Use of different eco-friendly management approaches for controlling root-knot nematode (Meloidogyne incognita L.) in tomato (Solanum lycopersicum L.)

Main Article Content

M.M.R. Sarker
M.A. Ali
M.S. Islam
M.S. Huda
I. Pun
R. Podder
A.F. Tomczak
A. Hossain

Abstract

Root-knot nematodes are growing concerns for tomato growers because chemical nematicides are gradually disappearing and environmentally not sound. Alternative techniques based on organic soil amendments and other nematodes antagonistic (biological control agents) are needed to be solved the problem. This review analyzed the recent studies related to these techniques and their combinations and identified the most effective ones. Also, this analysis focused on a description of eco-friendly management techniques rather than chemical control. Several alternative techniques such as organic manure, plant products, organic wastes, antagonistic fungi, and bacteria are considered to control knot nematode (Meloidogyne incognita) in tomato production. The review analyzed the effect of each practice and interactions among the techniques. A remarkable variation was also found among the studies. Organic soil amendments enhance the activities of microorganisms that can significantly suppress root-knot nematode by the release of nematotoxic compounds. On the other hand, nematode antagonistic (nematophagous fungi, bacteria, etc.) also control root-knot nematode without any hazard to the environment. This study will help to find out the most effective, economical, eco-friendly management method for controlling nematode for encouraging tomato production.

Article Details

Section
Review Articles

References

Abad, P., B. Favery, M.N. Rosso and P. Castagnone-Sereno. 2003. Root-knot nematode parasitism and host response: molecular basis of a sophisticated interaction. Mol. Plant Pathol. 4: 217–224.

Abo-Elyousar, K.A., Z. Khan, M.E.M. Award and M.F. Abedel-Moneim. 2010. Evaluation of plant extracts and Pseudomonas spp. for control of root-knot nematode Meloidogyne incognita on tomato. Nematropica. 40: 289–299.

Ahmad, F., M.A. Rather and M.A. Siddiqui. 2010. Influence of organic additives on the incidence of root-knot nematode, Meloidogyne javanica in roots of tomato plants. Arch. Phytopathol. Plant Protect. 43(2): 168–173.

Akhtar, M. and A. Malik. 2000. Roles of organic soil amendments and soil organisms in the biological control of plant-parasitic nematodes: a review. Bioresour. Technol. 74(1): 35–47.

Al-Rehiayani, S.M. and M. Bellal. 2009. Effect of solarization on Heterodera avenae and wheat yield in Al-Qassim, Saudi Arabia, pp. 233–236. In: Proceedings of the First Workshop of the International Cereal Cyst Nematode Initiative, 21–23 October 2009, Antalya, Turkey.

Anastasiadis, I.A., I.O. Giannakou, D.A. Prophetou-Athanasiadou and S.R. Gowen. 2008. The combined effect of the application of a biocontrol agent Paecilomyces lilacinus, with various practices for the control of root-knot nematodes. Crop Prot. 27: 352–361.

Anwar-ul-Haq, M., S.A. Anwar, M. Shahid, N. Javed, S.A. Khan and K. Mehamood. 2011. Management of root-knot nematode Meloidogyne incognita by plant growth promoting rhizobacteria on tomato. Pakistan J. Zool. 43(6): 1027–1031.

Ashoub, A.H., S.A. Montasser, M.H. Mourad and M. Gamal. 2009. Impact of some fungi species as biocontrol agent against the root-knot nematode, Meloidogyne incognita. Aust. J. Basic Appl. Sci. 3(4): 3617–3624.

Aslam, S. and Saifullah. 2013. Organic management of root-knot nematodes in tomato with spent mushroom compost. Sarhad J. Agric. 29(1): 63–69.

Bansal, R.K., R.S. Dahiya, K. Lakshminarayana, S. Suneja, R.C. Anand and N. Narula. 1999. Effect of rhizospheric bacteria on plant growth of wheat infected with Heterodera avenae. Nematol. Mediterr. 27: 311–314.

