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Evaluation of Paecilomyces tenuis producing Huperzine A for the management of root-knot nematode Meloidogyne incognita (Nematoda: Meloidogynidae)

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Abstract

Root-knot nematodes (Meloidogyne spp.) are notorious plant-parasitic nematodes that affect agricultural crops. These obligate soil-dwelling parasites typically maneuver the host plant physiology by forming specialized feeding cells resulting in heavy yield losses. Scant management tools are available to effectively combat this pest. In an exploratory attempt of identifying new fungal biocontrol agent(s) for M. incognita from India, a Paecilomyces tenuis isolate from rhizosphere soil was found to incur > 90% mortality of the infective second-stage juveniles (J2s) at 24 h post-exposure to the fungal filtrate with about 87% parasitization. The fungal filtrate also significantly reduced the egg hatching and host-root penetration of M. incognita under in vitro and in vivo conditions revealing its effectiveness in curbing nematode pathogenicity with positive effects on plant growth. Chromatographic analyses revealed the presence of Huperzine A (433.56 mg L−1) in the P. tenuis isolate. Besides, the isolate possessed acetylcholinesterase inhibition attribute with an IC50 of 2.85 ± 0.12 mg mL−1 of the fungal filtrate. Further, GC-MS analysis revealed the production of other nematicidal compounds by the fungus including acetic acid. To conceptualize the mode of nematicidal action, RNA-Seq was done post-treatment of the M. incognita J2s and model worm Caenorhabditis elegans with fungal filtrate and pure Huperzine A. The transcriptomic profile unraveled the molecular intricacies underlying the nematicidal action affecting several biological pathways and developmental checkpoints of the nematode. Thus, the P. tenuis isolate offers significant potential to be used as a biocontrol agent against M. incognita along with its commercial use for Huperzine A production.

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Data availability

The raw reads were deposited in the NCBI Sequence Read Archive (SRA) database under the BioProject no. PRJNA800591; study accession no. SRP356762; Biosample accession nos. SAMN25258043 and SAMN25258042; and SRA accession nos. SRR17756040–SRR17756055.

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Acknowledgements

The authors sincerely acknowledge Dr. Jayarama D. Bhat, D. Sc., Formerly Professor of Botany, Goa University, Goa, India, for his constructive comments and suggestions during the manuscript preparation and final drafting. We also acknowledge Mr. Purshotam and Mr. Vivek for helping in culture maintenance.

Funding

This work was supported by the Genomics Assisted Crop Improvement and Management project under World Bank and Indian Council of Agricultural Research sponsored National Agricultural Higher Education Project-Centre for Advanced Agricultural Science and Technology (NAHEP-CAAST) project.

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Contributions

All authors contributed to the study conception and design. Material preparation and data collection were performed by RK, NJ, AH, JY, MC, CGB, JM, VSR and GC; analyses were performed by UR, VP, RK, RB, JG, AK and VSS; the first draft of the manuscript was written by RK, VP, NJ, VSS and UR; final drafting and critical revision of the manuscript were done by UR, VP and VSS. All authors commented on the previous versions of the manuscript. All authors read and approved the final manuscript.

Corresponding authors

Correspondence to Victor Phani, Vishal S. Somvanshi or Uma Rao.

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The authors have no relevant financial or non-financial interests to disclose.

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Communicated by Aurelio Ciancio.

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Kassam, R., Jaiswal, N., Hada, A. et al. Evaluation of Paecilomyces tenuis producing Huperzine A for the management of root-knot nematode Meloidogyne incognita (Nematoda: Meloidogynidae). J Pest Sci 96, 723–743 (2023). https://doi.org/10.1007/s10340-022-01521-4

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  • DOI: https://doi.org/10.1007/s10340-022-01521-4

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