Abstract
Plant-parasitic nematodes from the genera Globodera, Heterodera (cyst-forming nematodes), and Meloidogyne (root-knot nematodes) are notorious and serious pests of crops. They cause tremendous economic losses between US $80 and 358 billion a year. Nematodes infect the roots of plants and induce the formation of specialised feeding structures (syncytium and giant cells, respectively) that nourish juveniles and adults of the nematodes. The specialised secretory glands enable nematodes to synthesise and secrete effectors that facilitate migration through root tissues and alter the morphogenetic programme of host cells. The formation of feeding sites is associated with the suppression of plant defence responses and deep reprogramming of the development and metabolism of plant cells.
In this chapter, we focus on syncytia induced by the sedentary cyst-forming nematodes and provide an overview of ultrastructural changes that occur in the host roots during syncytium formation in conjunction with the most important molecular changes during compatible and incompatible plant responses to infection with nematodes.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abd-Elgawad MMM, Askary TH (2015) Impact of phytonematodes on agriculture economy. In: Askary TH, Martinelli PRP (eds) Biocontrol agents of phytonematodes. CAB, Wallingford, pp 3–49
Ali S, Magne M, Chen S, Obradovic N, Jamshaid L, Wang X, Bélair G, Moffett P (2015) Analysis of Globodera rostochiensis effectors reveals conserved functions of SPRYSEC proteins in suppressing and eliciting plant immune responses. Front Plant Sci 6:623. https://doi.org/10.3389/fpls.2015.00623
Anjam MS, Shah SJ, Matera C, Różańska E, Sobczak M, Siddique S, Grundler FMW (2020) Host factors influence the sex of nematodes parasitizing roots of Arabidopsis thaliana. Plant Cell Environ 43:1160–1174. https://doi.org/10.1111/pce.13728
Assefa AD, Kim SH, Mani V, Ko HR, Hahn BS (2021) Metabolic analysis of the development of the plant-parasitic cyst nematodes Heterodera schachtii and Heterodera trifolii by capillary electrophoresis time-of-flight mass spectrometry. Int J Mol Sci 22:10488. https://doi.org/10.3390/ijms221910488
Baggs E, Dagdas G, Krasileva K (2017) NLR diversity, helpers and integrated domains: making sense of the NLR IDentity. Curr Opin Plant Biol 38:59–67. https://doi.org/10.1016/j.pbi.2017.04.012
Bakker E, Achenbach U, Bakker J, van Vliet J, Peleman J, Segers B, van der Heijden S, van der Linde P, Graveland R, Hutten R, van Eck H, Coppoolse E, van der Vossen E, Bakker J, Goverse A (2004) A high-resolution map of the H1 locus harbouring resistance to the potato cyst nematode Globodera rostochiensis. Theor Appl Genet 109:146–152. https://doi.org/10.1007/s00122-004-1606-z
Balint-Kurti P (2019) The plant hypersensitive response: concepts, control and consequences. Mol Plant Pathol 20:1163–1178. https://doi.org/10.1111/mpp.12821
Baranowski Ł, Różańska E, Sańko-Sawczenko I, Matuszkiewicz M, Znojek E, Filipecki M, Grundler FMW, Sobczak M (2019) Arabidopsis tonoplast intrinsic protein and vacuolar H+-adenosinetriphosphatase reflect vacuole dynamics during development of syncytia induced by the beet cyst nematode Heterodera schachtii. Protoplasma 256:419–429. https://doi.org/10.1007/s00709-018-1303-4
Benedetti M, Pontiggia D, Raggi S, Cheng Z, Scaloni F, Ferrari S, Ausubel FM, Cervone F, Lorenzo GD (2015) Plant immunity triggered by engineered in vivo release of oligogalacturonides, damage-associated molecular patterns. Proc Natl Acad Sci USA 112:5533–5538. https://doi.org/10.1073/pnas.1504154112
Bhattarai KK, Li Q, Liu Y, Dinesh-Kumar SP, Kaloshian I (2007) The Mi-1-mediated pest resistance requires Hsp90 and Sgt1. Plant Physiol 144:312–323. https://doi.org/10.1104/pp.107.097246
Blaxter ML, De Ley P, Garey JR, Liu LX, Scheldeman P, Vierstraete A, Vanfleteren JR, Mackey LY, Dorris M, Frisse LM, Vida JT, Thomas WK (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392:71–75. https://doi.org/10.1038/32160
Böckenhoff A, Grundler FMW (1994) Studies on the nutrient uptake by the beet cyst nematode Heterodera schachtii by in situ microinjection of fluorescent probes into the feeding structures in Arabidopsis thaliana. Parasitology 109:249–255. https://doi.org/10.1017/S003118200007637X
Cai D, Kleine M, Kifle S, Harloff J, Sandal N, Marcker A, Klein-Lankhorst M, Salentijn M, Lange W, Stiekema J, Wyss U, Grundler FM, Jung C (1997) Positional cloning of a gene for nematode resistance in sugar beet. Science 275:832–834. https://doi.org/10.1126/science.275.5301.832
