Drechslerella dactyloides and Dactylaria brochopaga mediated induction of defense related mediator molecules in tomato plants pre-challenged with Meloidogyne incognita

  • Udai B. SinghEmail author
  • Shailendra Singh
  • Wasiullah Khan
  • Deepti Malviya
  • Pramod K. Sahu
  • Rajan Chaurasia
  • Sushil K. Sharma
  • A. K. Saxena
Research Article


The present investigation was aimed to isolate and characterize the strains of Drechslerella dactyloides and Dactylaria brochopaga from decaying root galls of tomato in order to investigate their role in reprogramming of root apoplast that enhance defence responses in tomato pre-challenged with Meloidogyne incognita. Out of 23 strains of D. brochopaga and D. dactyloides were isolated from decaying root galls of tomato, three strains of D. dactyloides and five strains of D. brochopaga were found effective and these were selected for further characterization under controlled laboratory conditions. Further, D. dactyloides NDAd-05 and D. brochopaga NDDb-15 were found most promising strains for control of M. incognita. The study elucidates multifarious effects of D. dactyloides NDAd-05 and D. brochopaga NDDb-15 inoculated either individually or in combination on tomato plants pre-challenged with M. incognita under nethouse conditions. Results of this investigation revealed that inoculation of D. dactyloides NDAd-05 and D. brochopaga NDDb-15 increased various attributes in plants to significant degree conferring defence against M. incognita. Both the strains were found to have potential to enhance site-specific accumulation and activation of defence-related mediator molecules, enzymes and thus, exhibited biocontrol potential against M. incognita. Further, application of D. dactyloides NDAd-05 and D. brochopaga NDDb-15 not only assisted in the growth promotion but also activated phenylpropanoid pathway in root apoplast in addition to direct trapping of M. incognita.


Nematode trapping fungi Drechslerella dactyloides Dactylaria brochopaga Induced systemic resistance Root-knot disease 



We would like to express our special thanks to Dr. R.K. Singh and Dr. K.P. Singh, Department of Mycology and Plant Pathology, Institute of Agricultural Sciences, BHU, Varanasi for providing technical support to carry out a part of this research work. Our special thanks goes to Science and Engineering Research Board (SERB), Department of Science and Technology, Ministry of Science & Technology, Government of India for providing financial support to Udai B. Singh, under Fast Track Scheme for Young Scientist (SR/FT/LS-42/2012) to carry out the research work.


