Translational biology of nematode effectors. Or, to put it another way, functional analysis of effectors – what’s the point?

in Nematology
Restricted Access
Get Access to Full Text
Rent on DeepDyve

Have an Access Token?

Enter your access token to activate and access content online.

Please login and go to your personal user account to enter your access token.


Have Institutional Access?

Access content through your institution. Any other coaching guidance?


There has been a huge amount of work put into identifying and characterising effectors from plant-parasitic nematodes in recent years. Although this work has provided insights into the mechanisms by which nematodes can infect plants, the potential translational outputs of much of this research are not always clear. This short article will summarise how developments in effector biology have allowed, or will allow, new control strategies to be developed, drawing on examples from nematology and from other pathosystems.


International Journal of Fundamental and Applied Nematological Research



AndolfoG.JupeF.WitekK.EtheringtonG.J.ErcolanoM.R.JonesJ.D.G. (2014). Defining the full tomato NB-LRR resistance gene repertoire using genomic and cDNA RenSeq. BMC Plant Biology 14, 120. DOI: 10.1186/1471-2229-14-120

BakhetiaM.UrwinP.E.AtkinsonH.J. (2008). Characterisation by RNAi of pioneer genes expressed in the dorsal pharyngeal gland cell of Heterodera glycines and the effects of combinatorial RNAi. International Journal for Parasitology 38, 1589-1597. DOI: 10.1016/j.ijpara.2008.05.003

BirdD.M.JonesJ.T.OppermanC.H.KikuchiT.DanchinE.G.J. (2015). Signatures of adaptation to plant parasitism in nematode genomes. Parasitology 142, S71-S84. DOI: 10.1017/S0031182013002163

CarpentierJ.EsquibetM.FouvilleD.Manzanares-DauleuxM.J.KerlanM.C.GrenierE. (2012). The evolution of the Gp-Rbp-1 gene in Globodera pallida includes multiple selective replacements. Molecular Plant Pathology 13, 546-555. DOI: 10.1111/j.1364-3703.2011.00769.x

ChapmanS.StevensL.J.BoevinkP.C.EngelhardtS.AlexanderC.J.HarrowerB.ChampouretN.McGeachyK.Van WeymersP.S.M.ChenX. (2014). Detection of the virulent form of AVR3a from Phytophthora infestans following artificial evolution of potato resistance gene R3a. PLoS ONE 9, e110158. DOI: 10.1371/journal.pone.0110158

ChenL.HaoL.ParryM.A.J.PhillipsA.L.HuY.-G. (2014). Progress in TILLING as a tool for functional genomics and improvement of crops. Journal of Integrative Plant Biology 56, 425-443. DOI: 10.1111/jipb.12192

ChenQ.RehmanS.SmantG.JonesJ.T. (2005). Functional analysis of pathogenicity proteins of the potato cyst nematode Globodera rostochiensis using RNAi. Molecular Plant-Microbe Interactions 18, 621-625. DOI: 10.1094/MPMI-18-0621

CookeD.E.L.CanoL.M.RaffaeleS.BainR.A.CookeL.R.EtheringtonG.J.DeahlK.L.FarrerR.A.GilroyE.M.GossE.M. (2012). Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen. PLoS Pathogens 8, e1002940. DOI: 10.1371/journal.ppat.1002940

CottonJ.A.LilleyC.J.JonesL.M.KikuchiT.ReidA.J.ThorpeP.TsaiI.J.BeasleyH.BlokV.C.CockP.J.A. (2014). The genome and life-stage specific transcriptomes of Globodera pallida elucidate key aspects of plant parasitism by a cyst nematode. Genome Biology 15, R43. DOI: 10.1186/gb-2014-15-3-r43