Bhatti, D.S. and R.K. Jain. 1977. Estimation of loss in okra, tomato and brinjal yield due to Meloidogyne incognita. Ind. J. Nematol. 7(1): 37–41.

Candido, V., T. D’Addabbo, M. Basile, D. Castronuovo and V. Miccolis. 2008. Greenhouse soil solarization: effect on weeds, nematodes and yield of tomato and melon. Agron. Sustain. Dev. 28(2): 221–230.

Carneiro, R.G., M.P. Moritz, A.P. Mônaco, K.C. Nakamura and A. Scherer. 2007. Reação de milho, sorgo e milheto a Meloidogyne incognita, M. javanica e M. paranaensis. Nematol. Bras. 31(2): 9–13.

Carson, A.G. and E. Otoo. 1996. Application of soil solarization to control root-knot nematodes and weeds in transplanted tomato. Ghana Jnl. Agric. Sci. 29(2): 91–98.

Chinheya, C.C., K.S. Yobo and M.D. Laing. 2017. Biological control of the root-knot nematode, Meloidogyne javanica (Chitwood) using Bacillus isolates, on soybean. Biol. Control. 109: 37–41.

Cho, H.U., Y.M. Kim, Y.N. Choi, H.G. Kim and J.M. Park. 2015. Influence of temperature on volatile fatty acid production and microbial community structure during anaerobic fermentation of microalgae. Bioresour. Technol. 191: 475–480.

D’addabbo, A., I. Papajova, N. Sasanelli, V. Radicci and M. Renco. 2011. Suppression of root-knot nematodes in potting mixes amended with different composted bio-wastes. Helminthologia. 48(4): 278–287.

Dallemole-Giaretta, R., L.G. de Freitas, E.A. Lopes, S. Ferraz, G.S. de Podestá and E.L. Agnes. 2011. Cover crops and Pochonia chlamydosporia for the control of Meloidogyne javanica. Nematology. 13(8): 919–926.

Davies, K.G., C.A. Flynn, V. Laird and B.R. Kerry. 1990. The life-cycle, population dynamics and host specificity of a parasite of Heterodera avenae, similar to Pasteuria penetrans. Revue Nématol. 13(3): 303–309.

de Freitas Soares, F.E., B.L. Sufiate and J.H. de Queiroz. 2018. Nematophagous fungi: far beyond the endoparasite, predator and ovicidal groups. Agric. Nat. Resour. 52: 1–8.

Dwivedi, D., B.N. Johri, K. Ineichen, V. Wray and A. Wiemken. 2009. Impact of antifungals producing rhizobacteria on the performance of Vigna radiate in the presence of arbuscular mycorrhizal fungi. Mycorrhiza. 19: 559–570.

Elsen, A., D. Gervacio, R. Swennen and D. De Waele. 2008. AMF-induced biocontrol against plant parasitic nematodes in Musa sp.: a systemic effect. Mycorrhiza. 18: 251–256.

Fan, H., M. Yao, H. Wang, Z. Di, X. Zhu, Y. Wang, X. Liu, Y. Duan and L. Chen. 2020. Isolation and effect of Trichoderma citrinoviride Snef1910 for the biological control of root-knot nematode, Meloidogyne incognita. BMC Microbiol. 20: 299.

Faruk, M.I., M.I. Rahman, M.R. Ali, M.M. Rahman and M.M.H. Mustafa. 2011. Efficacy of two organic amendments and a nematicide to manage root-knot nematode (Meloidogyne incognita) of tomato (Lycopersicon esculentum L.). Bangladesh J. Agric. Res. 36(3): 477–486.

Ferraz, S. and L.G. de Freitas. 2004. Use of antagonistic plants and natural products, pp. 931–977. In: Z.X. Chen, S.Y. Chen and D.W. Dickson, (Eds.), Nematology Advances and Perspectives. Tsinghua University Press, Beijing, China.

Ferris, H. and M.M. Matute. 2003. Structural and functional succession in the nematode fauna of a soil food web. Appl. Soil Ecol. 23: 93–110.

