Mechanistic insights toward identification and interaction of plant parasitic nematodes: A review

Highlights

● Nematode identification serves as an important parameter to study their behaviour, importance and pathogenicity.

● Application of classical morphometric based identification methods prove to be lacking due to insufficient knowledge on morphological variations among closely related taxa. Molecular approaches such as DNA and protein-based information, microarray, probing, sequence-based methods and others have been used to supplement morphology-based methods for nematode identification.

● Ascarosides and certain protein-based nematode-associated molecular patterns (NAMPs), can be perceived by the host plants, and can initiate a signalling cascade.

● This review primarily emphasizes on an updated account of different classical and modern tools used for the identification of nematodes. Besides we also summarize the mechanism of some important signalling pathways which are involved in the different plant nematode interactions.

Abstract

Nematodes constitute most diverse and least studied group of soil inhabiting invertebrates. They are ecologically and physiologically important, however, wide range of nematodes show harmful impact on the individuals that live within their vicinity. Plant parasitic nematodes (PPNs) are transparent, pseudocoelomate, free living or parasitic microorganisms. PPNs lack morphometric identification methods due to insufficient knowledge on morphological variations among closely related taxa. As such, molecular approaches such as DNA and protein-based information, microarray, probing, sequence-based methods and others have been used to supplement morphology-based methods for their identification. To invade the defense response of different plant species, parasitic nematodes have evolved different molecular strategies. Ascarosides and certain protein-based nematode-associated molecular patterns (NAMPs), can be perceived by the host plants, and can initiate a signaling cascade. To overcome the host confrontation and develop certain nematode feeding sites, some members can inject effectors into the cells of susceptible hosts to reprogram the basal resistance signaling. This review primarily emphasizes on an updated account of different classical and modern tools used for the identification of PPNs. Besides we also summarize the mechanism of some important signaling pathways which are involved in the different plant nematode interactions.

Graphical abstract

Keywords

nematode identification / plant nematode interaction / DNA fingerprinting / nematode-associated molecular patterns / signaling pathways

References

[1] Abad, P., Gouzy, J., Aury, J.M., Castagnone-Sereno, P., Danchin, E.G., Deleury, E., Wincker, P., 2008. Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nature Biotechnology26, 909–915.

[2] Abd Elazim, A.M., Khashaba, E.H., Ibrahim, S.A., 2019. Genetic polymorphism among seven entomopathogenic nematode species (Steinernematidae) revealed by RAPD and SRAP analyses. Egyptian Journal of Biological Pest Control29, 1–7.

[3] Abd-Elgawad, M.M., 2021. Biological control of nematodes infecting eggplant in Egypt. Bulletin of the National Research Center45, 1–9.

[4] Abebe, E., Mekete, T., Thomas, W.K., 2011. A critique of current methods in nematode taxonomy. African Journal of Biotechnology10, 312–323.

[5] Absmanner, B., Stadler, R., Hammes, U.Z., 2013. Phloem development in nematode-induced feeding sites: the implications of auxin and cytokinin. Frontiers in Plant Science4, 241.

[6] Adams, B.J., 2001. The species delimitation uncertainty principle. Journal of Nematology33, 153.

[7] Akintayo, A., Tylka, G.L., Singh, A.K., Ganapathysubramanian, B., Singh, A., Sarkar, S., Ganapathysubramanian B, Singh A, Sarkar S., 2018. A deep learning framework to discern and count microscopic nematode eggs. Scientific Reports8, 9145.

[8] Akram, S., Khan, S.A., Javed, N., Ahmad, S., 2020. Integrated management of root knot nematode Meloidogyne graminicola golden and Birchfield Parasitizing on wheat. Pakistan Journal of Zoology52, 1299.

[9] Ali, M.A., Azeem, F., Li, H., Bohlmann, H., 2017. Smart parasitic nematodes use multifaceted strategies to parasitize plants. Frontiers in Plant Science8, 1699.

[10] Ali, M.A., Wieczorek, K., Kreil, D.P., Bohlmann, H., 2014. The beet cyst nematode Heterodera schachtii modulates the expression of WRKY transcription factors in syncytia to favour its development in Arabidopsis roots. PLoS One9, e102360.

[11] Bartel, D.P., 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell116, 281–297.

[12] Basyoni, M., Rizk, E., 2016. Nematodes ultrastructure: complex systems and processes. Journal of Parasitic Diseases : Official Organ of the Indian Society for Parasitology40, 1130–1140.

[13] Baujard, P., Martiny, B., 1994. Transport of nematodes by wind in the peanut cropping area of Senegal, West Africa. Fundamental and Applied Nematology17, 543–550.

[14] Bekal, S., Niblack, T.L., Lambert, K.N., 2003. A chorismate mutase from the soybean cyst nematode Heterodera glycine shows polymorphisms that correlate with virulence. Molecular Plant-Microbe Interactions16, 439–446.