DanchinE.G.J.ArguelM.-J.Campan-FournierA.Perfus-BarbeochL.MaglianoM.RossoM.N.Da RochaM.Da SilvaC.NottetN.LabadieK. (2013). Identification of novel target genes for safer and more specific control of root-knot nematodes from a pan-genome mining. PLoS Pathogens 9, e1003745. DOI: 10.1371/journal.ppat.1003745

DanchinE.G.J.GuzeevaE.A.MantelinS.BerepikiA.JonesJ.T. (2016). Horizontal gene transfer from bacteria has enabled the plant-parasitic nematode Globodera pallida to feed on host-derived sucrose. Molecular Biology and Evolution 33, 1571-1579. DOI: 10.1093/molbev/msw041

DinhP.T.Y.BrownC.R.EllingA.A. (2014). RNA interference of effector gene Mc16D10L confers resistance against Meloidogyne chitwoodi in Arabidopsis and potato. Phytopathology 104, 1098-1106. DOI: 10.1094/PHYTO-03-14-0063-R

DjameiA.SchipperK.RabeF.GhoshA.VinconV.KahntJ.OsorioS.TohgeT.FernieA.R.FeussnerI. (2011). Metabolic priming by a secreted fungal effector. Nature 478, 395-398. DOI: 10.1038/nature10454

DuJ.VleeshouwersV.G.A.A. (2014). The do’s and don’ts of effectoromics. In: BirchP.R.J.JonesJ.T.BosJ.I.B. (Eds). Plant-pathogen interactions: methods and protocols. New York, NY, USA, Springer, pp.  257-268. DOI: 10.1007/978-1-62703-986-4

Eves-van den AkkerS.LilleyC.J.JonesJ.T.UrwinP.E. (2014a). Identification and characterisation of a hyper-variable apoplastic effector gene family of the potato cyst nematodes. PLoS Pathogens 10, e1004391. DOI: 10.1371/journal.ppat.1004391

Eves-van den AkkerS.LilleyC.J.DanchinE.G.J.RancurelC.CockP.J.A.UrwinP.E.JonesJ.T. (2014b). The transcriptome of Nacobbus aberrans reveals insights into the evolution of sedentary endoparasitism in plant-parasitic nematodes. Genome Biology and Evolution 6, 2181-2194. DOI: 10.1093/gbe/evu171

Eves-van den AkkerS.LaetschD.R.ThorpeP.LilleyC.J.DanchinE.G.J.Da RochaM.RancurelC.HolroydN.E.CottonJ.A.SzitenbergA. (2016). The genome of the yellow potato cyst nematode, Globodera rostochiensis, reveals insights into the basis of parasitism and virulence. Genome Biology 17, 124. DOI: 10.1186/s13059-016-0985-1

FireA.XuS.Q.MontgomeryM.K.KostasS.A.DriverS.E.MelloC.C. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806-811. DOI: 10.1038/35888

GaoB.AllenR.MaierT.R.DavisE.L.BaumT.J.HusseyR.S. (2003). The parasitome of the phytonematode Heterodera glycines. Molecular Plant-Microbe Interactions 16, 720-726. DOI: 10.1094/MPMI.2003.16.8.720

GillU.S.LeeS.MysoreK.S. (2015). Host versus nonhost resistance: distinct wars with similar arsenals. Phytopathology 105, 580-587. DOI: 10.1094/PHYTO-11-14-0298-RVW

GoverseA.SmantG. (2014). The activation and suppression of plant innate immunity by parasitic nematodes. Annual Review of Phytopathology 52, 243-265. DOI: 10.1146/annurev-phyto-102313-050118

HaegemanA.JacobJ.VanholmeB.KyndtT.MitrevaM.GheysenG. (2009). Expressed sequence tags of the peanut pod nematode Ditylenchus africanus: the first transcriptome analysis of an anguinid nematode. Molecular and Biochemical Parasitology 167, 32-40. DOI: 10.1016/j.molbiopara.2009.04.004

