Effectiveness of Volatiles Emitted by Streptomyces abikoensis TJGA-19 for Managing Litchi Downy Blight Disease
Abstract
1. Introduction
2. Materials and Methods
2.1. Microorganisms and Plant Materials
2.2. Screening Antagonistic Actinomycetes for Volatile Mediated Antifungal Activity against P. litchii
2.3. Production of S. abikoensis TJGA-19 Volatile Substances
2.4. The Effect of Cultivation Time on the Antifungal Activity of Volatiles Produced by S. abikoensis TJGA-19
2.5. Testing Antifungal Spectrum of Volatiles of S. abikoensisTJGA-19
2.6. Preparation of P. litchii Sporangia Suspension
2.7. Inhibitory Activity of Volatiles from S. abikoensisTJGA-19 In Vitro
2.8. Observation of Morphology by Electron Microscopy
2.9. Inoculation Bioassay In Vivo
2.10. Collection and Analysis of Volatiles Produced by S. abikoensis TJGA-19
2.11. Statistical Analysis
3. Results
3.1. Screening Actinomycetes for Antagonistic Activity
3.2. The Antifungal Activity of Volatile Substances from S. abikoensis TJGA-19 at Different Cultivation Times against P. litchii
3.3. Determination of the Antifungal Spectrum of S. abikoensis TJGA-19 Volatiles
3.4. Antifungal Activity of Volatiles from S. abikoensis TJGA-19 on P. litchii
3.5. Volatiles Resulted in Morphological and Ultrastructural Changes in P. litchii
3.6. The Inhibitory Effects of S. abikoensis TJGA-19 Volatiles on Litchi Downy Blight in Litchi Leaves and Fruits
3.7. Analysis of Volatiles Produced by S. abikoensis TJGA-19
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Zhao, L.; Wang, K.; Wang, K.; Zhu, J.; Hu, Z. Nutrient components, health benefits, and safety of litchi (Litchi chinensis Sonn.): A review. Compr. Rev. Food. Sci. Food Saf. 2020, 19, 2139–2163. [Google Scholar] [CrossRef] [PubMed]
- Situ, J.; Zheng, L.; Xu, D.; Gu, C.; Xi, P.; Deng, Y.; Hsiang, T.; Jiang, Z. Screening of effective biocontrol agents against postharvest litchi downy blight caused by Peronophythora litchii. Postharvest Biol. Technol. 2023, 198, 112249. [Google Scholar] [CrossRef]
- Wang, H.; Qian, Z.; Ma, S.; Zhou, Y.; Qu, H. Energy status of ripening and postharvest senescent fruit of litchi (Litchi chinensis Sonn.). BMC Plant Biol. 2013, 13, 55. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.; Sun, H.; Ma, J.; Stammler, G.; Zhou, M. Fungicide Effectiveness during the Various Developmental Stages of Peronophythora litchii In Vitro. J. Phytopathol. 2009, 157, 407–412. [Google Scholar] [CrossRef]
- Peikun, C.; Sueping, P. On downy blight of litchi chinensis sonn.i.the pathogen and its infection process. Acta Phytopathol. Sin. 1984, 14, 113–119. [Google Scholar]
- Niazian, M.; Sabbatini, P. Traditional in vitro strategies for sustainable production of bioactive compounds and manipulation of metabolomic profile in medicinal, aromatic and ornamental plants. Planta 2021, 254, 111. [Google Scholar] [CrossRef] [PubMed]
- Demain, A.L. Microbial Secondary Metabolism: A New Theoretical Frontier for Academia, a New Opportunity for Industry. In Ciba Foundation Symposium 171-Secondary Metabolites: Their Function and Evolution: Secondary Metabolites: Their Function and Evolution: Ciba Foundation Symposium 171; John Wiley & Sons: Chichester, UK, 2007; pp. 3–23. [Google Scholar]
- Kim, T.; Jang, J.; Yu, N.; Chi, W.; Bae, C.; Yeo, J.; Park, A.; Hur, J.; Park, H.; Park, J. Nematicidal activity of grammicin produced by Xylaria grammica KCTC 13121BP against Meloidogyne incognita. Pest Manag. Sci. 2018, 74, 384–391. [Google Scholar] [CrossRef]
