Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

Interactions of endoparasitic and ectoparasitic nematodes within the plant root system

Francine Perrine-Walker https://orcid.org/0000-0002-9895-232X
+ Author Affiliations
- Author Affiliations

Sydney Institute of Agriculture, School of Life and Environmental Sciences, University of Sydney, Biomedical Building C81, 1 Central Avenue, Australian Technology Park, Eveleigh, NSW 2015, Australia. Email: marie.perrine-walker@sydney.edu.au

Functional Plant Biology 46(4) 295-303 https://doi.org/10.1071/FP18176
Submitted: 5 July 2018  Accepted: 7 December 2018   Published: 8 January 2019

Abstract

Root-knot and cyst nematodes have sophisticated mechanisms to invade their plant hosts to reprogram the plant developmental program to induce feeding structures essential for nematode survival and reproduction. This has a detrimental effect on the plant as this sedentary endoparasitic interaction affects the growth and yields of many crop plants. However, other migratory endoparasitic nematodes that do not establish root feeding sites are as aggressive on many crop plants. With new information gained from the genome and transcriptomes of the migratory endoparasitic nematode, Pratylenchus spp., this review compares the different lifestyles and the pathogenic interactions these nematodes have with their plant host. Pratylenchus spp. utilises a common arsenal of effectors involved in plant cell wall degradation and the manipulation of plant host innate immunity. The absence of specific cell reprogramming effector genes may explain its migratory endoparasitic lifestyle, making it relevant to pest management approaches in Australia.

Additional keywords: auxin, cytokinin, effectors, giant cell, intracellular and intercellular infection, Pratylenchus, root development, syncytium.


References

Abad P, Gouzy J, Aury JM, Castagnone-Sereno P, Danchin EG, Deleury E, Perfus-Barbeoch L, Anthouard V, Artiguenave F, Blok VC, et al (2008) Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nature Biotechnology 26, 909–915.
Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita.Crossref | GoogleScholarGoogle Scholar | 18660804PubMed |

Absmanner B, Stadler R, Hammes UZ (2013) Phloem development in nematode-induced feeding sites: the implications of auxin and cytokinin. Frontiers of Plant Science 4, 241
Phloem development in nematode-induced feeding sites: the implications of auxin and cytokinin.Crossref | GoogleScholarGoogle Scholar |

Ali S, Magne M, Chen S, Côté O, Stare BG, Obradovic N, Jamshaid L, Wang X, Bélair G, Moffett P (2015) Analysis of putative apoplastic effectors from the nematode, Globodera rostochiensis, and identification of an expansin-like protein that can induce and suppress host defenses. PLoS One 10, e0115042
Analysis of putative apoplastic effectors from the nematode, Globodera rostochiensis, and identification of an expansin-like protein that can induce and suppress host defenses.Crossref | GoogleScholarGoogle Scholar | 26658948PubMed |

Bartlem DG, Jones MGK, Hammes UZ (2014) Vascularization and nutrient delivery at root-knot nematode feeding sites in host roots. Journal of Experimental Botany 65, 1789–1798.
Vascularization and nutrient delivery at root-knot nematode feeding sites in host roots.Crossref | GoogleScholarGoogle Scholar | 24336493PubMed |

Bert W, Leliaert F, Vierstraete AR, Vanfleteren JR, Borgonie G (2008) Molecular phylogeny of the Tylenchina and evolution of the female gonoduct (Nematoda:Rhabditida). Molecular Phylogenetics and Evolution 48, 728–744.
Molecular phylogeny of the Tylenchina and evolution of the female gonoduct (Nematoda:Rhabditida).Crossref | GoogleScholarGoogle Scholar | 18502668PubMed |

Blair BL, Stirling GR (2007) The role of plant-parasitic nematodes in reducing yield of sugarcane in fine-textured soils in Queensland, Australia. Australian Journal of Experimental Agriculture 47, 620–634.
The role of plant-parasitic nematodes in reducing yield of sugarcane in fine-textured soils in Queensland, Australia.Crossref | GoogleScholarGoogle Scholar |

Blair BL, Stirling GR, Whittle PJL (1999) Distribution of pest nematodes on sugarcane in south Queensland and relationship to soil texture, cultivar, crop age and region. Australian Journal of Experimental Agriculture 39, 43–49.
Distribution of pest nematodes on sugarcane in south Queensland and relationship to soil texture, cultivar, crop age and region.Crossref | GoogleScholarGoogle Scholar |

Bohlmann H, Sobczak M (2014) The plant cell wall in the feeding sites of cyst nematodes. Frontiers of Plant Science 5, 89
The plant cell wall in the feeding sites of cyst nematodes.Crossref | GoogleScholarGoogle Scholar |

Bridge J, Fogain R, Speijer P (1997) The root lesion nematodes of banana. Pratylenchus coffeae (Zimmermann, 1898) Filip. & Schu. Stek., 1941. Pratylenchus goodeyi Sher & Allen, 1953. Musa Pest Fact Sheet No. 2. INIBAP, Montpellier, France.

