Characterization of antagonistic actinomycetes against the dragon fruit fungal pathogen Neoscytalidium dimidiatum

Hanh Thi Dieu Nguyen; Anh Thu Thi Ma; Ngoc An Nguyen; Tan Viet Pham

doi:10.56093/ijas.v96i6.166497

Authors

Hanh Thi Dieu Nguyen Institute of Biotechnology and Food Technology, Industrial University of Ho Chi Minh City, Ho Chi Minh City, Vietnam
Anh Thu Thi Ma Department of Science and Technology, Ba Ria - Vung Tau Province, Vietnam, 78055
Ngoc An Nguyen Institute of Biotechnology and Food Technology, Industrial University of Ho Chi Minh City, Ho Chi Minh City, Vietnam, 727010
Tan Viet Pham Institute of Biotechnology and Food Technology, Industrial University of Ho Chi Minh City, Ho Chi Minh City, Vietnam, 727010

https://doi.org/10.56093/ijas.v96i6.166497

Keywords:

Antifungal, Dragon fruit, Neoscytalidium dimidiatum, Pitahaya, Streptomyces

Abstract

Pitahaya or dragon fruit (Hylocereus spp.), renowned for its nutritional value and taste, is among the important economic crops in subtropical and tropical regions. However, global dragon fruit cultivation is threatened by fungal pathogens, notably Neoscytalidium dimidiatum, which causes stem canker and fruit rot. To address this issue through environmentally sustainable methods, 36 out of 50 isolated actinomycetes were shown to exhibit antagonistic activity against N. dimidiatum. Among these, strain CNXK121 exhibiting the most potent antifungal activity was selected. Morphological and molecular analyses revealed that strain CNXK121 shared 100% sequence identity with Streptomyces plicatus, and it was subsequently designated as Streptomyces sp. CNXK121. This strain demonstrated the ability to biosynthesize chitinase and protease, enzymes that compromise the integrity of the fungal cell wall. Volatile organic compounds produced by Streptomyces sp. CNXK121 were observed to inhibit N. dimidiatum growth. Further investigations revealed that the culture of Streptomyces sp. CNXK121 suppressed fungal spore germination and caused abnormalities in fungal mycelia. Experiments conducted on plant fruits and stems confirmed the efficacy of Streptomyces sp. CNXK121 in controlling stem canker and fruit rot. These findings underscore the potential of Streptomyces sp. CNXK121 as a biological control agent and its applicability in sustainable agricultural practices.

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References

Abd-Allah E. 2001. Streptomyces plicatus as a model biocontrol agent. Folia microbiologica 46: 309-314. https://doi.org/10.1007/BF02815619

Aghighi S, Bonjar G S and Saadoun I. 2004. First report of antifungal properties of a new strain of Streptomyces plicatus (strain101) against four Iranian phytopathogenic isolates of Verticillium dahliae, a new horizon in biocontrol agents. Biotechnology 3(1): 90-97. https://doi.org/10.3923/biotech.2004.90.97

Al Hamad B M, Al Raish S M, Ramadan G A, Saeed E E, Alameri S S, Al Senaani S S, AbuQamar S F and El-Tarabily K A. 2021. Effectiveness of augmentative biological control of Streptomyces griseorubens UAE2 depends on 1-aminocyclopropane-1-carboxylic acid deaminase activity against Neoscytalidium dimidiatum. Journal of Fungi 7(11): 885. https://doi.org/10.3390/jof7110885

Al Raish S M, Saeed E E, Alyafei D M, El-Tarabily K A and AbuQamar S F. 2021. Evaluation of streptomycete actinobacterial isolates as biocontrol agents against royal poinciana stem canker disease caused by the fungal pathogen Neoscytalidium dimidiatum. Biological Control 164: 104783. https://doi.org/10.1016/j.biocontrol.2021.104783

Baharlouei A, Sharifi-Sirchi G and Bonjar G S. 2010. Identification of an antifungal chitinase from a potential biocontrol agent, Streptomyces plicatus strain 101, and its new antagonistic spectrum of activity. Philippine Agricultural Scientist 93(4): 439-445. https://api.semanticscholar.org/CorpusID:83109309

Balendres M A, Taguiam J D, Evallo E, Estigoy J and Cortaga C. 2022. Fruit brown rot caused by Neoscytalidium dimidiatum on Selenicereus monacanthus in the Philippines. MycoAsia - Journal of Modern Mycology 2022/06: 1-10. https://doi.org/10.59265/mycoasia.2022-06