Chen R, Li H, Zhang L, Zhang J, Xiao J, Ye Z (2007) CaMi, a root-knot nematode resistance gene from hot pepper (Capsicum annuum L.) confers nematode resistance in tomato. Plant Cell Rep 26:895–905. https://doi.org/10.1007/s00299-007-0304-0
Chopra D, Hasan MS, Matera C, Chitambo O, Mendy B, Mahlitz SV, Naz AA, Szumski S, Janakowski S, Sobczak M, Mithöfer A, Kyndt T, Grundler FMW, Siddique S (2021) Plant parasitic cyst nematodes redirect host indole metabolism via NADPH oxidase-mediated ROS to promote infection. New Phytol 232:318–331. https://doi.org/10.1111/nph.17559
Cohn E, Spiegel Y (1991) Root-nematode interactions. In: Weisel Y, Eshel A, Kafkafi U (eds) Plant roots; The hidden part. Marcel Dekker, New York, pp 789–805
Coll NS, Epple P, Dangl JL (2011) Programmed cell death in the plant immune system. Cell Death Differ 18:1247–1256. https://doi.org/10.1038/cdd.2011.37
Cotton JA, Lilley CJ, Jines LM, Kikuchi T, Reid AJ, Thorpe P, Tsai IJ, Beasley H, Blok V, Cock PJA, Eves-van den Akker S, Holroyd N, Hunt M, Mantelin S, Naghra H, Pain A, Palomares-Rius JE, Zarowiecki M, Berriman M, Jones JT, Urwin PE (2014) The genome and life-stage specific transcriptomes of Globodera pallida elucidate key aspects of plant parasitism by a cyst nematode. Genome Biol 15:R43. https://doi.org/10.1186/gb-2014-15-3-r43
Dangl JL, Jones JDG (2019) A pentangular plant inflammasome. Science 364:31–32. https://doi.org/10.1126/science.aax0174
Davies LJ, Lilley CJ, Knox JP, Urwin PE (2012) Syncytia formed by adult female Heterodera schachtii in Arabidopsis thaliana roots have a distinct cell wall molecular architecture. New Phytol 196:238–246. https://doi.org/10.1111/j.1469-8137.2012.04238.x
de Almeida Engler J, Van Poucke K, Karimi M, De Groodt R, Gheysen G, Engler G, Gheysen G (2004) Dynamic cytoskeleton rearrangements in giant cells and syncytia of nematode-infected roots. Plant J 38:12–26. https://doi.org/10.1111/j.1365-313X.2004.02019.x
de Almeida Engler J, Kyndt T, Vieira P, Van Cappelle E, Boudolf V, Sanchez V, Escobar C, De Veylder L, Engler G, Abad P, Gheysen G (2012) CCS52 and DEL1 genes are key components of the endocycle in nematode-induced feeding sites. Plant J 72:185–198. https://doi.org/10.1111/j.1365-313X.2012.05054.x
de Majnik J, Ogbonnaya FC, Moullet O, Lagudah ES (2003) The Cre1 and Cre3 nematode resistance genes are located at homeologous loci in the wheat genome. Mol Plant Microbe Interact 16:1129–1134. https://doi.org/10.1094/mpmi.2003.16.12.1129
De Meutter J, Tytgat T, Witters E, Gheysen G, Onckelen V, Gheysen G (2003) Identification of cytokinins produced by the plant parasitic nematodes Heterodera schachtii and Meloidogyne incognita. Mol Plant Pathol 4:271–277. https://doi.org/10.1046/j.1364-3703.2003.00176.x
Derevnina L, Contreras MP, Adachi H, Upson J, Vergara Cruces A, Xie R, Sklenar J, Menke FLH, Mugford ST, MacLean D, Ma W, Hogenhout SA, Goverse A, Maqbool A, Wu CH, Kamoun S (2021) Plant pathogens convergently evolved to counteract redundant nodes of an NLR immune receptor network. PLoS Biol 19:e3001136. https://doi.org/10.1371/journal.pbio.3001136
Diaz-Granados A, Petrescu AJ, Goverse A, Smant G (2016) SPRYSEC effectors: A versatile protein-binding platform to disrupt plant innate immunity. Front Plant Sci 7:1575. https://doi.org/10.3389/fpls.2016.01575
Dowd CD, Chronis D, Radakovic ZS, Siddique S, Schmülling T, Werner T, Kakimoto T, Grundler FMW, Mitchum MG (2017) Divergent expression of cytokinin biosynthesis, signaling and catabolism genes underlying differences in feeding sites induced by cyst and root-knot nematodes. Plant J 92:211–228. https://doi.org/10.1111/tpj.13647
Elashry AM, Habash SS, Vijayapalani P, Brocke-Ahmadinejad N, Blümel R, Seetharam A, Schoof H, Grundler FMW (2020) Transcriptome and parasitome analysis of beet cyst nematode Heterodera schachtii. Sci Rep 10:3315. https://doi.org/10.1038/s41598-020-60186-0
Endo BY (1978) Feeding plug formation in soybean roots infected with the soybean cyst nematode. Phytopathology 68:1022–1031
Endo BY (1991) Ultrastructure of initial responses of susceptible and resistant soybean roots to infection by Heterodera glycines. Rev Nématol 14:73–94
Ernst K, Kumar A, Kriseleit D, Dorothee-U K, Phillips MS, Ganal MW (2002) The broad-spectrum potato cyst nematode resistance gene (Hero) from tomato is the only member of a large gene family of NBS-LRR genes with an unusual amino acid repeat in the LRR region. Plant J 31:127–136. https://doi.org/10.1046/j.1365-313x.2002.01341.x
Eves-van den Akker S, Lilley CJ, Jones JT, Urwin PE (2015) Plant-parasitic nematode feeding tubes and plugs: new perspectives on function. Nematology 17:1–9. https://doi.org/10.1163/15685411-00002832