Burke M, Scholl EH, Bird DM, Schaff JE, Colman SD, Crowell R, Diener S, Gordon O, Graham S, Wang X, Windham E, Wright GM, Opperman CH (2015) The plant parasite Pratylenchus coffeae carries a minimal nematode genome. Nematology 17, 621–637.
The plant parasite Pratylenchus coffeae carries a minimal nematode genome.Crossref | GoogleScholarGoogle Scholar |

Castillo P, Vovlas N (2007) Pratylenchus (Nematoda: Pratylenchidae): diagnosis, biology, pathogenicity and management. In ‘Nematology monographs and perspectives. Vol. 6’. (Eds DJ Hunt, RN Perry) pp. 305–407. (Brill Publishers: Leiden, The Netherlands)

Chen Q, Rehman S, Smant G, Jones JT (2005) Functional analysis of pathogenicity proteins of the potato cyst nematode Globodera rostochiensis using RNAi. Molecular Plant-Microbe Interactions 18, 621–625.
Functional analysis of pathogenicity proteins of the potato cyst nematode Globodera rostochiensis using RNAi.Crossref | GoogleScholarGoogle Scholar | 16042007PubMed |

Collins S, Wilkinson C, Kelly S, Hunter H, DeBrincat L (2013) Root lesion nematode has a picnic in 2013. DAFWA Bulletin. http://www.giwa.org.au/pdfs/2014/Presented_Papers/Collins%20Sarah_Root%20lesion%20nematode%20has%20a%20picnic%20in%202013_PAPER%20DR.pdf [Verified 11 December 2018]

Curtis RHC (2007) Do phytohormones influence nematode invasion and feeding site establishment? Nematology 9, 155–160.
Do phytohormones influence nematode invasion and feeding site establishment?Crossref | GoogleScholarGoogle Scholar |

Davis EL, Haegeman A, Kikuchi T (2011) Degradation of the plant cell wall by nematodes. In ‘Genomics and molecular genetics of plant–nematode interactions’. (Eds J Jones, G Gheysen, C Fenoll) pp. 255–272. (Springer: Dordrecht, The Netherlands)

de Almeida-Engler J, Siqueira KMS, Nascimento DC, Costa TG, Engler G (2016) A cellular outlook of galls induced by root-knot nematodes in the model host Arabidopsis thaliana. Nematoda 1, e062016

Decraemer W, Hunt DJ (2006) Structure and classification. In ‘Plant nematology’. (Eds RN Perry, M Moens) pp. 3–32. (CABI Publishing: Wallingford, CA, USA)

Denver DR, Brown AMV, Howe DK, Peetz AB, Zasada IA (2016) Genome skimming: a rapid approach to gaining diverse biological insights into multicellular pathogens. PLoS Pathogens 12, e1005713
Genome skimming: a rapid approach to gaining diverse biological insights into multicellular pathogens.Crossref | GoogleScholarGoogle Scholar | 27490201PubMed |

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. The Plant Journal 92, 211–228.
Divergent expression of cytokinin biosynthesis, signaling and catabolism genes underlying differences in feeding sites induced by cyst and root-knot nematodes.Crossref | GoogleScholarGoogle Scholar | 28746737PubMed |

Dubreuil G, Deleury E, Magliano M, Jaouannet M, Abad P, Rosso MN (2011) Peroxiredoxins from the plant parasitic root-knot nematode, Meloidogyne incognita, are required for successful development within the host. International Journal for Parasitology 41, 385–396.
Peroxiredoxins from the plant parasitic root-knot nematode, Meloidogyne incognita, are required for successful development within the host.Crossref | GoogleScholarGoogle Scholar | 21145323PubMed |

Endo BY (1978) Feeding plug formation in soybean roots infected with the soybean cyst nematode. Phytopathology 68, 1022–1031.
Feeding plug formation in soybean roots infected with the soybean cyst nematode.Crossref | GoogleScholarGoogle Scholar |