Chen P-H, Chen R-Y and Chou J-Y. 2018. Screening and evaluation of yeast antagonists for biological control of Botrytis cinerea on strawberry fruits. Mycobiology 46(1): 33-46. https://doi.org/10.1080/12298093.2018.1454013

Chen Y-Y, Chen P-C and Tsay T-T. 2016. The biocontrol efficacy and antibiotic activity of Streptomyces plicatus on the oomycete Phytophthora capsici. Biological Control 98: 34-42. https://doi.org/10.1016/j.biocontrol.2016.02.011

Choub V, Ajuna H B, Won S-J, Moon J-H, Choi S-I, Maung C E H, Kim C-W and Ahn Y S. 2021. Antifungal activity of Bacillus velezensis CE 100 against anthracnose disease (Colletotrichum gloeosporioides) and growth promotion of walnut (Juglans regia L.) trees. International journal of molecular sciences 22(19): 10438. https://doi.org/10.3390/ijms221910438

Chuang M, Ni H, Yang H, Shu S, Lai S and Jiang Y. 2012. First report of stem canker disease of pitaya (Hylocereus undatus and H. polyrhizus) caused by Neoscytalidium dimidiatum in Taiwan. Plant Disease 96(6): 906. https://doi.org/10.1094/PDIS-08-11-0689-PDN

Cordovez V, Carrion V J, Etalo D W, Mumm R, Zhu H, Van Wezel G P and Raaijmakers J M. 2015. Diversity and functions of volatile organic compounds produced by Streptomyces from a disease-suppressive soil. Frontiers in Microbiology 6: 1081. https://doi.org/10.3389/fmicb.2015.01081

Derviş S and Özer G. 2023. Plant-associated Neoscytalidium dimidiatum - Taxonomy, host range, epidemiology, virulence, and management strategies: A comprehensive review. Journal of Fungi 9(11): 1048. https://doi.org/10.3390/jof9111048

Dy K S, Wonglom P, Pornsuriya C and Sunpapao A. 2022. Morphological, molecular identification and pathogenicity of Neoscytalidium dimidiatum causing stem canker of Hylocereus polyrhizus in southern Thailand. Plants 11(4): 504. https://doi.org/10.3390/plants11040504

Espinoza-Lozano L, Sumba M, Calero A, Jiménez M I and Quito-Avila D. 2023. First report of Neoscytalidium dimidiatum causing stem canker on yellow dragon fruit (Hylocereus megalantus) in Ecuador. Plant Disease 107(6): 1949. https://doi.org/10.1094/PDIS-06-22-1403-PDN

Fredriksson N J, Hermansson M and Wilén B-M. 2013. The choice of PCR primers has great impact on assessments of bacterial community diversity and dynamics in a wastewater treatment plant. PloS one 8(10): e76431. https://doi.org/10.1371/journal.pone.0076431

Fullerton R, Sutherland P, Rebstock R, Nguyen T H, Nguyen N A T, Dang T L, Ngo T K T and Nguyen V H. 2018. The life cycle of dragon fruit canker caused by Neoscytalidium dimidiatum and implications for control. Management 11: 71-80. https://doi.org/10.56669/RDWM5341

Gotor-Vila A, Teixidó N, Di Francesco A, Usall J, Ugolini L, Torres R and Mari M. 2017. Antifungal effect of volatile organic compounds produced by Bacillus amyloliquefaciens CPA-8 against fruit pathogen decays of cherry. Food Microbiology 64: 219-225. https://doi.org/10.1016/j.fm.2017.01.006

Hassan E A, Mostafa Y S, Alamri S, Hashem M and Nafady N A. 2021. Biosafe management of Botrytis grey mold of strawberry fruit by novel bioagents. Plants 10(12): 2737. https://doi.org/10.3390/plants10122737

Herrington P, Craig J and Sheridan J. 1987. Methyl vinyl ketone: A volatile fungistatic inhibitor from Streptomyces griseoruber. Soil Biology and Biochemistry 19(5): 509-512. https://doi.org/10.1016/0038-0717(87)90092-7

Islam T, Danishuddin, Tamanna N T, Matin M N, Barai H R and Haque M A. 2024. Resistance mechanisms of plant pathogenic fungi to fungicide, environmental impacts of fungicides, and sustainable solutions. Plants (Basel) 13(19): 2737. https://doi.org/10.3390/plants13192737

