as a node of convergence for jasmonic acid- and auxin-mediated signaling in jasmonic acid-induced leaf senescence. Plant Cell. 2014, 26, 230–245. [Google Scholar] [CrossRef] [Green Version]
- Staiger, D.; Korneli, C.; Lummer, M.; Navarro, L. Emerging role for RNA-based regulation in plant immunity. New Phytol. 2013, 197, 394–404. [Google Scholar] [CrossRef]
- Lopez, A.; Ramirez, V.; Garcia-Andrade, J.; Flors, V.; Vera, P. The RNA silencing enzyme RNA polymerase v is required for plant immunity. PLoS Genet. 2011, 7, e1002434. [Google Scholar] [CrossRef] [Green Version]
- Cai, Q.; Qiao, L.; Wang, M.; He, B.; Lin, F.M.; Palmquist, J.; Huang, S.D.; Jin, H. Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. Science 2018, 360, 1126–1129. [Google Scholar] [CrossRef] [Green Version]
- Jeong, B.R.; Lin, Y.; Joe, A.; Guo, M.; Korneli, C.; Yang, H.; Wang, P.; Yu, M.; Cerny, R.L.; Staiger, D.; et al. Structure function analysis of an ADP ribosyltransferase type III effector and its RNA-binding target in plant immunity. J. Biol. Chem. 2011, 286, 43272–43281. [Google Scholar] [CrossRef] [Green Version]
- Islam, M.T.; Lee, B.R.; Park, S.H.; La, V.H.; Jung, W.J.; Bae, D.W.; Kim, T.H. Hormonal regulations in soluble and cell-wall bound phenolics accumulation in two cultivars of Brassica napus contrasting susceptibility to Xanthomonas campestris pv. campestris. Plant Sci. 2019, 285, 132–140. [Google Scholar] [CrossRef]
- Saito, S.; Michailides, T.J.; Xiao, C.L. Fungicide resistance profiling in Botrytis cinerea populations from blueberry in California and Washington and their impact on control of gray mold. Plant Dis. 2016, 100, 2087–2093. [Google Scholar] [CrossRef] [Green Version]
- Veloukas, T.; Kalogeropoulou, P.; Markoglou, A.N.; Karaoglanidis, G.S. Fitness and competitive ability of Botrytis cinerea field-isolates with dual resistance to SDHI and QoI fungicides, associated with several sdhB and the cytb G134A mutations. Phytopathology 2014, 104, 347–356. [Google Scholar] [CrossRef] [Green Version]
- Dias, M.C. Phytotoxicity: An overview of the physiological responses of plants exposed to fungicides. J. Bot. 2012, 2012, 135479. [Google Scholar] [CrossRef] [Green Version]
- Vuković, S.; Inđić, D.; Gvozdenac, S. Phytotoxic effects of fungicides, insecticides and nonpesticidal components on pepper depending on water quality. Pestic. Phytomed. 2014, 29, 145–153. [Google Scholar]
- Gupta, P.K. Toxicity of fungicides. In Veterinary Toxicology, 3rd ed.; Gupta, R.C., Ed.; Academic Press: Cambridge, MA, USA, 2018; pp. 569–580. [Google Scholar]
- Amiri, A.; Heath, S.M.; Peres, N.A. Phenotypic characterization of multifungicide resistance in Botrytis cinerea isolates from strawberry fields in Florida. Plant Dis. 2013, 97, 393–401. [Google Scholar] [CrossRef] [Green Version]
- Weber, R.W.S. Resistance of Botrytis cinerea to multiple fungicides in Northern German small-fruit production. Plant Dis. 2011, 95, 1263–1269. [Google Scholar] [CrossRef] [Green Version]
- Panebianco, A.; Castello, I.; Cirvilleri, G.; Perrone, G.; Epifani, F.; Ferrara, M.; Polizzia, G.; Walters, D.R.; Vitale, A. Detection of Botrytis cinerea field isolates with multiple fungicide resistance from table grape in Sicily. Crop. Protect. 2015, 77, 65–73. [Google Scholar] [CrossRef]
