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Guzmán-Piedrahita, Óscar A. ., Zamorano-Montañez, C. ., & López-Nicora, H. D. . (2020). Physiological interactions of plants with plant-parasitic nematodes: A review. Boletín Científico. Centro De Museos, 24(2), 190–205. https://doi.org/10.17151/bccm.2020.24.2.13
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Authors
Óscar Adrián Guzmán-Piedrahita
Perfil Google Scholar
Carolina Zamorano-Montañez
Horacio Daniel López-Nicora
Abstract
The plant parasitic nematodes are among the most damaging pathogens worldwide, affecting plant growth and yield. The plant responses to damage caused by nematodes is closely related to their food habitat, either ectoparasites or endoparasites, and the type of cell damage such as cell destruction caused by species of Pratylenchus and Radopholus; syncytia, related with species of Heterodera and Globodera; and, giant cells, produced by species of Meloidogyne. The objective of this review was to analyze the scope of current research results on understanding the physiological implications of plant interaction with plant-parasitic nematodes, mainly those that destroy the cell, form syncytia and giant cells. In general, the plant parasitic nematodes, regardless of the type of damage they cause, reduce the physiological functions of the roots by affecting the absorption of water and nutrients, create macro and micro-nutriment imbalances that induce physiological changes in the roots and aerial organs of plants, and produce yield losses. More research is required related with the nutritional status of the plants, when interacting with plant parasitic nematodes, in order to get better physiological responses of the plants, which will allow to have less impact of the parasitism of the nematodes on the plants, contributing to a better the management of these.
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References
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Abbasi y Hisamuddin. (2014). Effect of different inoculum levels of Meloidogyne incognita on growth and biochemical parameters of Vigna radiata. Asian J. Nematol. 3(1): 15-20.
Agrios, G.N. (2005). Plant pathology. 5thed. Nueva York: Elsevier Academic Press. 922p.
Asmus, G.L., y Ferraz, L.C.C.B. (2002). Effect of population densities of Heterodera glycines race 3 on leaf area, photosynthesis and yield of soybean. Fitopatologia Brasileira, 27: 273-278.
Been, T.H., y Schomaker, C.H. (1986). Quantitative analysis of growth, mineral composition and ion balance of the potato cultivar Irene infested with Globodera pallida (Stone). Nematologica 32: 339-355.
Bolaños, M.M.; Ramírez, J.; Esquivel, F., y Martínez, E. (2011). Prácticas sostenibles para el manejo de nematodos fitoparásitos en cultivos de guayaba. Corporación Colombiana de Investigación Agropecuaria, Corpoica.
Cabrera, J., Barcala, M., Fenoll, C., y Escobar, C. (2016). The power of omics to identify plant susceptibility factors and to study resistance to root-knot nematodes. Curr. Issues Mol. Biol. 19: 53-72.
Cabrera, J., Bustos, R., Favery, B., Fenoll, C., y Escobar, C. (2014). NEMATIC: a simple and versatile tool for the in-silico analysis of plant-nematode interactions. Mol. Plant Pathol. 15: 627-636.
Chen, J., Lin, B., Huang, Q., Hu, L., Zhuo, K., y Liao, J. (2017). A novel Meloidogyne graminicola effector, MgGPP, is secreted into host cells and undergoes glycosylation in concert with proteolysis to suppress plant defenses and promote parasitism. PLoS Pathog. 13: 1-24.
Dorhout, R., Gommers, F.J., y Kolloffel, C. (1991). Water transport through tomato roots infected with Meloidogyne incognita. Phytopathology 81: 379-385.
Fatemy, F., y Evans, K. (1986). Growth, water uptake and calcium content of potato cultivars in relation to tolerance of cyst nematodes. RevueNématol. 9(2): 171-179.
Fogain, R. (2000). Effect of Radopholus similis on plant growth and yield of plantain (Musa AAB). Nematology 2: 129-133.
Gelpud, C., Mora, E., Salazar, C., y Betancourth, C. (2011). Susceptibility of genotypes of Solanum spp. to the nematode causative of the root knot Meloidogyne spp. (Chitwood). ActaAgron. 60(1): 50-67.