[15] Bhatta, H., Goldys, E.M., Learmonth, R.P., 2006. Use of fluorescence spectroscopy to differentiate yeast and bacterial cells. Applied Microbiology and Biotechnology71, 121–126.

[16] Bhattarai, K.K., Xie, Q.G., Mantelin, S., Bishnoi, U., Girke, T., Navarre, D.A., Kaloshian, I., 2008. Tomato susceptibility to root-knot nematodes requires an intact jasmonic acid signaling pathway. Molecular Plant-Microbe Interactions21, 1205–1214.

[17] Bird, A.F., 1959. The attractiveness of roots to the plant parasitic nematodes Meloidogyne javanica and M. hapla. Nematologica4, 322–335.

[18] Bird, A.F., 1964. Serological studies on the plant parasitic nematode, Meloidogyne javanica. Experimental Parasitology15, 350–360.

[19] Bird, D.M., Kaloshian, I., 2003. Are roots special? Nematodes have their say. Physiological and Molecular Plant Pathology62, 115–123.

[20] Blaxter, M., Mann, J., Chapman, T., Thomas, F., Whitton, C., Floyd, R., Abebe, E., 2011. Defining operational taxonomic units using DNA barcode data. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences360, 1935–1943.

[21] Blaxter, M.L., De Ley, P., Garey, J.R., Liu, L.X., Scheldeman, P., Vierstraete, A., Vanfleteren, J.R., Mackey, L.Y., Dorris, M., Frisse, L.M., Vida, J.T., Thomas, W.K., 1998. A molecular evolutionary framework for the phylum Nematoda. Nature392, 71–75.

[22] Boerma, H.R., Hussey, R.S., 1992. Breeding plants for resistance to nematodes. Journal of Nematology24, 242.

[23] Borges, F., Martienssen, R.A., 2015. The expanding world of small RNAs in plants. Nature Reviews. Molecular Cell Biology16, 727–741.

[24] Branch, C., Hwang, C.F., Navarre, D.A., Williamson, V.M., 2004. Salicylic acid is part of the Mi-1-mediated defense response to root-knot nematode in tomato. Molecular Plant-Microbe Interactions17, 351–356.

[25] Brandt, J.P., Ringstad, N., 2015. Toll-like receptor signaling promotes development and function of sensory neurons required for a C. elegans pathogen-avoidance behavior. Current Biology25, 2228–2237.

[26] Bu, Y., Niu, H., Zhang, L., 2013. Phylogenetic analysis of the genus Cylicocyclus (Nematoda: Strongylidae) based on nuclear ribosomal sequence data. Acta Parasitologica58, 167–173.

[27] Cabrera, J., Barcala Rodríguez, M., García Ruiz, A., Río-Machín, A., Medina, C., Jaubert- Possamai, S., Favery, B., Maizel, A., Ruiz-Ferrer, V., Fenoll, C., Escobar, C., 2015. Differentially expressed small RNAs in Arabidopsis galls formed by Meloidogyne javanica: a functional role for miR390 and its TAS3-derived tasiRNAs. New Phytologist209, 1625–1640.

[28] Chitwood, B.G., 1949. ‘Root-knot nematodes’. Part 1. A revision of the genus Meloidogyne Goeldi, 1887. Proceedings of the Helminthological Society of Washington 16, 90–114

[29] 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 Biology22, 772–780.

[30] Choi, H.W., Klessig, D.F., 2016. DAMPs, MAMPs, and NAMPs in plant innate immunity. BMC Plant Biology16, 1–10.

[31] Cook, R., Noel, G.R., 2002. Cyst Nematodes: Globodera and Heterodera species. In: Starr, J.L., Cook, R., Bridge, J., eds. Plant Resistance to Parasitic Nematodes. CABI: Wallingford, CT, USA, 71–105, ISBN 9780851994666

[32] Correa, V.R., Dos Santos, M.F.A., Almeida, M.R.A., Peixoto, J.R., Castagnone-Sereno, P., Carneiro, R.M.D.G., 2013. Species-specific DNA markers for identification of two root-knot nematodes of coffee: Meloidogyne arabicida and M. izalcoensis. European Journal of Plant Pathology137, 305–313.

[33] Cui, H., Tsuda, K., Parker, J.E., 2015. Effector-triggered immunity: from pathogen perception to robust defense. Annual Review of Plant Biology66, 487–511.

[34] Da Cunha, T.G., Visôtto, L.E., Lopes, E.A., Oliveira, C.M.G., God, P.I.V.G., 2018. Diagnostic methods for identification of root-knot nematode species from Brazil. Ciência Rural,48, 1–11.