Eves-van den Akker S, Laetsch DR, Thorpe P, Lilley CJ, Danchin EG, Da Rocha M, Rancurel C, Holroyd NE, Cotton JA, Szitenberg A, Grenier E, Montarry J, Mimee B, Duceppe M-O, Boyes I, Marvin JMC, Jones LM, Yusup HB, Lafond-Napalme J, Esquibet M, Sabeh M, Rott M, Overmars H, Finkers-Tomczak A, Smant G, Koutsovoulos G, Blok V, Mantelin S, Cock PJA, Phillips W, Henrissat B, Urwin PE, Blaxter M, Jones JT (2016) The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence. Genome Biol 17:124. https://doi.org/10.1186/s13059-016-0985-1
Fattah F, Webster JM (1984) Fine structure of the giant cells induced by Meloidogyne javanica in lima bean. Can J Bot 62:429–436
Filipecki M, Żurczak M, Matuszkiewicz M, Święcicka M, Kurek W, Olszewski J, Koter MD, Lamont D, Sobczak M (2021) Profiling the proteome of cyst nematode-induced syncytia on tomato roots. Int J Mol Sci 22:12147. https://doi.org/10.3390/ijms222212147
Flor HH (1942) Inheritance of pathogenicity in Melampsora lini. Phytopathology 32:653–669
Gao B, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS (2003) The parasitome of the phytonematode Heterodera glycines. Mol Plant-Microbe Interact 16:720–726. https://doi.org/10.1094/mpmi.2003.16.8.720
Gheysen G, Mitchum MG (2011) How nematodes manipulate plant development pathways for infection. Curr Opin Plant Biol 14:415–421. https://doi.org/10.1016/j.pbi.2011.03.012
Gheysen G, Mitchum MG (2019) Phytoparasitic nematode control of plant hormone pathways. Plant Physiol 179:1212–1226. https://doi.org/10.1104/pp.18.01067
Golinowski W, Grundler FMW, Sobczak M (1996) Changes in the structure of Arabidopsis thaliana during female development of the plant-parasitic nematode Heterodera schachtii. Protoplasma 194:103–116. https://doi.org/10.1007/BF01273172
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. Mol Plant Microbe Interact 13:1121–1129. https://doi.org/10.1094/MPMI.2000.13.10.1121
Grundler FMW, Sobczak M, Golinowski W (1998) Formation of wall openings in root cells of Arabidopsis thaliana following infection by the plant-parasitic nematode Heterodera schachtii. Eur J Plant Pathol 104:545–551
Grunewald W, Cannoot B, Friml J, Gheysen G (2009) Parasitic nematodes modulate PIN-mediated auxin transport to facilitate infection. PLoS Pathog 5:e1000266. https://doi.org/10.1371/journal.ppat.1000266
Habash SS, Sobczak M, Siddique S, Voigt B, Elashry A, Grundler FMW (2017) Identification and characterization of a putative protein disulfide isomerase (HsPDI) as an alleged effector of Heterodera schachtii. Sci Rep 7:13536. https://doi.org/10.1038/s41598-017-13418-9
Hamamouch N, Li C, Hewezi T, Baum TJ, Mitchum MG, Hussey RS, Vodkin LO, Davis EL (2012) The interaction of the novel 30C02 cyst nematode effector protein with a plant β-1,3-endoglucanase may suppress host defence to promote parasitism. J Exp Bot 63:3683–3695. https://doi.org/10.1093/jxb/ers058
Hewezi T, Howe P, Maier TR, Baum TJ (2008) Arabidopsis small RNAs and their targets during cyst nematode parasitism. Mol Plant Microbe Interact 21:1622–1634. https://doi.org/10.1094/mpmi-21-12-1622
Hewezi T, Juvale PS, Piya S, Maier TR, Rambani A, Rice JH, Mitchum MG, Davis EL, Hussey RS, Baum TJ (2015) The cyst nematode effector protein 10A07 targets and recruits host posttranslational machinery to mediate its nuclear trafficking and to promote parasitism in Arabidopsis. Plant Cell 27:891–907. https://doi.org/10.1105/tpc.114.135327
Hofmann J, El Ashry AN, Anwar S, Erban A, Kopka J, Grundler F (2010) Metabolic profiling reveals local and systemic responses of host plants to nematode parasitism. Plant J 62:1058–1071. https://doi.org/10.1111/j.1365-313X.2010.04217.x
Hu Y, You J, Li C, Williamson VM, Wang C (2017) Ethylene response pathway modulates attractiveness of plant roots to soybean cyst nematode Heterodera glycines. Sci Rep 7:41282. https://doi.org/10.1038/srep41282
Huang CS, Maggenti AR (1969) Mitotic aberrations and nuclear changes of developing giant cells in Vicia faba caused by root knot nematode, Meloidogyne javanica. Phytopathology 59:447–455
Hussey RS, Mims CW (1991) Ultrastructure of feeding tubes formed in giant-cells induced in plants by the root-knot nematode Meloidogyne incognita. Protoplasma 162:99–107
Hussey RS, Mims CW, Westcott SW III (1992) Ultrastructure of root cortical cells parasitized by the ring nematode Criconemella xenoplax. Protoplasma 167:55–65
Hütten M, Geukes M, Misas-Villamil JC, van der Hoorn RAL, Grundler FMW, Siddique S (2015) Activity profiling reveals changes in the diversity and activity of proteins in Arabidopsis roots in response to nematode infection. Plant Physiol Biochem 97:36–43. https://doi.org/10.1016/j.plaphy.2015.09.008