Fiume, F. 1994. Tomato root-knot nematode control by chemical treatments, soil solarization and resistant varieties. Acta Hortic. 376: 399–406.

Ghasemzadeh, A., S. Jamali, M. Esfahani and H. Pedramfar. 2019. Assessment of photosynthetic fluorescence in tomato cultivars infested with root-knot nematode. Pak. J. Nematol. 37(1): 91–101.

Giovannucci, E. 1999. Tomatoes, tomato-based products, lycopene, and cancer: review of the epidemiologic literature. J. Natl. Cancer Inst. 91(4): 317–331.

Haroon, S.A., O. Ezzat and M. Reham. 2009. The effect of root exudates from certain Egyptian medicinal plants on the cyst nematode, Heterodera zeae, pp. 227–232. In: Proceedings of the First Workshop of the International Cereal Cyst Nematode Initiative, 21–23 October 2009, Antalya, Turkey.

Hashem, M. and K.A. Abo-Elyousr. 2011. Management of root-knot nematode Meloidogyne incognita on tomato with combinations of different biocontrol organisms. Crop Prot. 30(3): 285–292.

Hassan, M.A., P.S. Chindo, P.S. Marley and M.D. Alegbejo. 2010. Management of root-knot nematodes (Meloidogyne spp.) on tomato (Lycopersicon lycopersicum) using organic wastes in Zaria, Nigeria. Plant Protect. Sci. 46(1): 34–38.

Hunt, D.J. and Z.A. Handoo. 2009. Taxonomy, identification and principal species, pp. 55–97. In: R.N. Perry, M. Moens and J.L. Starr, (Eds.), Root-knot Nematodes. CABI Publishing, Oxford shire, UK.

Kim, T.Y., J.Y. Jang, N.H. Yu, W.J. Chi, C.H. Bae and J.H. Yeo. 2018. Nematicidal activity of grammicin produced by Xylaria grammica KCTC 13121BP against Meloidogyne incognita. Pest Manag. Sci. 74: 384–391.

Koenning, S.R., C. Overstreet, J.W. Noling, P.A. Donald, J.O. Becker and B.A. Fortnum. 1999. Survey of crop losses in response to phytoparasitic nematodes in the United States for 1994. J. Nematol. 31: 587–618.

Krishnappa, K. 1985. Nematology in developing countries: India-IMP Region VIII, pp. 379–398. In: J.N. Sasser and C.C. Carter, (Eds.), An Advanced Treatise on Meloidogyne. Volume 1. Biology and Control. North Carolina State University Graphics, Raleigh, North Carolina, USA.

Kumar, K.K. and S.K. Dara. 2021. Fungal and bacterial endophytes as microbial control agents for plant-parasitic nematodes. Int. J. Environ. Res. Public Health. 18: 4269.

Lambert, K. and S. Bekal. 2002. Introduction to plant-parasitic nematodes. Plant Health Instr. 10: 1094–1218.

Lear, B. 1956. Results of laboratory experiments with Vapam for control of nematodes. Plant Dis. Rep. 40: 847–852.

Lee, W.S., A.S.M. Chua, H.K. Yeoh and G.C. Ngoh. 2014. A review of the production and applications of waste-derived volatile fatty acids. Chem. Eng. J. 235: 83–99.

Lima, E.A., J.K. Mattros, A.W. Moita, R.G. Carneiro and R.M.D.G. Carneiro. 2009. Host status of different crops for Meloidogyne ethiopica control. Trop. Plant Pathol. 34(3): 152–157.

Liu, R., D. Mei, W. Xia, L. Min and L. Xingzhong. 2011. Suppression of the root-knot nematode (Meloidogyne incognita) on tomato by dual inoculation with arbuscular mycorrhizal fungi and plant growth-promoting rhizobacteria. Mycorrhiza. 22: 289–296.

Lutuf, H. 2015. Identification of Nematodes and Morphological Characterization of Meloidogyne incognita Associated with Solanum lycopersicum L. in the Ashanti, Brong Ahafo and Upper East Regions of Ghana. PhD Thesis, University of Ghana, Accra, Ghana.