- Konstantinou, S.; Veloukas, T.; Leroch, M.; Menexes, G.; Hahn, M.; Karaoglanidis, G. Population structure, fungicide resistance profile, and sdhB mutation frequency of Botrytis cinerea from strawberry and greenhouse-grown tomato in Greece. Plant Dis. 2015, 99, 240–248. [Google Scholar] [CrossRef] [Green Version]
- Choquer, M.; Fournier, E.; Kunz, C.; Levis, C.; Pradier, J.M.; Simon, A.; Viaud, M. Botrytis cinerea virulence factors: New insights into a necrotrophic and polyphageous pathogen. FEMS Microbiol. Lett. 2007, 277, 1–10. [Google Scholar] [CrossRef] [Green Version]
- Soulie, M.C.; Perino, C.; Piffeteau, A.; Choquer, M.; Malfatti, P.; Cimerman, A.; Kunz, C.; Boccara, M.; Anne Vidal-Croset, A. Botrytis cinerea virulence is drastically reduced after disruption of chitin synthase class III gene (Bcchs3a). Cell Microbiol. 2006, 8, 1310–1321. [Google Scholar] [CrossRef]
- Schulze Gronover, C.S.; Kasulke, D.; Tudzynski, P.; Tudzynski, B. The role of G protein alpha subunits in the infection process of the gray mold fungus Botrytis cinerea. Mol. Plant Microbe Interact. 2001, 14, 1293–1302. [Google Scholar] [CrossRef] [Green Version]
- Doehlemann, G.; Berndt, P.; Hahn, M. Different signaling pathways involving a Galpha protein, cAMP and a MAP kinase control germination of Botrytis cinerea conidia. Mol. Microbiol. 2006, 59, 821–835. [Google Scholar] [CrossRef]
- Dubrovina, A.S.; Kiselev, K.V. Exogenous RNAs for gene regulation and plant resistance. Int. J. Mol. Sci. 2019, 20, 2282. [Google Scholar] [CrossRef] [Green Version]
- Mitter, N.; Worrall, E.A.; Robinson, K.E.; Li, P.; Jain, R.G.; Taochy, C.; Fletcher, S.J.; Carroll, B.J.; Lu, G.Q.; Xu, Z.P. Clay nanosheets for topical delivery of RNAi for sustained protection against plant viruses. Nat. Plants 2017, 3, 16207. [Google Scholar] [CrossRef]
- Worrall, E.A.; Hamid, A.; Mody, K.T.; Mitter, N.; Pappu, H.R. Nanotechnology for plant disease management. Agronomy 2018, 8, 285. [Google Scholar] [CrossRef] [Green Version]
- Huang, G.Z.; Allen, R.; Davis, E.L.; Baum, T.J.; Hussey, R.S. Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene. Proc. Natl. Acad. Sci. USA 2006, 103, 14302–14306. [Google Scholar] [CrossRef] [Green Version]
- Nowara, D.; Gay, A.; Lacomme, C.; Shaw, J.; Ridout, C.; Douchkov, D.; Hensel, G.; Kumlehn, J.; Schweizeret, P. HIGS: Host-Induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell. 2010, 22, 3130–3141. [Google Scholar] [CrossRef] [Green Version]
- Nunes, C.C.; Dean, R.A. Host-induced gene silencing: A tool for understanding fungal host interaction and for developing novel disease control strategies. Mol. Plant Pathol. 2012, 13, 519–529. [Google Scholar] [CrossRef]
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Islam, M.T.; Sherif, S.M. RNAi-Based Biofungicides as a Promising Next-Generation Strategy for Controlling Devastating Gray Mold Diseases. Int. J. Mol. Sci. 2020, 21, 2072. https://doi.org/10.3390/ijms21062072
Islam MT, Sherif SM. RNAi-Based Biofungicides as a Promising Next-Generation Strategy for Controlling Devastating Gray Mold Diseases. International Journal of Molecular Sciences. 2020; 21(6):2072. https://doi.org/10.3390/ijms21062072
Chicago/Turabian StyleIslam, Md Tabibul, and Sherif M. Sherif. 2020. "RNAi-Based Biofungicides as a Promising Next-Generation Strategy for Controlling Devastating Gray Mold Diseases" International Journal of Molecular Sciences 21, no. 6: 2072. https://doi.org/10.3390/ijms21062072