Abstract
Nacobbus aberrans is an endophytic parasitic nematode that induces root galls, negatively affecting plant growth and development, and decreasing the production of economically important crops. Currently, low environmental impact alternatives are being developed for the control of nematodes, such as biological control agents, to reduce the use of soil disinfectants. Nematophagous fungi are microorganisms that can suppress nematode reproduction due to different mechanisms, such as parasitism of eggs, toxin production and stimulation of plant growth. The aim of this study was to investigate the effect of inoculation with nematophagous fungi on N. aberrans in greenhouse-grown pepper (Capsicum anuumm L.) plants and to analyze the response of the infected plants. Two fungal isolates, Purpureocillium lilacimum and Pleurotus ostreatus were tested. The plants were inoculated with these fungi at the time of transplantation in the presence and absence of N. aberrans. The reproduction factor of the nematode was 23.17; 5.90 and 36.4 for P. lilacinum, P. ostreatus and control, respectively. Both in plants parasitized and not parasitized by nematodes, the fungi increased the content of soluble proteins and photosynthetic pigments. Additionally, a favorable impact on growth parameters was also observed. This beneficial effect was also verified by a lower accumulation of proline and sugars, metabolites used by plants as osmoregulators in stress situations, and a low accumulation of malondialdehyde, a metabolite resulting from oxidative stress. These results show that both fungi are suitable for use in the biocontrol of N. aberrans and as growth promoters in plants.
Similar content being viewed by others
References
Abd-Elgawad MM, Askary TH (2018) Fungal and bacterial nematicides in integrated nematode management strategies. Egypt J Biol Pest Control 28(1):1–24. https://doi.org/10.1186/s41938-018-0080-x
Askary TH, Martinelli PRP (eds) (2015) Biocontrol agents of phytonematodes. CAB International. Wallingford, UK, pp 446–454
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for waterstress studies. Plant Soil 39(1):205–207. https://doi.org/10.1007/BF00018060
Bradford M (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Coolen WA (1979) Methods for the extraction of Meloidogyne spp. and other nematodes from roots and soil. In: Lamberti F, Taylor CE (eds) Root-knot Nematodes (Meloidogyne species) Systematics, Biology and Control. Academic Press, New York, U.S.A, pp 317–330
Cristóbal AJ, Cid del Prado I, Marbán-Mendoza N, Sánchez GP, Mora-Aguilera G, Manzanilla-López RH (2001) Sobrevivencia de estadíos biológicos de Nacobbus aberrans en condiciones de campo. Nematropica 31:229–235
Cronin D, Smith S (1979) A simple and rapid procedure for the analysis of reducing, total and individual sugars in potato. Potato Res 22:99–105. https://doi.org/10.1007/BF02366940
Elíades LA, Cabello MN, Voget C, Galarza B, Saparrat MCN (2010) Screening for alkaline keratinolytic activity in fungi isolated from soils of the biosphere reserve ‘“Parque Costero del Sur”’ (Argentina). World J Microbiol Biotechnol 26:2105–2111. https://doi.org/10.1007/s11274-010-0389-4
EPPO (2019) PQR-EPPO Database on Quarantine Pests. http://www.eppo.int
Gams W (1992) The analysis of communities of saprophytic microfungi with special reference to soil fungi. In: Winterhoff W (ed) Fungi in vegetation science Handbook of vegetation science, 19. Springer, Dordrecht. https://doi.org/10.1007/978-94-011-2414-0_7
Genier HLA, de Freitas Soares FE, de Queiroz JH, de Souza Gouveia A, Araújo JV, Braga FR, Kasuya MCM (2015) Activity of the fungus Pleurotus ostreatus and of its proteases on Panagrellus sp larvae. Afr J Biotechnol 14(17):1496–1503. https://doi.org/10.5897/AJB2015.14447