Gheysen, G. y Mitchum, M.G. (2019). Phytoparasitic nematode control of plant hormone pathways. PlantPhysiol. 179: 1212-1226.
Golinowski, W., Sobczak, M., Kurek, W., y Gry-Maszewska, G. (1997). The structure of syncytia. Pp. 80-97. In: Fen- noll, C., Grundler, F.M.W. & Ohl, S.A. (Eds). Cellular and Molecular Aspects of Plant-Nematode Interactions. Dordrecht, The Netherlands, Kluwer.
Goverse, A. y Smant, G. (2014). The Activation and suppression of plant innate immunity by parasitic nematodes. Annu. Rev. Phytopathol. 52: 243-65.
Guzmán-Piedrahita., O.A., Castaño-Zapata, J. y Villegas-Estrada, B. (2012). Efectividad de la sanidad de cormos de plátano Dominico Hartón (Musa AAB Simmonds), sobre nematodos fitoparásitos y rendimiento del cultivo. Rev. Acad. Colomb. Cienc. 36(138): 45-55.
Guzmán-Piedrahita., O.A. y Castaño-Zapata, J. (2020). Nematodos fitoparásitos en cultivos tropicales. Manual de diagnóstico. 277p.
Haegeman, A., Mantelin, S., Jones, J.T., y Gheysen, G. (2012). Functional roles of effectors of plant-parasitic nematodes. Gene 492:19-31.
Herradura, L.E., Lobres, M.A., De Waele, D., Davide, R.G., y Van Den Bergh, I. (2012). Yield response of four popular banana varieties from southeast Asia to infection with a population of Radopholus similis from Davao, Philippines. Nematology 14(7): 889-897.
Hogenhout, S.A., Van Der Hoorn, R.A.L., Terauchi, R., y Kamoun, S. (2009). Emerging concepts in effector biology of plant-associated organisms. Mol. Plant Microbe Interac. 22:115-122.
Hojat Jalali, A.A., Ghasempour, H.R., y Madadzadeh, F. (2007). Impact of sugar beet cyst nematode, Heterodera schachtii, on some physiological aspects of two sugar beet cultivars, nemakill and 7233, in the rhizosphere condition. PlantPathologyJournal 6(1): 60-65.
Ibrahim, H.M.M., Ahmad, E.M., Martínez-Medina, A., Aly, M.A.M. (2019). Effective approaches to study the plant-root knot nematode interaction. Plant Physiology and Biochemistry 141: 332-342.
Jaleel, C.A., Manivannan, P., Wahid, A., Farooq, M., Somasundaram, R., y Panneerselvam, R. (2009). Drought stress in plants: a review on morphological characterization. International Journal of Agriculture and Biology 11: 100-105.
Jones, J.T., Haegeman, A., Danchin, E.G.J., Gaur, H.S., Helder, J., Jones, M.G.K., Kikuchi, T., Manzanilla-López, R., PalomaresRius, J.E., Wesemael, W.M.L., y Perry, R.N. (2013). Review: Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular PlantPathology 14(9): 946-961.
Karanastasi, E., Kostara, T., Malamos, N., y Zervoudakis, G. (2018). Catalase activity, lipid peroxidation, and protein concentration in leaves of tomato infected with Meloidogyne javanica. Nematropica 48: 15-20.
Kyndt, T., Nahar, K., Haegeman, A., De Vleesschauwer, D., Hofte, M., y Gheysen, G. (2012). Comparing systemic defense-related gene expression changes upon migratory and sedentary nematode attack in rice. Plant Biol. 14:73-82.
Kyndt, T., Vieira, P., Gheysen, G., De Almeida‐Engler, J. (2013). Nematode feeding sites: unique organs in plant roots. Planta 238:807-818.
Ko, M.P., Barker, K.R., y Huang, J.S. (1984). Nodulation of soybeans as affected by half-root infection with Heterodera glycines. Journal of Nematology 16: 97-105.