[35] Dautova, M., Rosso, M.N., Abad, P., Gommers, F., Bakker, J., Smant, G., 2001. Single pass cDNA sequencing-a powerful tool to analyse gene expression in preparasitic juveniles of the southern root-knot nematode Meloidogyne incognita. Nematology3, 129–139.

[36] Davies, K.G., Spiegel, Y., 2011. Biological control of plant-parasitic nematodes: towards understanding field variation through molecular mechanisms. In Genomics and molecular genetics of plant-nematode interactions. Springer, Dordrecht. pp. 493–516

[37] De-Oliveira, C., Monteiro, A.R., Blok, V.C., 2011. Morphological and molecular diagnostics for plant-parasitic nematodes: working together to get the identification done. Tropical Plant Pathology36, 65–73.

[38] Derycke, S., Vanaverbeke, J., Rigaux, A., Backeljau, T., Moens, T., 2010. Exploring the use of cytochrome oxidase c subunit 1 (COI) for DNA barcoding of free-living marine nematodes. PLoS One5, e13716.

[39] Dodds, P.N., Rathjen, J.P., 2010. Plant immunity: towards an integrated view of plant–pathogen interactions. Nature Reviews Genetics11, 539–548.

[40] Doyle, E.A., Lambert, K.N., 2002. Cloning and characterization of an esophageal-gland-specific pectate lyase from the root-knot nematode Meloidogyne javanica. Molecular Plant-Microbe Interactions15, 549–556.

[41] Eisenback, J.D., Hunt, D.J., 2009. General Morphology. In Perry, R.N., Moens, M., Starr, J.L., eds. Root Knot Nematodes. CABI: Wallingford, CT, USA, 18–54, ISBN 9781845934927

[42] Eisenback, J.D., Hirschmann, H., Triantaphyllou, A.C., 1980. Morphological comparison of Meloidogyne female head structures, perineal patterns, and stylets. Journal of Nematology12, 300.

[43] Elling, A., 2013. Major emerging problems with minor Meledogyne species. Phytopathology103, 1092–1102.

[44] El-Sagheer, A.M., 2019. Plant Responses to Phytonematodes Infestations. In: Ansari, R.A., Mahmood, I., eds. Plant Health Under Biotic Stress. Springer, Singapore. pp. 161–175

[45] Esbenshade, P.R., Triantaphyllou, A.C., 1990. Use of enzyme phenotypes for identification of Meloidogyne species. Journal of Nematology17, 6.

[46] Evans, A.A., Perry, R.N., 2009. Survival Mechanisms. CABI: Wallingford, CT, USA, 201–222

[47] Floyd, R., Abebe, E., Papert, A., Blaxter, M. 2002. Molecular barcodes for soil nematode identification. Molecular Ecology11, 839–850.

[48] François, C., Kebdani, N., Barker, I., Tomlinson, J., Boonham, N., Castagnone-Sereno, P., 2006. Towards specific diagnosis of plant-parasitic nematodes using DNA oligonucleotide microarray technology: a case study with the quarantine species Meloidogyne chitwoodi. Molecular and Cellular Probes20, 64–69.

[49] Fuller, V.L., Lilley, C.J., Urwin, P.E., 2008. Nematode resistance. New Phytologist180, 27–44.

[50] Gang, S.S., Hallem, E.A., 2016. Mechanisms of host seeking by parasitic nematodes. Molecular and Biochemical Parasitology208, 23–32.

[51] Gebremikael, M.T., Steel, H., Buchan, D., Bert, W., De Neve, S., 2016. Nematodes enhance plant growth and nutrient uptake under C and N-rich conditions. Scientific Reports6, 1–10.

[52] Ghareeb, R.Y., Hafez, E.E., Ibrahim, D.S., 2020. Current Management Strategies for Phytoparasitic Nematodes. In: Ansari, R.A., Rizvi, R., Mahmood, I., eds. Management of Phytonematodes: Recent Advances and Future Challenges. Springer, Singapore, pp. 339–352

[53] Gheysen, G., Mitchum, M.G., 2011. How nematodes manipulate plant development pathways for infection. Current Opinion in Plant Biology14, 415–421.

[54] Goellner, M., Smant, G., De Boer, J.M., Baum, T.J., Davis, E.L., 2000. Isolation of beta-1,4-endoglucanase genes from Globodera tabacum and their expression during parasitism. Journal of Nematology32, 154.

[55] Goggin, F.L., Williamson, V.M., Ullman, D.E., 2001. Variability in the response of Macrosiphum euphorbiae and Myzus persicae (Hemiptera: Aphididae) to the tomato resistance gene Mi. Environmental Entomology30, 101–106.

[56] Goverse, A., Overmars, H., Engelbertink, J., Schots, A., Bakker, J., Helder, J., 2000. Both induction and morphogenesis of cyst nematode feeding cells are mediated by auxin. Molecular Plant-Microbe Interactions13, 1121–1129.

