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Potential Effects of Nematophagous Fungi Against Meloidogyne javanica Infection of Tomato Plants Under in vitro and in vivo Conditions

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Abstract

The root-knot nematode (RKN) Meloidogyne javanica is one of the most economically important plant pathogens. Due to the high toxicity of chemical nematicides, the use of nematophagous fungi represents a promising alternative in nematode management. These biological agents offer a more sustainable and environmentally friendly approach to controlling plant parasitic nematodes (PPNs). The present study aimed to isolate and evaluate the nematicidal activity of three nematophagous fungi, viz., Paraconiothyrium cyclothyrioides, Aspergillus oryzae, and Lecanicillium psalliotae, against M. javanica under laboratory and greenhouse conditions. Three densities (1 × 106, 1 × 107, and 1 × 108 spores/ml) of each fungus were used. In vitro, the results revealed that all the tested isolates were effective at inhibiting egg hatching and mortality in second juveniles (J2s). However, the mortality of J2s and hatching inhibition of eggs were proportional to the fungal concentration and duration of the exposure period. Among the isolates, A. oryzae at a concentration of 1 × 108 spores/ml had the highest percentage of egg-hatching inhibition (95.5%) after 72 h of incubation. The highest juvenile mortality (100%) was recorded for P. cyclothyrioides at 1 × 108 spores/ml after 72 h. The in vivo results showed that all the tested isolates significantly reduced the number of galls, egg masses, and eggs in tomato roots and J2s in soil. In general, the greatest reductions in the galling index (40%) and number of egg masses per root (88.8%) were recorded for P. cyclothyrioides at 1 × 108 spores/ml, while the greatest reductions in the numbers of eggs (96.7) and J2s (98.1) were recorded for A. oryzae at 1 × 108 spores/ml. Moreover, the treatment of soil with P. cyclothyrioides, A. oryzae, L. psalliotae, and NemGuard granules resulted in significant increases in root and shoot length; in contrast, a decrease in root fresh weight was observed. Therefore, these data suggest that the three isolates, viz., P. cyclothyrioides, A. oryzae, and L. psalliotae, are essential elements for integrated M. javanica control in tomato crops.

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The data that supports the findings of this study are available on request from the corresponding author.

References

  • Alves NM, Guimarães RA, Guimarães SSC, Faria AF, Santos IAFM, Medeiros FHV, Jank L, Cardoso PGA (2021) Trojan horse approach for white mold biocontrol: Paraconiothyrium endophytes promotes grass growth and inhibits Sclerotinia sclerotiorum. Biol Control 160:104685

    Article  Google Scholar 

  • Anisha C, Sachidanandan P, Radhakrishnan EK (2018) Endophytic Paraconiothyrium sp. from Zingiber officinale Rosc. displays broad-spectrum antimicrobial activity by producing danthron. Curr Microbiol 75:343–352

    Article  CAS  PubMed  Google Scholar 

  • Baker SE, Bennett JW (2008) An overview of the genus Aspergillus. In: Goldman GH, Osmani SA (eds) The Aspergilli: genomics, medical aspects, biotechnology, and research methods. CRC Press. Taylor and Francis, London, New York, pp 3–13

    Google Scholar 

  • Cao J, Wu X, Lin S (2012) Identification of fungus Lecanicillium psalliotae and its colonization in different life stages of Meloidogyne incognita. Sci Agric Sin 45:2404–2411

    CAS  Google Scholar 

  • Costa MGS, Garcia MJDM, Perdoná MJ, Wilcken SRS (2020) Resistance of macadamia walnut against Meloidogyne enterolobii and Meloidogyne javanica. Phytoparasitica 48:397–405

    Article  CAS  Google Scholar 

  • Daykin ME, Hussey RS (1985) Staining and histo-pathological techniques in nematology. In: Barker KR, Carter CC, Sasser JN (eds) An advanced treatise on Meloidogyne. North Carolina State University Graphics, Raleigh, pp 39–48