Fanelli E, Troccoli A, Picardi E, Pousis C, De Luca F (2014) Molecular characterization and functional analysis of four β-1,4-endoglucanases from the root-lesion nematode Pratylenchus vulnus. Plant Pathology 63, 1436–1445.
Molecular characterization and functional analysis of four β-1,4-endoglucanases from the root-lesion nematode Pratylenchus vulnus.Crossref | GoogleScholarGoogle Scholar |

Fosu-Nyarko J, Jones MGK (2016) Advances in understanding the molecular mechanisms of root lesion nematode host interactions. Annual Review of Phytopathology 54, 253–278.
Advances in understanding the molecular mechanisms of root lesion nematode host interactions.Crossref | GoogleScholarGoogle Scholar | 27296144PubMed |

Fosu-Nyarko J, Tan JA, Gill R, Agrez VG, Rao U, Jones MG (2016) De novo analysis of the transcriptome of Pratylenchus zeae to identify transcripts for proteins required for structural integrity, sensation, locomotion and parasitism. Molecular Plant Pathology 17, 532–552.
De novo analysis of the transcriptome of Pratylenchus zeae to identify transcripts for proteins required for structural integrity, sensation, locomotion and parasitism.Crossref | GoogleScholarGoogle Scholar | 26292651PubMed |

Giebel J (1970) Phenolic content in roots of some solanaceae and its influence on IAA-oxidase activity as an indicator of resistance to Heterodera rostochiensis. Nematologica 16, 22–32.
Phenolic content in roots of some solanaceae and its influence on IAA-oxidase activity as an indicator of resistance to Heterodera rostochiensis.Crossref | GoogleScholarGoogle Scholar |

Giebel J (1974) Biochemical mechanisms of plant resistance to nematodes: a review. Journal of Nematology 6, 175–184.

Goellner M, Smant G, De Boer JM, Baum TJ, Davis EL (2000) Isolation of β-1,4-endoglucanase genes from Globodera tabacum and their expression during parasitism. Journal of Nematology 32, 154–165.

Golinowski W, Sobczak M, Kurek W, Grymaszewska G (1997) The structure of syncytia. In ‘Cellular and molecular aspects of plant–nematode interactions.’ (Eds C Fenoll, FMW Grundler FMW, S Ohl S) pp. 80–97. (Kluwer Academic Publisher: Dordrecht, the Netherlands)

Grunewald W, Cannoot B, Friml J, Gheysen G (2009) Parasitic nematodes modulate PIN-mediated auxin transport to facilitate infection. PLoS Pathogens 5, e1000266
Parasitic nematodes modulate PIN-mediated auxin transport to facilitate infection.Crossref | GoogleScholarGoogle Scholar | 19148279PubMed |

Gutierrez OA, Wubben MJ, Howard M, Roberts B, Hanlon E, Wilkinson JR (2009) The role of phytohormones ethylene and auxin in plant-nematode interactions. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 56, 1–5.
The role of phytohormones ethylene and auxin in plant-nematode interactions.Crossref | GoogleScholarGoogle Scholar |

Haegeman A, Jones John T, Etienne G, Danchin J (2011a) Horizontal gene transfer in nematodes: a catalyst for plant parasitism? Molecular Plant-Microbe Interactions 24, 879–887.
Horizontal gene transfer in nematodes: a catalyst for plant parasitism?Crossref | GoogleScholarGoogle Scholar | 21539433PubMed |

Haegeman A, Joseph S, Gheysen G (2011b) Analysis of the transcriptome of the root lesion nematode Pratylenchus coffeae generated by 454 sequencing technology. Molecular and Biochemical Parasitology 178, 7–14.
Analysis of the transcriptome of the root lesion nematode Pratylenchus coffeae generated by 454 sequencing technology.Crossref | GoogleScholarGoogle Scholar | 21513748PubMed |

Haegeman A, Mantelin S, Jones JT, Gheysen G (2012) Functional roles of effectors of plant-parasitic nematodes. Gene 492, 19–31.
Functional roles of effectors of plant-parasitic nematodes.Crossref | GoogleScholarGoogle Scholar | 22062000PubMed |

Hassan S, Behm CA, Mathesius U (2010) Effectors of plant parasitic nematodes that re-program root cell development. Functional Plant Biology 37, 933–942.
Effectors of plant parasitic nematodes that re-program root cell development.Crossref | GoogleScholarGoogle Scholar |

