Bioefficacy of Trichoderma Species Against Javanese Root-Knot Nematode, Meloidogyne javanica, in Green Gram

Bioeffektivität von Trichoderma-Arten gegen den Wurzelgallennematoden Meloidogyne javanica bei Mungbohnen

Abstract

Root-knot nematodes are mainly controlled by using synthetic nematicides, but their excessive use is prohibited due to associated health hazards which demand for suitable alternatives. The overreliance on nematicides can be curtailed by using biological control agents possessing nematicidal or nematostatic properties. Therefore, in the present study, effectiveness of seven indigenous species of Trichoderma were tested for their ability to suppress the population of Javanese root-knot nematode, Meloidogyne javanica, and improve growth variables of green gram. All the Trichoderma species resulted in an increase in shoot and root lengths and shoot weight while a decrease was observed in root weight. Maximum increase in shoot length (45.5%) was found in case of T. harzianum followed by T. hamatum and T. viride whereas the increase was the minimum where T. pseudokoningii and T. koningii were applied. Similarly, maximum increase in shoot weight was recorded with T. viride (56.1%) followed by T. harzianum (55%) and the minimum with T. pseudokoningii. As regards root length, it was the maximum in treatments with T. hamatum (46.2%) and T. harzianum (45.1%) and minimum with those where T. koningii and T. pseudokoningii were applied. Contrarily, maximum reduction in root weight was observed in treatments where T. harzianum (37.8%) and T. viride (35.8%) were applied while T. koningii and T. pseudokoningii resulted in minimum decrease. All the Trichoderma species significantly caused reductions in the number of galls and eggs and reproductive factor of the nematode over control. Maximum reduction in numbers of galls and eggs were observed with T. viride (49 and 53%) followed by T. harzianum (46 and 53%) while the minimum reduction was recorded with T. pseudokoningii followed by T. atroviride. Likewise, T. viride caused the maximum reduction in reproductive factor of M. javanica (81%) followed by T. harzianum (78%) and T. asperellum (75%). On the other hand, the minimum reductions in reproductive factor were observed with T. pseudokoningii and T. koningii.

Zusammenfassung

Wurzelgallennematoden werden hauptsächlich mit synthetischen Nematiziden bekämpft, deren übermäßiger Einsatz jedoch aufgrund der damit verbundenen Gesundheitsgefahren verboten ist und nach geeigneten Alternativen verlangt. Der übermäßige Einsatz von Nematiziden kann durch die Verwendung von biologischen Bekämpfungsmitteln, die nematizide oder nematostatische Eigenschaften besitzen, eingedämmt werden. Daher wurde in der vorliegenden Studie die Wirksamkeit von sieben einheimischen Trichoderma-Arten auf ihre Fähigkeit getestet, die Population des Wurzelgallennematoden Meloidogyne javanica zu unterdrücken und die Wachstumsvariablen von Mungbohnen zu verbessern. Alle Trichoderma-Arten führten zu einer Zunahme der Spross- und Wurzellänge sowie des Sprossgewichts, während beim Wurzelgewicht eine Abnahme beobachtet wurde. Die maximale Zunahme der Sprosslänge (45,5 %) wurde bei T. harzianum festgestellt, gefolgt von T. hamatum und T. viride, während die Zunahme bei der Anwendung von T. pseudokoningii und T. koningii am geringsten war. In ähnlicher Weise wurde die maximale Zunahme des Sprossgewichts mit T. viride (56,1 %) verzeichnet, gefolgt von T. harzianum (55 %) und dem Minimum mit T. pseudokoningii. Die Wurzellänge war bei den Behandlungen mit T. hamatum (46,2 %) und T. harzianum (45,1 %) am höchsten und bei T. koningii und T. pseudokoningii am geringsten. Im Gegensatz dazu wurde die maximale Reduktion des Wurzelgewichts bei Behandlungen mit T. harzianum (37,8 %) und T. viride (35,8 %) beobachtet, während T. koningii und T. pseudokoningii zu einer minimalen Abnahme führten. Alle Trichoderma-Arten bewirkten eine signifikante Verringerung der Anzahl an Gallen und Eiern sowie des Reproduktionsfaktors des Nematoden gegenüber der Kontrolle. Die maximale Reduktion der Anzahl der Gallen und Eier wurde mit T. viride (49 und 53 %) beobachtet, gefolgt von T. harzianum (46 und 53 %), während die minimale Reduktion mit T. pseudokoningii, gefolgt von T. atroviride, festgestellt wurde. Ebenso verursachte T. viride die maximale Reduzierung des Reproduktionsfaktors von M. javanica (81 %), gefolgt von T. harzianum (78 %) und T. asperellum (75 %). Auf der anderen Seite wurden die geringsten Reduzierungen des Reproduktionsfaktors bei T. pseudokoningii und T. koningii beobachtet.

