Plant-parasitic nematode infective juveniles (J2) use phytochemical signals released into the rhizosphere to locate host roots. Amino acids are the second most abundant metabolites of root exudates, but it is unknown if they are associated with J2 chemotaxis. In this study, J2 chemotaxis and mortality of the soybean cyst nematode (Heterodera glycines) and root-knot nematodes (Meloidogyne incognita and M. hapla) were examined in response to 15 amino acids and the corresponding pH values for tested amino acid solutions were measured. Responses varied by amino acid and among the species. Significant attraction, determined by J2 count within amino acid solution dispensers after 24 h exposure, occurred with 19 out of 45 J2-amino acid combinations. Heterodera glycines, M. hapla and M. incognita were attracted to nine, three and seven amino acids, respectively. Strongest attractions were to acidic polar amino acids aspartate and glutamate (H. glycines, M. hapla) and basic polar arginine (M. hapla), as previously reported, acid and basic pH attracting nematodes, thereby indicating that pH might be one of the attraction factors for these amino acids. All three nematodes exhibited clustering behaviours, such as halo or balling formations, just outside amino acid solution dispensers, with H. glycines, M. hapla and M. incognita responding to four, 12 and two amino acids, respectively. Six of 15 amino acid solutions, representing a range of pH values, caused increased mortality. Certain aspartate and glutamate affected both H. glycines and M. hapla; arginine, aspartate, cysteine, lysine, methionine affected M. incognita; and cysteine caused complete mortality in M. hapla. All the results suggest that amino acids affect nematode attraction and mortality.
Purchase
Buy instant access (PDF download and unlimited online access):
Institutional Login
Log in with Open Athens, Shibboleth, or your institutional credentials
Personal login
Log in with your brill.com account
Badri, D.V. & Vivanco, J.M. (2009). Regulation and function of root exudates. Plant Cell & Environment 32, 666-681. DOI: 10.1111/j.1365-3040.2009.01926.x
Bhagavan, N.V. & Ha, C.-E. (2015). Amino acids. In: Bhagavan, N.V. & Ha, C.-E. (Eds). Essentials of medical biochemistry, 2nd edition. Amsterdam, The Netherlands, Elsevier, pp. 21-29. DOI: 10.1016/B978-0-12-416687-5.00003-8
Bian, J., Zhang, H., Meng, S. & Liu, Y. (2018). Chemotaxis of Caenorhabditis elegans toward volatile organic compounds from Stropharia rugosoannulata induced by amino acids. Journal of Nematology 50, 3-8. DOI: 10.21307/jofnem-2018-003
Blümel, R.C., Fischer, D.F. & Grundler, F.M.W. (2018). Effects of exogenous amino acid applications on the plant-parasitic nematode Heterodera schachtii. Nematology 20, 713-727. DOI: 10.1163/15685411-00003169
Bobille, H., Fustec, J., Robins, R.J., Cukier, C. & Limami, A.M. (2019). Effect of water availability on changes in root amino acids and associated rhizosphere on root exudation of amino acids in Pisum sativum L. Phytochemistry 161, 75-85. DOI: 10.1016/j.phytochem.2019.01.015
Braendle, C. (2012). Pheromones: evolving language of chemical communication in nematodes. Current Biology 22, R294-R296. DOI: 10.1016/j.cub.2012.03.035
Canarini, A., Kaiser, C., Merchant, A., Richter, A. & Wanek, W. (2019). Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Frontiers in Plant Science 10, 157. DOI: 10.3389/fpls.2019.00157
Choe, A., von Reuss, S.H., Kogan, D., Gasser, R.B., Platzer, E.G., Schroeder, F.C. & Sternberg, P.W. (2012). Ascaroside signaling is widely conserved among nematodes. Current Biology 22, 772-780. DOI: 10.1016/j.cub.2012.03.024
Cooper, A.F. Jr & Van Gundy, S.D. (1971). Senescence, quiescence, and cryptobiosis. In: Zuckerman, B.M., Mai, W.F. & Rohde, R.A. (Eds). Plant parasitic nematodes, vol. II. New York, NY, USA, Academic Press, pp. 297-318.