Korayem, A. (2013). Damage threshold of root-knot nematode, Meloidogyne arenaria on peanut in relation to date of planting and irrigation system. Canadian Journal of Plant Protection, 1(4): 117-124.
Liu, W. y Park, S.W. (2018). Underground mystery: Interactions between plant roots and parasitic nematodes. Current Plant Biology 15: 25-29.
Lopez-Nicora, H.D., y Niblack, T.L. (2018). Chapter 12: Interactions with other pathogens. Pp. 271-304. In: Cyst Nematodes. Perry, R.N., Moens, M. y Jones, J.T. (Eds.). CABI Publishing.
Loveys, B.R., y Bird, A.F. (1973). The influence of nematodes on photosynthesis in tomato plants. Physiological Plant Pathology 3: 525-629.
Mateille, T. (1993). Effects of banana-parasitic nematodes on Musa acuminata (AAA group) cvs. Poyo and Gros Michel in vitro plants. Tropical Agriculture Trinidad 70(4): 325-331.
Melakeberhan, H., Webster, J.M., y Brooke, R.C. (1985). Response of Phaseolus vulgaris to a single generation of Meloidogyne incognita. Nematologica 31: 190-202.
Melakeberhan, H., Brooke, R.C., y Webster, J.M. (1986). Relationship between physiological response of French beans of different age to Meloidogyne incognita and subsequent yield loss. Plant Pathology 35: 203-213.
Melakeberhan, H., y Ferris, H. (1989). Impact of Meloidogyne incognita on Physiological Efficiency of Vitis vinifera. Journal of Nematology 21(1): 74-80.
Melakeberhan, H. (1999). Effects of nutrient source on the physiological mechanisms of Heterodera glycines and soybean genotypes interactions. Nematology 1: 113-120.
Melakeberhan, H. (2004). Physiological interactions between nematodes and their host plants (Chapter 15). In: Chen, Z.X., Chen,
S.Y., y Dickson, D.W. (2004). Nematology – Advances and Perspectives. Volume II: Nematode Management and Utilization. CABI Publishing.
Moens, T., Araya, M., Swennen, R., y De Waele, D. (2006). Reproduction and pathogenicity of Helicotylenchus multicinctus, Meloidogyne incognita and Pratylenchus coffeae, and their interaction with Radopholus similis on Musa. Nematology 8(1): 45-58.
Moens, M., Perry, R., y Jones, J. (2018). Cyst nematodes – life cycle and economic importance. Pp. 1-26. In: Cyst Nematodes. Perry, R., Moens, M., y Jones, J. (Eds.). CABI Publishing.
Nicol, J.M., Turner, S.J., Coyne, D.L., Den Nijs, L., Hockland, S., y Maafi, Z.T. (2011). Current nematode threats to world agriculture. Pp. 21–44. In: Genomics and Molecular Genetics of Plant–Nematode Interactions. Jones, J.T., Gheysen, G., y Fenoll, C. (Eds.). Heidelberg: Springer.
Oramas Nival, D., y Román, J. (2006). Histopatología de los nematodos Radopholus similis, Pratylenchus coffeae, Rotylenchulus reniformis y Meloidogyne incognita en plátano (Musa acumulata X M. balbisiana, AAB). J. Agric. Univ. P.R., 90(1-2): 83-97.
Palomares-Rius, J.E., Escobar, C., Cabrera, J., Vovlas, A., Castillo, P. (2017). Anatomical alterations in plant tissues induced by plantparasitic nematodes. Front. Plant Sci. 8:1-16.
Postuka, J.W., Dropkin, V.H., y Nelson, C.J. (1986). Photosynthesis, photorespiration, and respiration of soybean after infection with root nematodes. Photosynthetica 20: 405-410.
Quentin, M., Abad, P., y Favery, B. (2013). Plant parasitic nematode effectors target host defense and nuclear functions to establish feeding cells. Front. Plant Sci., 4: 1:7.
Rahi, G.S., Rich, J.R., y Hodge, C. (1988). Effect Meloidogyne incognita and M. javanica on leaf water potential and water use of tobacco. Journal of Nematology 20(4): 516-522.