    Google Scholar 

  • Desaeger JA, Watson TT (2019) Evaluation of new chemical and biological nematicides for managing Meloidogyne javanica in tomato production and associated double crops in Florida. Pest Manag Sci 75:3363–3370

    Article  CAS  PubMed  Google Scholar 

  • Doyle J (1990) Isolation of plant DNA from fresh tissue. FOC 12:13–15

    Google Scholar 

  • El Aimani A, Mokrini F, Houari A, Laasli SE, Sbaghi M, Mentag R, Iraqi D, Udupa SM, Dababat AA, Lahlali R (2021) Potential of indigenous entomopathogenic nematodes for controlling tomato leaf miner, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) under laboratory and field conditions in Morocco. Physiol Mol Plant Pathol 116:101710

    Article  Google Scholar 

  • Fatima S, Khan F, Asif M, Alotaibi SS, Islam K, Shariq M, Khan A, Ikram M, Ahmad F, Khan TA et al (2022) Root-knot disease suppression in eggplant based on three growth ages of Ganoderma lucidum. Microorganisms 10:1068

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fortnum BA, Decoteau DR, Kasperbauer MJ, Bridges W (1995) Effect of colored mulch on root knot of tomato. Phytopathology 85:312–318

    Article  Google Scholar 

  • Gan Z, Yang J, Tao N, Liang L, Mi Q, Li J, Zhang KQ (2007) Cloning of the gene Lecanicillium psalliotae chitinase Lpchi1 and identification of its potential role in the biocontrol of root-knot nematode Meloidogyne incognita. Appl Microbiol Biotechnol 76:1309–1317

    Article  CAS  PubMed  Google Scholar 

  • Guédira A, Rammah A, Chlyah H, Chlyah B, Haïcour R (2004) Evaluation de la résistance à deux nématodes : Radopholus similis et Meloidogyne spp. Chez quatre génotypes de bananiers au Maroc. C R Biol 327:745–751

    Article  PubMed  Google Scholar 

  • Hajihassani A, Lawrence KS, Jagdale GB (2018) Plant parasitic nematodes in Georgia and Alabama. In: Subbotin SA, Chitambar JJ (eds) Plant parasitic nematodes in sustainable agriculture of North America. Northeastern, midwestern and southern USA. Springer, Cham, pp 357–391

    Chapter  Google Scholar 

  • Hooper DJ (1986) Extraction of free-living nematode stages from soil. In: Southey JF (ed) Laboratory methods for work with plant and soil nematodes. Her Majesty’s Stationery Office, London, pp 5–22

    Google Scholar 

  • Hu Y, Zhang W, Zhang P, Ruan W, Zhu X (2013) Nematicidal activity of chaetoglobosin A poduced by Chaetomium globosum NK102 against Meloidogyne incognita. J Agric Food Chem 61:41–46

    Article  CAS  PubMed  Google Scholar 

  • Huang SK, Maharachchikumbura SSN, Jeewon R, Bhat DJ, Phookamsak R, Hyde KD et al (2018) Lecanicillium subprimulinum (Cordycipitaceae, Hypocreales), a novel species from Baoshan, Yunnan. Phytotaxa 348:99–108

    Article  Google Scholar 

  • Hussain M, Zouhar M, Rysanek P (2017) Comparison between biological and chemical management of sugar beet nematode, Heterodera schachtii. Pak J Zool 49:45–50

    Article  CAS  Google Scholar 

  • Hussey RS, Barker KR (1973) A comparison of methods of collecting inocula of Meloidogyne spp., including a new technology. Plant Dis Rep 57:1025–1028

    Google Scholar 

  • Jan FG, Hamayun M, Moon YS, Jan G, Shafique M, Ali S (2022) Endophytic Aspergillus oryzae reprograms Abelmoschus esculentus L. to higher growth under salt stress via regulation of physiochemical attributes and antioxidant system. Biologia 77:2805–2818