Dalangin, R., Kim, A. & Campbell, R.E. (2020). The role of amino acids in neurotransmission and fluorescent tools for their detection. International Journal of Molecular Sciences 21, 6197. DOI: 10.3390/ijms21176197
de Bono, M. & Maricq, A.V. (2005). Neuronal substrates of complex behaviors in C. elegans. Annual Review of Neuroscience 28, 451-501. DOI: 10.1146/annurev.neuro.27.070203.144259
Glick, B.R. & Gamalero, E. (2021). Recent developments in the study of plant microbiomes. Microorganisms 9, 1533. DOI: 10.3390/microorganisms9071533
Hamada, N., Yimer, H.Z., Williamson, V.M. & Siddique, S. (2020). Chemical hide and seek: nematode’s journey to its plant host. Molecular Plant 13, 541-543. DOI: 10.1016/j.molp.2020.03.005
Hoque, A.K.M.A., Bhuiyan, M.R., Khan, M.A.I., Mahmud, A. & Ahmad, M.U. (2014). Effect of amino acids on root-knot nematode (Meloidogyne javanica) infecting tomato plant. Archives of Phytopathology and Plant Protection 47, 1921-1928. DOI: 10.1080/03235408.2013.862039
Hu, L., Robert, C.A.M., Cadot, S., Zhang, X., Ye, M., Li, B., Manzo, D., Chervet, N., Steinger, T., van der Heijden, M.G.A. et al. (2018). Root exudate metabolites drive plant-soil feedbacks on growth and defense by shaping the rhizosphere microbiota. Nature Communications 9, 2738. DOI: 10.1038/s41467-018-05122-7
Hua, C., Li, C., Hu, Y., Mao, Y., You, J., Wang, M., Chen, J., Tian, Z. & Wang, C. (2018). Identification of HG types of soybean cyst nematode Heterodera glycines and resistance screening on soybean genotypes in northeast China. Journal of Nematology 50, 41-50. DOI: 10.21307/jofnem-2018-007
Hua, C., Li, C., Jiang, Y., Huang, M., Williamson, V.M. & Wang, C. (2020). Response of soybean cyst nematode (Heterodera glycines) and root-knot nematodes (Meloidogyne spp.) to gradients of pH and inorganic salts. Plant and Soil 455, 305-318. DOI: 10.1007/s11104-020-04677-z
Hussey, R.S. & Barker, K.R. (1973). A comparison of methods of collecting inocula of Meloidogyne spp., including a new technique. Plant Disease Reporter 57, 1025-1028.
Jaeger III, C.H., Lindow, S.E., Miller, W., Clark, E. & Firestone, M.K. (1999). Mapping of sugar and amino acid availability in soil around roots with bacterial sensors of sucrose and tryptophan. Applied and Environmental Microbiology 65, 2685-2690. DOI: 10.1128/AEM.65.6.2685-2690.1999
Jones, D.L. & Darrah, P.R. (1994). Amino-acid influx at the soil-root interface of Zea mays L. and its implications in the rhizosphere. Plant and Soil 163, 1-12. DOI: 10.1007/BF00033935
Jones, D.L., Shannon, D., Junvee-Fortune, T. & Farrar, J.F. (2005). Plant capture of free amino acids is maximized under high soil amino acid concentrations. Soil Biology and Biochemistry 37, 179-181. DOI: 10.1016/j.soilbio.2004.07.021
Jones, J.T., Haegeman, A., Danchin, E.G.J., Gaur, H.S., Helder, J., Jones, M.G.K., Kikuchi, T., Manzanilla-López, R., Palomares-Rius, J.E., Wesemael, W.M.L. et al. (2013). Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology 14, 946-961. DOI: 10.1111/mpp.12057