Golovko O, Kaczmarek M, Asp H, Bergstrand KJ, Ahrens L, Hultberg M (2022) Uptake of perfluoroalkyl substances, pharmaceuticals, and parabens by oyster mushrooms (Pleurotus ostreatus) and exposure risk in human consumption. Chemosphere 291:132–898. https://doi.org/10.1016/j.chemosphere.2021.132898
Gortari MC, Hours RA (2019) In vitro antagonistic activity of Argentinean isolates of Purpureocillium lilacinum on Nacobbus aberrans eggs. Curr Res Environ Appl Mycol 9(1):164–174. https://doi.org/10.5943/cream/9/1/14
Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198. https://doi.org/10.1016/0003-9861(68)90654-1
Hestbjerg H, Willumsen PA, Christensen M, Andersen O, Jacobsen CS (2003) Bioaugmentation of tar-contaminated soils under field conditions using Pleurotus ostreatus refuse from commercial mushroom production. Environ Toxicol Chem 22(4):692–698. https://doi.org/10.1002/etc.5620220402
Hussey RS, Barker KR (1973) A comparison of methods of collecting inocula of Meloidogyne spp., including a new technique. Plant Dis 57:1025–1028
Inalbon MC, Mocchiutti P, Zanuttini MA, Balatti PA, Rajchenberg M, Saparrat MC (2015) Applying ligninolytic fungi on Eucalyptus grandis wood for pulping pretreatment or fractionation. Procedía Mater Sci 8:1099–1107. https://doi.org/10.1016/j.mspro.2015.04.173
Jones JT, Haegeman A, Danchin EG, Gaur HS, Helder J, Jones MG, Perry RN (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Mol Plant Pathol 14(9):946–961. https://doi.org/10.1111/mpp.12057
Khun-in A, Sukhakul S, Chamswarng C, Tangkijchote P, Sasnarukkit A (2015) Culture filtrate of Pleurotus ostreatus isolate Poa3 effect on egg mass hatching and juvenile 2 of Meloidogyne incognita and its potential for biological control. J ISSAAS 21(1):46–54
Kiewnick S, Sikora RA (2006a) Biological control of the root-knot nematode Meloidogyne incognita by Paecilomyces lilacinus strain 251. Biol Control 38(2):179–187. https://doi.org/10.1016/j.biocontrol.2005.12.006
Kiewnick S, Sikora RA (2006b) Evaluation of Paecilomyces lilacinus strain 251 for the biological control of the northern root-knot nematode Meloidogyne hapla Chitwood. Nematology 8(1):69–78. https://doi.org/10.1163/156854106776179926
Kwok OCH, Plattner R, Weisleder D, Wicklow DT (1992) A nematicidal toxin from Pleurotus ostreatus NRRL 3526. J Chem Ecol 18(2):127–136. https://doi.org/10.1007/BF00993748
Lax P, Dueñas JCR, Coronel NB, Gardenal CN, Bima P, Doucet ME (2011) Host range study of Argentine Nacobbus aberrans sensu Sher populations and comments on the differential host test. Crop Prot 30(11):1414–1420. https://doi.org/10.1016/j.cropro.2011.06.001
Lax P, Marro N, Agaras B, Valverde C, Doucet ME, Becerra A (2013) Biological control of the false root-knot nematode Nacobbus aberrans by Pseudomonas protegens under controlled conditions. Crop Prot 52:97–102. https://doi.org/10.1016/j.cropro.2013.02.020
Luangsa-Ard J, Houbraken J, van Doorn T, Hong SB, Borman AM, Hywel-Jones NL, Samson RA (2011) Purpureocillium, a new genus for the medically important Paecilomyces lilacinus. FEMS Microbiol Lett 321(2):141–149. https://doi.org/10.1111/j.1574-6968.2011.02322.x
Manzanilla-López RH, Costilla MA, Doucet M, Franco J, Inserra RN, Lehman PS, Evans K (2002) The genus Nacobbus Thorne & Allen, 1944 (Nematoda: Pratylenchidae): systematics, distribution, biology and management. Nematropica 32:149–228
Mostafa DM, Awd Allah SFA, Awad-Allah EFA (2019) Potential of Pleurotus sajor-caju compost for controlling Meloidogyne incognita and improve nutritional status of tomato plants. J Plant Sci Phytopathol 3:118–127. https://doi.org/10.29328/journal.jpsp.1001042
Mukhtar T, Arshad Hussain M, Zameer Kayani M (2013) Biocontrol potential of Pasteuria penetrans, Pochonia chlamydosporia, Paecilomyces lilacinus and Trichoderma harzianum against Meloidogyne incognita in okra. Phytopathol Mediterr 52:66–76