- Barthélemy, M.; Elie, N.; Genta-Jouve, G.; Stien, D.; Eparvier, V. Identification of Antagonistic Compounds between the Palm Tree Xylariale Endophytic Fungi and the Phytopathogen Fusarium oxysporum. J. Agric. Food Chem. 2021, 69, 10893–10906. [Google Scholar] [CrossRef]
- Strobel, G. Muscodor albus and its biological promise. J. Ind. Microbiol. Biotechnol. 2006, 33, 514. [Google Scholar] [CrossRef]
- Contarino, R.; Brighina, S.; Fallico, B.; Cirvilleri, G.; Parafati, L.; Restuccia, C. Volatile organic compounds (VOCs) produced by biocontrol yeasts. Food Microbiol. 2019, 82, 70–74. [Google Scholar] [CrossRef]
- Ryu, C.; Farag, M.A.; Hu, C.; Reddy, M.S.; Kloepper, J.W.; Pare, P.W. Bacterial Volatiles Induce Systemic Resistance in Arabidopsis. Plant Physiol. 2004, 134, 1017–1026. [Google Scholar] [CrossRef] [PubMed]
- Yuan, J.; Raza, W.; Shen, Q.; Huang, Q. Antifungal Activity of Bacillus amyloliquefaciens NJN-6 Volatile Compounds against Fusarium oxysporum f. sp. cubense. Appl. Environ. Microbiol. 2012, 78, 5942–5944. [Google Scholar] [CrossRef] [PubMed]
- You, J.; Li, G.; Li, C.; Zhu, L.; Yang, H.; Song, R.; Gu, W. Biological control and plant growth promotion by volatile organic compounds of Trichoderma koningiopsis T-51. J. Fungi 2022, 8, 131. [Google Scholar] [CrossRef] [PubMed]
- Delgado, N.; Olivera, M.; Cádiz, F.; Bravo, G.; Montenegro, I.; Madrid, A.; Fuentealba, C.; Pedreschi, R.; Salgado, E.; Besoain, X. Volatile Organic Compounds (VOCs) Produced by Gluconobacter cerinus and Hanseniaspora osmophila Displaying Control Effect against Table Grape-Rot Pathogens. Antibiotics 2021, 10, 663. [Google Scholar] [CrossRef] [PubMed]
- Cuervo, L.; Álvarez-García, S.; Salas, J.A.; Méndez, C.; Olano, C.; Malmierca, M.G. The Volatile Organic Compounds of Streptomyces spp.: An In-Depth Analysis of Their Antifungal Properties. Microorganisms 2023, 11, 1820. [Google Scholar] [CrossRef] [PubMed]
- Campos-Avelar, I.; Colas De La Noue, A.; Durand, N.; Cazals, G.; Martinez, V.; Strub, C.; Fontana, A.; Schorr-Galindo, S. Aspergillus flavus growth inhibition and aflatoxin B1 decontamination by Streptomyces isolates and their metabolites. Toxins 2021, 13, 340. [Google Scholar] [CrossRef] [PubMed]
- Jepsen, T.; Jensen, B.; Jørgensen, N.O. Volatiles produced by Streptomyces spp. delay rot in apples caused by Colletotrichum acutatum. Curr. Res. Microb. Sci. 2022, 3, 100121. [Google Scholar] [CrossRef]
- Corral, D.A.P.; Paz, J.D.J.O.; Orozco, G.I.O.; Muñiz, C.H.A.; Marina, M.Á.S.; Cisneros, M.F.R.; Corral, F.J.M.; Pavía, S.P.F.; Velasco, C.R. Antagonistic effect of volatile and non-volatile compounds from Streptomyces strains on cultures of several phytopathogenic fungi. Emir. J. Food Agric. 2020, 32, 879–889. [Google Scholar] [CrossRef]
- Wan, M.; Li, G.; Zhang, J.; Jiang, D.; Huang, H. Effect of volatile substances of Streptomyces platensis F-1 on control of plant fungal diseases. Biol. Control 2008, 46, 552–559. [Google Scholar] [CrossRef]
- Li, Q.; Ning, P.; Zheng, L.; Huang, J.; Li, G.; Hsiang, T. Effects of volatile substances of Streptomyces globisporus JK-1 on control of Botrytis cinerea on tomato fruit. Biol. Control 2012, 61, 113–120. [Google Scholar] [CrossRef]
- Danaei, M.; Baghizadeh, A.; Shahram, P.; Mohammadmehdi, Y. Effect of volatile substances of Streptomyces coelicolor on control of Botrytis cinerea and Penicillium chrysogenum. Casp. J. Appl. Sci. Res. 2013, 2, 45–51. [Google Scholar]
