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Effects of Arugula Vermicompost on the Root-Knot Nematode (Meloidogyne javanica) and the Promotion of Resistance Genes in Tomato Plants

  • Rostami, Mahsa (Department of Plant Protection, School of Agriculture, Shiraz University) ;
  • Karegar, Akbar (Department of Plant Protection, School of Agriculture, Shiraz University) ;
  • Ghorbani, Abozar (Plant Virology Research Centre, College of Agriculture, Shiraz University)
  • Received : 2022.01.14
  • Accepted : 2022.04.04
  • Published : 2022.08.01

Abstract

Root-knot nematodes are the most important plant-parasitic nematodes worldwide. Many efforts have been made to find non-chemical, risk-free, and environmentally friendly methods for nematode control. In this study, the effects of compost and vermicompost of arugula (Eruca sativa) on Meloidogyne javanica were investigated in three glasshouse experiments. In addition, the expression of the defense-related genes nonexpressor of pathogenesis-related 1 (NPR1) and lipoxygenase 1 (LOX1) was detected in tomato plants treated with vermicompost of arugula at 0, 2, 7, and 14 days after nematode inoculation. The result showed that the vermicompost of arugula significantly reduced the reproduction factor of the nematode by 54.4% to 70.5% in the three experiments and increased the dry weight of shoots of infected tomato plants. Gene expression analysis showed that LOX1 expression increased on the second and seventh day after nematode inoculation, while NPR1 expression decreased. The vermicompost of arugula showed stronger nematode inhibitory potential than the vermicompost of animal manure. The vermicompost of arugula is superior to arugula compost in suppressing the activity of M. javaniva and reducing its impact. It manipulates the expression of resistance genes and could induce systemic resistance against root-knot nematodes.

Keywords

Acknowledgement

The authors gratefully acknowledge the financial support from Shiraz University and Iran National Science Foundation (INSF). The authors declare that the present article is part of the result of the first author's doctoral dissertation project approved by the Vice-Chancellor of Education and Postgraduate Studies, Shiraz University. Furthermore, they declare that all relevant ethical issues have been taken into consideration in conducting the research and writing the manuscript.

References

  1. Adam, M., Heuer, H. and Hallmann, J. 2014. Bacterial antagonists of fungal pathogens also control root-knot nematodes by induced systemic resistance of tomato plants. PLoS ONE 9:e90402. https://doi.org/10.1371/journal.pone.0090402
  2. Adhikary, S. 2012. Vermicompost, the story of organic gold: a review. Agric. Sci. 3:905-917. https://doi.org/10.4236/as.2012.37110
  3. Aissani, N., Urgeghe, P. P., Oplos, C., Saba, M., Tocco, G., Petretto, G. L., Eloh, K., Menkissoglu-Spiroudi, U., Ntalli, N. and Caboni, P. 2015. Nematicidal activity of the volatilome of Eruca sativa on Meloidogyne incognita. J. Agric. Food Chem. 63:6120-6125. https://doi.org/10.1021/acs.jafc.5b02425
  4. Akhtar, M. and Mahmood, I. 1993. Control of plant-parasitic nematodes with "Nimin" and some plant oils by bare-root dip treatment. Nematol. Mediterr. 21:89-92.
  5. Akram, A., Ongena, M., Duby, F., Dommes, J. and Thonart, P. 2008. Systemic resistance and lipoxygenase-related defence response induced in tomato by Pseudomonas putida strain BTP1. BMC Plant Biol. 8:113. https://doi.org/10.1186/1471-2229-8-113
  6. An, C. and Mou, Z. 2011. Salicylic acid and its function in plant immunity. J. Integr. Plant Biol. 53:412-428. https://doi.org/10.1111/j.1744-7909.2011.01043.x
  7. Arancon, N. Q., Edwards, C. A., Lee, S. S. and Yardim, E. 2002. Management of plant parasitic nematode populations by use of vermicomposts. In: Proceedings of brighton crop protection conference-pests and diseases, pp. 705-710. British Crop Protection Council, Farnham, UK.
  8. Aydinli, G. and Mennan, S. 2018. Biofumigation studies by using Raphanus sativus and Eruca sativa as a winter cycle crops to control root-knot nematodes. Braz. Arch. Biol. Technol. 61:e18180249.