Kim, S. & Whang, K. (2012). [Nematicidal effect of root-knot nematode (Meloidogyne incognita) by amino acids biochemical agent extracted from chicken feather.] Journal of Applied Biological Chemistry 55, 247-252. DOI: 10.3839/jabc.2012.039
Li, C., Hu, Y. & Wang, C. (2016). [Identification of species and races of root-knot nematodes in greenhouse from Daqing City in Heilongjiang province.] Soils and Crops 5, 105-109. DOI: 10.11689/j.issn.2095-2961.2016.02.006
Macosko, E.Z., Pokala, N., Feinberg, E.H., Chalasani, S.H., Butcher, R.A., Clardy, J. & Bargmann, C.I. (2009). A hub-and-spoke circuit drives pheromone attraction and social behaviour in C. elegans. Nature 458, 1171-1175. DOI: 10.1038/nature07886
Madhukar, S.M., Raha, P. & Singh, R.K. (2018). Identification of amino acids and sugars in root exudate of mungbean (Vigna radiata L.). Journal of Pharmacognosy and Phytochemistry 7, 1676-1680. https://www.phytojournal.com/archives/2018/vol7issue2/PartX/7-2-97-734.pdf
Manohar, M., Tenjo-Castano, F., Chen, S., Zhang, Y.K., Kumari, A., Williamson, V.M., Wang, X., Klessig, D.F. & Schroeder, F.C. (2020). Plant metabolism of nematode pheromones mediates plant-nematode interactions. Nature Communications 11, 208. DOI: 10.1038/s41467-019-14104-2
McSorley, R. (2003). Adaptations of nematodes to environmental extremes. Florida Entomologist 86, 138-142. DOI: 10.1653/0015-4040(2003)086[0138:AONTEE]2.0.CO;2
Olanrewaju, O.S., Ayangbenro, A.S., Glick, B.R. & Babalola, O.C. (2019). Plant health: feedback effect of root exudates-rhizobiome interactions. Applied Microbiology and Biotechnology 103, 1155-1166. DOI: 10.1007/s00253-018-9556-6
Oliveira, D.F., Carvalho, H.W.P., Nunes, A.S., Silva, G.H., Campos, V.P., Júnior, H.M.S. & Cavalheiro, A.J. (2009). The activity of amino acids produced by Paenibacillus macerans and from commercial sources against the root-knot nematode Meloidogyne exigua. European Journal of Plant Pathology 124, 57-63. DOI: 10.1007/s10658-008-9392-0
Ortiz, C.O., Faumont, S., Takayama, J., Ahmed, H.K., Goldsmith, A.D., Pocock, R., McCormick, K.E., Kunimoto, H., Iino, Y., Lockery, S. et al. (2009). Lateralized gustatory behavior of C. elegans is controlled by specific receptor-type guanylyl cyclases. Current Biology 19, 996-1004. DOI: 10.1016/j.cub.2009.05.043
Osman, A.A. & Vigierochio, D.R. (1981). Meloidogyne incognita development on soybean treated with selected amino acids by alternate methods. Revue de Nématologie 4, 172-174.
Osman, G.Y. (1993). Effect of amino acids and ascorbic acid on Meloidogyne javanica Chitw. (Tylenchidae, Nematoda). Anzeiger für Schädlingskunde, Pflanzenschutz, Umweltschutz 66, 140-142. DOI: 10.1007/BF01906844
Osman, H., Ameen, H., Mohamed, M.M., Alkelany, U.S. & Dawood, M. (2017). Comparative study on the integrated application of environmental friendly compounds and a chemical nematicide in controlling root knot nematode Meloidogyne incognita infecting sunflower plants; a field study. Agricultural Engineering International: CIGR Journal 19, 132-137.
Perry, R.N. (2005). An evaluation of types of attractants enabling plant-parasitic nematodes to locate plant roots. Russian Journal of Nematology 13, 83-88.