- Wang, Z.; Wang, C.; Li, F.; Li, Z.; Chen, M.; Wang, Y.; Qiao, X.; Zhang, H. Fumigant activity of volatiles from Streptomyces alboflavus TD-1 against Fusarium moniliforme Sheldon. J. Microbiol. 2013, 51, 477–483. [Google Scholar] [CrossRef] [PubMed]
- Zheng, L.; Situ, J.; Zhu, Q.; Xi, P.; Zheng, Y.; Liu, H.; Zhou, X.; Jiang, Z. Identification of volatile organic compounds for the biocontrol of postharvest litchi fruit pathogen Peronophythora litchii. Postharvest Biol. Technol. 2019, 155, 37–46. [Google Scholar] [CrossRef]
- Xing, M.; Zhao, J.; Zhang, J.; Wu, Y.; Khan, R.A.A.; Li, X.; Wang, R.; Li, T.; Liu, T. 6-Pentyl-2H-pyran-2-one from Trichoderma erinaceum Is Fungicidal against Litchi Downy Blight Pathogen Peronophythora litchii and Preservation of Litchi. J. Agric. Food Chem. 2023, 71, 19488–19500. [Google Scholar] [CrossRef]
- Xing, M.; Zheng, L.; Deng, Y.; Xu, D.; Xi, P.; Li, M.; Kong, G.; Jiang, Z. Antifungal Activity of Natural Volatile Organic Compounds against Litchi Downy Blight Pathogen Peronophythora litchii. Molecules 2018, 23, 358. [Google Scholar] [CrossRef] [PubMed]
- Xing, M.; Xu, D.; Wu, Y.; Liu, T.; Xi, P.; Wang, R.; Zhao, J.; Jiang, Z. Biocontrol of Litchi Downy Blight Dependent on Streptomyces abikoensis TJGA-19 Fermentation Filtrate Antagonism Competition with Peronophythora litchii. Fermentation 2023, 9, 1011. [Google Scholar] [CrossRef]
- Khan, R.A.A.; Najeeb, S.; Hussain, S.; Xie, B.; Li, Y. Bioactive Secondary Metabolites from Trichoderma spp. against Phytopathogenic Fungi. Microorganisms 2020, 8, 817. [Google Scholar] [CrossRef] [PubMed]
- Zhan, X.; Khan, R.A.A.; Zhang, J.; Chen, J.; Yin, Y.; Tang, Z.; Wang, R.; Lu, B.; Liu, T. Control of postharvest stem-end rot on mango by antifungal metabolites of Trichoderma pinnatum LS029-3. Sci. Hortic. 2023, 310, 111696. [Google Scholar] [CrossRef]
- Kanchiswamy, C.N.; Malnoy, M.; Maffei, M.E. Chemical diversity of microbial volatiles and their potential for plant growth and productivity. Front. Plant Sci. 2015, 6, 151. [Google Scholar] [CrossRef]
- Boukaew, S.; Petlamul, W.; Bunkrongcheap, R.; Chookaew, T.; Kabbua, T.; Thippated, A.; Prasertsan, P. Fumigant activity of volatile compounds of Streptomyces philanthi RM-1-138 and pure chemicals (acetophenone and phenylethyl alcohol) against anthracnose pathogen in postharvest chili fruit. Crop Prot. 2018, 103, 1–8. [Google Scholar] [CrossRef]
- Gong, Y.; Liu, J.; Xu, M.; Zhang, C.; Gao, J.; Li, C.; Xing, K.; Qin, S. Antifungal Volatile Organic Compounds from Streptomyces setonii WY228 Control Black Spot Disease of Sweet Potato. Appl. Environ. Microbiol. 2022, 88, e2317–e2321. [Google Scholar] [CrossRef] [PubMed]
- Boukaew, S.; Cheirsilp, B.; Prasertsan, P.; Yossan, S. Antifungal effect of volatile organic compounds produced by Streptomyces salmonis PSRDC-09 against anthracnose pathogen Colletotrichum gloeosporioides PSU-03 in postharvest chili fruit. J. Appl. Microbiol. 2021, 131, 1452–1463. [Google Scholar] [CrossRef] [PubMed]
- Li, Q.; Ning, P.; Zheng, L.; Huang, J.; Li, G.; Hsiang, T. Fumigant activity of volatiles of Streptomyces globisporus JK-1 against Penicillium italicum on Citrus microcarpa. Postharvest Biol. Technol. 2010, 58, 157–165. [Google Scholar] [CrossRef]