  9. Backer, R., Naidoo, S. and van den Berg, N. 2019. The nonexpressor of pathogenesis-related genes 1 (NPR1) and related family: mechanistic insights in plant disease resistance. Front. Plant Sci.10:102. https://doi.org/10.3389/fpls.2019.00102
  10. Bremner, J. M. and Mulvaney, C. S. 1982. Nitrogen-total. In: Methods of soil analysis, Part 2: chemical and microbiological properties, eds. by A. L. Page, R. H. Miller and D. R. Keeney, pp. 595-624. American Society of Agronomy, Madison, WI, USA.
  11. Burkett-Cadena, M., Kokalis-Burelle, N., Lawrence, K. S., van Santen, E. and Kloepper, J. W. 2008. Suppressiveness of rootknot nematodes mediated by rhizobacteria. Biol. Control 47:55-59. https://doi.org/10.1016/j.biocontrol.2008.07.008
  12. Chapman, H. D. and Pratt, P. F. 1961. Methods of analysis for soils, plants and waters. University of California, Berkeley, CA, USA. 309 pp.
  13. Coyne, D. L., Nicol, J. M. and Claudius-Cole, B. 2007. Practical plant nematology: a field and laboratory guide. International Institute of Tropical Agriculture, Cotonou, Benin. 91 pp.
  14. Curto, G., Dallavalle, E. and Lazzeri, L. 2005. Life cycle duration of Meloidogyne incognita and host status of Brassicaceae and Capparaceae selected for glucosinate content. Nematology 7:203-212. https://doi.org/10.1163/1568541054879494
  15. Daneel, M., Engelbrecht, E., Fourie, H. and Ahuja, P. 2018. The host status of Brassicaceae to Meloidogyne and their effects as cover and biofumigant crops on root-knot nematode populations associated with potato and tomato under South African field conditions. Crop Prot. 110:198-206. https://doi.org/10.1016/j.cropro.2017.09.001
  16. de Medeiros, H. A., de Araujo Filho, J. V., de Freitas, L. G., Castillo, P., Rubio, M. B., Hermosa, R. and Monte, E. 2017. Tomato progeny inherit resistance to the nematode Meloidogyne javanica linked to plant growth induced by the biocontrol fungus Trichoderma atroviride. Sci. Rep. 7:40216. https://doi.org/10.1038/srep40216
  17. Dong, K., Dean, R. A., Fortnum, B. A. and Lewis, S. A. 2001. Development of PCR primers to identify species of root-knot nematodes: Meloidogyne arenaria, M. hapla, M. incognita and M. javanica. Nematropica 31:271-280.
  18. Dong, L. Q. and Zhang, K. Q. 2006. Microbial control of plant-parasitic nematodes: a five-party interaction. Plant Soil 288:31-45. https://doi.org/10.1007/s11104-006-9009-3
  19. Edwards, C. A., Arancon, N. Q. and Sherman, R. L. 2011. Vermiculture technology: earthworms, organic wastes, and environmental management. CRC Press, Boca Raton, FL, USA. 624 pp.
  20. Edwards, S. and Ploeg, A. 2014. Evaluation of 31 potential biofumigant brassicaceous plants as hosts for three Meloiodogyne species. J. Nematol. 46:287-295.
  21. Fourie, H., Ahuja, P., Lammers, J. and Daneel, M. 2016. Brassicacea-based management strategies as an alternative to combat nematode pests: a synopsis. Crop Prot. 80:21-41. https://doi.org/10.1016/j.cropro.2015.10.026
  22. Gao, X., Starr, J., Gobel, C., Engelberth, J., Feussner, I., Tumlinson, J. and Kolomiets, M. 2008. Maize 9-lipoxygenase ZmLOX3 controls development, root-specific expression of defense genes, and resistance to root-knot nematodes. Mol. Plant-Microbe Interact. 21:98-109. https://doi.org/10.1094/mpmi-21-1-0098
  23. Garg, P., Gupta, A. and Satya, S. 2006. Vermicomposting of different types of waste using Eisenia foetida: a comparative study. Bioresour. Technol. 97:391-395. https://doi.org/10.1016/j.biortech.2005.03.009
  24. Ghasemi Pirbalouti, A., Sajjadi, S. E. and Parang, K. 2014. A review (research and patents) on jasmonic acid and its derivatives. Arch. Pharm. 347:229-239. https://doi.org/10.1002/ardp.201300287
  25. Gopinath, R. and Prakash, M. 2014. Isolation of plant growth promoting rhizobacteria (PGPR) from vermicompost and effect on growth of green gram (Vigna radiata L.). Int. J. Curr. Microbiol. Appl. Sci. 3:1072-1081.