  1. Anastasiadis IA, Giannakou IO, Prophetou-Athanasiadou DA, Gowen SR (2008) The combined effect of the application of a biocontrol agent Paecilomyces lilacinus, with various practices for the control of RKNs. Crop Protect 27:352–361CrossRefGoogle Scholar
  2. Anonymous (1986) Annual report. Plant Pathology Division, Gazipur, p 68Google Scholar
  3. Barron GL (1977) The nematode destroying fungi. Canadian biological. Publication Ltd., Guelph, p 140Google Scholar
  4. Bhatti DS (1994) Management of phytonematodes: an introduction. In: Bhatti DS, Walia RK (eds) Nematode pest management in crops. CBS Publication and Distributors, New Delhi, pp 1–6Google Scholar
  5. Bordallo JJ, Lopez-Llorca LV, Jansson HB, Salinas J et al (2002) Colonization of plant roots by egg-parasitic and nematode trapping fungi. New Phytol 154:491–499CrossRefGoogle Scholar
  6. Bridge J, Page SJ, Jordan W (1981) An improved method for staining nematodes in roots. Report Rothamsted Experimental Station, Harpenden, p 171Google Scholar
  7. Ciancio A, Colagiero M, Pentimone I, Rosso LC (2016) Formulation of Pochonia chlamydosporia for plant and nematode management. In: Arora N, Mehnaz S, Balestrini R (eds) Bioformulations: for sustainable agriculture. Springer, New Delhi, pp 177–197Google Scholar
  8. Clarke CR, Vinatzer BA (2017) Characterizing the immune-eliciting activity of putative microbe-associated molecular patterns in tomato. Methods Mol Biol 1578:249–261CrossRefGoogle Scholar
  9. Cooke RC, Godfrey BES (1964) A key to the nematode destroying fungi. Trans Brit Mycol Soc 51:555–561CrossRefGoogle Scholar
  10. den Belder E, Jansen E (1994) Capture of Plant parasitic nematodes by adhesive hyphae forming isolate of Arthrobotrys oligospora and some other nematode trapping fungi. Nematologica 40:423–437CrossRefGoogle Scholar
  11. Djian-Caporalino C, Molinari S, Palloix A et al (2011) The reproductive potential of the root-knot nematode Meloidogyne incognita is affected by selection for virulence against major resistance genes from tomato and pepper. Eur J Plant Pathol 131:431CrossRefGoogle Scholar
  12. Elhady A, Adss S, Hallmann J, Heuer H (2018) Rhizosphere microbiomes modulated by pre-crops assisted plants in defense against plant-parasitic nematodes. Front Microbiol 9:1133CrossRefGoogle Scholar
  13. Escudero N, Lopez-Moya F, Ghahremani Z, Zavala-Gonzalez EA, Alaguero-Cordovilla A, Ros-Ibañez C, Lacasa A, Sorribas FJ, Lopez-Llorca LV (2017) Chitosan increases tomato root colonization by Pochonia chlamydosporia and their combination reduces root-knot nematode damage. Front Plant Sci 8:1415. CrossRefGoogle Scholar
  14. Gupta R et al (2015a) Exploitation of microbes for enhancing bacoside content and reduction of Meloidogyne incognita infestation in Bacopa monnieri L. Protoplasma 252:53–61CrossRefGoogle Scholar
  15. Gupta R, Saikia SK, Pandey R (2015b) Bioconsortia augments antioxidant and yield in Matricaria recutita L. against Meloidogyne incognita (Kofoid and White) Chitwood infestation. Proc Natl Acad Sci India Sect B Biol Sci. Google Scholar
  16. Gupta R et al (2017a) Microbial modulation of bacoside a biosynthetic pathway and systemic defense mechanism in Bacopa monnieri under Meloidogyne incognita stress. Sci Rep 7:41867. CrossRefGoogle Scholar
  17. Gupta R, Singh A, Ajayakumar PV, Pandey R (2017b) Microbial interference mitigates Meloidogyne incognita mediated oxidative stress and augments bacoside content in Bacopa monnieri L. Microbiol Res 199:67–78CrossRefGoogle Scholar
  18. Haard K (1968) Taxonomic studies on the genus Arthrobotrys Corda. Mycologia 60:1140–1159CrossRefGoogle Scholar