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References

  1. Affokpon A, Coyne DL, Htay CC, Agbèdè RD, Lawouin L, Coosemans J (2011) Biocontrol potential of native Trichoderma isolates against root-knot nematodes in West African vegetable production systems. Soil Biol Biochem 43(3):600–608

    CAS  Article  Google Scholar 

  2. Akladious SA, Abbas SM (2014) Application of Trichoderma harzianum T22 as a biofertilizer potential in maize growth. J Plant Nutr 37(1):30–49

    CAS  Article  Google Scholar 

  3. Al-Hazmi AS, Javeed MT (2016) Effects of different inoculum densities of Trichoderma harzianum and Trichoderma viride against Meloidogyne javanica on tomato. Saudi J Biol Sci 23:288–292

    PubMed  Article  Google Scholar 

  4. Anonymous (2018) Agricultural statistics of Pakistan. Ministry of Food, Agriculture and Live Stock, Agriculture and Livestock Division, Islamabad

    Google Scholar 

  5. Asghar A, Mukhtar T, Raja MU, Gulzar A (2020) Interaction between Meloidogyne javanica and Ralstonia solanacearum in chili. Pak J Zool 52:1525–1530

    Article  Google Scholar 

  6. Aslam MA, Javed K, Javed H, Mukhtar T, Bashir MS (2019a) Infestation of Helicoverpa armigera Hübner (Noctuidae: Lepidoptera) on soybean cultivars in Pothwar region and relationship with physico-morphic characters. Pak J Agric Sci 56(2):401–405

    Google Scholar 

  7. Aslam MN, Mukhtar T, Jamil M, Nafees M (2019b) Analysis of aubergine germplasm for resistance sources to bacterial wilt incited by Ralstonia solanacearum. Pak J Agri Sci 56(1):119–122

    Google Scholar 

  8. Azeem W, Mukhtar T, Hamid T (2021) Evaluation of Trichoderma harzianum and Azadirachta indica in the management of Meloidogyne incognita in Tomato. Pak J Zool 53(1):119–125

    Google Scholar 

  9. Bae S‑J, Mohanta TK, Chung JY, Ryu M, Park G, Shim S et al (2016) Trichoderma metabolites as biological control agents against Phytophthora pathogens. Biol Control 92:128–138

    CAS  Article  Google Scholar 

  10. Benitez T, Rincon AM, Limon MC, Codon AC (2004) Biocontrol mechanisms of Trichoderma strains. Int Microbiol 7(4):249–260

    CAS  PubMed  Google Scholar 

  11. Bhuiyan S, Garlick K, Anderson J, Wickramasinghe P, Stirling G (2018) Biological control of root-knot nematode on sugarcane in soil naturally or artificially infested with Pasteuria penetrans. Australas Plant Pathol 47(1):45–52

    CAS  Article  Google Scholar 

  12. Bokhari FM (2009) Efficacy of some Trichoderma species in the control of Rotylenchulus reniformis and Meloidogyne javanica. Arch Phytopathol Plant Protect 42(4):361–369

    CAS  Article  Google Scholar 

  13. Castagnone-Sereno P, Danchin EG, Perfus-Barbeoch L, Abad P (2013) Diversity and evolution of root-knot nematodes, genus Meloidogyne: new insights from the genomic era. Ann Rev Phytopathol 51:203–220

    CAS  Article  Google Scholar 

  14. Chen L‑L, Liu L‑J, Shi M, Song X‑Y, Zheng C‑Y, Chen X‑L, Zhang Y‑Z (2009) Characterization and gene cloning of a novel serine protease with nematicidal activity from Trichoderma pseudokoningii SMF2. FEMS Microbiol Lett 299(2):135–142