  26. Hildebrand, D. F. 1989. Lipoxygenases. Physiol. Plant. 76:249-253. https://doi.org/10.1111/j.1399-3054.1989.tb05641.x
  27. Hoenig, M. 2005. Sample dissolution for elemental analysis: dry ashing. In: Encyclopedia of analytical science, 2nd ed., eds. by P. Worsfold, A. Townshend and C. Poole, pp. 131-136. Elsevier Academic Press, Amsterdam, Netherlands.
  28. Hoitink, H. A. J. and Grebus, M. E. 1997. Composts and the control of plant diseases. In: Humic substances, peats and sludges: health and environmental aspects, eds. by M. H. B. Hayes and W. S. Wilson, pp. 359-366. The Royal Society of Chemistry, Cambridge, UK.
  29. Hussey, R. S. and Barker, K. R. 1973. A comparison of methods of collecting inocula of Meloidogyne spp., including a new technique. Plant Dis. Rep. 57:1025-1028.
  30. Kammerhofer, N., Radakovic, Z., Regis, J. M. A., Dobrev, P., Vankova, R., Grundler, F. M. W., Siddique, S., Hofmann, J. and Wieczorek, K. 2015. Role of stress-related hormones in plant defence during early infection of the cyst nematode Heterodera schachtii in Arabidopsis. New Phytol. 207:778-789. https://doi.org/10.1111/nph.13395
  31. Kerry, B. R. 2000. Rhizosphere interactions and the exploitation of microbial agents for the biological control of plant-parasitic nematodes. Annu. Rev. Phytopathol. 38:423-441. https://doi.org/10.1146/annurev.phyto.38.1.423
  32. Kyndt, T., Vieira, P., Gheysen, G. and de Almeida-Engler, J. 2013. Nematode feeding sites: unique organs in plant roots. Planta 238:807-818. https://doi.org/10.1007/s00425-013-1923-z
  33. Lazcano, C., Gomez-Brandon, M. and Dominguez, J. 2008. Comparison of the effectiveness of composting and vermicomposting for the biological stabilization of cattle manure. Chemosphere 72:1013-1019. https://doi.org/10.1016/j.chemosphere.2008.04.016
  34. Leone, A., Melillo, M. T. and Bleve-Zacheo, T. 2001. Lipoxygenase in pea roots subjected to biotic stress. Plant Sci. 161:703-717. https://doi.org/10.1016/S0168-9452(01)00458-7
  35. Li, N., Han, X., Feng, D., Yuan, D. and Huang, L.-J. 2019. Signaling crosstalk between salicylic acid and ethylene/jasmonate in plant defense: do we understand what they are whispering? Int. J. Mol. Sci .20:671. https://doi.org/10.3390/ijms20030671
  36. Liu, D., Han, W., Zhang, Y. and Jiang, Y. 2019. Evaluation of vermicompost and extracts on tomato root-knot nematode. Bangladesh J. Bot. 48:845-851.
  37. Livak, K. J. and Schmittgen, T. D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402-408. https://doi.org/10.1006/meth.2001.1262
  38. Matthiessen, J. N. and Kirkegaard, J. A. 2006. Biofumigation and enhanced biodegradation: opportunity and challenge in soilborne pest and disease management. Crit. Rev. Plant Sci. 25:235-265. https://doi.org/10.1080/07352680600611543
  39. Melakeberhan, H., Xu, A., Kravchenko, A., Mennan, S. and Riga, E. 2006. Potential use of arugula (Eruca sativa L.) as a trap crop for Meloidogyne hapla. Nematology 8:793-799. https://doi.org/10.1163/156854106778877884
  40. Melan, M. A., Dong, X., Endara, M. E., Davis, K. R., Ausubel, F. M. and Peterman, T. K. 1993. An Arabidopsis thaliana lipoxygenase gene can be induced by pathogens, abscisic acid, and methyl jasmonate. Plant Physiol. 101:441-450. https://doi.org/10.1104/pp.101.2.441
  41. Mishra, S., Wang, K.-H., Sipes, B. S. and Tian, M. 2018. Induction of host-plant resistance in cucumber by vermicompost tea against root-knot nematode. Nematropica 48:164-171.