Ramakrishnan, S., y Rajendran, G. (1999). Changes induced by Meloidogyne incognita and Rotylenchulus reniformis, individually and in combination on physiology, chlorophyll and nutrients content of papaya. Nematol. Medit. 27: 111-122.
Sasser, J.N., y Freckman, D.W. (1987). A world perspective on nematology: the role of the society. Pp. 7-20. In: Vistas on Nematology. Veech, J.A., y Dickson, D.W. (Eds.). Hyattsville, Maryland.
Schans, J. (1991). Reduction of leaf photosynthesis and transpiration rates of potato plants by second-stage juveniles of Globodera pallida. Plant, Cell and Environment 14: 707-712.
Siddique, S., Radakovic, Z.S., De La Torre, C.M., Chronis, D., Novák, O., Ramireddy, E., Holbein, J., Matera, C., Hütten, M., Gutbrod, P., Shahzad Anjam, M., Rozanska, E., Habash, S., Elashry, A., Sobczak, M., Kakimoto, T., Strnad, M., Schmülling, T., Mitchum, M.G., y Grundler, F.M.W. (2015). A parasitic nematode releases cytokinin that controls cell division and orchestrates feeding site formation in host plants. Proc Natl Acad Sci USA 112: 12669-12674.
Sikora, R., Coyne, D., y Quénéhervé, P. (2018). Chapter 17: Nematode parasites of bananas and plantains. Pp. 617-657. In: Plant Parasitic Nematodes in Subtropical and Tropical Agriculture. Sikora, R., Coyne, D., Hallmann, J. y Timper, P. (Eds.). CABI Publishing.
Swain, B., y Prasad, J. (1989). Photosynthetic rate in rice as influenced by the root-knot nematode, Meloidogyne graminicola, infection. Revue Nématol. 12(4): 431-432.
Thakur, S.K. (2014). Effect of Meloidogyne incognita on chlorophyll, carotenoid content and physiological function of Mentha arvensis. Agric. Sci. Digest. 34(3): 219: 222.
Van Den Akker, S.E., y Birch, P.R.J. (2016). Opening the effector protein toolbox for plant – parasitic cyst nematode interactions. Mol. Plant 9: 1451-1453.
Wallace, H.R. (1974). The influence of root-knot nematode, Meloidogyne javanica on photosynthesis and on nutrient demand by roots of tomato plants. Nematologica 20: 27-33.
Wang, J., Niblack, T.L., Tremaine, J.N., Wiebold, W.J., Tylka, G.L., Marett, C.C., Noel, G.R., Myers, O., y Schmidt, M. (2003). The soybean cyst nematode reduces soybean yield without causing obvious symptoms. Plant Disease 87: 623-628.
Abbasi y Hisamuddin. (2014). Effect of different inoculum levels of Meloidogyne incognita on growth and biochemical parameters of Vigna radiata. Asian J. Nematol. 3(1): 15-20.
Agrios, G.N. (2005). Plant pathology. 5thed. Nueva York: Elsevier Academic Press. 922p.
Asmus, G.L., y Ferraz, L.C.C.B. (2002). Effect of population densities of Heterodera glycines race 3 on leaf area, photosynthesis and yield of soybean. Fitopatologia Brasileira, 27: 273-278.
Been, T.H., y Schomaker, C.H. (1986). Quantitative analysis of growth, mineral composition and ion balance of the potato cultivar Irene infested with Globodera pallida (Stone). Nematologica 32: 339-355.
Bolaños, M.M.; Ramírez, J.; Esquivel, F., y Martínez, E. (2011). Prácticas sostenibles para el manejo de nematodos fitoparásitos en cultivos de guayaba. Corporación Colombiana de Investigación Agropecuaria, Corpoica.
Cabrera, J., Barcala, M., Fenoll, C., y Escobar, C. (2016). The power of omics to identify plant susceptibility factors and to study resistance to root-knot nematodes. Curr. Issues Mol. Biol. 19: 53-72.