[57] Green, C.D., 1975. The vulval cone and associated structures of some cyst nematodes (Genus Heterodera). Nematologica,21, 134–144.

[58] Guo, X., Wang, J., Gardner, M., Fukuda, H., Kondo, Y., Etchells, J.P., Wang, X., Mitchum, M.G., 2017. Identification of cyst nematode B-type CLE peptides and modulation of the vascular stem cell pathway for feeding cell formation. PLoS Pathogens13, e1006142.

[59] Guo, Y., Ni, J., Denver, R., Wang, X., Clark, S.E., 2011. Mechanisms of molecular mimicry of plant CLE peptide ligands by the parasitic nematode Globodera rostochiensis. Plant Physiology157, 476–484.

[60] Hadziavdic, K., Lekang, K., Lanzen, A., Jonassen, I., Thompson, E.M., Troedsson, C., 2014. Characterization of the 18S rRNA gene for designing universal eukaryote specific primers. PLoS One9, e87624.

[61] Hamamouch, N., Li, C., Seo, P.J., Park, C.M., Davis, E.L., 2011. Expression of Arabidopsis pathogenesis-related genes during nematode infection. Molecular Plant Pathology12, 355–364.

[62] Handoo, Z.A., Skantar, A.M., Hafez, S.L., Kantor, M.R., Hult, M.N., Rogers, S.A., 2020. Molecular and morphological characterization of the alfalfa cyst nematode, from Utah. Journal of Nematology 52, 1–4

[63] Hebert, P.D., Ratnasingham, S., De Waard, J.R., 2003. Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London. Series B, Biological Sciences270, S96–S99.

[64] Hewezi, T., 2015. Cellular signaling pathways and posttranslational modifications mediated by nematode effector proteins. Plant Physiology169, 1018–1026.

[65] Hewezi, T., Baum, T.J., 2015. Manipulation of plant cells by cyst and root-knot nematode effectors. Molecular Plant-Microbe Interactions26, 9–16.

[66] Hewezi, T., Howe, P., Maier, T.R., Baum, T.J., 2008. Arabidopsis small RNAs and their targets during cyst nematode parasitism. Molecular Plant-Microbe Interactions21, 1622–1634.

[67] Hewezi, T., Maier, T.R., Nettleton, D., Baum, T.J., 2012. The Arabidopsis microRNA396- GRF1/GRF3 regulatory module acts as a developmental regulator in the reprogramming of root cells during cyst nematode infection. Plant Physiology159, 321–335.

[68] Holbein, J., Grundler, F.M., Siddique, S., 2016. Plant basal resistance to nematodes: an update. Journal of Experimental Botany67, 2049–2061.

[69] Hugenholtz, P., Goebel, B.M., Pace, N.R., 1998. Impact of culture-independent studies on the emerging phylogenetic view of bacterial diversity. Journal of Bacteriology180, 4765–4774.

[70] Ivarson, K.C., Sowden, F.J., 1969. Free amino acid composition of the plant root environment under field conditions. Canadian Journal of Soil Science49, 121–127.

[71] Janeway, C.A. Jr, Medzhitov, R., 2002. Innate immune recognition. Annual Review of Immunology20, 197–216.

[72] Jones, J.T., Haegeman, A., Danchin, E.G., Gaur, H.S., Helder, J., Jones, M.G., Kikuchi, T., Manzanilla-López, R., Palomares-Rius, J.E., Wesemael, W.M.L., Perry, R.N., 2013. Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology14, 946–961.

[73] Kandoth, P.K., Ithal, N., Recknor, J., Maier, T., Nettleton, D., Baum, T.J., Mitchum, M.G., 2018. The soybean Rhg1 locus for resistance to the soybean cyst nematode Heterodera glycines regulates the expression of a large number of stress-and defense-related genes in degenerating feeding cells. Plant Physiology155, 1960–1975.

[74] Kaplan, F., Srinivasan, J., Mahanti, P., Ajredini, R., Durak, O., Nimalendran, R., Sternberg, P.W., Teal, P.E.A., Schroeder, F.C., Edison, A.S., Alborn, H.T., 2011. Ascaroside expression in Caenorhabditis elegans is strongly dependent on diet and developmental stage. PLoS One6, e17804.

[75] Karssen, G., Van Aelst, A., 2001. Root-knot nematode perineal pattern development: a reconsideration. Nematology3, 95–111.

[76] Klingler, J., 1965. On the orientation of plant nematodes and of some other soil animals. Nematologica11, 4–18.

[77] Krishna, P.B., Eapen, S.J., 2019. Development of a real-time PCR based protocol for quantifying Radopholus similis in field samples. Journal of Spices and Aromatic Crops28, 52–60.