  42. Molinari, S., Fanelli, E. and Leonetti, P. 2014. Expression of tomato salicylic acid (SA)-responsive pathogenesis-related genes in Mi-1-mediated and SA-induced resistance to root-knot nematodes. Mol. Plant Pathol. 15:255-264. https://doi.org/10.1111/mpp.12085
  43. Nahar, K., Kyndt, T., De Vleesschauwer, D., Hofte, M. and Gheysen, G. 2011. The jasmonate pathway is a key player in systemically induced defense against root knot nematodes in rice. Plant Physiol. 157:305-316. https://doi.org/10.1104/pp.111.177576
  44. Ntalli, N. and Caboni, P. 2017. A review of isothiocyanates bio-fumigation activity on plant parasitic nematodes. Phytochem. Rev. 16:827-834. https://doi.org/10.1007/s11101-017-9491-7
  45. Ntalli, N., Zioga, D., Argyropoulou, D. M., Papatheodorou, M. E., Menkissoglu-Spiroudi, U. and Monokrousos, N. 2019. Anise, parsley and rocket as nematicidal soil amendments and their impact on non-target soil organisms. Appl. Soil Ecol. 143:17-25. https://doi.org/10.1016/j.apsoil.2019.05.024
  46. Parkhi, V., Kumar, V., Campbell, L. M., Bell, A. A., Shah, J. and Rathore, K. S. 2010. Resistance against various fungal pathogens and reniform nematode in transgenic cotton plants expressing Arabidopsis NPR1. Transgenic Res. 19:959-975. https://doi.org/10.1007/s11248-010-9374-9
  47. Pasini, F., Verardo, V., Cerretani, L., Caboni, M. F. and D'Antuono, L. F. 2011. Rocket salad (Diplotaxis and Eruca spp.) sensory analysis and relation with glucosinolate and phenolic content. J. Sci. Food Agric. 91:2858-2864. https://doi.org/10.1002/jsfa.4535
  48. Pathma, J. and Sakthivel, N. 2012. Microbial diversity of vermicompost bacteria that exhibit useful agricultural traits and waste management potential. SpringerPlus 1:26. https://doi.org/10.1186/2193-1801-1-26
  49. Priya, D. B., Somasekhar, N., Prasad, J. S. and Kirti, P. B. 2011. Transgenic tobacco plants constitutively expressing Arabidopsis NPR1 show enhanced resistance to root-knot nematode, Meloidogyne incognita. BMC Res. Notes 4:231. https://doi.org/10.1186/1756-0500-4-231
  50. Puga-Freitas, R., Barot, S., Taconnat, L., Renou, J.-P. and Blouin, M. 2012. Signal molecules mediate the impact of the earthworm Aporrectodea caliginosa on growth, development and defence of the plant Arabidopsis thaliana. PLoS ONE 7:e49504. https://doi.org/10.1371/journal.pone.0049504
  51. Ramamoorthy, V., Viswanathan, R., Raguchander, T., Prakasam, V. and Samiyappan, R. 2001. Induction of systemic resistance by plant growth promoting rhizobacteria in crop plants against pests and diseases. Crop Prot. 20:1-11. https://doi.org/10.1016/S0261-2194(00)00056-9
  52. Raphael, K. and Velmourougane, K. 2011. Chemical and microbiological changes during vermicomposting of coffee pulp using exotic (Eudrilus eugeniae) and native earthworm (Perionyx ceylanesis) species. Biodegradation 22:497-507. https://doi.org/10.1007/s10532-010-9422-4
  53. Rostami, M., Olia, M. and Arabi, M. 2014. Evaluation of the effects of earthworm Eisenia fetida-based products on the pathogenicity of root-knot nematode (Meloidogyne javanica) infecting cucumber. Int. J. Recycl. Org. Waste Agric. 3:58. https://doi.org/10.1007/s40093-014-0058-y
  54. Rubio, M. B., Quijada, N. M., Perez, E., Dominguez, S., Monte, E. and Hermosa, R. 2014. Identifying beneficial qualities of Trichoderma parareesei for plants. Appl. Environ. Microbiol. 80:1864-1873. https://doi.org/10.1128/AEM.03375-13