Hodda M, Cook DC (2009) Economic impact from unrestricted spread of potato cyst nematodes in Australia. Phytopathology 99, 1387–1393.
Economic impact from unrestricted spread of potato cyst nematodes in Australia.Crossref | GoogleScholarGoogle Scholar | 19900005PubMed |

Hodda M, Nobbs J (2008) A review of current knowledge on particular taxonomic features of the Australasian nematode fauna, with special emphasis on plant feeders. Australasian Plant Pathology 37, 308–317.
A review of current knowledge on particular taxonomic features of the Australasian nematode fauna, with special emphasis on plant feeders.Crossref | GoogleScholarGoogle Scholar |

Holterman M, Karssen G, van den Elsen S, van Megen H, Bakker J, Helder J (2009) Small subunit rDNA-based phylogeny of the Tylenchida sheds light on relationships among some high-impact plant-parasitic nematodes and the evolution of plant feeding. Phytopathology 99, 227–235.
Small subunit rDNA-based phylogeny of the Tylenchida sheds light on relationships among some high-impact plant-parasitic nematodes and the evolution of plant feeding.Crossref | GoogleScholarGoogle Scholar | 19203274PubMed |

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.
Ultrastructure of feeding tubes formed in giant-cells induced in plants by the root-knot nematode Meloidogyne incognita.Crossref | GoogleScholarGoogle Scholar |

Imanishi L, Perrine-Walker FM, Ndour A, Vayssières A, Conejero G, Lucas M, Champion A, Laplaze L, Wall L, Svistoonoff S (2014) Role of auxin during intercellular infection of Discaria trinervis by Frankia. Frontiers of Plant Science 5, 399
Role of auxin during intercellular infection of Discaria trinervis by Frankia.Crossref | GoogleScholarGoogle Scholar |

Jaouannet M, Rosso MN (2013) Effectors of root sedentary nematodes target diverse plant cell compartments to manipulate plant functions and promote infection. Plant Signaling & Behavior 8, e25507
Effectors of root sedentary nematodes target diverse plant cell compartments to manipulate plant functions and promote infection.Crossref | GoogleScholarGoogle Scholar |

Jaouannet M, Magliano M, Arguel MJ, Gourgues M, Evangelisti E, Abad P, Rosso MN (2013) The root-knot nematode calreticulin Mi-CRT is a key effector in plant defense suppression. Molecular Plant-Microbe Interactions 26, 97–105.
The root-knot nematode calreticulin Mi-CRT is a key effector in plant defense suppression.Crossref | GoogleScholarGoogle Scholar | 22857385PubMed |

Jaubert S, Laffaire J-B, Abad P, Rosso M-N (2002) A polygalacturonase of animal origin isolated from the root-knot nematode Meloidogyne incognita. FEBS Letters 522, 109–112.
A polygalacturonase of animal origin isolated from the root-knot nematode Meloidogyne incognita.Crossref | GoogleScholarGoogle Scholar | 12095628PubMed |

Jaubert S, Milac AL, Petrescu AJ, de Almeida-Engler J, Abad P, Rosso M-N (2005) In planta secretion of a calreticulin by migratory and sedentary stages of root-knot nematode. Molecular Plant-Microbe Interactions 18, 1277–1284.
In planta secretion of a calreticulin by migratory and sedentary stages of root-knot nematode.Crossref | GoogleScholarGoogle Scholar | 16478047PubMed |

Jones JT, Haegeman A, Danchin EG, Gaur HS, Helder J, Jones MG, Kikuchi T, Manzanilla-López R, Palomares-Rius JE, Wesemael WM, Perry RN (2013) Top 10 plant-parasitic nematodes in molecular plant pathology. Molecular Plant Pathology 14, 946–961.
Top 10 plant-parasitic nematodes in molecular plant pathology.Crossref | GoogleScholarGoogle Scholar | 23809086PubMed |

Kudla U, Qin L, Milac A, Kielak A, Maissen C, Overmars H, Popeijus H, Roze E, Petrescu A, Smant G, Bakker J, Helder J (2005) Origin, distribution and 3D-modeling of Gr-EXPB1, an expansin from the potato cyst nematode Globodera rostochiensis. FEBS Letters 579, 2451–2457.
Origin, distribution and 3D-modeling of Gr-EXPB1, an expansin from the potato cyst nematode Globodera rostochiensis.Crossref | GoogleScholarGoogle Scholar | 15848187PubMed |