Mahgoob, A.E.A. and T.S.E. Tayeb. 2010. Biological control of the root-knot nematode, Meloidogyne incognita on tomato using plant growth promoting bacteria. Egypt. J. Biol. Pest Control. 20(2): 95–103.

Mashela, P.W., H.A. Shimelis and F.N. Mudau, 2008. Comparison of the efficacy of ground wild cucumber fruits, aldicarb and fenamiphos on suppression of Meloidogyne incognita in tomato. J. Phytopathol. 156(5): 264–267.

Miheret, S., A. Seid and N. Hailu. 2019. Distribution and management of root-knot nematodes (Meloidogyne spp.) in tomato (Lycopersicum esculentum) in North Shoa Zone, Ethiopia. Pak. J. Nematol. 37(2): 123–134.

Mokrini, F., N. Viaene, L. Waeyenberge, M. Afechtal, A. Essarioui and M. Moens. 2017. The importance, biology and management of cereal cyst nematodes (Heterodera spp.). Rev. Mar. Sci. Agron. Vét. 5(4): 414–421.

Moslehi, S., S. Pourmehr, A. Shirzad. and R. Khakvar. 2021. Potential of some endophytic bacteria in biological control of root-knot nematode Meloidogyne incognita. Egypt. J. Biol. Pest Control. 31: 50.

Naz, I., J.E. Palomares‐Rius, Saifullah, V. Blok, M.R. Khan, S. Ali and S. Ali. 2013. In vitro and in planta nematicidal activity of Fumaria parviflora (Fumariaceae) against the southern root-knot nematode Meloidogyne incognita. Plant Pathol. 62(4): 943–952.

Naz, I., Saifullah, J.E. Palomares-Rius, S.M. Khan, S. Ali and A. Baig. 2015a. Sustainable management of the southern root-knot nematode, Meloidogyne incognita (Kofoid and White) Chitwood, by amendments of Fumaria parviflora. Int. J. Agric. Biol. 17(2): 289–296.

Naz, I., Saifullah, J.E. Palomares-Rius, S.M. Khan, S. Ali, M. Ahmad, A. Ali and A. Khan. 2015b. Control of southern root-knot nematode Meloidogyne incognita (Kofoid and White) Chitwood on tomato using green manure of Fumaria parviflora Lam (Fumariaceae). Crop Prot. 67: 121–129.

Nekouam, N. 2004. Biological Control of Striga hermonthica by Fusarium oxysforum. PhD Thesis, Ahmadu Bello University, Zaria, Nigeria.

Ngala, B.M., P.P.J. Haydock, S. Woods and M.A. Back. 2015. Biofumigation with Brassica juncea, Raphanus sativus and Eruca sativa for the management of field populations of the potato cyst nematode Globodera pallida. Pest Manag. Sci. 71: 759–769.

Oka, Y. 2010. Mechanisms of nematode suppression by organic soil amendment–a review. Appl. Soil Ecol. 44(2): 101–115.

Oka, Y., N. Shapira and P. Fine. 2007. Control of root-knot nematodes in organic farming systems by organic amendments and soil solarization. Crop Prot. 26(10): 1556–1565.

Pakeerathan, K., G. Mikunthan and N. Tharsani. 2009a. Effect of different animal manures on Meloidogyne incognita (Kofoid and White) on tomato. World J. Agric. Sci. 5(4): 432–435.

Pakeerathan, K., G. Mikunthan and N. Tharshani. 2009b. Eco-friendly management of root-knot nematode Meloidogyne incognita (Kofid and White) Chitwood using different green leaf manures on tomato under field conditions. American-Eurasian J. Agric. Environ. Sci. 6(5): 494–497.

Poveda, J., P. Abril-Urias and C. Escobar. 2020. Biological control of plant-parasitic nematodes by filamentous fungi inducers of resistance: Trichoderma, mycorrhizal and endophytic fungi. Front. Microbiol. 11: 992.