[78] Lambert, K., Bekal, S., 2002. Introduction to plant-parasitic nematodes. The Plant Health Instructor10, 1094–1218.

[79] Lee, D.L., ed., 2002. The Biology of Nematodes. CRC Press

[80] Lee, Y., Kim, M., Han, J., Yeom, K.H., Lee, S., Baek, S.H., Kim, V.N., 2004. MicroRNA genes are transcribed by RNA polymerase II. EMBO Journal23, 4051–4060.

[81] Lehman, P.S., 1994. Dissemination of phytoparasitic nematodes. Nematology Circular, No. 208. Gainesville, Florida, USA

[82] Long, E.O., Dawid, I.B., 1980. Repeated genes in eukaryotes. Annual Review of Biochemistry49, 727–764.

[83] Macho, A.P., Zipfel, C., 2014. Plant PRRs and the activation of innate immune signaling. Molecular Cell54, 263–272.

[84] Mathews, H.J.P., 1970. Morphology of the nettle cyst nematode Heterodera urticae Cooper, 1955. Nematologica,16, 503–510.

[85] Maggenti, A. 1981.General Nematology. Springer-Verlag, New York, NY

[86] Manosalva, P., Manohar, M., Von Reuss, S.H., Chen, S., Koch, A., Kaplan, F., Choe, A., Micikas, R.J., Wang, X., Kogel, K.H., Sternberg, P.W., Williamson, V.M., Schroeder, F.C., Klessig, D.F., 2015. Conserved nematode signalling molecules elicit plant defenses and pathogen resistance. Nature Communications6, 1–8.

[87] Mao, G., Meng, X., Liu, Y., Zheng, Z., Chen, Z., Zhang, S., 2011. Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell23, 1639–1653.

[88] Marek, M., Zouhar, M., Rysanek, P., Havranek, P., 2005. Analysis of ITS sequences of nuclear rDNA and development of a PCR-based assay for the rapid identification of the stem nematode Ditylenchus dipsaci (Nematoda: Anguinidae) in plant tissues. Helminthologia42, 49.

[89] Mburu, H., Cortada, L., Haukeland, S., Ronno, W., Nyongesa, M., Kinyua, Z., Bargul, J.L., Coyne, D., 2020. Potato cyst nematodes: a new threat to potato production in East Africa. Frontiers in Plant Science11, 670.

[90] McCarter, J.P., Clifton, S.W., Bird, D.M., Waterson, R.H., 2002. Nematode gene sequences, update for June 2002. Journal of nematology,34( 2), 71.

[91] McCuiston, J.L., Hudson, L.C., Subbotin, S.A., Davis, E.L., Warfield, C.Y., 2007. Conventional and PCR detection of Aphelenchoides fragariae in diverse ornamental host plant species. Journal of Nematology39, 343.

[92] Medina, C., Da Rocha, M., Magliano, M., Ratpopoulo, A., Revel, B., Marteu, N., et al, . 2017. Characterization of microRNAs from Arabidopsis galls highlights a role for miR159 in the plant response to the root-knot nematode Meloidogyne incognita. New Phytologist216, 882–896.

[93] Mesa-Valle, C.M., Garrido-Cardenas, J.A., Cebrian-Carmona, J., Talavera, M., Manzano-Agugliaro, F., 2020. Global research on plant nematodes. Agronomy (Basel)10, 1148.

[94] Misaghi, I., McClure, M.A., 1974. Antigenic Relationship of Meloidogyne incognita, M. javanica, and M. arenaria. Phytopathology64, 698–701.

[95] Montarry, J., Mimee, B., Danchin, E.G., Koutsovoulos, G.D., Ste-Croix, D.T., Grenier, E., 2021. Recent advances in population genomics of plant-parasitic nematodes. Phytopathology111, 40–48.

[96] Mulvey, R.H., 1972. Identification of Heterodera cysts by terminal and cone top structures. Canadian Journal of Zoology50, 1277–1292.

[97] Murfin, K.E., Dillman, A.R., Foster, J.M., Bulgheresi, S., Slatko, B.E., Sternberg, P.W., Goodrich-Blair, H., 2012. Nematode-bacterium symbioses—cooperation and conflict revealed in the “Omics” age. Biological Bulletin223, 85–102.

[98] Navas, A., López, J.A., Espárrago, G., Camafeita, E., Albar, J.P., 2002. Protein variability in Meloidogyne spp. (Nematoda: Meloidogynidae) revealed by two-dimensional gel electrophoresis and mass spectrometry. Journal of Proteome Research1, 421–427.

[99] Naz, I., Rius, J.E.P., Blok, V., 2013. Species Identification of Root Knot Nematodes in Pakistan By Random Amplified Polymorphic DNA (RAPD-PCR). Sarhad Journal of Agriculture29, 71–78.