Kyndt T, Goverse A, Haegeman A, Warmerdam S, Wanjau C, Jahani M, Engler G, de Almeida Engler J, Gheysen G (2016) Redirection of auxin flow in Arabidopsis thaliana roots after infection by root-knot nematodes. Journal of Experimental Botany 67, 4559–4570.
Redirection of auxin flow in Arabidopsis thaliana roots after infection by root-knot nematodes.Crossref | GoogleScholarGoogle Scholar | 27312670PubMed |

Ledger TN, Jaubert S, Bosselut N, Abad P, Rosso MN (2006) Characterization of a new β-1,4-endoglucanase gene from the root-knot nematode Meloidogyne incognita and evolutionary scheme for phytonematode family 5 glycosyl hydrolases. Gene 382, 121–128.
Characterization of a new β-1,4-endoglucanase gene from the root-knot nematode Meloidogyne incognita and evolutionary scheme for phytonematode family 5 glycosyl hydrolases.Crossref | GoogleScholarGoogle Scholar | 16962258PubMed |

Lee C, Chronis D, Kenning C, Péret 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 Physiology 155, 866–880.
The novel cyst nematode effector protein 19C07 interacts with the Arabidopsis auxin influx transporter LAX3 to control feeding site development.Crossref | GoogleScholarGoogle Scholar | 21156858PubMed |

Liu J, Peng H, Cui J, Huang W, Kong L, Clarke JL, Jian H, Wang GL, Peng D (2016) Molecular characterization of a novel effector expansin-like protein from Heterodera avenae that induces cell death in Nicotiana benthamiana. Scientific Reports 6, 35677
Molecular characterization of a novel effector expansin-like protein from Heterodera avenae that induces cell death in Nicotiana benthamiana.Crossref | GoogleScholarGoogle Scholar | 27808156PubMed |

Lohar DP, Schaff JE, Laskey JG, Kieber JJ, Bilyeu KD, Bird DM (2004) Cytokinins play opposite roles in lateral root formation, and nematode and rhizobial symbioses. The Plant Journal 38, 203–214.
Cytokinins play opposite roles in lateral root formation, and nematode and rhizobial symbioses.Crossref | GoogleScholarGoogle Scholar | 15078325PubMed |

Luc M (1987) A reappraisal of Tylenchina (Nemata): 7. The family Pratylenchidae Thorne, 1949. Revue de Nématologie 10, 203–218.

Maier TR, Hewezi T, Peng J, Baum TJ (2013) Isolation of whole esophageal gland cells from plant-parasitic nematodes for transcriptome analyses and effector identification. Molecular Plant-Microbe Interactions 26, 31–35.
Isolation of whole esophageal gland cells from plant-parasitic nematodes for transcriptome analyses and effector identification.Crossref | GoogleScholarGoogle Scholar | 22876962PubMed |

Melillo MT, Leonetti P, Bongiovanni M, Castagnone-Sereno P, Bleve-Zacheo T (2006) Modulation of reactive oxygen species activities and H2O2 accumulation during compatible and incompatible tomato–root-knot nematode interactions. New Phytologist 170, 501–512.
Modulation of reactive oxygen species activities and H2O2 accumulation during compatible and incompatible tomato–root-knot nematode interactions.Crossref | GoogleScholarGoogle Scholar | 16626472PubMed |

Mitchum MG, Wang X, Wang J, Davis EL (2012) Role of nematode peptides and other small molecules in plant parasitism. Annual Review of Phytopathology 50, 175–195.
Role of nematode peptides and other small molecules in plant parasitism.Crossref | GoogleScholarGoogle Scholar | 22578179PubMed |

Mitreva-Dautova M, Roze E, Overmars H, de Graaff L, Schots A, Helder J, Goverse A, Bakker J, Smant G (2006) A symbiont-independent endo-1,4-β-xylanase from the plant-parasitic nematode Meloidogyne incognita. Molecular Plant-Microbe Interactions 19, 521–529.
A symbiont-independent endo-1,4-β-xylanase from the plant-parasitic nematode Meloidogyne incognita.Crossref | GoogleScholarGoogle Scholar | 16673939PubMed |

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.
Three-dimensional ultrastructure of feeding tubes and interconnected endoplasmic reticulum in root-knot nematode-induced giant cells in rose balsam.Crossref | GoogleScholarGoogle Scholar | 28204899PubMed |

Miyashita N, Yabu T, Kurihara T, Koga H (2014) The feeding behavior of adult root-knot nematodes (Meloidogyne incognita) in rose balsam and tomato. Journal of Nematology 46, 296–301.