Phillips, D.A., Fox, T.C., King, M.D., Bhuvaneswari, T.V. & Teuber, L.R. (2004). Microbial products trigger amino acid exudation from plant roots. Plant Physiology 136, 2887-2894. DOI: 10.1104/pp.104.044222
Rizaludin, M.S., Stopnisek, N., Raaijmakers, J.M. & Garbeva, P. (2021). The chemistry of stress: understanding the ‘cry for help’ of plant roots. Metabolites 11, 357. DOI: 10.3390/metabo11060357
Shivakumara, T.N., Dutta, T.K., Chaudhary, S., von Reuss, S.H., Williamson, V.M. & Rao, U. (2019). Homologs of Caenorhabditis elegans chemosensory genes have roles in behavior and chemotaxis in the root-knot nematode Meloidogyne incognita. Molecular Plant-Microbe Interactions 32, 876-887. DOI: 10.1094/MPMI-08-18-0226-R
Sikder, M.M. & Vestergård, M. (2020). Impacts of root metabolites on soil nematodes. Frontiers in Plant Science 10, 1792. DOI: 10.3389/fpls.2019.01792
Talavera, M. & Mizukubo, T. (2005). Effects of DL-methionine on hatching and activity of Meloidogyne incognita eggs and juveniles. Pest Management Science 61, 413-416. DOI: 10.1002/ps.974
Tanda, A.S., Atwal, A.S. & Bajaj, Y.P.S. (1989). In vitro inhibition of root-knot nematode Meloidogyne incognita by sesame root exudate and its amino acids. Nematologica 35, 115-124. DOI: 10.1163/002825989X00124
Tawaraya, K., Horie, R., Shinano, T., Wagatsuma, T., Saito, K. & Oikawa, A. (2014). Metabolite profiling of soybean root exudates under phosphorus deficiency. Soil Science and Plant Nutrition 60, 679-694. DOI: 10.1080/00380768.2014.945390
Wang, C., Bruening, G. & Williamson, V.M. (2009a). Determination of preferred pH for root-knot nematode aggregation using Pluronic F-127 gel. Journal of Chemical Ecology 35, 1242-1251. DOI: 10.1007/s10886-009-9703-8
Wang, C., Lower, S. & Williamson, V.M. (2009b). Application of Pluronic gel to the study of root-knot nematode behaviour. Nematology 11, 453-464. DOI: 10.1163/156854109x447024
Wang, C., Lower, S., Thomas, V.P. & Williamson, V.M. (2010). Root-knot nematodes exhibit strain-specific clumping behavior that is inherited as a simple genetic trait. PLoS ONE 5, e15148. DOI: 10.1371/journal.pone.0015148
Wang, C., Masler, E.P. & Rogers, S.T. (2018). Responses of Heterodera glycines and Meloidogyne incognita infective juveniles to root tissues, root exudates, and root extracts from three plant species. Plant Disease 102, 1733-1740. DOI: 10.1094/PDIS-09-17-1445-RE
All Time | Past 365 days | Past 30 Days | |
---|---|---|---|
Abstract Views | 831 | 316 | 69 |
Full Text Views | 64 | 15 | 0 |
PDF Views & Downloads | 112 | 29 | 0 |
Plant-parasitic nematode infective juveniles (J2) use phytochemical signals released into the rhizosphere to locate host roots. Amino acids are the second most abundant metabolites of root exudates, but it is unknown if they are associated with J2 chemotaxis. In this study, J2 chemotaxis and mortality of the soybean cyst nematode (Heterodera glycines) and root-knot nematodes (Meloidogyne incognita and M. hapla) were examined in response to 15 amino acids and the corresponding pH values for tested amino acid solutions were measured. Responses varied by amino acid and among the species. Significant attraction, determined by J2 count within amino acid solution dispensers after 24 h exposure, occurred with 19 out of 45 J2-amino acid combinations. Heterodera glycines, M. hapla and M. incognita were attracted to nine, three and seven amino acids, respectively. Strongest attractions were to acidic polar amino acids aspartate and glutamate (H. glycines, M. hapla) and basic polar arginine (M. hapla), as previously reported, acid and basic pH attracting nematodes, thereby indicating that pH might be one of the attraction factors for these amino acids. All three nematodes exhibited clustering behaviours, such as halo or balling formations, just outside amino acid solution dispensers, with H. glycines, M. hapla and M. incognita responding to four, 12 and two amino acids, respectively. Six of 15 amino acid solutions, representing a range of pH values, caused increased mortality. Certain aspartate and glutamate affected both H. glycines and M. hapla; arginine, aspartate, cysteine, lysine, methionine affected M. incognita; and cysteine caused complete mortality in M. hapla. All the results suggest that amino acids affect nematode attraction and mortality.
All Time | Past 365 days | Past 30 Days | |
---|---|---|---|
Abstract Views | 831 | 316 | 69 |
Full Text Views | 64 | 15 | 0 |
PDF Views & Downloads | 112 | 29 | 0 |