  19. Havir EA (1987) L-Phenylalanine ammonia lyase from soybean cell suspension culture. Methods Enzymol 142:248–253CrossRefGoogle Scholar
  20. Huang WK, Sun JH, Cui JK, Wang GF et al (2014) Efficacy evaluation of fungus Syncephalastrum racemosum and nematicide avermectin against the RKN Meloidogyne incognita on cucumber. PLoS ONE 9:e89717CrossRefGoogle Scholar
  21. Kerry BR (2000) Rhizosphere interactions and the exploitation of microbial agents for the biological control of plant-parasitic nematodes. Annu Rev Phytopathol 38:423–441CrossRefGoogle Scholar
  22. Kumar D, Singh KP (2006a) Assessment of predacity and effect of Arthrobotrys dactyloides for biological control of root knot disease of tomato. J Phytopathol 154:1–5CrossRefGoogle Scholar
  23. Kumar D, Singh KP (2006b) Variability in Indian isolates of Arthrobotrys dactyloides Drechsler: a nematode-trapping fungus. Curr Microbiol 20:1–8Google Scholar
  24. Kumar D, Singh KP, Jaiswal RK (2005) Screening of different media and substrates for cultural variability and mass culture of Arthrobotrys dactyloides Drechsler. Mycobiol 33:215–222CrossRefGoogle Scholar
  25. Kumar R, Bohra A, Pandey AK, Pandey MK, Kumar A (2017) Metabolomics for plant improvement: status and prospects. Front Plant Sci 8:1302CrossRefGoogle Scholar
  26. Leonetti P, Zonno MC, Molinari S, Altomare C (2017) Induction of SA-signaling pathway and ethylene biosynthesis in Trichoderma harzianum-treated tomato plants after infection of the root-knot nematode Meloidogyne incognita. Plant Cell Rep 36:621–631CrossRefGoogle Scholar
  27. Li L, Ma M, Liu Y, Zhou J, Qu Q, Lu K, Fu D, Ke-Qin Zhang (2011) Induction of trap formation in nematode-trapping fungi by a bacterium. FEMS Microbiol Lett 322:157–165CrossRefGoogle Scholar
  28. Nordbring-Hertz B, Jansson HB, Tunlid A (2006) Nematophagous Fungi. Encycl Life Sci. pp. 1–11Google Scholar
  29. Pandey R, Mishra AK, Tiwari S, Kalra A (2011) Nematode inhibiting organic materials and a strain of Trichoderma harzianum effectively manages Meloidogyne incognita in Withania somnifera fields. Biocontrol Sci Tech 21:1495–1499CrossRefGoogle Scholar
  30. Patel JS, Kharwar RN, Singh HB, Upadhyay RS, Sarma BK (2017) Trichoderma asperellum (T42) and Pseudomonas fluorescens (OKC)-Enhances resistance of pea against Erysiphepisi through enhanced ROS generation and lignifications. Front Microbiol 8:306Google Scholar
  31. Qin Y, Shang Q, Zhang Y, Li P, Chai Y (2017) Bacillus amyloliquefaciens L-S60 reforms the rhizosphere bacterial community and improves growth conditions in cucumber plug seedling. Front Microbiol 8:2620. CrossRefGoogle Scholar
  32. Sadasivam S, Manickam A (1996) Biochemical Methods.New Age International (P) Ltd. New Delhi, India. 256Google Scholar
  33. Saikia SK, Tiwari S, Pandey R (2013) Rhizospheric biological weapons for growth enhancement and Meloidogyne incognita management in Withania somnifera cv. Poshita Biol Control 65:225–234CrossRefGoogle Scholar
  34. Singh UB, Sahu A, Sahu N, Singh RK et al (2012a) Co-inoculation of Dactylaria brochopaga and Monacrosporium eudermatum affects disease dynamics and biochemical responses in tomato (Lycopersicon esculentum Mill.) to enhance bioprotection against Meloidogyne incognita. Crop Protect 35:102–109CrossRefGoogle Scholar
  35. Singh UB, Sahu A, Singh RK, Singh DP et al (2012b) Evaluation of biocontrol potential of Arthrobotrys oligospora against Meloidogyne graminicola and Rhizoctonia solani in Rice (Oryza sativa L.). Biol Control 60:262–270CrossRefGoogle Scholar