[100] Naz, I., Palomares-Rius, J.E., Blok, V., Ahmad, M., Ali, S., Nombela, G., Williamson, V.M., Muñiz, M., 2003. The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Molecular Plant-Microbe Interactions 16, 645–649

[101] Nzogela, Y.B., 2020. Characterization of Plant-Parasitic Nematodes and Host Resistance in Rice Production in Tanzania. Doctoral dissertation. Ghent University

[102] Olsen, A.N., Skriver, K., 2003. Ligand mimicry? Plant-parasitic nematode polypeptide with similarity to CLAVATA3.. Trends in Plant Science8, 55–57.

[103] Panda, O., Akagi, A.E., Artyukhin, A.B., Judkins, J.C., Le, H.H., Mahanti, P., Cohen, S.M., Sternberg, P.W., Schroeder, F.C., 2017. Biosynthesis of Modular Ascarosides in C. elegans. Angewandte Chemie129, 4807–4811.

[104] Perry, R.N., 1996. Chemoreception in plant parasitic nematodes. Annual Review of Phytopathology34, 181–199.

[105] Piya, S., Kihm, C., Rice, J.H., Baum, T.J., Hewezi, T., 2017. Cooperative regulatory functions of miR858 and MYB83 during cyst nematode parasitism. Plant Physiology174, 1897–1912.

[106] Pline, M., Dusenbery, D.B., 1987. Responses of plant-parasitic nematode Meloidogyne incognita to carbon dioxide determined by video camera-computer tracking. Journal of Chemical Ecology13, 873–888.

[107] Popeijus, H., Blok, V., Cardle, L., Bakker, E., Phillips, M., Helder, J., Smant, G., Jones, J., 2000. Analysis of genes expressed in second stage juveniles of the potato cyst nematodes Globodera rostochiensis and G. pallida using the expressed sequence tag approach. Nematology2, 567–574.

[108] Poveda, J., Abril-Urias, P., Escobar, C., 2020. Biological control of plant-parasitic nematodes by filamentous fungi inducers of resistance: Trichoderma, mycorrhizal and endophytic fungi. Frontiers in Microbiology11, 992.

[109] Powers, T.O., Todd, T.C., Burnell, A.M., Murray, P.C.B., Fleming, C.C., Szalanski, A.L., Adams, B.A., Harris, T.S., 1997. The rDNA internal transcribed spacer region as a taxonomic marker for nematodes. Journal of Nematology29, 441–450.

[110] Pujol, N., Link, E.M., Liu, L.X., Kurz, C.L., Alloing, G., Tan, M.W., Ray, K.P., Solari, R., Johnson, C.D., Ewbank, J.J., 2001. A reverse genetic analysis of components of the Toll signaling pathway in Caenorhabditis elegans. Current Biology11, 809–821.

[111] Pulavarty, A., Egan, A., Karpinska, A., Horgan, K., Kakouli-Duarte, T., 2021. Plant Parasitic Nematodes: A review on their behaviour, host interaction, management approaches and their occurrence in two sites in the Republic of Ireland. Plants10, 2352.

[112] Qazi, F., Khalid, A., Poddar, A., Tetienne, J.P., Nadarajah, A., Aburto-Medina, A., Tomljenovic-Hanic, S., 2020. Real-time detection and identification of nematode eggs genus and species through optical imaging. Scientific Reports10, 1–12.

[113] Randig, O., Leroy, F., Castagnone-Sereno, P., 2001. RAPD characterization of single females of the root-knot nematodes, Meloidogyne spp. European Journal of Plant Pathology107, 639–643.

[114] Rasmann, S., Ali, J.G., Helder, J., Van der Putten, W.H., 2012. Ecology and evolution of soil nematode chemotaxis. Journal of Chemical Ecology38, 615–628.

[115] Reinhart, B.J., Weinstein, E.G., Rhoades, M.W., Bartel, B., Bartel, D.P., 2002. MicroRNAs in plants. Genes & Development16, 1616–1626.

[116] Rengarajan, S., Hallem, E.A., 2016. Olfactory circuits and behaviors of nematodes. Current Opinion in Neurobiology41, 136–148.

[117] Replogle, A., Wang, J., Paolillo, V., Smeda, J., Kinoshita, A., Durbak, A., Tax, F.E., Wang, X., Sawa, S., Mitchum, M.G., 2013. Synergistic interaction of CLAVATA1, CLAVATA2, and RECEPTOR- LIKE PROTEIN KINASE 2 in cyst nematode parasitism of Arabidopsis. Molecular Plant-Microbe Interactions26, 87–96.

[118] Ricci-Azevedo, R., Roque-Barreira, M.C., Gay, N.J., 2017. Targeting and recognition of toll-like receptors by plant and pathogen lectins. Frontiers in Immunology8, 1820.