  55. Sarikamis, G., Aydinli, G. and Mennan, S. 2017. Glucosinolates in some brassica species as sources of bioactive compounds against root knot nematodes. Int. J. Adv. Res. 5:271-278. https://doi.org/10.21474/IJAR01/5530
  56. Sasser, J. N. 1977. Worldwide dissemination and importance of the root-knot nematodes, Meloidogyne spp. J. Nematol. 9:26-29
  57. Siddiqui, I. A. and Shaukat, S. S. 2002. Rhizobacteria-mediated induction of systemic resistance (ISR) in tomato against Meloidogyne javanica. J. Phytopathol. 150:469-473. https://doi.org/10.1046/j.1439-0434.2002.00784.x
  58. Sikora, R. A., Pocasangre, L., zum Felde, A., Niere, B., Vu, T. T. and Dababat, A. A. 2008. Mutualistic endophytic fungi and in-planta suppressiveness to plant parasitic nematodes. Biol. Control 46:15-23. https://doi.org/10.1016/j.biocontrol.2008.02.011
  59. Singh, A., Karmegam, N., Singh, G. S., Bhadauria, T., Chang, S. W., Awasthi, M. K., Sudhakar, S., Arunachalam, K. D., Biruntha, M. and Ravindran, B. 2020. Earthworms and vermicompost: an eco-friendly approach for repaying nature's debt. Environ. Geochem. Health 42:1617-1642. https://doi.org/10.1007/s10653-019-00510-4
  60. Tognetti, C., Laos, F., Mazzarino, M. J. and Hernandez, M. T. 2005. Composting vs. vermicomposting: a comparison of end product quality. Compost Sci. Util. 13:6-13. https://doi.org/10.1080/1065657X.2005.10702212
  61. Tripathi, G. and Bhardwaj, P. 2004. Comparative studies on biomass production, life cycles and composting efficiency of Eisenia fetida (Savigny) and Lampito mauritii (Kinberg). Bioresour. Technol. 92:275-283. https://doi.org/10.1016/j.biortech.2003.09.005
  62. Villatoro-Pulido, M., Priego-Capote, F., Alvarez-Sanchez, B., Saha, S., Philo, M., Obregon-Cano, S., De Haro-Bailon, A., Font, R. and Del Rio-Celestino, M. 2013. An approach to the phytochemical profiling of rocket [Eruca sativa (Mill.) Thell]. J. Sci. Food Agric. 93:3809-3819. https://doi.org/10.1002/jsfa.6286
  63. Viswanath, K. K., Varakumar, P., Pamuru, R. R., Basha, S. J., Mehta, S. and Rao, A. D. 2020. Plant lipoxygenases and their role in plant physiology. J. Plant Biol. 63:83-95. https://doi.org/10.1007/s12374-020-09241-x
  64. Whitehead, A. G. and Hemming, J. R. 1965. A comparison of some quantitative methods of extracting small vermiform nematodes from soil. Ann. Appl. Biol. 55:25-38. https://doi.org/10.1111/j.1744-7348.1965.tb07864.x
  65. Wu, Y., Zhang, D., Chu, J. Y., Boyle, P., Wang, Y., Brindle, I. D., De Luca, V. and Despres, C. 2012. The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell Rep. 1:639-647. https://doi.org/10.1016/j.celrep.2012.05.008
  66. Wubben, M. J. E., Jin, J. and Baum, T. J. 2008. Cyst nematode parasitism of Arabidopsis thaliana is inhibited by salicylic acid (SA) and elicits uncoupled SA-independent pathogenesis-related gene expression in roots. Mol. Plant-Microbe Interact. 21:424-432. https://doi.org/10.1094/MPMI-21-4-0424
  67. Wubie, M. and Temesgen, Z. 2019. Resistance mechanisms of tomato (Solanum lycopersicum) to root-knot nematodes (Meloidogyne species). J. Plant Breed. Crop Sci. 11:33-40. https://doi.org/10.5897/jpbcs2018.0780
  68. Xiao, Z., Liu, M., Jiang, L., Chen, X., Griffiths, B. S., Li, H. and Hu, F. 2016. Vermicompost increases defense against root-knot nematode (Meloidogyne incognita) in tomato plants. Appl. Soil Ecol. 105:177-186. https://doi.org/10.1016/j.apsoil.2016.04.003
  69. Zhang, Y. and Li, X. 2019. Salicylic acid: biosynthesis, perception, and contributions to plant immunity. Curr. Opin. Plant Biol. 50:29-36. https://doi.org/10.1016/j.pbi.2019.02.004