Cabrera, J., Bustos, R., Favery, B., Fenoll, C., y Escobar, C. (2014). NEMATIC: a simple and versatile tool for the in-silico analysis of plant-nematode interactions. Mol. Plant Pathol. 15: 627-636.
Chen, J., Lin, B., Huang, Q., Hu, L., Zhuo, K., y Liao, J. (2017). A novel Meloidogyne graminicola effector, MgGPP, is secreted into host cells and undergoes glycosylation in concert with proteolysis to suppress plant defenses and promote parasitism. PLoS Pathog. 13: 1-24.
Dorhout, R., Gommers, F.J., y Kolloffel, C. (1991). Water transport through tomato roots infected with Meloidogyne incognita. Phytopathology 81: 379-385.
Fatemy, F., y Evans, K. (1986). Growth, water uptake and calcium content of potato cultivars in relation to tolerance of cyst nematodes. RevueNématol. 9(2): 171-179.
Fogain, R. (2000). Effect of Radopholus similis on plant growth and yield of plantain (Musa AAB). Nematology 2: 129-133.
Gelpud, C., Mora, E., Salazar, C., y Betancourth, C. (2011). Susceptibility of genotypes of Solanum spp. to the nematode causative of the root knot Meloidogyne spp. (Chitwood). ActaAgron. 60(1): 50-67.
Gheysen, G. y Mitchum, M.G. (2019). Phytoparasitic nematode control of plant hormone pathways. PlantPhysiol. 179: 1212-1226.
Golinowski, W., Sobczak, M., Kurek, W., y Gry-Maszewska, G. (1997). The structure of syncytia. Pp. 80-97. In: Fen- noll, C., Grundler, F.M.W. & Ohl, S.A. (Eds). Cellular and Molecular Aspects of Plant-Nematode Interactions. Dordrecht, The Netherlands, Kluwer.
Goverse, A. y Smant, G. (2014). The Activation and suppression of plant innate immunity by parasitic nematodes. Annu. Rev. Phytopathol. 52: 243-65.
Guzmán-Piedrahita., O.A., Castaño-Zapata, J. y Villegas-Estrada, B. (2012). Efectividad de la sanidad de cormos de plátano Dominico Hartón (Musa AAB Simmonds), sobre nematodos fitoparásitos y rendimiento del cultivo. Rev. Acad. Colomb. Cienc. 36(138): 45-55.
Guzmán-Piedrahita., O.A. y Castaño-Zapata, J. (2020). Nematodos fitoparásitos en cultivos tropicales. Manual de diagnóstico. 277p.
Haegeman, A., Mantelin, S., Jones, J.T., y Gheysen, G. (2012). Functional roles of effectors of plant-parasitic nematodes. Gene 492:19-31.
Herradura, L.E., Lobres, M.A., De Waele, D., Davide, R.G., y Van Den Bergh, I. (2012). Yield response of four popular banana varieties from southeast Asia to infection with a population of Radopholus similis from Davao, Philippines. Nematology 14(7): 889-897.
Hogenhout, S.A., Van Der Hoorn, R.A.L., Terauchi, R., y Kamoun, S. (2009). Emerging concepts in effector biology of plant-associated organisms. Mol. Plant Microbe Interac. 22:115-122.
Hojat Jalali, A.A., Ghasempour, H.R., y Madadzadeh, F. (2007). Impact of sugar beet cyst nematode, Heterodera schachtii, on some physiological aspects of two sugar beet cultivars, nemakill and 7233, in the rhizosphere condition. PlantPathologyJournal 6(1): 60-65.
Ibrahim, H.M.M., Ahmad, E.M., Martínez-Medina, A., Aly, M.A.M. (2019). Effective approaches to study the plant-root knot nematode interaction. Plant Physiology and Biochemistry 141: 332-342.
Jaleel, C.A., Manivannan, P., Wahid, A., Farooq, M., Somasundaram, R., y Panneerselvam, R. (2009). Drought stress in plants: a review on morphological characterization. International Journal of Agriculture and Biology 11: 100-105.