Ilyas M, Hörger AC, Bozkurt TO, van den Burg HA, Kaschani F, Kaiser M, Belhaj K, Smoker M, Joosten MHAJ, Kamoun S, van der Hoorn RAL (2015) Functional divergence of two secreted immune proteases of tomato. Curr Biol 25:2300–2306. https://doi.org/10.1016/j.cub.2015.07.030
Ithal N, Recknor J, Nettleton D, Maier T, Baum TJ, Mitchum MG (2007) Developmental transcript profiling of cyst nematode feeding cells in soybean roots. Mol Plant Microbe Interact 20:510–525. https://doi.org/10.1094/mpmi-20-5-0510
Jablonska B, Ammiraju JSS, Bhattarai KK, Mantelin S, Martinez de Ilarduya O, Roberts PA, Kaloshian I (2007) The Mi-9 gene from Solanum arcanum conferring heat-stable resistance to root-knot nematodes is a homolog of Mi-1. Plant Physiol 143:1044–1054. https://doi.org/10.1104/pp.106.089615
Jagdale S, Rao U, Giri AP (2021) Effectors of root-knot nematodes: An arsenal for successful parasitism. Front Plant Sci 12:800030. https://doi.org/10.3389/fpls.2021.800030
Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329. https://doi.org/10.1038/nature05286
Jones MGK, Northcote DH (1972) Nematode-induced syncytium-a multinucleate transfer cell. J Cell Sci 10:789–809
Jones JT, Furlanetto C, Bakker E, Banks B, Blok V, Chen Q, Phillips M, Prior A (2003) Characterization of a chorismate mutase from the potato cyst nematode Globodera pallida. Mol Plant Pathol 4:43–50. https://doi.org/10.1046/j.1364-3703.2003.00140.x
Jones JT, Haegeman A, Danchin EGJ, Gaur HS, Helder J, Jones MGK, Kikuchi T, Manzanilla-López R, Palomares-Rius JE, Wesemael WML, Perry RN (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Mol Plant Pathol 14:946–961. https://doi.org/10.1111/mpp.12057
Kadota Y, Shirasu K (2012) The HSP90 complex of plants. Biochim Biophys Acta 1823:689–697. https://doi.org/10.1016/j.bbamcr.2011.09.016
Kaloshian I, Desmond OJ, Atamian HS (2011) Disease resistance-genes and defense responses during incompatible interactions. In: Jones J, Gheysen G, Fenoll C (eds) Genomics and molecular genetics of plant-nematode interactions. Springer, Dordrecht, pp 309–324. https://doi.org/10.1007/978-94-007-0434-3_15
Kammerhofer N, Radakovic Z, Regis JMA, Dobrev P, Vankova R, Grundler FMW, Siddique S, Hofmann J, Wieczorek K (2015) Role of stress-related hormones in plant defence during early infection of the cyst nematode Heterodera schachtii in Arabidopsis. New Phytol 207:778–789. https://doi.org/10.1111/nph.13395
Kandoth PK, Ithal N, Recknor J, Maier T, Nettleton D, Baum TJ, Mitchum MG (2011) 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 Physiol 155:1960–1975. https://doi.org/10.1104/pp.110.167536
Kikuchi T, Eves-van den Akker S, Jones JT (2017) Genome evolution of plant-parasitic nematodes. Annu Rev Phytopathol 55:333–354. https://doi.org/10.1146/annurev-phyto-080516-035434
Koter MD, Święcicka M, Matuszkiewicz M, Pacak A, Derebecka N, Filipecki M (2018) The miRNAome dynamics during developmental and metabolic reprogramming of tomato root infected with potato cyst nematode. Plant Sci 268:18–29. https://doi.org/10.1016/j.plantsci.2017.12.003
Kourelis J, van der Hoorn RAL (2018) Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function. Plant Cell 30:285–299. https://doi.org/10.1105/tpc.17.00579
Labudda M, Różańska E, Czarnocka W, Sobczak M, Dzik JM (2018) Systemic changes in photosynthesis and reactive oxygen species homeostasis in shoots of Arabidopsis thaliana infected with the beet cyst nematode Heterodera schachtii. Mol Plant Pathol 19:1690–1704. https://doi.org/10.1111/mpp.12652
Labudda M, Różańska E, Muszyńska E, Marecka D, Głowienka M, Roliński P, Prabucka B (2020) Heterodera schachtii infection affects nitrogen metabolism in Arabidopsis thaliana. Plant Pathol 69:794–803. https://doi.org/10.1111/ppa.13152
Lambert KN, Allen KD, Sussex IM (1999) Cloning and characterization of an esophageal-gland-specific chorismate mutase from the phytoparasitic nematode Meloidogyne javanica. Mol Plant Microbe Interact 12:328–336. https://doi.org/10.1094/mpmi.1999.12.4.328
Lee C, Chronis D, Kenning C, Peret B, Hewezi T, Davis EL, Baum TJ, Hussey R, Bennett M, Mitchum MG (2011) The novel cyst nematode effector protein 19C07 interacts with the Arabidopsis auxin influx transporter LAX3 to control feeding site development. Plant Physiol 155:866–880. https://doi.org/10.1104/pp.110.167197
Lilley CJ, Maqbool A, Wu D, Yusup HB, Jones LM, Birch PRJ, Banfield MJ, Urwin PE, Eves-van den Akker S (2018) Effector gene birth in plant parasitic nematodes: Neofunctionalization of a housekeeping glutathione synthetase gene. PLoS Genet 14:e1007310. https://doi.org/10.1371/journal.pgen.1007310