Qamar, F., S. Begum, S.M. Raza, A. Wahab and B.S. Siddiqui. 2005. Nematicidal natural products from the aerial parts of Lantana camara Linn. Nat. Prod. Res. 19: 609–613.

Radwan, M.A., E.K. EI-Maadawy, S.I. Kassem and M.M. Abu-Elamayem. 2011. Oil cakes soil amendment effects on Meloidogyne incognita, root-knot nematode infecting tomato. Arch. Phytopathol. Plant Protect. 42(1): 58–64.

Radwan, M.A., S.A.A. Farrag, M.M. Abu-Elamayem and N.S. Ahmed. 2012a. Efficacy of dried seed powder of some plant species as soil amendment against Meloidogyne incognota on tomato. Arch. Phytopathol. Plant Protect. 45(10): 1246–1251.

Radwan, M.A., S.A.A. Farrag, M.M. Abu-Elamayem and N.S. Ahmed. 2012b. Biological control of the root-knot nematode, Meloidogyne incognita on tomato using bioproducts of microbial origin. Appl. Soil Ecol. 56: 58–62.

Ralmi, N.H.A.A., M.M. Khandaker and N. Mat. 2016. Occurrence and control of root knot nematode in crops: a review. Aust. J. Crop Sci. 10(12): 1649–1654.

Ramamoorthy, V. and R. Samiyappan. 2001. Induction of defense-related genes in Pseudomonas fluorescens-treated chili plants in response to infection by Colletotrichum capsici. J. Mycol. Pl. Pathol. 31(2): 146–155.

Riley, I.T., S. Hou and S. Chen. 2010. Crop rotational and spatial determinants of variation in Heterodera avenae (cereal cyst nematode) population density at village scale in spring cereals grown at high altitude on the Tibetan Plateau, Qinghai, China. Australas. Plant Pathol. 39(5): 424–430.

Sasser, J.N. 1979. Economic importance of Meloidogyne in tropical countries, pp. 359–374. In: F. Lamberti and C.E. Taylor, (Eds.), Root-knot Nematodes (Meloidogyne species): Systematics, Biology and Control. Academic Press, London, UK.

Seid, A., C. Fininsa, T. Mekete, W. Decraemer and W.M.L. Wesemael. 2015. Tomato (Solanum lycopersicum) and root-knot nematodes (Meloidogyne spp.)–a century-old battle. Nematology. 17(9): 995–1009.

Serfoji, P., S. Rajeshkumar and T. Selvaraj. 2010. Management of root-knot nematode, Meloidogyne incognita on tomato cv. Pusa Ruby. by using vermicompost, AM fungus, Glomus aggregatum and mycorrhiza helper bacterium, Bacillus coagulans. Int. J. Agric. Technol. 6(1): 37–45.

Shreenivasa, K.R., K. Krishnappa and N.G. Ravichandra. 2007. Survival and penetration of Meloidogyne incognita larvae in tomato roots in presence of arbuscular mycorrhizal fungus, Glomus fasciculatum. Karnataka J. Agric. Sci. 20: 57–61.

Siddiqui, Z.A. and I. Mahmood. 1999. Role of bacteria in the management of plant parasitic nematodes: a review. Bioresour. Technol. 69(2): 167–179.

Singh, S. and N. Mathur. 2010. Biological control of root-knot nematode, Meloidogyne incognita infesting tomato. Biocontrol Sci. Technol. 20(8): 865–874.

Singh, S.P. and L.S. Devi. 2012. Management of root-knot nematode, Meloidogyne incognita on brinjal (Solanum melongena L.) with some plant extracts. Curr. Nematol. 23(1–2): 65–72.

Sivakumar, M. and K. Gunasekara. 2011. Management of root-knot nematodes in tomato, chilli and brinjal by neem oil formulations. J. Biopestic. 4(2): 198–200.

Slavin, J.L. and B. Lloyd. 2012. Health benefits of fruits and vegetables. Adv. Nutr. 3(4): 506–516.