Moens M, Perry RN (2009) Migratory plant endoparasitic nematodes: a group rich in contrast and divergence. Annual Review of Phytopathology 47, 313–332.
Migratory plant endoparasitic nematodes: a group rich in contrast and divergence.Crossref | GoogleScholarGoogle Scholar | 19400647PubMed |

Murray GM, Brennan JP (2009) Estimating disease losses to the Australian wheat industry. Australasian Plant Pathology 38, 558–570.
Estimating disease losses to the Australian wheat industry.Crossref | GoogleScholarGoogle Scholar |

Murray GM, Brennan JP (2010) Estimating disease losses to the Australian barley industry. Australasian Plant Pathology 39, 85–96.
Estimating disease losses to the Australian barley industry.Crossref | GoogleScholarGoogle Scholar |

Ng JL, Perrine-Walker F, Wasson AP, Mathesius U (2015) The control of auxin transport in parasitic and symbiotic root–microbe interactions. Plants 4, 606–643.
The control of auxin transport in parasitic and symbiotic root–microbe interactions.Crossref | GoogleScholarGoogle Scholar | 27135343PubMed |

Nicol JM, Rivoal R (2007) Global knowledge and its application for the integrated control and management of nematodes on wheat. In ‘Integrated Management and Biocontrol of Vegetable and Grain Crop Nematodes.’ (Eds A Ciancio, K G Mukerji) pp. 251–294. (Springer: Dordrecht)

Nicol P, Gill R, Fosu-Nyarko J, Jones MG (2012) De novo analysis and functional classification of the transcriptome of the root lesion nematode, Pratylenchus thornei, after 454 GS FLX sequencing. International Journal for Parasitology 42, 225–237.
De novo analysis and functional classification of the transcriptome of the root lesion nematode, Pratylenchus thornei, after 454 GS FLX sequencing.Crossref | GoogleScholarGoogle Scholar | 22309969PubMed |

Ohri P, Pannu SK (2010) Effect of phenolic compounds on nematodes – a review. Journal of Applied and Natural Science 2, 344–350.
Effect of phenolic compounds on nematodes – a review.Crossref | GoogleScholarGoogle Scholar |

Patel N, Hamamouch N, Li C, Hewezi T, Hussey RS, Baum TJ, Mitchum MG, Davis EL (2010) A nematode effector protein similar to annexins in host plants. Journal of Experimental Botany 61, 235–248.
A nematode effector protein similar to annexins in host plants.Crossref | GoogleScholarGoogle Scholar | 19887499PubMed |

Peer WA, Murphy AS (2006) Flavonoids as Signal Molecules: Targets of Flavonoid Action. In ‘The Science of Flavonoids’. (Ed. E Grotewold) pp. 239–268. (Springer: Berlin)

Peng H, Cui J, Long H, Huang W, Kong L, Liu S, He W, Hu X, Peng D (2016) Novel pectate lyase genes of Heterodera glycines play key roles in the early stage of parasitism. PLoS One 11, e0149959
Novel pectate lyase genes of Heterodera glycines play key roles in the early stage of parasitism.Crossref | GoogleScholarGoogle Scholar | 27835689PubMed |

Perrine-Walker F, Doumas P, Lucas M, Vaissayre V, Beauchemin NJ, Band LR, Chopard J, Crabos A, Conejero G, Péret B, King JR, Verdeil JL, Hocher V, Franche C, Bennett MJ, Tisa LS, Laplaze L (2010) Auxin carriers localization drives auxin accumulation in plant cells infected by Frankia in Casuarina glauca actinorhizal nodules. Plant Physiology 154, 1372–1380.
Auxin carriers localization drives auxin accumulation in plant cells infected by Frankia in Casuarina glauca actinorhizal nodules.Crossref | GoogleScholarGoogle Scholar | 20826704PubMed |

Perrine-Walker F, Gherbi H, Imanishi L, Hocher V, Ghodhbane-Gtari F, Lavenus J, Benabdoun FM, Nambiar-Veetil M, Svistoonoff S, Laplaze L (2011) Symbiotic signaling in actinorhizal symbioses. Current Protein & Peptide Science 12, 156–164.
Symbiotic signaling in actinorhizal symbioses.Crossref | GoogleScholarGoogle Scholar |