Jones, J.T., Haegeman, A., Danchin, E.G.J., Gaur, H.S., Helder, J., Jones, M.G.K., Kikuchi, T., Manzanilla-López, R., PalomaresRius, J.E., Wesemael, W.M.L., y Perry, R.N. (2013). Review: Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular PlantPathology 14(9): 946-961.
Karanastasi, E., Kostara, T., Malamos, N., y Zervoudakis, G. (2018). Catalase activity, lipid peroxidation, and protein concentration in leaves of tomato infected with Meloidogyne javanica. Nematropica 48: 15-20.
Kyndt, T., Nahar, K., Haegeman, A., De Vleesschauwer, D., Hofte, M., y Gheysen, G. (2012). Comparing systemic defense-related gene expression changes upon migratory and sedentary nematode attack in rice. Plant Biol. 14:73-82.
Kyndt, T., Vieira, P., Gheysen, G., De Almeida‐Engler, J. (2013). Nematode feeding sites: unique organs in plant roots. Planta 238:807-818.
Ko, M.P., Barker, K.R., y Huang, J.S. (1984). Nodulation of soybeans as affected by half-root infection with Heterodera glycines. Journal of Nematology 16: 97-105.
Korayem, A. (2013). Damage threshold of root-knot nematode, Meloidogyne arenaria on peanut in relation to date of planting and irrigation system. Canadian Journal of Plant Protection, 1(4): 117-124.
Liu, W. y Park, S.W. (2018). Underground mystery: Interactions between plant roots and parasitic nematodes. Current Plant Biology 15: 25-29.
Lopez-Nicora, H.D., y Niblack, T.L. (2018). Chapter 12: Interactions with other pathogens. Pp. 271-304. In: Cyst Nematodes. Perry, R.N., Moens, M. y Jones, J.T. (Eds.). CABI Publishing.
Loveys, B.R., y Bird, A.F. (1973). The influence of nematodes on photosynthesis in tomato plants. Physiological Plant Pathology 3: 525-629.
Mateille, T. (1993). Effects of banana-parasitic nematodes on Musa acuminata (AAA group) cvs. Poyo and Gros Michel in vitro plants. Tropical Agriculture Trinidad 70(4): 325-331.
Melakeberhan, H., Webster, J.M., y Brooke, R.C. (1985). Response of Phaseolus vulgaris to a single generation of Meloidogyne incognita. Nematologica 31: 190-202.
Melakeberhan, H., Brooke, R.C., y Webster, J.M. (1986). Relationship between physiological response of French beans of different age to Meloidogyne incognita and subsequent yield loss. Plant Pathology 35: 203-213.
Melakeberhan, H., y Ferris, H. (1989). Impact of Meloidogyne incognita on Physiological Efficiency of Vitis vinifera. Journal of Nematology 21(1): 74-80.
Melakeberhan, H. (1999). Effects of nutrient source on the physiological mechanisms of Heterodera glycines and soybean genotypes interactions. Nematology 1: 113-120.
Melakeberhan, H. (2004). Physiological interactions between nematodes and their host plants (Chapter 15). In: Chen, Z.X., Chen,
S.Y., y Dickson, D.W. (2004). Nematology – Advances and Perspectives. Volume II: Nematode Management and Utilization. CABI Publishing.
Moens, T., Araya, M., Swennen, R., y De Waele, D. (2006). Reproduction and pathogenicity of Helicotylenchus multicinctus, Meloidogyne incognita and Pratylenchus coffeae, and their interaction with Radopholus similis on Musa. Nematology 8(1): 45-58.
Moens, M., Perry, R., y Jones, J. (2018). Cyst nematodes – life cycle and economic importance. Pp. 1-26. In: Cyst Nematodes. Perry, R., Moens, M., y Jones, J. (Eds.). CABI Publishing.
Nicol, J.M., Turner, S.J., Coyne, D.L., Den Nijs, L., Hockland, S., y Maafi, Z.T. (2011). Current nematode threats to world agriculture. Pp. 21–44. In: Genomics and Molecular Genetics of Plant–Nematode Interactions. Jones, J.T., Gheysen, G., y Fenoll, C. (Eds.). Heidelberg: Springer.