    Article  CAS  Google Scholar 

  • Janati S, Houari A, Wifaya A, Essarioui A, Mimouni A, Hormatallah A, Sbaghi S, Dababat AA, Mokrini F (2018) Occurrence of the root-knot nematode species in vegetable crops in Souss region of Morocco. Plant Pathol J 34:308

    Article  PubMed  PubMed Central  Google Scholar 

  • Johnson LF, Curl EA (1972) Methods for research on the ecology of soil-borne plant pathogens. Burgess Publishing Company, Minneapolis, p 247

    Google Scholar 

  • Jones JT, Haegeman A, Danchin EG, Gaur HS, Helder J, Jones MG et al (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Mol Plant Pathol 14:946–961

    Article  PubMed  PubMed Central  Google Scholar 

  • Karssen G, Wesemael W, Moens M (2013) Root-knot nematodes. In: Perry RN, Moens M (eds) Plant nematology, 2nd edn. CABI, Wallingford, pp 73–108

    Chapter  Google Scholar 

  • Kepeneki L, Dura O, Dura S (2017) Determination of nematicidal effects of some bio pesticides against root-knot nematode Meloidogyne incognita on kiwifruit. J Agric Sci Technol 7:546–551

    Google Scholar 

  • Khan A, Sayed M, Shaukat SS, Handoo ZA (2008) Efficacy of four plant extracts on nematodes associated with papaya in Sindh, Pakistan. Nematol Medit 36:93–98

    Google Scholar 

  • Kim TY, Jang JY, Jeon SJ, Lee HW, Bae CH, Yeo JH, Lee HB, Kim IS, Park HW, Kim JC (2016) Nematicidal activity of kojic acid produced by Aspergillus oryzae against Meloidogyne incognita. J Microbiol Biotechnol 26:1383–1391

    Article  CAS  PubMed  Google Scholar 

  • Krif G, Mokrini F, Aissami AE, Laasli SE, Imren M, Özer G, Paulitz T, Lahlali R, Dababat AA (2020) Diversity and management strategies of plant parasitic nematodes in Moroccan organic farming and their relationship with soil physico-chemical properties. Agriculture 10:447

    Article  CAS  Google Scholar 

  • Krif G, Lahlali R, El Aissami A, Laasli SE, Mimouni A, Serderidis S, Picaud T, Moens A, Dababat AA, Fahad K, Mokrini F (2022) Efficacy of authentic bionematicides against the root-knot nematode, Meloidogyne javanica infecting tomato under greenhouse conditions. Physiol Mol Plant Pathol 118:101803

    Article  CAS  Google Scholar 

  • Kumar CS, Jacob TK, Devasahayam S, Thomas S, Geethu C (2018) Multifarious plant growth promotion by an entomopathogenic fungus Lecanicillium psalliotae. Microbiol Res 207:153–160

  • Lima FS, Correa VR, Nogueira SR, Santos PR (2017) Nematodes affecting soybean and sustainable practices for their management. In: Kasai M (ed) Soybean—the basis of yield, biomass and productivity. IntechOpen, London, pp 95–110

    Google Scholar 

  • Manzanilla-Lopez RH, Kenneth E, Bridge J (2004) Plant diseases caused by nematodes. In: Chen ZX, Chen SY, Dickson DW (eds) Nematology: advanced and perspectives. Nematode management and utilization, vol II. CAB International, Wallingford, pp 637–716

    Chapter  Google Scholar 

  • Mei X, Wang X, Li G (2021) Pathogenicity and volatile nematicidal metabolites from Duddingtonia flagrans against Meloidogyne incognita. Microorganisms 9:2268

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meyer SLF, Johnson G, Dimock M, Fahey JW, Huettel RN (1997) Field efficacy of Verticillium lecanii, sex pheromone, and pheromone analogs as potential management agents for soybean cyst nematode. J Nematol 29:282–288