- Boukaew, S.; Plubrukam, A.; Prasertsan, P. Effect of volatile substances from Streptomyces philanthi RM-1-138 on growth of Rhizoctonia solani on rice leaf. Biocontrol 2013, 58, 471–482. [Google Scholar] [CrossRef]
- Xu, D.; Deng, Y.; Xi, P.; Zhu, Z.; Kong, X.; Wan, L.; Situ, J.; Li, M.; Gao, L.; Jiang, Z. Biological activity of pterostilbene against Peronophythora litchii, the litchi downy blight pathogen. Postharvest Biol. Technol. 2018, 144, 29–35. [Google Scholar] [CrossRef]
- Liao, L.; Zhou, J.; Wang, H.; He, F.; Liu, S.; Jiang, Z.; Chen, S.; Zhang, L. Control of litchi downy blight by zeamines produced by Dickeya zeae. Sci. Rep. 2015, 5, 15719. [Google Scholar] [CrossRef]
- Luo, J.; Li, Z.; Wang, J.; Weng, Q.; Chen, S.; Hu, M. Antifungal activity of isoliquiritin and its inhibitory effect against Peronophythora litchii Chen through a membrane damage mechanism. Molecules 2016, 21, 237. [Google Scholar] [CrossRef]
- Xu, L.; Xue, J.; Wu, P.; Wang, D.; Wei, X. Antifungal Activity of Hypothemycin against Peronophythora litchii In Vitro and In Vivo. J. Agric. Food Chem. 2013, 61, 10091–10095. [Google Scholar] [CrossRef]
Volatile Organic Compounds a | RT b (min) | Area (%) |
---|---|---|
Arsenous acid, tris(trimethylsilyl) ester | 14.9147 | 3.5529 |
Benzonitrile, 2-(2-hydroxy-5-nitrobenzylidenamino)- | 18.1902 | 3.2558 |
2-Methylisoborneol | 18.9705 | 25.9287 |
4-(2-Methyl-cyclohex-1-enyl)-but-3-en-2-one | 20.9163 | 1.5504 |
Cyclotetrasiloxane, octamethyl- | 21.8342 | 2.8193 |
Tridecane | 24.4551 | 1.6461 |
Naphthalene,1,2,4a,5,8,8a-hexahydro-4,7-dimethyl-1-(1-methylethyl)-, (1.alpha.,4a.beta.,8a.alpha.)- | 25.7243 | 5.2184 |
1,3,5,7,9-Pentaethylcyclopentasiloxane | 25.9002 | 2.1199 |
2-Methyltetracosane | 27.2091 | 1.9879 |
Benzoic acid, hexyl ester | 27.585 | 2.3067 |
Dodecane, 2,6,10-trimethyl- | 27.7489 | 9.9877 |
4-(1-methyl-1-cyclobutyl)phenol | 28.0618 | 4.9239 |
(2Z,4E)-3,7,11-Trimethyl-2,4,10-dodecatriene | 28.3478 | 3.0363 |
Tetradecane | 28.7473 | 7.8256 |
(1R,4aS,8aR)-1,4a-Dimethyl-7-(prop-1-en-2-yl)-1,2,3,4,4a,5,6,8a-octahydronaphthalene | 28.8855 | 2.9132 |
Disparlure | 29.1225 | 2.3421 |
2,6,10-Trimethyltridecane | 31.3051 | 6.2293 |
1H-Cyclopropa[a]naphthalene, 1a,2,3,3a,4,5,6,7b-octahydro-1,1,3a,7-tetramethyl-, [1aR-(1a.alpha.,3a.alpha.,7b.alpha.)]- | 31.4971 | 3.8272 |
Octacosane | 32.6604 | 2.1236 |
Pentadecane | 32.8364 | 2.234 |
Hexadecane | 34.4358 | 1.2136 |
Longifolene | 36.7445 | 2.9574 |
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Xing, M.; Sun, T.; Liu, T.; Jiang, Z.; Xi, P. Effectiveness of Volatiles Emitted by Streptomyces abikoensis TJGA-19 for Managing Litchi Downy Blight Disease. Microorganisms 2024, 12, 184. https://doi.org/10.3390/microorganisms12010184
Xing M, Sun T, Liu T, Jiang Z, Xi P. Effectiveness of Volatiles Emitted by Streptomyces abikoensis TJGA-19 for Managing Litchi Downy Blight Disease. Microorganisms. 2024; 12(1):184. https://doi.org/10.3390/microorganisms12010184
Chicago/Turabian StyleXing, Mengyu, Tao Sun, Tong Liu, Zide Jiang, and Pinggen Xi. 2024. "Effectiveness of Volatiles Emitted by Streptomyces abikoensis TJGA-19 for Managing Litchi Downy Blight Disease" Microorganisms 12, no. 1: 184. https://doi.org/10.3390/microorganisms12010184
APA StyleXing, M., Sun, T., Liu, T., Jiang, Z., & Xi, P. (2024). Effectiveness of Volatiles Emitted by Streptomyces abikoensis TJGA-19 for Managing Litchi Downy Blight Disease. Microorganisms, 12(1), 184. https://doi.org/10.3390/microorganisms12010184