Nematicidal activity of Trichoderma harzianum-derived secondary metabolites against Meloidogyne incognita and metabolomic profiling of selected potent isolates

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ANKARDIANSYAH PANDU PRADANA
SOFIATUS SHOLEHAH
DWI ROSIDAH ANDRIYANI
MOHAMMAD HOESAIN
WIDI ASTUTI
RAHMI UTAMI HADIANI
RACHMI MASNILAH
MUH ADIWENA
DIANA PUTRI

Abstract

Abstract. Pradana AP, Sholehah S, Andriyani DR, Hoesain M, Astuti W, Hadiani RU, Masnilah R, Adiwena M, Putri D. 2025. Nematicidal activity of Trichoderma harzianum-derived secondary metabolites against Meloidogyne incognita and metabolomic profiling of selected potent isolates. Asian J Agric 9: 326-338. Root-knot nematodes, especially Meloidogyne incognita, reduce global crop yields, necessitating the development of safe and effective management approaches. While chemical nematicides can mitigate infestations, they often present environmental concerns and potentially foster resistance in target nematodes. Consequently, using antagonistic fungi, particularly Trichoderma harzianum, has gained traction as an eco-friendly solution. Nonetheless, the viability of T. harzianum under field conditions is often compromised by abiotic and biotic factors. This study investigated the nematicidal efficacy and secondary metabolite composition of four T. harzianum isolates (AJG, TGL, SBS, and SKS) collected from distinct geographical regions. In vitro assays revealed that the AJG and TGL isolates elicited the most potent effects, achieving >75% egg-hatching inhibition and >93% juvenile mortality at 168 hours post-treatment. Gas chromatography-mass spectrometry indicated that fatty acid esters, including methyl palmitate and methyl oleate, were the major contributors to nematicidal effects through membrane disruption. Notable differences in metabolite profiles between isolates highlight isolate-specific biochemical pathways impacting suppressive capacity. The predominance of fatty acids underscores their critical function in controlling nematodes, offering prospects for developing stable, environmentally friendly formulations. These results underscore the potential of T. harzianum-derived metabolites for integrated nematode management. They also emphasize the importance of isolate selection and metabolite profiling in designing targeted, sustainable strategies to combat root-knot nematodes, empowering the audience with this crucial knowledge.

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PRADANA, A. P. ., SHOLEHAH, S. ., ANDRIYANI, D. R. ., HOESAIN, M. ., ASTUTI, W. ., HADIANI, R. U. ., MASNILAH, R. ., ADIWENA, M. ., & PUTRI, D. . (2025). Nematicidal activity of Trichoderma harzianum-derived secondary metabolites against Meloidogyne incognita and metabolomic profiling of selected potent isolates. Asian Journal of Agriculture, 9(1). https://doi.org/10.13057/asianjagric/g090134

References

Adiwena M, Murtilaksono A, Egra S, Hoesain M, Asyiah IN, Pradana AP, Izatika ZN. 2023. The effects of micronutrient-enriched media on the efficacy of Bacillus subtilis as biological control agent against Meloidogyne incognita. Biodiversitas Journal of Biological Diversity 24(1): 33-39. DOI: 10.13057/biodiv/d240105.

Asyiah IN, Mudakir I, Budiman A, Pradana AP. 2025. Media optimization for nematode-trapping fungus Orbilia jesu-laurae and its effect in managing Meloidogyne incognita. Cogent Food & Agriculture 11(1): 2442667. DOI: 10.1080/23311932.2024.2442667.

Ayaz M, Li C-H, Ali Q, Zhao W, Chi Y-K, Shafiq M, Ali F, Yu X-Y, Yu Q, Zhao J-T. 2023. Bacterial and fungal biocontrol agents for plant disease protection: Journey from lab to field, current status, challenges, and global perspectives. Molecules 28(18): 6735. DOI: 10.3390/molecules28186735.

Azlay L, El Boukhari MEM, Mayad EH, Barakate M. 2023. Biological management of root-knot nematodes (Meloidogyne spp.): a review. Organic Agriculture 13(1): 99-117. DOI: 10.1007/s13165-022-00417-y.