Liu S, Kandoth PK, Warren SD, Yeckel G, Heinz R, Alden J, Yang C, Jamai A, El-Mellouki T, Juvale PS, Hill J, Baum TJ, Cianzio S, Whitham SA, Korkin D, Mitchum MG, Meksem K (2012) A soybean cyst nematode resistance gene points to a new mechanism of plant resistance to pathogens. Nature 492:256–260. https://doi.org/10.1038/nature11651
Lozano-Torres JL, Wilbers RHP, Gawronski P, Boshoven JC, Finkers-Tomczak A, Cordewener JHG, America AHP, Overmars HA, Van’t Klooster JW, Baranowski L, Sobczak M, Ilyas M, van der Hoorn RAL, Schots A, de Wit PJGM, Bakker J, Goverse A, Smant G (2012) Dual disease resistance mediated by the immune receptor Cf-2 in tomato requires a common virulence target of a fungus and a nematode. Proc Natl Acad Sci USA 109:10119–10124. https://doi.org/10.1073/pnas.1202867109
Maier TR, Masonbrink RE, Vijayapalani P, Gardner M, Howland AD, Mitchum MG, Baum TJ (2021) Esophageal gland RNA-seq resource of a virulent and avirulent population of the soybean cyst nematode Heterodera glycines. Mol Plant Microbe Interact 34:1084–1087. https://doi.org/10.1094/MPMI-03-21-0051-A
Manosalva P, Manohar M, von Reuss SH, Chen S, Koch A, Kaplan F, Choe A, Micikas RJ, Wang X, Kogel KH, Sternberg PW, Williamson VM, Schroeder FC, Klessig DF (2015) Conserved nematode signalling molecules elicit plant defenses and pathogen resistance. Nat Commun 6:7795. https://doi.org/10.1038/ncomms8795
Marhavý P, Kurenda A, Siddique S, Dénervaud Tendon V, Zhou F, Holbein J, Hasan MS, Grundler FMW, Farmer EE, Geldner N (2019) Single-cell damage elicits regional, nematode-restricting ethylene responses in roots. EMBO J 38:e100972. https://doi.org/10.15252/embj.2018100972
Masonbrink R, Maier TR, Muppirala U, Seetharam AS, Lord E, Juvale PS, Schmutz J, Johnson NT, Korkin D, Mitchum MG, Mimee B, Eves-van den Akker S, Hudson M, Severin AKJ, Baum TJ (2019) The genome of the soybean cyst nematode (Heterodera glycines) reveals complex patterns of duplications involved in the evolution of parasitism genes. BMC Genomics 20:119. https://doi.org/10.1186/s12864-019-5485-8
Matthews BF, Beard H, MacDonald MH, Kabir S, Youssef RM, Hosseini P, Brewer E (2013) Engineered resistance and hypersusceptibility through functional metabolic studies of 100 genes in soybean to its major pathogen, the soybean cyst nematode. Planta 237:1337–1357. https://doi.org/10.1007/s00425-013-1840-1
Matuszkiewicz M, Sobczak M, Cabrera J, Escobar C, Karpiński S, Filipecki M (2018) The role of programmed cell death regulator LSD1 in nematode-induced syncytium formation. Front Plant Sci 9:314. https://doi.org/10.3389/fpls.2018.00314
Matuszkiewicz M, Koter MD, Filipecki M (2019) Limited ventilation causes stress and changes in Arabidopsis morphological, physiological and molecular phenotype during in vitro growth. Plant Physiol Biochem 135:554–562. https://doi.org/10.1016/j.plaphy.2018.11.003
Mei Y, Thorpe P, Guzha A, Haegeman A, Blok VC, MacKenzie K, Gheysen G, Jones JT, Mantelin S (2015) Only a small subset of the SPRY domain gene family in Globodera pallida is likely to encode effectors, two of which suppress host defences induced by the potato resistance gene Gpa2. Nematology 17:409–424. https://doi.org/10.1163/15685411-00002875
Mei Y, Wright KM, Haegeman A, Bauters L, Diaz-Granados A, Goverse A, Gheysen G, Jones JT, Mantelin S (2018) The Globodera pallida SPRYSEC effector GpSPRY-414-2 that suppresses plant defenses targets a regulatory component of the dynamic microtubule network. Front Plant Sci 9:1019. https://doi.org/10.3389/fpls.2018.01019
Mendy B, Wang’ombe MW, Radakovic ZS, Holbein J, Ilyas M, Chopra D, Holton N, Zipfel C, Grundler FMW, Siddique S (2017) Arabidopsis leucine-rich repeat receptor-like kinase NILR1 is required for induction of innate immunity to parasitic nematodes. PLoS Pathog 13:e1006284. https://doi.org/10.1371/journal.ppat.1006284
Miller HN, DiEdwardo AA (1962) Leaf galls on Siderasis fuscata caused by root-knot nematode Meloidogyne incognita incognita. Phytopathology 52:1070–1073
Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM (1998) The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10:1307–1319. https://doi.org/10.1105/tpc.10.8.1307
Mitchum M, Liu X (2022) Peptide effectors in phytonematode parasitism and beyond. Annu Rev Phytopathol 60:97–119. https://doi.org/10.1146/annurev-phyto-021621-115932
Mitreva M, Blaxter ML, Bird DM, McCarter JP (2005) Comparative genomics of nematodes. Trends Genet 21:573–581. https://doi.org/10.1016/j.tig.2005.08.003
Miyashita N, Koga H (2017) Three-dimensional ultrastructure of feeding tubes and interconnected endoplasmic reticulum in root-knot nematode-induced giant cells in rose balsam. Protoplasma 254:1941–1951. https://doi.org/10.1007/s00709-016-1072-x
Müller J, Rehbock K, Wyss U (1982) Growth of Heterodera schachtii with remarks on amounts of food consumed. Rev Nématol 4:227–234
Mundo-Ocampo M, Baldwin JG (1983) Host response to Meloidodera spp. (Heteroderidae). J Nematol 15:544–554
Mur LAJ, Kenton P, Lloyd AJ, Ougham H, Prats E (2008) The hypersensitive response; The centenary is upon us but how much do we know? J Exp Bot 59:501–520. https://doi.org/10.1093/jxb/erm239
Ngou BPM, Ding P, Jones JDG (2022) Thirty years of resistance: Zig-zag through the plant immune system. Plant Cell 34:1447–1478. https://doi.org/10.1093/plcell/koac041
Ohtsu M, Sato Y, Kurihara D, Suzaki T, Kawaguchi M, Maruyama D, Higashiyama T (2017) Spatiotemporal deep imaging of syncytium induced by the soybean cyst nematode Heterodera glycines. Protoplasma 254:2107–2115. https://doi.org/10.1007/s00709-017-1105-0
Oosterbeek M, Lozano-Torres JL, Bakker J, Goverse A (2021) Sedentary plant-parasitic nematodes alter auxin homeostasis via multiple strategies. Front Plant Sci 12:668548. https://doi.org/10.3389/fpls.2021.668548
Paal J, Henselewski H, Muth J, Meksem K, Menéndez CM, Salamini F, Ballvora A, Gebhardt C (2004) Molecular cloning of the potato Gro1-4 gene conferring resistance to pathotype Ro1 of the root cyst nematode Globodera rostochiensis, based on a candidate gene approach. Plant J 38:285–297. https://doi.org/10.1111/j.1365-313X.2004.02047.x
Palomares-Rius JE, Escobar C, Cabrera J, Vovlas A, Castillo P (2017) Anatomical alterations in plant tissues induced by plant-parasitic nematodes. Front Plant Sci 8:1987. https://doi.org/10.3389/fpls.2017.01987
Paulson RE, Webster JM (1970) Giant cell formation in tomato roots caused by Meloidogyne incognita and Meloidogyne hapla (Nematoda) infection. A light and electron microscope study. Can J Bot 48:271–276
Paulson RE, Webster JM (1972) Ultrastructure of the hypersensitive reaction in roots of tomato, Lycopersicon esculentum L. to infection by the root-knot nematode, Meloidogyne incognita. Physiol Plant Pathol 2:227–234
Piya S, Binder BM, Hewezi T (2018) Canonical and noncanonical ethylene signaling pathways that regulate Arabidopsis susceptibility to the cyst nematode Heterodera schachtii. New Phytol 221:946–959. https://doi.org/10.1111/nph.15400
Radakovic ZS, Anjam MS, Escobar E, Chopra D, Cabrera J, Silva AC, Escobar C, Sobczak M, Grundler FMW, Siddique S (2018) Arabidopsis HIPP27 is a host susceptibility gene for the beet cyst nematode Heterodera schachtii. Mol Plant Pathol 19:1917–1928. https://doi.org/10.1111/mpp.12668
Raski DJ (1950) The life history and morphology of the sugar-beet nematode, Heterodera schachtii Schmidt. Phytopathology 40:135–152
Rebois RV (1980) Ultrastructure of a feeding peg and tube associated with Rotylenchulus reniformis in cotton. Nematologica 26:396–405
Różańska E, Czarnocka W, Baranowski Ł, Mielecki J, de Almeida EJ, Sobczak M (2018) Expression of both Arabidopsis γ-tubulin genes is essential for development of a functional syncytium induced by Heterodera schachtii. Plant Cell Rep 37:1279–1292. https://doi.org/10.1007/s00299-018-2312-7
Rumpenhorst HJ (1984) Intracellular feeding tubes associated with sedentary plant parasitic nematodes. Nematologica 30:77–85
Rutter WB, Franco J, Gleason C (2022) Rooting out the mechanisms of root-knot nematode-plant interactions. Annu Rev Phytopathol 60:43–76. https://doi.org/10.1146/annurev-phyto-021621-120943
Sacco MA, Koropacka K, Grenier E, Jaubert MJ, Blanchard A, Goverse A, Smant G, Moffett P (2009) The cyst nematode SPRYSEC protein RBP-1 elicits Gpa2- and RanGAP2-dependent plant cell death. PLoS Pathog 5:e1000564. https://doi.org/10.1371/journal.ppat.1000564
Sasser JN, Freckman DW (1987) A world perspective on nematology: The role of the society. In: Veech JA, Dickson DW (eds) Vistas on nematology. Society of Nematologists, Hyattsville, pp 7–14
Sembdner G (1963) Anatomie der Heterodera-rostochiensis-Gallen an Tomatenwurzeln. Nematologica 9:55–64
Shah SJ, Anjam MS, Mendy B, Anwer MA, Habash SS, Lozano-Torres JL, Grundler FMW, Siddique S (2017) Damage-associated responses of the host contribute to defence against cyst nematodes but not root-knot nematodes. J Exp Bot 68:5949–5960. https://doi.org/10.1093/jxb/erx374
Siddique S, Grundler FMW (2018) Parasitic nematodes manipulate plant development to establish feeding sites. Curr Opin Microbiol 46:102–108. https://doi.org/10.1016/j.mib.2018.09.004
Siddique S, Matera C, Radakovic ZS, Hasan MS, Gutbrod P, Rozanska E, Sobczak M, Torres MA, Grundler FMW (2014) Parasitic worms stimulate host NADPH oxidases to produce reactive oxygen species that limit plant cell death and promote infection. Sci Signal 7:ra33. https://doi.org/10.1126/scisignal.2004777
Siddique S, Radakovic ZS, De La Torre CM, Chronis D, Novák O, Ramireddy E, Holbein J, Matera C, Hütten M, Gutbrod P, Anjam MS, Rozanska E, Habash S, Elashry A, Sobczak M, Kakimoto T, Strnad M, Schmülling T, Mitchum MG, Grundler FMW (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. https://doi.org/10.1073/pnas.1503657112
Siddique S, Radakovic Z, Hiltl C, Pellegrin C, Baum TJ, Beasley H, Bent AF, Chitambo O, Chopra D, Danchin EGJ, Grenier E, Habash SS, Hasan MS, Helder J, Hewezi T, Holbein J, Holterman M, Janakowski S, Koutsovoulos GD, Kranse OP, Lozano-Torres JL, Maier TR, Masonbrink RE, Mendy B, Riemer E, Sobczak M, Sonawala U, Sterken MG, Thorpe P, van Steenbrugge JJM, Zahid N, Grundler F, Eves-van den Akker S (2022) The genome and lifestage-specific transcriptomes of a plant-parasitic nematode and its host reveal susceptibility genes involved in trans-kingdom synthesis of vitamin B5. Nat Commun 13:6190. https://doi.org/10.1038/s41467-022-33769-w
Sijmons PC, Grundler FMW, von Mende N, Burrows PR, Wyss U (1991) Arabidopsis thaliana as a new model host for plant-parasitic nematodes. Plant J 1:245–254
Sijmons PC, Atkinson HJ, Wyss U (1994) Parasitic strategies of root nematodes and associated host cell responses. Annu Rev Phytopathol 32:235–259
Smant G, Jones J (2011) Suppression of plant defences by nematodes. In: Jones J, Gheysen G, Fenoll C (eds) Genomics and molecular genetics of plant-nematode interactions. Springer, Dordrecht, pp 273–286. https://doi.org/10.1007/978-94-007-0434-3_13
Smant G, Stokkermans JPWG, Yan Y, de Boer JM, Baum TJ, Wang X, Hussey RS, Gommers FJ, Henrissat B, Davis EL, Helder J, Schots A, Bakker J (1998) Endogenous cellulases in animals: Isolation of β-1,4-endoglucanase genes from two species of plant-parasitic cyst nematodes. Proc Natl Acad Sci USA 95:4906–4911. https://doi.org/10.1073/pnas.95.9.4906
Sobczak M, Golinowski W (2011) Cyst nematodes and syncytia. In: Jones J, Gheysen G, Fenoll C (eds) Genomics and molecular genetics of plant-nematode interactions. Springer, Dordrecht, pp 61–82. https://doi.org/10.1007/978-94-007-0434-3_4
Sobczak M, Golinowski W, Grundler FMW (1997) Changes in the structure of Arabidopsis thaliana roots induced during development of males of the plant parasitic nematode Heterodera schachtii. Eur J Plant Pathol 103:113–124. https://doi.org/10.1023/A:1008609409465
Sobczak M, Golinowski W, Grundler FMW (1999) Ultrastructure of feeding plugs and feeding tubes formed by Heterodera schachtii. Nematology 1:363–374
Sobczak M, Avrova A, Jupowicz J, Phillips MS, Ernst K, Kumar A (2005) Characterization of susceptibility and resistance responses to potato cyst nematode (Globodera spp.) infection of tomato lines in the absence and presence of the broad-spectrum nematode resistance Hero gene. Mol Plant Microbe Interact 18:158–168. https://doi.org/10.1094/mpmi-18-0158
Szakasits D, Heinen P, Wieczorek K, Hofmann J, Wagner F, Kreil DP, Sykacek P, Grundler FMW, Bohlmann H (2009) The transcriptome of syncytia induced by the cyst nematode Heterodera schachtii in Arabidopsis roots. Plant J 57:771–784. https://doi.org/10.1111/j.1365-313x.2008.03727.x
Tameling WIL, Baulcombe DC (2007) Physical association of the NB-LRR resistance protein Rx with a Ran GTPase-activating protein is required for extreme resistance to Potato virus X. Plant Cell 19:1682–1694. https://doi.org/10.1105/tpc.107.050880
Tang J, Bassham DC (2018) Autophagy in crop plants: what’s new beyond Arabidopsis? Open Biol 8:180162. https://doi.org/10.1098/rsob.180162
van der Hoorn RAL, Kamoun S (2008) From guard to decoy: A new model for perception of plant pathogen effectors. Plant Cell 20:2009–2017. https://doi.org/10.1105/tpc.108.060194
van der Voort JR, Wolters P, Folkertsma R, Hutten R, van Zandvoort P, Vinke H, Kanyuka K, Bendahmane A, Jacobsen E, Janssen R, Bakker J (1997) Mapping of the cyst nematode resistance locus Gpa2 in potato using a strategy based on comigrating AFLP markers. Theor Appl Genet 95:874–880. https://doi.org/10.1007/s001220050638
Vanholme B, Kast P, Haegeman A, Jacob J, Grunewald W, Gheysen G (2009) Structural and functional investigation of a secreted chorismate mutase from the plant-parasitic nematode Heterodera schachtii in the context of related enzymes from diverse origins. Mol Plant Pathol 10:189–200. https://doi.org/10.1111/j.1364-3703.2008.00521.x
van Megen H, 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. Nematology 11:927–950. https://doi.org/10.1163/156854109X456862
Varypatakis K, Véronneau P-Y, Thorpe P, Cock PJA, Lim JT-Y, Armstrong MR, Janakowski S, Sobczak M, Hein I, Mimee B, Jones JT, Blok VC (2020) The genomic impact of selection for virulence against resistance in the potato cyst nematode, Globodera pallida. Genes 11:1429. https://doi.org/10.3390/genes11121429
Verma A, Lee C, Morriss S, Odu F, Kenning C, Rizzo N, Spollen WG, Lin M, McRae AG, Givan SA, Hewezi T, Hussey R, Davis EL, Baum TJ, Mitchum MG (2018) The novel cyst nematode effector protein 30D08 targets host nuclear functions to alter gene expression in feeding sites. New Phytol 219:697–713. https://doi.org/10.1111/nph.15179
Vijayapalani P, Hewezi T, Pontvianne F, Baum TJ (2018) An effector from the cyst nematode Heterodera schachtii derepresses host rRNA genes by altering histone acetylation. Plant Cell 30:2795–2812. https://doi.org/10.1105/tpc.18.00570
Wang X, Mitchum MG, Gao B, Li C, Diab H, Baum TJ, Hussey RS, Davis EL (2005) A parasitism gene from a plant-parasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana. Mol Plant Pathol 6:187–191. https://doi.org/10.1111/j.1364-3703.2005.00270.x
Wang J, Hu M, Wang J, Qi J, Han Z, Wang G, Qi Y, Wang HW, Zhou JM, Chai J (2019a) Reconstitution and structure of a plant NLR resistosome conferring immunity. Science 364:eaav5870. https://doi.org/10.1126/science.aav5870
Wang J, Wang J, Hu M, Wu S, Qi J, Wang G, Han Z, Qi Y, Gao N, Wang HW, Zhou JM, Chai J (2019b) Ligand-triggered allosteric ADP release primes a plant NLR complex. Science 364:eaav5868. https://doi.org/10.1126/science.aav5868
Wasilewska L (1979) Structure and function of soil nematode communities in natural ecosystems and agrocenoses. Pol Ecol Stud 5:97–146. https://agris.fao.org/agris-search/search.do?recordID=US201302822891
Wu CH, Abd-El-Haliem A, Bozkurt TO, Belhaj K, Terauchi R, Vossen JH, Kamoun S (2017) NLR network mediates immunity to diverse plant pathogens. Proc Natl Acad Sci USA 114:8113–8118. https://doi.org/10.1073/pnas.1702041114
Wubben MJ, Su H, Rodermel SR, Baum TJ (2001) Susceptibility to the sugar beet cyst nematode is modulated by ethylene signal transduction in Arabidopsis thaliana. Mol Plant Microbe Interact 14:1206–1212. https://doi.org/10.1094/MPMI.2001.14.10.1206
Wubben MJE, Jin J, Baum TJ (2008) Cyst nematode parasitism of Arabidopsis thaliana is inhibited by salicylic acid (SA) and elicits uncoupled SA-independent pathogenesis-related gene expression in roots. Mol Plant Microbe Interact 21:424–432. https://doi.org/10.1094/MPMI-21-4-0424
Wyss U (1992) Observations on the feeding behaviour of Heterodera schachtii throughout development, including events during moulting. Fundam Appl Nematol 15:75–89
Wyss U (1997) Root parasitic nematodes: An overview. In: Fenoll C, Grundler FMW, Ohl S (eds) Cellular and molecular aspects of plant-nematode interactions. Developments in plant pathology, vol 10. Springer, Dordrecht, pp 5–22
Wyss U, Zunke U (1986) Observations on the behaviour of second stage juveniles of Heterodera schachtii inside host roots. Rev Nématol 9:153–165
Zhang H, Deery MJ, Gannon L, Powers SJ, Lilley KS, Theodoulou FL (2015) Quantitative proteomics analysis of the Arg/N-end rule pathway of targeted degradation in Arabidopsis roots. Proteomics 15:2447–2457. https://doi.org/10.1002/pmic.201400530
Zhang H, Kjemtrup-Lovelace S, Li C, Luo Y, Chen LP, Song BH (2017) Comparative RNA-seq analysis uncovers a complex regulatory network for soybean cyst nematode resistance in wild soybean (Glycine soja). Sci Rep 7:9699. https://doi.org/10.1038/s41598-017-09945-0
Zheng Q, Putker V, Goverse A (2021) Molecular and cellular mechanisms involved in host-specific resistance to cyst nematodes in crops. Front Plant Sci 12:641582. https://doi.org/10.3389/fpls.2021.641582
Zhuo K, Chen J, Lin B, Wang J, Sun F, Hu L, Liao J (2017) A novel Meloidogyne enterolobii effector MeTCTP promotes parasitism by suppressing programmed cell death in host plants. Mol Plant Pathol 18:45–54. https://doi.org/10.1111/mpp.12374
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2024 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Matuszkiewicz, M., Sobczak, M. (2024). Syncytium Induced by Plant-Parasitic Nematodes. In: Kloc, M., Uosef, A. (eds) Syncytia: Origin, Structure, and Functions. Results and Problems in Cell Differentiation, vol 71. Springer, Cham. https://doi.org/10.1007/978-3-031-37936-9_18
Download citation
DOI: https://doi.org/10.1007/978-3-031-37936-9_18
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-37935-2
Online ISBN: 978-3-031-37936-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)