[119] Robert-Seilaniantz, A., Grant, M., Jones, J.D., 2011. Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annual Review of Phytopathology49, 317–343.

[120] Rushton, P.J., Somssich, I.E., Ringler, P., Shen, Q.J., 2010. WRKY transcription factors. Trends in Plant Science15, 247–258.

[121] Sani, Z.R., Haruna, A., 2020. Assessment of soil root-knot nematodes in some selected plant cultivated at nagwamatse farm, Gusau, Zamfara State Nigeria. International Journal for Science for Global Sustainability 6

[122] Sasser, J.N., Freckman, A.J. 1987. A world perspective on nematology: the role of the society. Vistas on Nematology., 7–14

[123] Schoch, C.L., Seifert, K.A., Huhndorf, S., Robert, V., White, M.M., 2012. Nuclear ribosomal internal transcribed spacer (ITS) region as a universal DNA barcode marker for Fungi. Proceedings of the National Academy of Sciences,109, 6241–6246.

[124] Schots, A., Hermsen, T., Schouten, S., Gommers, F.J., Egberts, E., 1989. Serological differentiation of the potato-cyst nematodes Globodera pallida and G. rostochiensis: II. reparation and characterization of species specific monoclonal antibodies. Hybridoma8, 401–413.

[125] Semblat, J.P., Wajnberg, E., Dalmasso, A., Abad, P., Castagnone-Sereno, P., 1998. High-resolution DNA fingerprinting of parthenogenetic root-knot nematodes using AFLP analysis. Molecular Ecology7, 119–125.

[126] Siddique, S., Grundler, F.M., 2018. Parasitic nematodes manipulate plant development to establish feeding sites. Current Opinion in Microbiology46, 102–108.

[127] Sidonskaya, E., Schweighofer, A., Shubchynskyy, V., Kammerhofer, N., Hofmann, J., Wieczorek, K., Meskiene, I., 2016. Plant resistance against the parasitic nematode Heterodera schachtii is mediated by MPK3 and MPK6 kinases, which are controlled by the MAPK phosphatase AP2C1 in Arabidopsis. Journal of Experimental Botany67, 107–118.

[128] Singh, V., Aballay, A., 2006. Heat shock and genetic activation of HSF-1 enhance immunity to bacteria. Cell Cycle (Georgetown, Tex.)5, 2443–2446.

[129] Smant, G., Stokkermans, J. P., Yan, Y., De Boer, J. M., Baum, T. J., Wang, X., Hussey, R.S., Gommers, F.J., Henrissat, B., Davis, E.L., Schota, A., Bakker, J. 1998. Endogenous cellulases in animals: isolation of β-1, 4-endoglucanase genes from two species. National Academy of Science, U.S.A.95, 4906–4911.

[130] Smith, T., Brito, J.A., Han, H., Kaur, R., Cetintas, R., Dickson, D.W., 2015. Identification of the peach root-knot nematode, Meloidogyne floridensis, using mtDNA PCR- RFLP. Nematropica45, 138–143.

[131] Sommerville, R.I., Davey, K.G., 2002. Diapause in parasitic nematodes. Canadian Journal of Zoology 80, 1817–1840 (review) doi:10.1139/z1817–1840

[132] Stael, S., Kmiecik, P., Willems, P., Van Der Kelen, K., Coll, N.S., Teige, M., Van Breusegem, N., 2015. Plant innate immunity–sunny side up?. Trends in Plant Science20, 3–11.

[133] Steiner, G., 1925. The Problem of Host Selection and Host Specialization of Certain Plant-Infesting Nemas and Its Application in the Study of Nemic Pests. Phytopathology,15, 499–534.

[134] Stirling, G.R., Pattison, A.B., 2008. Beyond chemical dependency for managing plant-parasitic nematodes: examples from the banana, pineapple and vegetable industries of tropical and subtropical Australia. Australasian Plant Pathology37, 254–267.

[135] Stone, A.R., 1977. Recent developments and some problems in the taxonomy of cyst nematodes, with a classification of the Heteroderoidea. Nematologica,23, 273–288.

[136] Stone, A.R., 1983. Three Approaches to the Status of a Species Complex, with A Revision of Some Species of Globodera (Nematoda: Heteroderidae). In: Stone, A.R., Platt, H.M., Khalil, L.F., Eds. Concepts in Nematode Systematics, Systematics Association Special Volume. Academic Press: London, UK, 221–223

[137] Tsuda, K., Katagiri, F., 2012. Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Current Opinion in Plant Biology13, 459–465.

[138] Turner, S.J., Subbotin, S.A., 2006. Cyst Nematodes. In: Perry, R.N., Moens, M., Eds. Plant Nematology. CABI: Wallingford, CT, USA, 109–143, ISBN 9781845930561

[139] Tytgat, T., De Meutter, J., Gheysen, G., Coomans, A., 2000. Sedentary endoparasitic nematodes as a model for other plant parasitic nematodes. Nematology2, 113–121.