Nesha R, Siddiqui ZA (2017) Effects of Paecilomyces lilacinus and Aspergillus niger alone and in combination on the growth, chlorophyll contents and soft rot disease complex of carrot. Sci Hortic 218:258–264. https://doi.org/10.1016/j.scienta.2016.11.027
Okorie CC, Ononuju CC, Okwujiako IA (2011) Management of Meloidogyne incognita with Pleurotus ostreatus and P. tuberregium in soybean. Int J Agric Biol 13(3):401–405
Oostenbrink, M (1966, September) Major characteristics of the relation between nematodes and plants. In: Proceedings of the 8th International Symposium of nematology, Antibes, France (8–14)
Papaspyridi LM, Aligiannis N, Christakopoulos P, Skaltsounis AL, Fokialakis N (2011) Production of bioactive metabolites with pharmaceutical and nutraceutical interest by submerged fermentation of Pleurotus ostreatus in a batch stirred tank bioreactor. Procedia Food Sci 1:1746–1752. https://doi.org/10.1016/j.profoo.2011.09.257
Puente M, García J, Rubio E, Perticari A (2010) Microorganismos promotores del crecimiento vegetal empleados como inoculantes en trigo. INTA–Estación Experimental Agropecuaria Rafaela. Publicación Miscelánea 116:39–44
Roy S, Barman S, Chakraborty U, Chakraborty B (2015) Evaluation of Spent Mushroom Substrate as biofertilizer for growth improvement of Capsicum annuum L. J Appl Biol Biotechno. https://doi.org/10.7324/JABB.2015.3305
Rumbos C, Mendoza A, Sikora R, Kiewnick S (2008) Persistence of the nematophagous fungus Paecilomyces lilacinus strain 251 in soil under controlled conditions. Biocontrol Sci Technol 18(10):1041–1050. https://doi.org/10.1080/09583150802526979
Sagüés MF, Purslow P, Fernández S, Fusé L, Iglesias L, Saumell C (2011) Hongos nematófagos utilizados para el control biológico de nematodos gastrointestinales en el ganado y sus formas de administración. Rev Iberoam Micol 28(4):143–147. https://doi.org/10.1016/j.riam.2011.06.009
Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144(3):307–313. https://doi.org/10.1016/S0176-1617(11)81192-2
Wille CN, Gomes CB, Minotto E, Nascimento JS (2019) Potential of aqueous extracts of basidiomycetes to control root-knot nematodes on lettuce. Hortic Bras 37:54–59. https://doi.org/10.1590/S0102-053620190108
Acknowledgements
The authors thank Laura Wahnan (CONICET) for the collaboration in field and laboratory tasks.
Funding
Financial support for this study was provided by PICT 2019–00207 to ANPCyT; the Proyecto de Incentivos a la Investigación (A344) and (A316) of the UNLP, Argentina; the grant provided by the Proyecto de Unidades Ejecutoras and PIP 11220200100527CO (CONICET), Argentina. National University of the Northwest of the Province of Buenos Aires (UNNOBA). EXP-0597/2019 approved by Resolution CS N ° 1623/2019.
Author information
Authors and Affiliations
Contributions
Performed the experiments, analyzed the data and wrote the paper: VFB Supervised the work, review and editing: MFR and MCNS Funding acquisition: MFR and MCNS All authors conceived and designed the experiment, contributed to the measurements, processing of the material and participated in the critical review of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
No potential conflict of interest was reported by the authors.
Ethical approval
There were no human and/or animal participants in the research.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Bernardo, V.F., Gonzalez, M.A., Garita, S.A. et al. Evaluation of two nematophagous fungi for the control of false root-knot nematode Nacobbus aberrans in pepper crops. J Gen Plant Pathol 89, 339–346 (2023). https://doi.org/10.1007/s10327-023-01145-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10327-023-01145-1