    CAS  PubMed  Article  Google Scholar 

  15. Dababat AA, Sikora RA, Hauschild R (2006) Use of Trichoderma harzianum and Trichoderma viride for the biological control of Meloidogyne incognita on tomato. Commun Agric Appl Biol Sci 71(3 Pt B):953–961

    CAS  PubMed  Google Scholar 

  16. d’Errico G, Marra R, Crescenzi A, Davino SW, Fanigliulo A, Woo SL, Lorito M (2019) Integrated management strategies of Meloidogyne incognita and Pseudopyrenochaeta lycopersici on tomato using a Bacillus firmus-based product and two synthetic nematicides in two consecutive crop cycles in greenhouse. Crop Prot 122:159–164

    Article  Google Scholar 

  17. Ghahremani Z, Escudero N, Saus E, Gabaldon T, Sorribas JF (2019) Pochonia chlamydosporia induces plant-dependent systemic resistance to Meloidogyne incognita. Front Plant Sci 10:945

    PubMed  PubMed Central  Article  Google Scholar 

  18. Ghazanfar MU, Raza M, Raza W, Qamar MI (2018) Trichoderma as potential biocontrol agent, its exploitation in agriculture: a review. Plant Prot 2:23–41

    Google Scholar 

  19. Giurgiu RM, Dumitraș A, Morar G, Scheewe P, Schroeder FG (2018) A study on the biological control of Fusarium oxysporum using Trichoderma spp., on soil and rockwool substrates in controlled environment. Notulae Bot Horti Agrobot Cluj Napoca 46(1):260–269

    CAS  Article  Google Scholar 

  20. Gulzar A, Mukhtar T, Wright DJ (2020) Effects of entomopathogenic nematodes Steinernema carpocapsae and Heterorhabditis bacteriophora on the fitness of a Vip3A resistant subpopulation of Heliothis virescens (Noctuidae: Lepidoptera). Bragantia 79(2):281–292

    Article  Google Scholar 

  21. Harman GE (2006) Overview of mechanisms and uses of Trichoderma spp. Phytopathology 96(2):190–194

    CAS  PubMed  Article  Google Scholar 

  22. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M (2004) Trichoderma species- opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2:43–56

    CAS  PubMed  Article  Google Scholar 

  23. Hhmau H, Wijesundera R, Chandrasekharan N, Wijesundera W, Kathriarachchi H (2015) Isolation and characterization of Trichoderma erinaceum for antagonistic activity against plant pathogenic fungi. Curr Res Environ Appl Mycol 5(2):120–127

    Article  Google Scholar 

  24. Huang W‑K, Cui J‑K, Liu S‑M, Kong L‑A, Wu Q‑S, Peng H, He W‑T, Sun J‑H, Peng D‑L (2016) Testing various biocontrol agents against the root-knot nematode (Meloidogyne incognita) in cucumber plants identifies a combination of Syncephalastrum racemosum and Paecilomyces lilacinus as being most effective. Biol Control 92:31–37

    Article  Google Scholar 

  25. Hussain MA, Mukhtar T (2019) Root-knot nematodes infecting okra in major vegetable growing districts of Punjab, Pakistan. Pak J Zool 51(3):1137–1143

    Article  Google Scholar 

  26. Iqbal U, Mukhtar T (2020a) Inhibitory effects of some fungicides against Macrophomina phaseolina causing charcoal rot. Pak J Zool 52(2):709–715

    CAS  Google Scholar 

  27. Iqbal U, Mukhtar T (2020b) Evaluation of biocontrol potential of seven indigenous Trichoderma species against charcoal rot causing fungus, Macrophomina phaseolina. Gesund Pflanz 72(2):195–202

    Article  Google Scholar 

  28. Javed K, Javed H, Mukhtar T, Qiu D (2019a) Efficacy of Beauveria bassiana and Verticillium lecanii for the management of whitefly and aphid. Pak J Agri Sci 56(3):669–674

    Google Scholar 

  29. Javed K, Javed H, Mukhtar T, Qiu D (2019b) Pathogenic effects of some entomopathogenic fungal strains against green peach aphid Myzus persicae (Homoptera: Aphididae). Egypt J Biol Pest Control 29:92. https://doi.org/10.1186/s41938-019-0183-z