Oramas Nival, D., y Román, J. (2006). Histopatología de los nematodos Radopholus similis, Pratylenchus coffeae, Rotylenchulus reniformis y Meloidogyne incognita en plátano (Musa acumulata X M. balbisiana, AAB). J. Agric. Univ. P.R., 90(1-2): 83-97.
Palomares-Rius, J.E., Escobar, C., Cabrera, J., Vovlas, A., Castillo, P. (2017). Anatomical alterations in plant tissues induced by plantparasitic nematodes. Front. Plant Sci. 8:1-16.
Postuka, J.W., Dropkin, V.H., y Nelson, C.J. (1986). Photosynthesis, photorespiration, and respiration of soybean after infection with root nematodes. Photosynthetica 20: 405-410.
Quentin, M., Abad, P., y Favery, B. (2013). Plant parasitic nematode effectors target host defense and nuclear functions to establish feeding cells. Front. Plant Sci., 4: 1:7.
Rahi, G.S., Rich, J.R., y Hodge, C. (1988). Effect Meloidogyne incognita and M. javanica on leaf water potential and water use of tobacco. Journal of Nematology 20(4): 516-522.
Ramakrishnan, S., y Rajendran, G. (1999). Changes induced by Meloidogyne incognita and Rotylenchulus reniformis, individually and in combination on physiology, chlorophyll and nutrients content of papaya. Nematol. Medit. 27: 111-122.
Sasser, J.N., y Freckman, D.W. (1987). A world perspective on nematology: the role of the society. Pp. 7-20. In: Vistas on Nematology. Veech, J.A., y Dickson, D.W. (Eds.). Hyattsville, Maryland.
Schans, J. (1991). Reduction of leaf photosynthesis and transpiration rates of potato plants by second-stage juveniles of Globodera pallida. Plant, Cell and Environment 14: 707-712.
Siddique, S., Radakovic, Z.S., De La Torre, C.M., Chronis, D., Novák, O., Ramireddy, E., Holbein, J., Matera, C., Hütten, M., Gutbrod, P., Shahzad Anjam, M., Rozanska, E., Habash, S., Elashry, A., Sobczak, M., Kakimoto, T., Strnad, M., Schmülling, T., Mitchum, M.G., y Grundler, F.M.W. (2015). A parasitic nematode releases cytokinin that controls cell division and orchestrates feeding site formation in host plants. Proc Natl Acad Sci USA 112: 12669-12674.
Sikora, R., Coyne, D., y Quénéhervé, P. (2018). Chapter 17: Nematode parasites of bananas and plantains. Pp. 617-657. In: Plant Parasitic Nematodes in Subtropical and Tropical Agriculture. Sikora, R., Coyne, D., Hallmann, J. y Timper, P. (Eds.). CABI Publishing.
Swain, B., y Prasad, J. (1989). Photosynthetic rate in rice as influenced by the root-knot nematode, Meloidogyne graminicola, infection. Revue Nématol. 12(4): 431-432.
Thakur, S.K. (2014). Effect of Meloidogyne incognita on chlorophyll, carotenoid content and physiological function of Mentha arvensis. Agric. Sci. Digest. 34(3): 219: 222.
Van Den Akker, S.E., y Birch, P.R.J. (2016). Opening the effector protein toolbox for plant – parasitic cyst nematode interactions. Mol. Plant 9: 1451-1453.
Wallace, H.R. (1974). The influence of root-knot nematode, Meloidogyne javanica on photosynthesis and on nutrient demand by roots of tomato plants. Nematologica 20: 27-33.
Wang, J., Niblack, T.L., Tremaine, J.N., Wiebold, W.J., Tylka, G.L., Marett, C.C., Noel, G.R., Myers, O., y Schmidt, M. (2003). The soybean cyst nematode reduces soybean yield without causing obvious symptoms. Plant Disease 87: 623-628.