Lee S Y, Tindwa H, Lee Y S, Naing K W, Hong S H, Nam Y and Kim K Y. 2012. Biocontrol of anthracnose in pepper using chitinase, beta-1, 3 glucanase, and 2-furancarboxaldehyde produced by Streptomyces cavourensis SY224. Journal of Microbiology and Biotechnology 22(10): 1359-1366. https://doi.org/10.4014/jmb.1203.02056

Li X, Li B, Cai S, Zhang Y, Xu M, Zhang C, Yuan B, Xing K and Qin S. 2020. Identification of rhizospheric actinomycete Streptomyces lavendulae sps-33 and the inhibitory effect of its volatile organic compounds against Ceratocystis fimbriata in postharvest sweet potato (Ipomoea batatas (L.) Lam.). Microorganisms 8(3): 319. https://doi.org/10.3390/microorganisms8030319

Li X, Zhang Y, Wei Z, Guan Z, Cai Y and Liao X. 2016. Antifungal activity of isolated Bacillus amyloliquefaciens SYBC H47 for the biocontrol of peach gummosis. PloS one 11(9): e0162125. https://doi.org/10.1371/journal.pone.0162125

Lin S, Chen X, Xie L, Zhang Y, Zeng F, Long Y, Ren L, Qi X and Wei J. 2023. Biocontrol potential of lipopeptides produced by Paenibacillus polymyxa AF01 against Neoscytalidium dimidiatum in pitaya. Frontiers in Microbiology 14: 1188722. https://doi.org/10.3389/fmicb.2023.1188722

Mayorquin J S, Wang D H, Twizeyimana M and Eskalen A. 2016. Identification, distribution, and pathogenicity of Diatrypaceae and Botryosphaeriaceae associated with citrus branch canker in the southern California desert. Plant Disease 100(12): 2402-2413. https://doi.org/10.1094/PDIS-03-16-0362-RE

Mélida H, Sandoval-Sierra J V, Diéguez-Uribeondo J and Bulone V. 2013. Analyses of extracellular carbohydrates in oomycetes unveil the existence of three different cell wall types. Eukaryotic cell 12(2): 194-203. https://doi.org/10.1128/EC.00288-12

Mohd M H, Salleh B and Zakaria L. 2013. Identification and molecular characterizations of Neoscytalidium dimidiatum causing stem canker of red‐fleshed dragon fruit (Hylocereus polyrhizus) in Malaysia. Journal of Phytopathology 161(11-12): 841-849. https://doi.org/10.1111/jph.12146

Nguyen N A, Hua H M T, Ho N H Y, Nguyen T D H, Nguyen L H H, Tran T T T, Bui T L and Pham T V. 2020. Isolation, identification and characterization of bacterial antagonists of the dragon fruit fungal pathogen Neoscytalidium dimidiatum. Journal of Science and Technology-IUH 44(02): 76-85. https://doi.org/10.46242/jst-iuh.v44i02.1036

Noegrohati S, Sulasmi S, Hernadi E and Asviastuti S. 2019. Dissipation pattern of azoxystrobin and difenoconazole in red dragon fruit (Hylocereus polyrhizus) cultivated in Indonesian highland (West Java) and coastal area (DI Jogyakarta) and its implication for dietary risk assessment. Food Quality and Safety 3(2): 99-106. https://doi.org/10.1093/fqsafe/fyz009

Orellana C and Mattos L. 2019. Characterization and control of the causal agent of leaf spot in strawberry (Fragaria ananassa) under greenhouse conditions. Peruvian Journal of Agronomy 3(2): 57-67. https://doi.org/10.21704/pja.v3i2.1315

Özer G, Günen T U, Koşar İ, Güney İ G and Derviş S. 2022. First report of Neoscytalidium dimidiatum causing blight of Melissa officinalis in Turkey. Journal of Plant Diseases and Protection 129(1): 197-199. https://doi.org/10.1007/s41348-021-00522-2

Paul N C, Kim W-K, Woo S-K, Park M-S and Yu S-H. 2007. Fungal endophytes in roots of Aralia species and their antifungal activity. The Plant Pathology Journal 23(4): 287-294. https://doi.org/10.5423/PPJ.2007.23.4.287

Polizzi G, Aiello D, Vitale A, Giuffrida F, Groenewald J and Crous P. 2009. First report of shoot blight, canker, and gummosis caused by Neoscytalidium dimidiatum on citrus in Italy. Plant Disease 93(11): 1215-1215. https://doi.org/10.1094/PDIS-93-11-1215A