Baazeem A, Almanea A, Manikandan P, Alorabi M, Vijayaraghavan P, Abdel-Hadi A. 2021. In vitro antibacterial, antifungal, nematocidal and growth promoting activities of Trichoderma hamatum FB10 and its secondary metabolites. Journal of Fungi 7(5): 331. DOI: 10.3390/jof7050331.

Calvo AM, Wilson RA, Bok JW, Keller NP. 2002. Relationship between secondary metabolism and fungal development. Microbiology and Molecular Biology Reviews 66(3): 447-459. DOI: 10.1128/MMBR.66.3.447-459.2002.

Chen Y-C, Seyedsayamdost MR, Ringstad N. 2020. A microbial metabolite synergizes with endogenous serotonin to trigger C. elegans reproductive behavior. Proceedings of the National Academy of Sciences 117(48): 30589-30598. DOI: 10.1073/pnas.2017918117.

Devi G. 2018. Utilization of nematode destroying fungi for management of plant-parasitic nematodes-a review. Biosciences Biotechnology Research Asia 15(2): 377-396. DOI: 10.13005/bbra/2642.

Elbanhawy AA, Elsherbiny EA, Abd El-Mageed AE, Abdel-Fattah GM. 2019. Potential of fungal metabolites as a biocontrol agent against cotton aphid, Aphis gossypii Glover and the possible mechanisms of action. Pesticide Biochemistry and Physiology 159: 34-40. DOI: 10.1016/j.pestbp.2019.05.013.

Eloh K, Demurtas M, Deplano A, Ngoutane Mfopa A, Murgia A, Maxia A, Onnis V, Caboni P. 2015. In vitro nematicidal activity of aryl hydrazones and comparative GC-MS metabolomics analysis. Journal of Agricultural and Food Chemistry 63(45): 9970-9976. DOI: 10.1021/acs.jafc.5b04815.

Fabiyi OA, Baker MT, Olatunji GA. 2022. Application of fatty acid esters on Meloidogyne incognita infected jew's mallow plants. Pakistan Journal of Nematology 40(2): 127-137. DOI: 10.17582/journal.pjn/2022/40.2.127.137.

Feyisa B, Lencho A, Selvaraj T, Amb P, Getaneh G. 2016. Evaluation of some botanicals and Trichoderma harzianum for the management of tomato root-knot nematode (Meloidogyne incognita (Kofoid and White) Chit Wood). Advances in Crop Science and Technology 4: 201. DOI: 10.5897/JEN2015.0145.

Forghani F, Hajihassani A. 2020. Recent advances in the development of environmentally benign treatments to control root-knot nematodes. Frontiers in Plant Science 11: 1125. DOI: 10.3389/fpls.2020.01125.

Ghazanfar MU, Raza M, Raza W, Qamar MI. 2018. Trichoderma as potential biocontrol agent, its exploitation in agriculture: a review. Plant Protection 2(3): 109-135.

Goyal S, Ramawat KG, Mérillon J-M. 2017. Different shades of fungal metabolites: an overview. Fungal Metabolites. Springer.

Hamrouni R, Regus F, Farnet Da Silva A-M, Orsiere T, Boudenne J-L, Laffont-Schwob I, Christen P, Dupuy N. 2025. Current status and future trends of microbial and nematode-based biopesticides for biocontrol of crop pathogens. Critical Reviews in Biotechnology 45(2): 333-352. DOI: 10.1080/07388551.2024.2370370.

Helal NM, Ibrahim N, Khattab H. 2019. Phytochemical analysis and antifungal bioactivity of Pulicaria undulata (L.) methanolic extract and essential oil. Egyptian Journal of Botany 59(3): 827-844. DOI: 10.21608/ejbo.2019.12259.1308.

Keller NP. 2019. Fungal secondary metabolism: regulation, function and drug discovery. Nature Reviews Microbiology 17(3): 167-180. DOI: 10.1038/s41579-018-0121-1.