Qin L, Kudla U, Roze EHA, Goverse A, Popeijus H, Nieuwland J, Overmars H, Jones JT, Schots A, Smant G, Bakker J, Helder J (2004) Plant degradation: a nematode expansin acting on plants. Nature 427, 30
Plant degradation: a nematode expansin acting on plants.Crossref | GoogleScholarGoogle Scholar | 14702076PubMed |

Rao AS (1990) Root flavonoids. Botanical Review 56, 1–84.
Root flavonoids.Crossref | GoogleScholarGoogle Scholar |

Robertson L, Robertson WM, Sobczak M, Helder J, Tetaud E, Ariyanayagam MR, Ferguson MA, Fairlamb A, Jones JT (2000) Cloning, expression and functional characterization of a peroxiredoxin from the potato cyst nematode Globodera rostochiensis. Molecular and Biochemical Parasitology 111, 41–49.
Cloning, expression and functional characterization of a peroxiredoxin from the potato cyst nematode Globodera rostochiensis.Crossref | GoogleScholarGoogle Scholar | 11087915PubMed |

Rosso MN, Favery B, Piotte C, Arthaud L, De Boer JM, Hussey RS, Bakker J, Baum TJ, Abad P (1999) Isolation of a cDNA encoding a β-1,4-endoglucanase in the root-knot nematode Meloidogyne incognita and expression analysis during plant parasitism. Molecular Plant-Microbe Interactions 12, 585–591.
Isolation of a cDNA encoding a β-1,4-endoglucanase in the root-knot nematode Meloidogyne incognita and expression analysis during plant parasitism.Crossref | GoogleScholarGoogle Scholar | 10478479PubMed |

Rybarczyk-Mydłowska K, Maboreke HR, van Megen H, van den Elsen S, Mooyman P, Smant G, Bakker J, Helder J (2012) Rather than by direct acquisition via lateral gene transfer, GHF5 cellulases were passed on from early Pratylenchidae to root-knot and cyst nematodes. BMC Evolutionary Biology 12, 221
Rather than by direct acquisition via lateral gene transfer, GHF5 cellulases were passed on from early Pratylenchidae to root-knot and cyst nematodes.Crossref | GoogleScholarGoogle Scholar | 23171084PubMed |

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. Proceedings of the National Academy of Sciences of the United States of America 112, 12669–12674.
A parasitic nematode releases cytokinin that controls cell division and orchestrates feeding site formation in host plants.Crossref | GoogleScholarGoogle Scholar | 26417108PubMed |

Smith BP, Morales NB, Thomas MR, Smith HM, Clingeleffer PR (2017) Grapevine rootstocks resistant to the root‐knot nematode Meloidogyne javanica. Australian Journal of Grape and Wine Research 23, 125–131.
Grapevine rootstocks resistant to the root‐knot nematode Meloidogyne javanica.Crossref | GoogleScholarGoogle Scholar |

Sobczak M, Golinowski W (2009) Structure of cyst nematode feeding sites. In ‘Cell biology of plant nematode parasitism’. (Eds RH Berg, CG Taylor) pp. 153–187. (Springer: Berlin)

Soriano IR, Asenstorfer RE, Schmidt O, Riley IT (2004) Inducible flavone in oats (Avena sativa) is a novel defense against plant-parasitic nematodes. Phytopathology 94, 1207–1214.
Inducible flavone in oats (Avena sativa) is a novel defense against plant-parasitic nematodes.Crossref | GoogleScholarGoogle Scholar | 18944456PubMed |

Stenlid G (1976) Effects of flavonoids on the polar transport of auxins. Physiologia Plantarum 38, 262–266.
Effects of flavonoids on the polar transport of auxins.Crossref | GoogleScholarGoogle Scholar |

Stirling G, Nicol J, Reay F (2002) A report for the Rural Industries Research and Development Cooperation (RIRDC) Biological Crop Protection Pty Ltd. RIRDC Publication no. 99/41. p. vi. Available at http://www.rirdc.gov.au [Verified 11 December 2018]

Thompson JP, Owen KJ, Stirling GR, Bell MJ (2008) Root-lesion nematodes (Pratylenchus thornei and P. neglectus): a review of recent progress in managing a significant pest of grain crops in northern Australia. Australasian Plant Pathology 37, 235–242.
Root-lesion nematodes (Pratylenchus thornei and P. neglectus): a review of recent progress in managing a significant pest of grain crops in northern Australia.Crossref | GoogleScholarGoogle Scholar |