  36. Singh UB, Sahu A, Sahu N, Singh RK, Renu S, Singh DP, Manna MC, Sarma BK, Singh HB, Singh KP (2012c) Arthrobotrys oligospora mediated biological control of diseases of tomato (Lycopersicon esculentum Mill.) caused by Meloidogyne incognita and Rhizoctonia solani. J Appl Microbiol 114:196–208CrossRefGoogle Scholar
  37. Singh UB, Sahu A, Sahu N, Singh BP et al (2013a) Can endophytic Arthrobotrys oligospora modulate accumulation of defence related biomolecules and induced systemic resistance in tomato (Lycopersicon esculentum Mill.) against root knot disease caused by Meloidogyne incognita. Appl Soil Ecol 63:45–56CrossRefGoogle Scholar
  38. Singh UB, Sahu A, Sahu N, Singh RK, Singh DK, Singh BP et al. (2013b) Nematophagous fungi: Catenaria anguillulae and Dactylaria brochopaga from seed galls as potential biocontrol agents of Anguina tritici and Meloidogyne graminicola in wheat (Triticum aestivum L.). Biol Control 67(3):475–482CrossRefGoogle Scholar
  39. Stringlis IA, Proietti S, Hickman R, Van Verk MC, Zamioudis C, Pieterse CMJ (2018a) Root transcriptional dynamics induced by beneficial rhizobacteria and microbial immune elicitors reveal signatures of adaptation to mutualists. The Plant J 93:166–180CrossRefGoogle Scholar
  40. Stringlis IA, Ke Yu, Feussner K, de Jonge R, Bentum SV, Verk MCV, Berendsen RL, Bakker PAHM, Feussner I, Pieterse CMJ (2018b) MYB72-dependent coumarin exudation shapes root microbiome assembly to promote plant health. Proc Natl Acad Sci. Google Scholar
  41. Su L, Shen Z, Ruan Y, Tao C, Chao Y, Li R, Shen Q (2017) Isolation of antagonistic endophytes from banana roots against Meloidogyne javanica and their effects on soil nematode community. Front Microbiol 8:2070CrossRefGoogle Scholar
  42. Thimmaiah SR (2012) Standard methods of biochemical analysis. Kalyani Publishers, New Delhi, p 545Google Scholar
  43. Upadhyay KD, Dwivedi K (2008) A Text Book of Plant Nematology. Aman Publishing House, Meerut, p 8Google Scholar
  44. Vacheron J, Desbrosses G, Bouffaud ML, Touraine B, Moenne-Loccoz Y, Muller D, Legendre L, Florence WD, Claire P (2013) Plant growth promoting rhizobacteria and root system functioning. Front Plant Sci 4:356CrossRefGoogle Scholar
  45. Walia RK, Bajaj HK (2003) Textbook on introductory plant nematology. Directorate of information and publication of agriculture. Indian Council of Agricultural Research, New Delhi, p 96Google Scholar
  46. Wang X, Guo-Hong Li, Cheng-Gang Zou, Xing-Lai Ji et al (2014) Bacteria can mobilize nematode-trapping fungi to kill nematodes. Nat Commun 5:5776CrossRefGoogle Scholar
  47. Yim W, Seshadri S, Kim K, Lee G, Sa T (2013) Ethylene emission and PR protein synthesis in ACC deaminase producing Methylobacterium spp. inoculated tomato plants (Lycopersicon esculentum Mill.) challenged with Ralstonia solanacearum under greenhouse conditions. Plant Physiol Biochem 67:95–104CrossRefGoogle Scholar
  48. Zhai Y, Shao Z, Cai M, Zheng L, Li G, Huang D, Cheng W, Thomashow LS, Weller DM, Yu Z, Zhang J (2018) Multiple modes of nematode control by volatiles of Pseudomonas putida 1A00316 from antarctic soil against Meloidogyne incognita. Front Microbiol 9:253CrossRefGoogle Scholar
  49. Zhu X, Xiao K, Cui H, Hu J (2017) Over expression of the Prunus sogdiana NBS-LRR subgroup gene PsoRPM2 promotes resistance to the root-knot nematode Meloidogyne incognita in tobacco. Front Microbiol 8:2113CrossRefGoogle Scholar

Copyright information

© Indian Phytopathological Society 2019

Authors and Affiliations

  1. 1.Plant–Microbe Interaction and Rhizosphere Biology LabICAR-National Bureau of Agriculturally Important MicroorganismsMaunath BhanjanIndia
  2. 2.Department of Botany, Faculty of SciencesBanaras Hindu UniversityVaranasiIndia

Personalised recommendations