Subramaniyan, S., G. Rajendran and S. Vadivelu. 1990. Estimation of loss in tomato due to Meloidogyne incognita and Rotylenchulus reniformis. Ind. J. Nematol. 20(2): 239–240.

Taye, W., P.K. Sakhuja and T. Tefera. 2013. Root-knot nematode (Meloidogyne incognita) management using botanicals in tomato. Acad. J. Agric. Res. 1(1): 9–16.

Terefe, M., T. Tefera and P.K. Sakhuja. 2009. Effect of a formulation of Bacillus firmus on root-knot nematode Meloidogyne incognita and the growth of tomato plants in the greenhouse and nursery. J. Invertebr. Pathol. 100(2): 94–99.

Tisserat, N. 2006. Root knot nematode of tomato. Fact sheets tomato. Extension Plant Pathology, Kansas State University, Manhattan, USA.

Van Gundy, S.D. 1985. Ecology of Meloidogyne spp.–emphasis on environmental factors affecting survival and pathogenicity, pp. 177–182. In: J.N. Sasser and C.C. Carter, (Eds.), An Advanced Treatise on Meloidogyne. Volume 1. Biology and Control. North Carolina State University Graphics, Raleigh, North Carolina, USA.

Vetrivelkalai, P. 2019. Evaluation of endophytic bacterial isolates against root knot nematode, Meloidogyne incognita in tomato under glasshouse condition. Int. J. Curr. Microbiol. App. Sci. 8(1): 2584–2589.

Viaene, N., D.L. Coyne and B.R. Kerry. 2006. Biological and cultural management, pp. 346–369. In: R.N. Perry and M. Moens, (Eds.), Plant Nematology. CABI Publishing, Oxford shire, UK.

Viaene, N., D.L. Coyne and K.G. Davies. 2013. Biological and cultural management, pp. 383–410. In: R.N. Perry and M. Moens, (Eds.), Plant Nematology. 2nd Edition. CABI Publishing, Wallingford, UK.

Wachira, P.M., J.W. Kimenju, S.A. Okoth and R.K. Mibey. 2009. Stimulation of nematode-destroying fungi by organic amendments applied in management of plant parasitic nematode. Asian J. Plant Sci. 8(2): 153–159.

Weller, D.M., J.M. Raaijmakers, B.B.M. Gardener and L.S. Thomashow. 2002. Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu. Rev. Phytopathol. 40(1): 309–348.

Xiang, N., K.S. Lawrence and P.A. Donald. 2018. Biological control potential of plant growth-promoting rhizobacteria suppression of Meloidogyne incognita on cotton and Heterodera glycines on soybean: a review. J. Phytopathol. 166: 449–458.

Yamada, E. and S. Takakura. 1975. Occurrence of Meloidogyne incognita (Kofoid & White, 1919) Chitwood, 1949 on the roots of tomato and cucumber plants grown in a greenhouse in Hokkaido. Bull. Hokkaido Pref. Agric. Exp. Sta. 31: 43–49.

Yue, L., S. Ahmed, Q. Liu and H. Jian. 2019. Management of Meloidogyne incognita on tomato with different biocontrol organisms. Pak. J. Nematol. 37(2): 161–170.

Zeng, Y., W. Ye and J. Kerns. 2014. First report and morphological and molecular characterization of Meloidogyne incognita from Radermachera sinica in China. Nematropica. 44(2): 118–129.

Zhang, S., Y. Gan and B. Xu. 2014. Efficacy of Trichoderma longibrachiatum in the control of Heterodera avenae. BioControl. 59(3): 319–331.

Zhang, Y., S. Li, H. Li, R. Wang, K.Q. Zhang and J. Xu. 2020. Fungi-nematode interactions: diversity, ecology, and biocontrol prospects in agriculture. J. Fungi. 6(4): 206.

Zhou, L., G. Yuen, Y. Wang, L. Wei and G. Ji. 2016. Evaluation of bacterial biological control agents for control of root-knot nematode disease on tomato. Crop Prot. 84: 8–13.