Thompson JP, Clewett TG, Sheedy JG, Reen RA, O’Reilly MM (2010) Occurrence of root-lesion nematodes (Pratylenchus thornei and P. neglectus) and stunt nematode (Merlinius brevidens) in the northern grain region of Australia. Australasian Plant Pathology 39, 254–264.
Occurrence of root-lesion nematodes (Pratylenchus thornei and P. neglectus) and stunt nematode (Merlinius brevidens) in the northern grain region of Australia.Crossref | GoogleScholarGoogle Scholar |

Tytgat T, Meutter J, Gheysen G, Coomans A (2000) Sedentary endoparasitic nematodes as a model for other plant parasitic nematodes. Nematology 2, 113–121.
Sedentary endoparasitic nematodes as a model for other plant parasitic nematodes.Crossref | GoogleScholarGoogle Scholar |

Vanholme B, Van Thuyne W, Vanhouteghem K, De Meutter J, Cannoot B, Gheysen G (2007) Molecular characterization and functional importance of pectate lyase secreted by the cyst nematode Heterodera schachtii. Molecular Plant Pathology 8, 267–278.
Molecular characterization and functional importance of pectate lyase secreted by the cyst nematode Heterodera schachtii.Crossref | GoogleScholarGoogle Scholar | 20507498PubMed |

Vanstone VA, Hollaway GJ, Stirling GR (2008) Managing nematode pests in the southern and western regions of the Australian cereal industry: continuing progress in a challenging environment. Australasian Plant Pathology 37, 220–224.
Managing nematode pests in the southern and western regions of the Australian cereal industry: continuing progress in a challenging environment.Crossref | GoogleScholarGoogle Scholar |

Vieira P, Eves-van den Akker S, Verma R, Wantoch S, Eisenback JD, Kamo K (2015) The Pratylenchus penetrans transcriptome as a source for the development of alternative control strategies: mining for putative genes involved in parasitism and evaluation of in planta RNAi. PLoS One 10, e0144674
The Pratylenchus penetrans transcriptome as a source for the development of alternative control strategies: mining for putative genes involved in parasitism and evaluation of in planta RNAi.Crossref | GoogleScholarGoogle Scholar | 26658731PubMed |

Vieira P, Maier TR, Eves-van den Akker S, Howe DK, Zasada I, Baum TJ, Eisenback JD, Kamo K (2018) Identification of candidate effector genes of Pratylenchus penetrans. Molecular Plant Pathology
Identification of candidate effector genes of Pratylenchus penetrans.Crossref | GoogleScholarGoogle Scholar | 29424950PubMed |

Viglierchio DR, Mjuge SG (1975) Auxin inactivation systems of nemic origin. Nematologica 21, 471–475.
Auxin inactivation systems of nemic origin.Crossref | GoogleScholarGoogle Scholar |

von Mende N (1997) Invasion and Migration Behaviour of Sedentary Nematodes. In ‘Cellular and Molecular Aspects of Plant-Nematode Interactions. Developments in Plant Pathology, vol 10.’ (Eds C Fenoll, FMW Grundler, SA Ohl) pp. 51–64. (Springer: Dordrecht)

Wieczorek K, Golecki B, Gerdes L, Heinen P, Szakasits D, Durachko DM, Cosgrove DJ, Kreil DP, Puzio PS, Bohlmann H, Grundler FM (2006) Expansins are involved in the formation of nematode-induced syncytia in roots of Arabidopsis thaliana. The Plant Journal 48, 98–112.
Expansins are involved in the formation of nematode-induced syncytia in roots of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 16942607PubMed |

Wyss U (1997) Root parasitic nematodes: an overview. In ‘Cellular and molecular aspects of plant–nematode interactions’. (Eds C Fenoll, FMW Grundler, SA Ohl) pp. 5–22. (Springer: Dordrecht, The Netherlands)

Wyss U, Zunke U (1986) Observations on the behaviour of second stage juveniles of Heterodera schachtii inside host roots. Revue de Nématologie 9, 153–165.

Wyss U, Grundler FMW, Münch A (1992) The parasitic behavior of second-stage juveniles in Meloidogyne incognita in roots of Arabidopsis thaliana. Nematologica 38, 98–111.
The parasitic behavior of second-stage juveniles in Meloidogyne incognita in roots of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |