Skip to main content

Nematode Communication

  • Chapter
  • First Online:
Biocommunication of Animals

Abstract

Nematodes, a diverse animal phylum that comprises an estimated million species, inhabit very broad ranges of ecological niches throughout earth. These animals, ranging from microscopic to a meter in size, are extremely successful in adapting different environments and have different lifestyles as free-living or parasitic to plants, animals and humans. As a result, nematodes have evolved to communicate with a wide variety of organisms that they live and interact with, including microbes, plants, insects, other animals, and nematodes of the same and different species. These communications play a key role in the mutualism, parasitism, predatory and prey, host and pathogen relationships between nematodes and other organisms and are critical to the ecological fitness of nematodes. In this chapter, we highlight examples of different types of communication among the nematodes and between nematodes and their natural trophic partners, and discuss their implications in nematode evolution.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Adhikari BN, Lin CY, Bai X, Ciche TA, Grewal PS, Dillman AR, Chaston JM, Shapiro-Ilan DI, Bilgrami AL, Gaugler R et al (2009) Transcriptional profiling of trait deterioration in the insect pathogenic nematode Heterorhabditis bacteriophora. BMC Genomics 10:609

    PubMed  Google Scholar 

  • Ali JG, Alborn HT, Stelinski LL (2011) Constitutive and induced subterranean plant volatiles attract both entomopathogenic and plant parasitic nematodes. J Ecol 99:26–35

    CAS  Google Scholar 

  • Avery L, Shtonda BB (2003) Food transport in the C. elegans pharynx. J Exp Biol 206:2441–2457

    PubMed  Google Scholar 

  • Avery L, You YJ (2012) C. elegans feeding. WormBook: the online review of C. elegans biology, 1–23

    Google Scholar 

  • Bai X, Grewal PS, Hogenhout SA, Adams BJ, Ciche TA, Gaugler R, Sternberg PW (2007) Expressed sequence tag analysis of gene representation in insect parasitic nematode Heterorhabditis bacteriophora. J Parasitol 93:1343–1349

    PubMed  CAS  Google Scholar 

  • Baird SE (1999) Natural and experimental associations of Caenorhabditis remanei with Trachelipus rathkii and other terrestrial isopods. Nematology 1:471–475

    Google Scholar 

  • Bargmann CI (2006) Chemosensation in C. elegans. In: The C. elegans Research Community (ed) WormBook. WormBook, Pasadena

    Google Scholar 

  • Barr M, Sternberg P (1999) A polycystic kidney-disease gene homologue required for male mating behaviour in C. elegans. Nature 401:386–389

    PubMed  CAS  Google Scholar 

  • Barr MM, DeModena J, Braun D, Nguyen CQ, Hall DH, Sternberg PW (2001) The Caenorhabditis elegans autosomal dominant polycystic kidney disease gene homologs lov-1 and pkd-2 act in the same pathway. Curr Biol 11:1341–1346

    PubMed  CAS  Google Scholar 

  • Barrière A, Félix M-A (2005) High local genetic diversity and low outcrossing rate in Caenorhabditis elegans natural populations. Curr Biol 15:1176–1184

    PubMed  Google Scholar 

  • Barron GL (1977) The nematode-destroying fungi. Canadian Biological Publications Ltd., Guelph

    Google Scholar 

  • Bird AF (1959) The attractiveness of roots to the plant parasitic nematodes Meloidogyne javanica and M. hapla. Nematologica 4:322–335

    Google Scholar 

  • Bird DMK, DiGennaro PM (2012) Nematode communication with plants is surprisingly complex and multidimensional. In: Witzany G, BaluÅ¡ka F (eds) Biocommunication of plants, signaling and communication in plants. Springer, Berlin/Heidelberg, pp 213–230

    Google Scholar 

  • Blaxter ML, Page AP, Rudin W, Maizels RM (1992) Nematode surface coats: actively evading immunity. Parasitol Today 8:243–247

    PubMed  CAS  Google Scholar 

  • Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406

    PubMed  CAS  Google Scholar 

  • Brivio MF, Pagani M, Restelli S (2002) Immune suppression of Galleria mellonella (Insecta, Lepidoptera) humoral defenses induced by Steinernema feltiae (Nematoda, Rhabditida): involvement of the parasite cuticle. Exp Parasitol 101:149–156

    PubMed  CAS  Google Scholar 

  • Burr AHJ, Robinson AF (2004) Locomotion behavior. In: Gaugler R, Bilgrami AL (eds) Nematode behavior. CABI, Trowbridge, pp 25–62

    Google Scholar 

  • Butcher RA, Fujita M, Schroeder FC, Clardy J (2007a) Small-molecule pheromones that control dauer development in Caenorhabditis elegans. Nat Chem Biol 3:420–422

    PubMed  CAS  Google Scholar 

  • Butcher RA, Fujita M, Schroeder FC, Clardy J (2007b) Small-molecule pheromones that control dauer development in Caenorhabditis elegans. Nat Chem Biol 3:420–422

    PubMed  CAS  Google Scholar 

  • Butcher RA, Ragains JR, Kim E, Clardy J (2008) A potent dauer pheromone component in Caenorhabditis elegans that acts synergistically with other components. Proc Natl Acad Sci 105:14288–14292

    PubMed  CAS  Google Scholar 

  • Butcher RA, Ragains JR, Clardy J (2009) An indole-containing dauer pheromone component with unusual dauer inhibitory activity at higher concentrations. Org Lett 11:3100–3103

    PubMed  CAS  Google Scholar 

  • Cassada RC, Russell RL (1975) The dauerlarva, a post-embryonic developmental variant of the nematode Caenorhabditis elegans. Dev Biol 46:326–342

    PubMed  CAS  Google Scholar 

  • Castro CE, Belser NO, Mckinney HE, Thomason IJ (1989) Quantitative bioassay for chemotaxis with plant parasitic nematodes – attractant and repellent fractions for Meloidogyne incognita from cucumber roots. J Chem Ecol 15:1297–1309

    Google Scholar 

  • Choe A, Chuman T, von Reuss SH, Dossey AT, Yim JJ, Ajredini R, Kolawa AA, Kaplan F, Alborn HT, Teal PEA et al (2012a) Sex-specific mating pheromones in the nematode Panagrellus redivivus. Proc Natl Acad Sci 109:20949–20954

    PubMed  CAS  Google Scholar 

  • Choe A, von Reuss SH, Kogan D, Gasser Robin B, Platzer Edward G, Schroeder Frank C, Sternberg PW (2012b) Ascaroside signaling is widely conserved among nematodes. Curr Biol 22:772–780

    PubMed  CAS  Google Scholar 

  • Ciche T (2007) The biology and genome of Heterorhabditis bacteriophora. WormBook : the online review of C elegans biology, 1–9

    Google Scholar 

  • Couillault C, Ewbank JJ (2002) Diverse bacteria are pathogens of Caenorhabditis elegans. Infect Immun 70:4705–4707

    PubMed  CAS  Google Scholar 

  • Daborn PJ, Waterfield N, Silva CP, Au CPY, Sharma S, Ffrench-Constant RH (2002) A single Photorhabdus gene, makes caterpillars floppy (mcf), allows Escherichia coli to persist within and kill insects. Proc Natl Acad Sci U S A 99:10742–10747

    PubMed  CAS  Google Scholar 

  • de Bono M, Bargmann CI (1998) Natural variation in a neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans. Cell 94:679–689

    PubMed  Google Scholar 

  • Dieterich C, Sommer RJ (2009) How to become a parasite – lessons from the genomes of nematodes. Trends Genet 25:203–209

    PubMed  CAS  Google Scholar 

  • Diez JA, Dusenbery DB (1989) Repellent of root-knot nematodes from exudate of host roots. J Chem Ecol 15:2445–2455

    Google Scholar 

  • Dillman AR, Sternberg PW (2012) Entomopathogenic nematodes. Curr Biol 22:R430–R431

    PubMed  CAS  Google Scholar 

  • Dillman AR, Chaston JM, Adams BJ, Ciche TA, Goodrich-Blair H, Stock SP, Sternberg PW (2012a) An entomopathogenic nematode by any other name. PLoS Pathog 8:e1002527

    PubMed  CAS  Google Scholar 

  • Dillman AR, Guillermin ML, Lee JH, Kim B, Sternberg PW, Hallem EA (2012b) Olfaction shapes host–parasite interactions in parasitic nematodes. Proc Natl Acad Sci 109:E2324–E2333

    PubMed  CAS  Google Scholar 

  • Dillman AR, Mortazavi A, Sternberg PW (2012c) Incorporating genomics into the toolkit of nematology. J Nematol 44:191–205

    PubMed  Google Scholar 

  • Dunphy GB, Thurston GS (1990) Insect immunity. In: Gaugler R, Kaya HK (eds) Entomopathogenic nematodes in biological control. CRC Press, Boca Raton, pp 301–323

    Google Scholar 

  • Dunphy GB, Webster JM (1984) Interaction of Xenorhabdus nematophilus subsp. nematophilus with the haemolymph of Galleria mellonella. J Insect Physiol 30:883–889

    Google Scholar 

  • Edmunds JE, Mai WF (1967) Effect of Fusarium oxysporum on movement of Pratylenchus penetrans toward Alfalfa roots. Phytopathology 57:468–471

    Google Scholar 

  • Engelmann I, Griffon A, Tichit L, Montanana-Sanchis F, Wang G, Reinke V, Waterston RH, Hillier LW, Ewbank JJ (2011) A comprehensive analysis of gene expression changes provoked by bacterial and fungal infection in C. elegans. PLoS One 6:e19055

    PubMed  CAS  Google Scholar 

  • Ewbank JJ (2006) Signaling in the immune response. WormBook: the online review of C. elegans biology, 1–12

    Google Scholar 

  • Felix MA, Braendle C (2010) The natural history of Caenorhabditis elegans. Curr Biol 20:R965–R969

    PubMed  CAS  Google Scholar 

  • Felix MA, Ashe A, Piffaretti J, Wu G, Nuez I, Belicard T, Jiang Y, Zhao G, Franz CJ, Goldstein LD et al (2011) Natural and experimental infection of Caenorhabditis nematodes by novel viruses related to nodaviruses. PLoS Biol 9:e1000586

    PubMed  CAS  Google Scholar 

  • ffrench-Constant RH, Bowen DJ (2000) Novel insecticidal toxins from nematode-symbiotic bacteria. Cell Mol Life Sci 57:828–833

    PubMed  CAS  Google Scholar 

  • Fiers M, Ku KL, Liu CM (2007) CLE peptide ligands and their roles in establishing meristems. Curr Opin Plant Biol 10:39–43

    PubMed  CAS  Google Scholar 

  • Fouquey C, Polonsky J, Lederer E (1957) Chemical structure of ascarylic alcohol isolated from Parascaris equorum. Bull Soc Chim Biol (Paris) 39:101–132

    Google Scholar 

  • Gallo M, Riddle D (2009) Effects of a Caenorhabditis elegans dauer pheromone ascaroside on physiology and signal transduction pathways. J Chem Ecol 35:272–279

    PubMed  CAS  Google Scholar 

  • Gao BL, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS (2001) Identification of putative parasitism genes expressed in the esophageal gland cells of the soybean cyst nematode Heterodera glycines. Mol Plant Microbe Interact 14:1247–1254

    PubMed  CAS  Google Scholar 

  • Garsin DA, Sifri CD, Mylonakis E, Qin X, Singh KV, Murray BE, Calderwood SB, Ausubel FM (2001) A simple model host for identifying Gram-positive virulence factors. Proc Natl Acad Sci U S A 98:10892–10897

    PubMed  CAS  Google Scholar 

  • Garsin DA, Villanueva JM, Begun J, Kim DH, Sifri CD, Calderwood SB, Ruvkun G, Ausubel FM (2003) Long-lived C. elegans daf-2 mutants are resistant to bacterial pathogens. Science 300:1921

    PubMed  CAS  Google Scholar 

  • Gatsogiannis C, Lang AE, Meusch D, Pfaumann V, Hofnagel O, Benz R, Aktories K, Raunser S (2013) A syringe-like injection mechanism in Photorhabdus luminescens toxins. Nature 495:520–523

    PubMed  CAS  Google Scholar 

  • Gheysen G, Mitchum MG (2011) How nematodes manipulate plant development pathways for infection. Curr Opin Plant Biol 14:415–421

    PubMed  Google Scholar 

  • Golden J, Riddle D (1982) A pheromone influences larval development in the nematode Caenorhabditis elegans. Science 218:578–580

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Green CD (1980) Nematode sex attractants. Helminthol Abstr Ser B 49:81–93

    Google Scholar 

  • Greet DN (1964) Observations on sexual attraction and copulation in the nematode Panagrolaimus rigidus (Schneider). Nature 204:96–97

    Google Scholar 

  • Grewal PS, Gaugler R, Selvan S (1993) Host recognition by entomopathogenic nematodes: behavioral response to contact with host feces. J Chem Ecol 19:1219–1231

    Google Scholar 

  • Grunewald W, Karimi M, Wieczorek K, Van de Cappelle E, Wischnitzki E, Grundler F, Inze D, Beeckman T, Gheysen G (2008) A role for AtWRKY23 in feeding site establishment of plant-parasitic nematodes. Plant Physiol 148:358–368

    PubMed  CAS  Google Scholar 

  • Grunewald W, Cannoot B, Friml J, Gheysen G (2009a) Parasitic nematodes modulate PIN-mediated auxin transport to facilitate infection. PLoS Pathog 5:e1000266

    PubMed  Google Scholar 

  • Grunewald W, van Noorden G, van Isterdael G, Beeckman T, Gheysen G, Mathesius U (2009b) Manipulation of auxin transport in plant roots during rhizobium symbiosis and nematode parasitism. Plant Cell 21:2553–2562

    PubMed  CAS  Google Scholar 

  • Hallem EA, Dillman AR, Hong AV, Zhang Y, Yano JM, DeMarco SF, Sternberg PW (2011) A sensory code for host seeking in parasitic nematodes. Curr Biol 21:377–383

    PubMed  CAS  Google Scholar 

  • Herrmann M, Mayer WE, Sommer RJ (2006) Nematodes of the genus Pristionchus are closely associated with scarab beetles and the Colorado potato beetle in Western Europe. Zoology 109:96–108

    PubMed  CAS  Google Scholar 

  • Herrmann M, Mayer WE, Hong RL, Kienle S, Minasaki R, Sommer RJ (2007) The nematode Pristionchus pacificus (Nematoda: Diplogastridae) is associated with the oriental beetle Exomala orientalis (Coleoptera: Scarabaeidae) in Japan. Zoolog Sci 24:883–889

    PubMed  CAS  Google Scholar 

  • Higgins ML, Pramer D (1967) Fungal morphogenesis: ring formation and closure by Arthrobotrys dactyloides. Science 155:345–346

    PubMed  CAS  Google Scholar 

  • Hodgkin J (1983) Male phenotypes and mating efficiency in Caenorhabditis elegans. Genetics 103:43–64

    PubMed  CAS  Google Scholar 

  • Hodgkin J, Kuwabara PE, Corneliussen B (2000) A novel bacterial pathogen, Microbacterium nematophilum, induces morphological change in the nematode C. elegans. Curr Biol 10:1615–1618

    PubMed  CAS  Google Scholar 

  • Hong RL, Sommer RJ (2006) Chemoattraction in Pristionchus nematodes and implications for insect recognition. Curr Biol 16:2359–2365

    PubMed  CAS  Google Scholar 

  • Hong RL, SvatoÅ¡ A, Herrmann M, Sommer RJ (2008) Species-specific recognition of beetle cues by the nematode Pristionchus maupasi. Evol Dev 10:273–279

    PubMed  Google Scholar 

  • Hsueh YP, Mahanti P, Schroeder FC, Sternberg PW (2013) Nematode-trapping fungi eavesdrop on nematode pheromones. Curr Biol 23:83–86

    PubMed  CAS  Google Scholar 

  • Hu PJ (2007) Dauer. In: The C. elegans Research Community (ed) WormBook. WormBook, Pasadena

    Google Scholar 

  • Huang GZ, Gao BL, Maier T, Allen R, Davis EL, Baum TJ, Hussey RS (2003) A profile of putative parasitism genes expressed in the esophageal gland cells of the root-knot nematode Meloidogyne incognita. Mol Plant Microbe Interact 16:376–381

    PubMed  CAS  Google Scholar 

  • Huang GZ, Dong RH, Allen R, Davis EL, Baum TJ, Hussey RS (2006) A root-knot nematode secretory peptide functions as a ligand for a plant transcription factor. Mol Plant Microbe Interact 19:463–470

    PubMed  CAS  Google Scholar 

  • Hutangura P, Mathesius U, Jones MGK, Rolfe BG (1999) Auxin induction is a trigger for root gall formation caused by root-knot nematodes in white clover and is associated with the activation of the flavonoid pathway. Aust J Plant Physiol 26:221–231

    CAS  Google Scholar 

  • Irazoqui JE, Troemel ER, Feinbaum RL, Luhachack LG, Cezairliyan BO, Ausubel FM (2010) Distinct pathogenesis and host responses during infection of C. elegans by P. aeruginosa and S. aureus. PLoS Pathog 6:e1000982

    PubMed  Google Scholar 

  • Jaffe H, Huettel RN, Demilo AB, Hayes DK, Rebois RV (1989) Isolation and identification of a compound from soybean cyst nematode Heterodera glycines, with sex pheromone activity. J Chem Ecol 15:2031–2043

    CAS  Google Scholar 

  • Janeway CA Jr, Medzhitov R (2002) Innate immune recognition. Annu Rev Immunol 20:197–216

    PubMed  CAS  Google Scholar 

  • Jeong P-Y, Jung M, Yim Y-H, Kim H, Park M, Hong E, Lee W, Kim YH, Kim K, Paik Y-K (2005) Chemical structure and biological activity of the Caenorhabditis elegans dauer-inducing pheromone. Nature 433:541–545

    PubMed  CAS  Google Scholar 

  • Jezky PF, Fairbairn D (1967) Ascarosides and ascaroside esters in Ascaris lumbricoides (Nematoda). Comp Biochem Physiol 23:691–705

    Google Scholar 

  • Jones J (2002) Nematode sense organs. In: Lee DL (ed) The biology of nematodes. CRC Press, London, pp 353–368

    Google Scholar 

  • Kaya HK, Gaugler R (1993) Entomopathogenic nematodes. Annu Rev Entomol 38:181–206

    Google Scholar 

  • Kerry BR (2002) Biological control. In: Lee DL (ed) The biology of nematodes. CRC Press, London, pp 483–510

    Google Scholar 

  • Kim K, Sato K, Shibuya M, Zeiger DM, Butcher RA, Ragains JR, Clardy J, Touhara K, Sengupta P (2009) Two chemoreceptors mediate developmental effects of dauer pheromone in C. elegans. Science 326:994–998

    PubMed  CAS  Google Scholar 

  • Kiontke K (1997) Description of Rhabditis (Caenorhabditis) drosophilae n. sp. and R. (C.) sonorae n. sp. (Nematoda: Rhabditida) from suguaro cactus rot in Arizona. Fundam Appl Nematol 20:305–315

    Google Scholar 

  • Kiontke K, Sudhaus W (2006) Ecology of Caenorhabditis species. In: The C. elegans Research Community (ed) WormBook. WormBook, Pasadena

    Google Scholar 

  • Kiontke K, Hironaka M, Sudhaus W (2002) Description of Caenorhabditis japonica n. sp. (Nematoda: Rhabditida) associated with the burrower bug Parastrachia japonensis (Heteroptera: Cydnidae) in Japan. Nematology 4:933–941

    Google Scholar 

  • Klass M, Hirsh D (1976) Non-ageing developmental variant of Caenorhabditis elegans. Nature 260:523–525

    PubMed  CAS  Google Scholar 

  • Krishnan A, Muralidharan S, Sharma L, Borges RM (2010) A hitchhiker’s guide to a crowded syconium: how do fig nematodes find the right ride? Funct Ecol 24:741–749

    Google Scholar 

  • Lans H, Jansen G (2007) Multiple sensory G proteins in the olfactory, gustatory and nociceptive neurons modulate longevity in Caenorhabditis elegans. Dev Biol 303:474–482

    PubMed  CAS  Google Scholar 

  • Lee DL (2002) Behavior. In: Lee DL (ed) The biology of nematodes. CRC Press, London, pp 369–387

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Li XY, Cowles RS, Cowles EA, Gaugler R, Cox-Foster DL (2007) Relationship between the successful infection by entomopathogenic nematodes and the host immune response. Int J Parasitol 37:365–374

    PubMed  CAS  Google Scholar 

  • Liou GY, Tzean SS (1997) Phylogeny of the genus Arthrobotyrs and allied nematode-trapping fungi based on rDNA sequences. Mycologia 89:876–884

    CAS  Google Scholar 

  • Lipton J, Kleemann G, Ghosh R, Lints R, Emmons SW (2004) Mate Searching in Caenorhabditis elegans: a genetic model for sex drive in a simple invertebrate. J Neurosci 24:7427–7434

    PubMed  CAS  Google Scholar 

  • Liu KS, Sternberg PW (1995) Sensory regulation of male mating behavior in Caenorhabditis elegans. Neuron 14:79–89

    PubMed  CAS  Google Scholar 

  • Liu KK, Tian JQ, Xiang MC, Liu XZ (2012) How carnivorous fungi use three-celled constricting rings to trap nematodes. Protein Cell 3:325–328

    PubMed  Google Scholar 

  • Lu SW, Chen S, Wang J, Yu H, Chronis D, Mitchum MG, Wang X (2009) Structural and functional diversity of CLAVATA3/ESR (CLE)-like genes from the potato cyst nematode Globodera rostochiensis. Mol Plant Microbe Interact 22:1128–1142

    PubMed  CAS  Google Scholar 

  • Ludewig AH, Schroeder FC (2013) Ascaroside signaling in C. elegans. In: The C. elegans Research Community (ed) WormBook. WormBook, Pasadena

    Google Scholar 

  • MacKinnon BM (1987) Sex attractants in nematodes. Parasitol Today 3:156–158

    PubMed  CAS  Google Scholar 

  • Maguire SM, Clark CM, Nunnari J, Pirri JK, Alkema MJ (2011) The C. elegans touch response facilitates escape from predacious fungi. Curr Biol 21:1326–1330

    PubMed  CAS  Google Scholar 

  • Mahajan-Miklos S, Tan MW, Rahme LG, Ausubel FM (1999) Molecular mechanisms of bacterial virulence elucidated using a Pseudomonas aeruginosa-Caenorhabditis elegans pathogenesis model. Cell 96:47–56

    PubMed  CAS  Google Scholar 

  • Mai WF, Abawi GS (1987) Interactions among root-knot nematodes and Fusarium wilt fungi on host plants. Annu Rev Phytopathol 25:317–338

    Google Scholar 

  • Mallo GV, Kurz CL, Couillault C, Pujol N, Granjeaud S, Kohara Y, Ewbank JJ (2002) Inducible antibacterial defense system in C. elegans. Curr Biol 12:1209–1214

    PubMed  CAS  Google Scholar 

  • Martikainen E, Huhta V (1990) Interactions between nematodes and predatory mites in raw humus soil – a microcosm experiment. Rev Ecol Biol Soc 27:13–20

    Google Scholar 

  • Masamune T, Anetai M, Takasugi M, Katsui N (1982) Isolation of a natural hatching stimulus, glycinoeclepin-a, for the soybean cyst nematode. Nature 297:495–496

    CAS  Google Scholar 

  • Mayer MG, Sommer RJ (2011) Natural variation in Pristionchus pacificus dauer formation reveals cross-preference rather than self-preference of nematode dauer pheromones. Proc R Soc B Biol Sci 278:2784–2790

    Google Scholar 

  • Mazarei M, Lennon KA, Puthoff DP, Rodermel SR, Baum TJ (2003) Expression of an Arabidopsis phosphoglycerate mutase homologue is localized to apical meristems, regulated by hormones, and induced by sedentary plant-parasitic nematodes. Plant Mol Biol 53:513–530

    PubMed  CAS  Google Scholar 

  • Mccallum ME, Dusenbery DB (1992) Computer tracking as a behavioral GC detector – nematode responses to vapor of host roots. J Chem Ecol 18:585–592

    CAS  Google Scholar 

  • McGrath PT, Xu Y, Ailion M, Garrison JL, Butcher RA, Bargmann CI (2011) Parallel evolution of domesticated Caenorhabditis species targets pheromone receptor genes. Nature 477:321–325

    PubMed  CAS  Google Scholar 

  • Morsci NS, Haas LA, Barr MM (2011) Sperm status regulates sexual attraction in Caenorhabditis elegans. Genetics 189:1341–1346

    PubMed  CAS  Google Scholar 

  • Noguez JH, Conner ES, Zhou Y, Ciche TA, Ragains JR, Butcher RA (2012) A novel ascaroside controls the parasitic life cycle of the entomopathogenic nematode Heterorhabditis bacteriophora. ACS Chem Biol 7(6):961–966

    PubMed  CAS  Google Scholar 

  • Nordbrin B (1973) Peptide-induced morphogenesis in nematode-trapping fungus Arthrobotrys oligospora. Physiol Plantarum 29:223–233

    Google Scholar 

  • Nordbringhertz B (1988) Nematophagous fungi – strategies for nematode exploitation and for survival. Microbiol Sci 5:108–116

    CAS  Google Scholar 

  • O’Rourke D, Baban D, Demidova M, Mott R, Hodgkin J (2006) Genomic clusters, putative pathogen recognition molecules, and antimicrobial genes are induced by infection of C. elegans with M. nematophilum. Genome Res 16:1005–1016

    PubMed  Google Scholar 

  • Okumura E, Tanaka R, Yoshiga T (2013) Species-specific recognition of the carrier insect by dauer larvae of the nematode Caenorhabditis japonica. J Exp Biol 216:568–572

    PubMed  CAS  Google Scholar 

  • Olsen AN, Skriver K (2003) Ligand mimicry? Plant-parasitic nematode polypeptide with similarity to CLAVATA3. Trends Plant Sci 8:55–57

    PubMed  CAS  Google Scholar 

  • Park D, O’Doherty I, Somvanshi RK, Bethke A, Schroeder FC, Kumar U, Riddle DL (2012) Interaction of structure-specific and promiscuous G-protein–coupled receptors mediates small-molecule signaling in Caenorhabditis elegans. Proc Natl Acad Sci 109:9917–9922

    PubMed  CAS  Google Scholar 

  • Poinar GO (1969) Arthropod immunity to worms. In: Jackson G, Herman R, Singer I (eds) Immunity to parasitic animals. Appleton-Century Crofts, New York, p 173

    Google Scholar 

  • Pramer D (1964) Nematode-trapping fungi – intriguing group of carnivorous plants inhabit microbial world. Science 144:382–388

    PubMed  CAS  Google Scholar 

  • Pramer D, Stoll NR (1959) Nemin – morphogenic substance causing trap formation by predaceous fungi. Science 129:966–967

    PubMed  CAS  Google Scholar 

  • Pujol N, Cypowyj S, Ziegler K, Millet A, Astrain A, Goncharov A, Jin Y, Chisholm AD, Ewbank JJ (2008a) Distinct innate immune responses to infection and wounding in the C. elegans epidermis. Curr Biol 18:481–489

    PubMed  CAS  Google Scholar 

  • Pujol N, Zugasti O, Wong D, Couillault C, Kurz CL, Schulenburg H, Ewbank JJ (2008b) Anti-fungal innate immunity in C. elegans is enhanced by evolutionary diversification of antimicrobial peptides. PLoS Pathog 4:e1000105

    PubMed  Google Scholar 

  • Pukkila-Worley R, Ausubel FM (2012) Immune defense mechanisms in the Caenorhabditis elegans intestinal epithelium. Curr Opin Immunol 24:3–9

    PubMed  CAS  Google Scholar 

  • Pukkila-Worley R, Ausubel FM, Mylonakis E (2011) Candida albicans infection of Caenorhabditis elegans induces antifungal immune defenses. PLoS Pathog 7:e1002074

    PubMed  CAS  Google Scholar 

  • Pungaliya C, Srinivasan J, Fox BW, Malik RU, Ludewig AH, Sternberg PW, Schroeder FC (2009) A shortcut to identifying small molecule signals that regulate behavior and development in Caenorhabditis elegans. Proc Natl Acad Sci 106:7708–7713

    PubMed  CAS  Google Scholar 

  • Rasmann S, Kollner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737

    PubMed  CAS  Google Scholar 

  • Rasmann S, Ali JG, Helder J, van der Putten WH (2012) Ecology and evolution of soil nematode chemotaxis. J Chem Ecol 38:615–628

    PubMed  CAS  Google Scholar 

  • Ribeiro C, Duvic B, Oliveira P, Givaudan A, Palha F, Simoes N, Brehélin M (1999) Insect immunity—effects of factors produced by a nematobacterial complex on immunocompetent cells. J Insect Physiol 45:677–685

    PubMed  CAS  Google Scholar 

  • Richardson WH, Schmidt TM, Nealson KH (1988) Identification of an anthraquinone pigment and a hydroxystilbene antibiotic from Xenorhabdus luminescens. Appl Environ Microb 54:1602–1605

    CAS  Google Scholar 

  • Rosen S, Ek B, Rask L, Tunlid A (1992) Purification and characterization of a surface lectin from the nematode-trapping fungus Arthrobotrys oligospora. J Gen Microbiol 138:2663–2672

    PubMed  CAS  Google Scholar 

  • Salt G (1963) The defence reactions of insects to metazoan parasites. Parasitology 53:527–642

    PubMed  CAS  Google Scholar 

  • Schackwitz WS, Inoue T, Thomas JH (1996) Chemosensory neurons function in parallel to mediate a pheromone response in C. elegans. Neuron 17:719–728

    PubMed  CAS  Google Scholar 

  • Schaedel ON, Gerisch B, Antebi A, Sternberg PW (2012) Hormonal signal amplification mediates environmental conditions during development and controls an irreversible commitment to adulthood. PLoS Biol 10:e1001306

    PubMed  CAS  Google Scholar 

  • Schenk H, Driessen RAJ, de Gelder R, Goubitz K, Nieboer H, Bruggemann-Rotgans IEM, Diepenhorst P (1999) Elucidation of the structure of Solanoeclepin A, a natural hatching factor of potato and tomato cyst nematodes, by single-crystal X-ray diffraction. Croat Chem Acta 72:593–606

    CAS  Google Scholar 

  • Schulte F (1989) The association between Rhabditis necromena Sudhaus Schulte, 1989 (Nematoda: Rhabditidae) and native and introduced millipedes in South Australia. Nematologica 35:82–89

    Google Scholar 

  • Schwartz HT, Antoshechkin I, Sternberg PW (2011) Applications of high-throughput sequencing to symbiotic nematodes of the genus Heterorhabditis. Symbiosis 55:111–118

    CAS  Google Scholar 

  • Shtonda BB, Avery L (2006) Dietary choice behavior in Caenorhabditis elegans. J Exp Biol 209:89–102

    PubMed  Google Scholar 

  • Simon JM, Sternberg PW (2002) Evidence of a mate-finding cue in the hermaphrodite nematode Caenorhabditis elegans. Proc Natl Acad Sci 99:1598–1603

    PubMed  CAS  Google Scholar 

  • Small RW, Grootaert P (1983) Observations on the predation abilities of some soil dwelling predatory nematodes. Nematologica 29:109–118

    Google Scholar 

  • Somvanshi VS, Sloup RE, Crawford JM, Martin AR, Heidt AJ, Kim KS, Clardy J, Ciche TA (2012) A single promoter inversion switches Photorhabdus between pathogenic and mutualistic states. Science 337:88–93

    PubMed  CAS  Google Scholar 

  • Srinivasan J, Kaplan F, Ajredini R, Zachariah C, Alborn HT, Teal PE, Malik RU, Edison AS, Sternberg PW, Schroeder FC (2008) A blend of small molecules regulates both mating and development in Caenorhabditis elegans. Nature 454:1115–1118

    PubMed  CAS  Google Scholar 

  • Srinivasan J, von Reuss SH, Bose N, Zaslaver A, Mahanti P, Ho MC, O’Doherty OG, Edison AS, Sternberg PW, Schroeder FC (2012) A modular library of small molecule signals regulates social behaviors in Caenorhabditis elegans. PLoS Biol 10:e1001237

    PubMed  CAS  Google Scholar 

  • Sudhaus W (2008) Evolution of insect parasitism in rhabditid and diplogastrid nematodes. In: Makarov S, Dimitrijevic R (eds) Advances in arachnology and developmental biology. SASA, Vienna/Belgrade/Sofia, pp 143–161

    Google Scholar 

  • Sudhaus W, Kiontke K (1996) Phylogeny of Rhabditis subgenus Caenorhabditis (Rhabditidae, Nematoda)*. J Zool Syst Evol Res 34:217–233

    Google Scholar 

  • Sudhaus W, Schulte F (1989) Rhabditis (Rhabditis) Necromena Sp. N. (Nematoda: Rhabditidae) from South Australian diplopoda with notes on its Siblings R. Myriophila Poinar, 1986 and R. Ca Uller Yi Maupas, 1919. Nematologica 35:15–24

    Google Scholar 

  • Tan MW, Ausubel FM (2000) Caenorhabditis elegans: a model genetic host to study Pseudomonas aeruginosa pathogenesis. Curr Opin Microbiol 3:29–34

    PubMed  CAS  Google Scholar 

  • Tan MW, Mahajan-Miklos S, Ausubel FM (1999a) Killing of Caenorhabditis elegans by Pseudomonas aeruginosa used to model mammalian bacterial pathogenesis. Proc Natl Acad Sci U S A 96:715–720

    PubMed  CAS  Google Scholar 

  • Tan MW, Rahme LG, Sternberg JA, Tompkins RG, Ausubel FM (1999b) Pseudomonas aeruginosa killing of Caenorhabditis elegans used to identify P. aeruginosa virulence factors. Proc Natl Acad Sci U S A 96:2408–2413

    PubMed  CAS  Google Scholar 

  • Thorson JS, Lo SF, Ploux O, He X, Liu HW (1994) Studies of the biosynthesis of 3,6-dideoxyhexoses: molecular cloning and characterization of the asc (ascarylose) region from Yersinia pseudotuberculosis serogroup VA. J Bacteriol 176:5483–5493

    PubMed  CAS  Google Scholar 

  • Torr P, Heritage S, Wilson MJ (2004) Vibrations as a novel signal for host location by parasitic nematodes. Int J Parasitol 34:997–999

    PubMed  CAS  Google Scholar 

  • Troemel ER, Chu SW, Reinke V, Lee SS, Ausubel FM, Kim DH (2006) p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLoS Genet 2:183

    Google Scholar 

  • Troemel ER, Felix MA, Whiteman NK, Barriere A, Ausubel FM (2008) Microsporidia are natural intracellular parasites of the nematode Caenorhabditis elegans. PLoS Biol 6:2736–2752

    PubMed  CAS  Google Scholar 

  • Tunlid A, Jansson HB, Nordbringhertz B (1992) Fungal attachment to nematodes. Mycol Res 96:401–412

    Google Scholar 

  • Vance RE, Isberg RR, Portnoy DA (2009) Patterns of pathogenesis: discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe 6:10–21

    PubMed  CAS  Google Scholar 

  • von Reuss SH, Bose N, Srinivasan J, Yim JJ, Judkins JC, Sternberg PW, Schroeder FC (2012) Comparative metabolomics reveals biogenesis of Ascarosides, a modular library of small-molecule signals in C. elegans. J Am Chem Soc 134:1817–1824

    Google Scholar 

  • Wang XH, Mitchum MG, Gao BL, Li CY, 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

    PubMed  Google Scholar 

  • Wang CL, Bruening G, Williamson VM (2009) Determination of preferred pH for root-knot nematode aggregation using pluronic F-127 Gel. J Chem Ecol 35:1242–1251

    PubMed  CAS  Google Scholar 

  • Wang JY, Lee C, Replogle A, Joshi S, Korkin D, Hussey R, Baum TJ, Davis EL, Wang XH, Mitchum MG (2010) Dual roles for the variable domain in protein trafficking and host-specific recognition of Heterodera glycines CLE effector proteins. New Phytol 187:1003–1017

    PubMed  CAS  Google Scholar 

  • Welch HE (1959) Taxonomy, life cycle, development, and habits of two new species of Allantonematidae (Nematoda) parasitic in drosophilid flies. Parasitology 49:83–103

    PubMed  CAS  Google Scholar 

  • Wootton LMO, Pramer D (1966) Valine-induced morphogenesis in Arthrobotrys conoides. Bacteriol Proc 75:225–232

    Google Scholar 

  • Wubben MJE, 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

    PubMed  CAS  Google Scholar 

  • Yang Y, Yang E, An Z, Liu X (2007) Evolution of nematode-trapping cells of predatory fungi of the Orbiliaceae based on evidence from rRNA-encoding DNA and multiprotein sequences. Proc Natl Acad Sci U S A 104:8379–8384

    PubMed  CAS  Google Scholar 

  • Zwaal RR, Mendel JE, Sternberg PW, Plasterk RHA (1997) Two neuronal G proteins are involved in chemosensation of the Caenorhabditis elegans Dauer-inducing pheromone. Genetics 145:715–727

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank our many collaborators and colleagues for making the study of nematode communication exciting and enjoyable, and for many conversations. We thank Hillel Schwartz for critical comments on the manuscript. PWS is an investigator with the Howard Hughes Medical Institute. D. L. is supported by National Institutes of Health USPHS training grant, GM07616.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paul W. Sternberg .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Hsueh, YP., Leighton, D.H.W., Sternberg, P.W. (2014). Nematode Communication. In: Witzany, G. (eds) Biocommunication of Animals. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-7414-8_21

Download citation

Publish with us

Policies and ethics