    Article  Google Scholar 

  30. Jindapunnapat K, Chinnasri B, Kwankuae S (2013) Biological control of root-knot nematodes (Meloidogyne enterolobii) in guava by the fungus Trichoderma harzianum. J Dev Sus Agri 8:110–118

    Google Scholar 

  31. Jones JT, Haegeman A, Danchin EG, Gaur HS, Helder J, Jones MGK, Kikuchi T, Manzanilla-López R, Palomares-Rius JE, Wesemael WML, Perry RN (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Mol Plant Pathol 14(9):946–961

    PubMed  PubMed Central  Article  Google Scholar 

  32. Khan MTA, Mukhtar T, Saeed M (2019) Resistance or susceptibility of eight aubergine cultivars to Meloidogyne javanica. Pak J Zool 51(6):2187–2192

    CAS  Google Scholar 

  33. Lombardi N, Vitale S, Turra D, Reverberi M, Fanelli C, Vinale F, Marra R, Ruocco M, Pascale A, d’Errico G, Woo SL, Lorito M (2018) Root exudates of stressed plants stimulate and attract Trichoderma soil fungi. Mol Plant Microbe Interact 31(10):982–994

    CAS  PubMed  Article  Google Scholar 

  34. Lorito M, Woo SL, Harman GE, Monte E (2010) Translational research on Trichoderma: from omics to the field. Annu Rev Phytopathol 48:395–417

    CAS  PubMed  Article  Google Scholar 

  35. Martínez-Medina A, Fernandez I, Lok GB, Pozo MJ, Pieterse CM, Van Wees SC (2017) Shifting from priming of salicylic acid-to jasmonic acid-regulated defences by Trichoderma protects tomato against the root knot nematode Meloidogyne incognita. New Phytol 213(3):1363–1377

    PubMed  Article  CAS  Google Scholar 

  36. Mastouri F, Bjorkman T, Harman GE (2010) Seed treatment with Trichoderma harzianum alleviates biotic, abiotic, and physiological stresses in germinating seeds and seedlings. Phytopathology 100(11):1213–1221

    PubMed  Article  CAS  Google Scholar 

  37. Mukhtar T (2018) Management of root-knot nematode, Meloidogyne incognita, in tomato with two Trichoderma species. Pak J Zool 50(4):1589–1592

    Google Scholar 

  38. Mukhtar T, Hussain MA (2019) Pathogenic potential of Javanese root-knot nematode on susceptible and resistant okra cultivars. Pak J Zool 51(5):1891–1897

    Article  Google Scholar 

  39. Mukhtar T, Kayani MZ (2019) Growth and yield responses of fifteen cucumber cultivars to root-knot nematode (Meloidogyne incognita). Acta Sci Pol Hortorum Cultus 18(3):45–52

    Article  Google Scholar 

  40. Mukhtar T, Kayani MZ (2020) Comparison of the damaging effects of Meloidogyne incognita on a resistant and susceptible cultivar of cucumber. Bragantia 79(1):83–93

    Article  Google Scholar 

  41. Nazir K, Mukhtar T, Javed H (2019) In vitro effectiveness of silver nanoparticles against root-knot nematode (Meloidogyne incognita). Pak J Zool 51(6):2077–2083

    CAS  Article  Google Scholar 

  42. Ragozzino A, d’Errico G (2011) Interactions between nematodes and fungi: a concise review. Redia 94:123–125

    Google Scholar 

  43. Rao M, Kamalnath M, Umamaheswari R, Rajinikanth R, Prabu P, Priti K, Grace G, Chaya M, Gopalakrishnan C (2017) Bacillus subtilis IIHR BS‑2 enriched vermicompost controls root knot nematode and soft rot disease complex in carrot. Sci Hortic 218:56–62

    Article  Google Scholar 

  44. Reino JL, Guerrero RF, Hernández-Galán R, Collado IG (2008) Secondary metabolites from species of the biocontrol agent Trichoderma. Phytochem Rev 7(1):89–123

    CAS  Article  Google Scholar 

  45. Saikia SK, Tiwari S, Pandey R (2013) Rhizospheric biological weapons for growth enhancement and Meloidogyne incognita management in Withania somnifera cv. Poshita. Biol Control 65(2):225–234