Rolshausen P, Akgül D, Perez R, Eskalen A and Gispert C. 2013. First report of wood canker caused by Neoscytalidium dimidiatum on grapevine in California. Plant Disease 97(11): 1511. https://doi.org/10.1094/PDIS-04-13-0451-PDN

Salunkhe V N, Bhagat Y S, Chavan S B, Lonkar S G and Kakade V D. 2023. First report of Neoscytalidium dimidiatum causing dragon fruit stem canker in India. Plant Disease 107(4): 1222. https://doi.org/10.1094/PDIS-04-22-0909-PDN

Serrato-Diaz L M and Goenaga R. 2021. First report of Neoscytalidium dimidiatum causing stem canker on dragon fruit (Hylocereus spp.) in Puerto Rico. Plant Disease 105(9): 2728. https://doi.org/10.1094/PDIS-10-20-2265-PDN

Taba S, Miyahira N, Nakazato M, Suzuki M, Suwa R and Sekine K T. 2022. Ecology of pitaya stem rot caused by Gilbertella persicaria and its biological control by phyllosphere bacteria. Plant Pathology 71(2): 426-436. https://doi.org/10.1111/ppa.13475

Wang C, Wang Z, Qiao X, Li Z, Li F, Chen M, Wang Y, Huang Y and Cui H. 2013. Antifungal activity of volatile organic compounds from Streptomyces alboflavus TD-1. FEMS microbiology letters 341(1): 45-51. https://doi.org/10.1111/1574-6968.12088

Wang F, Zhang R, Yuan Z and Chen P. 2021. Biological prevention and control of pitaya fruit canker disease using endophytic fungi isolated from papaya. Archives of Microbiology 203(7): 4033-4040. https://doi.org/10.1007/s00203-021-02378-4

Wang Q. 2015. Screening and identification of chitinolytic actinomycetes and study on the inhibitory activity against turfgrass root rot disease fungi. Journal of Biosciences and Medicines 3(03): 56. https://doi.org/10.4236/jbm.2015.33009

Wang S, Ruan C, Yi L, Deng L, Yao S and Zeng K. 2020. Biocontrol ability and action mechanism of Metschnikowia citriensis against Geotrichum citri-aurantii causing sour rot of postharvest citrus fruit. Food Microbiology 87: 103375. https://doi.org/10.1016/j.fm.2019.103375

Wu Y, Yuan J, E Y, Raza W, Shen Q and Huang Q. 2015. Effects of volatile organic compounds from Streptomyces albulus NJZJSA2 on growth of two fungal pathogens. Journal of basic microbiology 55(9): 1104-1117. https://doi.org/10.1002/jobm.201400906

Xie P, Zhang Y, Fang Z, Zhang S, Li H, Gao W and Sha S. 2024. First report of stem canker disease caused by Neoscytalidium dimidiatum on Euphrates Poplar in Xinjiang, China. Plant Disease 108(10): 3178. https://doi.org/10.1094/PDIS-12-23-2780-PDN

Xing M, Sun T, Liu T, Jiang Z and 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

Yi R H, ling lin Q, Mo J J, Wu F F and Chen J. 2015. Fruit internal brown rot caused by Neoscytalidium dimidiatum on pitahaya in Guangdong province, China. Australasian Plant Disease Notes 10: 1-4. https://doi.org/10.1007/s13314-015-0166-1

Zhang S, Wu Z, Yang Y and Li K. 2020. Antifungal action of antifungalmycin N2 against Rhizoctonia solani by disrupting cell membrane and inhibiting succinate dehydrogenase. Current Microbiology 77(2): 254-260. https://doi.org/10.1007/s00284-019-01837-y

Zhang X, Guo X, Wu C, Li C, Zhang D and Zhu B. 2020. Isolation, heterologous expression, and purification of a novel antifungal protein from Bacillus subtilis strain Z-14. Microbial Cell Factories 19: 1-10. https://doi.org/10.1186/s12934-020-01475-1

Zubrod J P, Bundschuh M, Arts G, Brühl C A, Imfeld G, Knäbel A, Payraudeau S, Rasmussen J J, Rohr J, Scharmüller A, Smalling K, Stehle S, Schulz R and Schäfer R B. 2019. Fungicides: An Overlooked Pesticide Class? Environmental Science & Technology 53(7): 3347-3365. https://doi.org/10.1021/acs.est.8b04392