Keswani C, Singh HB, Hermosa R, García-Estrada C, Caradus J, He Y-W, Mezaache-Aichour S, Glare TR, Borriss R, Vinale F. 2019. Antimicrobial secondary metabolites from agriculturally important fungi as next biocontrol agents. Applied Microbiology and Biotechnology 103: 9287-9303. DOI: 10.1007/s00253-019-10209-2.

Khan A, Aiman SI, Baber Y, Hassan F, Usman HM, Sohail MA, Abbas A. 2021. An overview of root-knot nematodes and their management. Journal of Entomology and Zoology Studies 9: 35-40.

Khan RAA, Najeeb S, Mao Z, Ling J, Yang Y, Li Y, Xie B. 2020. Bioactive secondary metabolites from Trichoderma spp. against phytopathogenic bacteria and root-knot nematode. Microorganisms 8(3): 401. DOI: 10.3390/microorganisms8030401.

Lopes A, Rivadavea W, Silva G. (2024). Trichoderma secondary metabolites for effective plant pathogen control. Nanohybrid Fungicides. Elsevier.

Lu Q, Liu T, Wang N, Dou Z, Wang K, Zuo Y. 2020. Nematicidal effect of methyl palmitate and methyl stearate against Meloidogyne incognita in bananas. Journal of Agricultural and Food Chemistry 68(24): 6502-6510. DOI: 10.1021/acs.jafc.0c00218.

Mansour T, Radwan WH, Mansour M, Gomaa M, Farouk F, Shepl M, Soliman AG, Abd-Elhalim BT, El-Senosy MM, Bakry A. 2023. Larvicidal potential, toxicological assessment, and molecular docking studies of four Egyptian bacterial strains against Culex pipiens L.(Diptera: Culicidae). Scientific Reports 13(1): 17230. DOI: 10.1038/s41598-023-44279-0.

Moo-Koh FA, Cristóbal-Alejo J, Andrés MF, Martín J, Reyes F, Tun-Suárez JM, Gamboa-Angulo M. 2022. In vitro assessment of organic and residual fractions of nematicidal culture filtrates from thirteen tropical Trichoderma strains and metabolic profiles of most-active. Journal of Fungi 8(1): 82. DOI: 10.3390/jof8010082.

Pathak VM, Verma VK, Rawat BS, Kaur B, Babu N, Sharma A, Dewali S, Yadav M, Kumari R, Singh S. 2022. Current status of pesticide effects on environment, human health and it’s eco-friendly management as bioremediation: A comprehensive review. Frontiers in Microbiology 13: 962619. DOI: 10.3389/fmicb.2022.962619.

Rangel LI, Hamilton O, de Jonge R, Bolton MD. 2021. Fungal social influencers: secondary metabolites as a platform for shaping the plant?associated community. The Plant Journal 108(3): 632-645. DOI: 10.1111/tpj.15490.

Rodrigo S, García-Latorre C, Santamaria O. 2021. Metabolites produced by fungi against fungal phytopathogens: Review, implementation and perspectives. Plants 11(1): 81. DOI: 10.3390/plants11010081.

Sall C, Djigal D, Faye O, Soumboundou M, Ndong A, Ndao M, Sylla SM. 2024. Chemical composition and evaluation of the nematicidal activity of Datura metel seed oil against Meloidogyne javanica. Journal of Agricultural Chemistry and Environment 14(1): 90-101. DOI: 10.4236/jacen.2025.141006.

Saravanan R, Saranya N, Ragapriya V, Rajaswaminathan V, Kavino M, Krishnamoorthy A, Nakkeeran S. 2022. Nematicidal property of clindamycin and 5-hydroxy-2-methyl furfural (HMF) from the banana endophyte Bacillus velezensis (YEBBR6) against banana burrowing nematode Radopholus similis. Indian Journal of Microbiology 62(3): 364-373. DOI: 10.1007/s12088-022-01011-2.