    CAS  PubMed  PubMed Central  Google Scholar 

  • Na JI, Hui XU, LI WJ, Wang XY, Qian LI, LIU SS, Pei LI, Zhao JL, Heng JI (2017) Field evaluation of Streptomyces rubrogriseus HDZ-9-47 for biocontrol of Meloidogyne incognita on tomato. J Integr Agric 16:1347–57

  • Nazir K, Mukhtar T, Javed H (2019) In vitro effectiveness of silver nanoparticles against rootknot nematode (Meloidogyne incognita). Pak J Zool 51:2077–2083

    Article  CAS  Google Scholar 

  • Nelson LS (1998) The Anderson-Darling test for normality. J Qual Technol 30:298–299

  • Nguyen VN, Ju WT, Kim YJ, Jung WJ, Kim KY, Park RD (2014) Suppression of cucumber root-knot nematode Meloidogyne incognita by chitinolytic fungi Lecanicillium pasalliotae A‑1 and Lecanicillium antillanum B‑3. J Chitin Chitosan 19:93–99

    Google Scholar 

  • Noureddine Y, Rocha MD, An J, Médina C, Mejias J, Mulet K, Quentin M, Abad P, Zouine M, Favery B, Jaubert-Possamai S (2022) miR167-ARF8, an auxin-responsive module involved in the formation of root-knot nematode-induced galls in tomato. bioRxiv 2022–2027

    Book  Google Scholar 

  • Peiris PUS, Li Y, Brown P, Xu C (2020) Fungal biocontrol against Meloidogyne spp. in agricultural crops: a systematic review and meta-analysis. Biol Control 144:104235

    Article  CAS  Google Scholar 

  • Ruanpanun P, Laatsch H, Tangchitsomkid N, Lumyong S (2011) Nematicidal activity of fervenulin isolated from a nematicidal actinomycete, Streptomyces sp. CMU-MH021, on Meloidogyne incognita. World J Microbiol Biotechnol 27:1373–1380

    Article  CAS  PubMed  Google Scholar 

  • Saxena G (2018) Biological control of root-knot and cyst nematodes using nematophagous fungi. Root Biol: 221–237

  • Silva JDO, Santana MV, Freire LL, Ferreira BDS, Rocha MRD (2017) Biocontrol agents in the management of Meloidogyne incognita in tomato. Cien Rural 47:e20161053

    Article  Google Scholar 

  • Sissell K (2008) EPA bans carbofuran residues; sued over endosulfan. Chem Week 170:29

    Google Scholar 

  • de Souza GD, Santos IAFM, de Abreu LM, de Medeiros FHV, Duarte WF, Cardoso PG (2018) Endophytic fungi from Brachiaria grasses in Brazil and preliminary screening of Sclerotinia sclerotiorum antagonists. Sci Agric 77:e20180210

    Google Scholar 

  • Sun BT, Akutse KS, Xia XF, Chen JH, Ai X, Tang Y, Wang Q, Feng BW, Goettel MS, You MS (2018) Endophytic effects of Aspergillus oryzae on radish (Raphanus sativus) and its herbivore, Plutella xylostella. Planta 248:705–714

    Article  CAS  PubMed  Google Scholar 

  • Taylor AL, Sasser JN (1978) Biology, Identification and Control of Root-Knot Nematodes (Meloidogyne Species). North Carolina State University graphics, Raleigh, p 111

    Google Scholar 

  • Turhan G (1993) Mycoparasitism of Alternaria alternata by an additional eight fungi indicating the existence of further unknown candidates for biological control. J Phytopathol 138:283–292

    Article  Google Scholar 

  • Wang D, Jiao X, Jia H, Cheng S, Jin X, Wang Y, Gao Y, Su X (2022) Detection and quantification of Verticillium dahliae and V. longisporum by droplet digital PCR versus quantitative real-time PCR. Front Cell Infect Microbiol 12:995705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis M, Gelfand D, Sninsky J, White T (eds) PCR protocols: a guide to methods and applications. Academic Press, pp 315–322