[140] Urwin, P.E., Lilley, C.J., Atkinson, H.J., 2002. Ingestion of double-stranded RNA by preparasitic juvenile cyst nematodes leads to RNA interference. Molecular Plant-Microbe Interactions15, 747–752.

[141] van Megen, H., van den Elsen, S., Holterman, M., Karssen, G., Mooyman, P., Bongers, T., Holovachov, O., Bakker, J., Helder, J., 2009. A phylogenetic tree of nematodes based on about 1200 full- length small subunit ribosomal DNA sequences. Nematology11, 927–950.

[142] Vanholme, B., De Meutter, J., Tytgat, T., Gheysen, G.D., Vanhoutte, I., Gheysen, G.D., 2002. An improved method for whole-mount in situ hybridization of Heterodera schachtii juveniles. Parasitology Research88, 731–733.

[143] Viglierchio, D.R., 1961. Attraction of parasitic nematodes by plant root emanations. Phytopathology5, 136–142.

[144] Villar-Luna, E., Goméz-Rodriguez, O., Rojas-Martínez, R.I., Zavaleta-Mejía, E., 2016. Presence of Meloidogyne enterolobii on jalapeño pepper (Capsicum annuum L. ) in Sinaloa, Mexico. Helminthologia53, 155–160.

[145] Wang, G., Fiers, M., 2010. CLE peptide signaling during plant development. Protoplasma240, 33–43.

[146] Weiberg, A., Jin, H., 2015. Small RNAs—the secret agents in the plant pathogen interactions. Current Opinion in Plant Biology26, 87–94.

[147] Williamson, V.M., 1999. Plant nematode resistance genes. Current Opinion in Plant Biology2, 327–331.

[148] Williamson, V.M., Hussey, R.S., 1996. Nematode pathogenesis and resistance in plants. Plant Cell8, 1735.

[149] Williamson, V.M., Kumar, A., 2006. Nematode resistance in plants: the battle underground. Trends in Genetics22, 396–403.

[150] Wubben, M.J. II, Su, H., Rodermel, S.R., Baum, T.J., 2001. Susceptibility to the sugar beet cyst nematode is modulated by ethylene signal transduction in Arabidopsis thaliana. Molecular Plant-Microbe Interactions14, 1206–1212.

[151] Wyss, U., Grundler, F.M.W., 1992. Feeding behavior of sedentary plant parasitic nematodes. Netherlands Journal of Plant Pathology98, 165–173.

[152] Yeates, M.G., 1993. Plant nematodes: methodology, morphology, systematics, biology and ecology. Nematology,11, 319–320.

[153] Zeppilli, D., Leduc, D., Fontanier, C., Fontaneto, D., Fuchs, S., Gooday, A.J., Goineau, A., Ingels, J., Ivanenko, V.N., Kristensen, R.M., Neves, R.C., Sanchez, N., Sandulli, R., Sarrazin, J., Sørensen, M.V., Tasiemski, A., Vanreusel, A., Autret, M., Bourdonnay, L., Claireaux, M., Coquillé, V., De Wever, L., Rachel, D., Marchant, J., Toomey, L., Fernandes, D., 2018. Characteristics of meiofauna in extreme marine ecosystems: a review. Marine Biodiversity48, 35–71.

[154] Zhao, L., Zhang, X., Wei, Y., Zhou, J., Zhang, W., Qin, P., Chinta, S., Kong, X., Liu, Y., Yu, H., Hu, S., Zou, Z., Butcher, R.A., Sun, J., 2016. Ascarosides coordinate the dispersal of a plant-parasitic nematode with the metamorphosis of its vector beetle. Nature Communications7, 1–8.

[155] Zhao, W., Li, Z., Fan, J., Hu, C., Yang, R., Qi, X., Chen, H., Zhao, F., Wang, S., 2015. Identification of jasmonic acid-associated microRNAs and characterization of the regulatory roles of the miR319/TCP4 module under root-knot nematode stress in tomato. Journal of Experimental Botany66, 4653–4667.

[156] Zipfel, C., 2014. Plant pattern-recognition receptors. Trends in Immunology35, 345–351.

[157] Zunnke, U., 1991. Observations on the invasion and endoparasitic behavior of the root lesion nematode Pratylenchus penetrans. Journal of Nematology22, 309.

Author contributions

All the authors have contributed equally in drafting the different sections of the manuscript.

Acknowledgements

Authors are highly thankful to Heads, Dept of Botany and Zoology, Baba Ghulam Shah Badshah University, Rajouri, for providing necessary facilities to compile this article. Authors thank Shafkat Wani for his help during the compilation of the manuscript.

RIGHTS & PERMISSIONS

2023 Higher Education Press