    Article  Google Scholar 

  46. Sharon E, Bareyal M, Chet I, Herreraestrella A, Kleifeld O, Spiegel Y (2001) Biological control of the root-knot nematode Meloidogyne javanica by Trichoderma harzianum. Phytopathology 91(7):687–693

    CAS  PubMed  Article  Google Scholar 

  47. Sharon E, Chet I, Viterbo A, Bar-Eyal M, Nagan H, Samuels GJ, Spiegel Y (2007) Parasitism of Trichoderma on Meloidogyne javanica and role of the gelatinous matrix. Eur J Plant Pathol 118:247–258

    Article  Google Scholar 

  48. Sonkar SS, Bhatt J, Meher J, Kashyap P (2018) Bio-efficacy of Trichoderma viride against the root-knot nematode (Meloidogyne incognita) in tomato plant. J Pharmacogn Phytochem 7(6):2010–2014

    CAS  Google Scholar 

  49. Spiegel Y, Sharon E, Chet I (2005) Mechanisms and improved biocontrol of the root-knot nematodes by Trichoderma spp. Acta Hortic 698:225–228

    Article  Google Scholar 

  50. Suarez B, Rey M, Castillo P, Monte E, Llobell A (2004) Isolation and characterization of PRA1, a trypsin-like protease from the biocontrol agent Trichoderma harzianum CECT 2413 displaying nematicidal activity. Appl Microbiol Biotechnol 65(1):46–55

    CAS  PubMed  Article  Google Scholar 

  51. Tariq-Khan M, Mukhtar T, Munir A, Hallmann J, Heuer H (2020) Comprehensive report on the prevalence of root-knot nematodes in the Poonch division of Azad Jammu and Kashmir, Pakistan. J Phytopathol 168:322–336

    CAS  Article  Google Scholar 

  52. Trudgill DL, Blok VC (2001) Apomictic, polyphagous root-knot nematodes: exceptionally successful and damaging biotrophic root pathogens. Ann Rev Phytopathol 39(1):53–77

    CAS  Article  Google Scholar 

  53. Vinale F, Sivasithamparam K, Ghisalberti EL, Marra R, Woo SL, Lorito M (2008) Trichoderma-plant-pathogen interactions. Soil Biol Biochem 40(1):1–10

    CAS  Article  Google Scholar 

  54. Xiao-Yan S, Qing-Tao S, Shu-Tao X, Xiu-Lan C, Cai-Yun S, Yu-Zhong Z (2006) Broadspectrum antimicrobial activity and high stability of Trichokonins from Trichoderma koningii SMF2 against plant pathogens. FEMS Microbiol Lett 260(1):119–125

    PubMed  Article  CAS  Google Scholar 

  55. Yang Z, Yu Z, Lei L, Xia Z, Shao L, Zhang K, Li G (2012) Nematicidal effect of volatiles produced by Trichoderma sp. J Asia Pac Entomol 15(4):647–650

    CAS  Article  Google Scholar 

  56. Yang Z‑S, Li G‑H, Zhao P‑J, Zheng X, Luo S‑L, Li L, Niu X‑M, Zhang K‑Q (2010) Nematicidal activity of Trichoderma spp. and isolation of an active compound. World J Microbiol Biotechnol 26(12):2297–2302

    CAS  Article  Google Scholar 

  57. Zhang S, Gan Y, Xu B (2015) Biocontrol potential of a native species of Trichoderma longibrachiatum against Meloidogyne incognita. Appl Soil Ecol 94:21–29

    Article  Google Scholar 

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Correspondence to Tariq Mukhtar.

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T. Mukhtar, M. Tariq-Khan and M.N. Aslam declare that they have no competing interests.

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Mukhtar, T., Tariq-Khan, M. & Aslam, M.N. Bioefficacy of Trichoderma Species Against Javanese Root-Knot Nematode, Meloidogyne javanica, in Green Gram. Gesunde Pflanzen (2021). https://doi.org/10.1007/s10343-021-00544-8

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Keywords

  • Biocontrol
  • Root-knot nematode
  • Trichoderma species
  • Vigna radiata L
  • Growth variables
  • Nematode infestations

Schlüsselwörter

  • Biokontrolle
  • Wurzelgallennematode
  • Trichoderma-Arten
  • Vigna radiata L
  • Wachstumsvariablen
  • Nematodenbefall