    Google Scholar 

  • Williams TI, Edgington S, Owen A, Gange AC (2021) Evaluating the use of seaweed extracts against root knot nematodes: a meta-analytic approach. Appl Soil Ecol 168:104170

    Article  Google Scholar 

  • Yang JI, Stadler M, Chuang WY, Wu S, Ariyawansa HA (2020) In vitro inferred interactions of selected entomopathogenic fungi from Taiwan and eggs of Meloidogyne graminicola. Mycol Prog 19:97–109

    Article  CAS  Google Scholar 

  • Yang JK, Huang XW, Tian BY, Wang M, Niu QH, Zhang KQ (2005) Isolation and characterization of a serine protease from the nematophagous fungus, Lecanicillium psalliotae, displaying nematicidal activity. Biotechnol Lett 27:1123–1128

    Article  CAS  PubMed  Google Scholar 

  • Youssef M, El-Nagdi W, Lotfy DE (2020) Evaluation of the fungal activity of Beauveria bassiana, Metarhizium anisopliae and Paecilomyces lilacinus as biocontrol agents against root-knot nematode, Meloidogyne incognita on cowpea. Bull Natl Res Cent 44:1–11

    Article  Google Scholar 

  • Zekeya N, Mtambo M, Ramasamy S, Chacha M, Ndakidemi PA, Mbega ER (2019) First record of an entomopathogenic fungus of tomato leafminer, Tuta absoluta (Meyrick) in Tanzania. Biocontrol Sci Technol 29:626–637

    Article  Google Scholar 

  • Zhang J, Ma JY, Yang YL, Yao J, Huang AL, Gao LM, Zhao WJ (2003) GC-MS analysis of volatile constituents from Rhododendron anthopogonoides. Chin Tradit Herb Drugs 34:304–305

    CAS  Google Scholar 

  • Zhang PF, You YW, Song Y, Wang YZ, Zhang L (2015) First record of Aspergillus oryzae (Eurotiales: Trichocomaceae) as an entomopathogenic fungus of the locust, Locusta migratoria (Orthoptera: Acrididae). Biocontrol Sci Technol 25:1285–1298

    Article  CAS  Google Scholar 

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Authors and Affiliations

  1. Laboratory of Botany, Mycology and Environment, Faculty of Science, Mohammed V University, Rabat, Morocco

    Ghizlane Krif & Aicha El Aissami

  2. Biotechnology Research Unit, Laboratory of Nematology, Regional Center of Agricultural Research, INRA-Morocco, Rabat, Morocco

    Ghizlane Krif & Fouad Mokrini

  3. Integrated Crop Protection Research Unit, Laboratory of Nematology, Regional Center of Agricultural Research, INRA-Morocco, Agadir, Morocco

    Ghizlane Krif & Abdelaziz Mimouni

  4. Phytopathology Unit, Department of Plant Protection, Ecole Nationale d’Agriculture de Meknes, 50001, Meknes, Morocco

    Rachid Lahlali & Salah-Eddine Laasli

  5. International Maize and Wheat Improvement Center (CIMMYT), 06810, Ankara, Turkey

    Abdelfattah A. Dababat

  6. Laboratory of Biotechnology, Environment, Agri-Food, and Health, Faculty of Sciences Dhar El Mahraz, Sidi Mohammed Ben Abdellah University, 30050, Fez, Morocco

    Btissam Zoubi

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  1. Ghizlane Krif
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  2. Rachid Lahlali
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Correspondence to Fouad Mokrini.

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G. Krif, R. Lahlali, A. El Aissami, S.-E. Laasli,A. Mimouni, A.A. Dababat, B. Zoubi and F. Mokrini declare that they have no competing interests.

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Krif, G., Lahlali, R., El Aissami, A. et al. Potential Effects of Nematophagous Fungi Against Meloidogyne javanica Infection of Tomato Plants Under in vitro and in vivo Conditions. Journal of Crop Health (2024). https://doi.org/10.1007/s10343-024-00989-7

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