Sergany M. 2024. Efficacy of certain organic extracts at three concentrations on tomato plants infected with the root-knot nematode with reference to GC-MS analysis. Egyptian Journal of Plant Protection Research Institute 7(4): 448-463. DOI: 10.4314/ejppri.v7i4.2.

Shahriar SA, Islam MN, Chun CNW, Kaur P, Rahim MA, Islam MM, Uddain J, Siddiquee S. 2022. Microbial metabolomics interaction and ecological challenges of Trichoderma species as biocontrol inoculant in crop rhizosphere. Agronomy 12(4): 900. DOI: 10.3390/agronomy12040900.

Soesanto L, Mugiastuti E, Manan A. 2019. Raw secondary metabolites application of two Trichoderma harzianum isolates towards vascular streak dieback on cocoa seedlings. Pelita Perkebunan 35(1): 22-32. DOI: 10.22302/iccri.jur.pelitaperkebunan.v35i1.346.

Sood M, Kapoor D, Kumar V, Sheteiwy MS, Ramakrishnan M, Landi M, Araniti F, Sharma A. 2020. Trichoderma: The “secrets” of a multitalented biocontrol agent. Plants 9(6): 762. DOI: https://doi.org/10.3390/plants9060762.

Subedi S, Thapa B, Shrestha J. 2020. Root-knot nematode (Meloidogyne incognita) and its management: a review. Journal of Agriculture and Natural Resources 3(2): 21-31. DOI: 10.3126/janr.v3i2.32298.

Tapia-Vázquez I, Montoya-Martínez AC, De los Santos-Villalobos S, Ek-Ramos MJ, Montesinos-Matías R, Martínez-Anaya C. 2022. Root-knot nematodes (Meloidogyne spp.) a threat to agriculture in Mexico: Biology, current control strategies, and perspectives. World Journal of Microbiology and Biotechnology 38(2): 26. DOI: 10.1007/s11274-021-03211-2.

Tudi M, Daniel Ruan H, Wang L, Lyu J, Sadler R, Connell D, Chu C, Phung DT. 2021. Agriculture development, pesticide application and its impact on the environment. International journal of environmental research and public health 18(3): 1112. DOI: 10.3390/ijerph18031112.

Vieira AF, Xatse MA, Murray SY, Olsen CP. 2023. Oleic acid metabolism in response to glucose in C. elegans. Metabolites 13(12): 1185. DOI: 10.3390/metabo13121185.

Wang X-Y, Xu T-T, Sun L-J, Cen R-H, Su S, Yang X-Q, Yang Y-B, Ding Z-T. 2021. The chemical diversity, the attractant, anti-acetylcholinesterase, and antifungal activities of metabolites from biocontrol Trichoderma harzianum uncovered by OSMAC strategy. Bioorganic Chemistry 114: 105148. DOI: 10.1016/j.bioorg.2021.105148.

Yan L, Khan RAA. 2021. Biological control of bacterial wilt in tomato through the metabolites produced by the biocontrol fungus, Trichoderma harzianum. Egyptian Journal of Biological Pest Control 31: 1-9. DOI: 10.1186/s41938-020-00351-9.

Yao X, Guo H, Zhang K, Zhao M, Ruan J, Chen J. 2023. Trichoderma and its role in biological control of plant fungal and nematode disease. Frontiers in Microbiology 14: 1160551. DOI: 10.3389/fmicb.2023.1160551.

Zaid R, Koren R, Kligun E, Gupta R, Leibman-Markus M, Mukherjee PK, Kenerley CM, Bar M, Horwitz BA. 2022. Gliotoxin, an immunosuppressive fungal metabolite, primes plant immunity: evidence from Trichoderma virens-tomato interaction. MBio 13(4): e00389-00322. DOI: 10.1128/mbio.00389-22.

Zeilinger S, Gruber S, Bansal R, Mukherjee PK. 2016. Secondary metabolism in Trichoderma–chemistry meets genomics. Fungal Biology Reviews 30(2): 74-90. DOI: 10.1016/j.fbr.2016.05.001.

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