HaegemanA.JosephS.GheysenG. (2011). Analysis of the transcriptome of the root lesion nematode Pratylenchus coffeae generated by 454 sequencing technology. Molecular and Biochemical Parasitology 178, 7-14. DOI: 10.1016/j.molbiopara.2011.04.001

HaegemanA.MantelinS.JonesJ.T.GheysenG. (2012). Functional roles of effectors of plant-parasitic nematodes. Gene 492, 19-31. DOI: 10.1016/j.gene.2011.10.040

HeweziT.HoweP.MaierT.R.HusseyR.S.MitchumM.G.DavisE.L.BaumT.J. (2008). Cellulose binding protein from the parasitic nematode Heterodera schachtii interacts with Arabidopsis pectin methylesterase: cooperative cell wall modification during parasitism. Plant Cell 20, 3080-3093. DOI: 10.1105/tpc.108.063065

HofmannJ.WieczorekK.BlöchlA.GrundlerF.M.W. (2007). Sucrose supply to nematode-induced syncytia depends on the apoplasmic and symplasmic pathways. Journal of Experimental Botany 58, 1591-1601. DOI: 10.1093/jxb/erl285

HuangG.GaoB.MaierT.R.AllenR.DavisE.L.BaumT.J.HusseyR.S. (2003). A profile of putative parasitism genes expressed in the esophageal gland cells of the root-knot nematode Meloidogyne incognita. Molecular Plant-Microbe Interactions 16, 376-381. DOI: 10.1094/MPMI.2003.16.5.376

HuangG.DongR.AllenR.DavisE.L.BaumT.J.HusseyR.S. (2006a). A root-knot nematode secretory peptide functions as a ligand for a plant transcription factor. Molecular Plant-Microbe Interactions 19, 463-470. DOI: 10.1094/MPMI-19-0463

HuangG.AllenR.DavisE.L.BaumT.J.HusseyR.S. (2006b). Engineering broad root-knot resistance in transgenic plants by RNAi silencing of a conserved and essential root-knot nematode parasitism gene. Proceedings of the National Academy of Sciences of the United States of America 103, 14302-14306. DOI: 10.1073/pnas.0604698103

HusseyR.S.MimsC.W. (1991). Ultrastructure of feeding tubes formed in giant-cells induced in plants by the root-knot nematode Meloidogyne incognita. Protoplasma 162, 99-107. DOI: 10.1007/BF02562553

IbizaV.P.CañizaresJ.NuezF. (2010). EcoTILLING in Capsicum species: searching for new virus resistances. BMC Genomics 11, 631. DOI: 10.1186/1471-2164-11-631

JaouannetM.MaglianoM.ArguelM.-J.GourguesM.EvangelistiE.AbadP.RossoM.N. (2013). The root-knot nematode calreticulin Mi-CRT is a key effector in plant defense suppression. Molecular Plant-Microbe Interactions 26, 97-105. DOI: 10.1094/mpmi-05-12-0130-r

JonesJ.D.G.DanglJ.L. (2006). The plant immune system. Nature 444, 323-329. DOI: 10.1038/nature05286

JonesJ.T.KumarA.PylypenkoL.A.ThirugnanasambandamA.CastelliL.ChapmanS.CockP.J.A.GrenierE.LilleyC.J.PhillipsM.S. (2009). Identification and functional characterization of effectors in expressed sequence tags from various life cycle stages of the potato cyst nematode Globodera pallida. Molecular Plant Pathology 10, 815-828. DOI: 10.1111/j.1364-3703.2009.00585.x

JupeF.WitekK.VerweijW.ŚliwkaJ.PritchardL.EtheringtonG.J.MacleanD.CockP.J.A.LeggettR.M.BryanG.J. (2013). Resistance gene enrichment sequencing (RenSeq) enables reannotation of the NB-LRR gene family from sequenced plant genomes and rapid mapping of resistance loci in segregating populations. The Plant Journal 76, 530-544. DOI: 10.1111/tpj.12307

KayS.HahnS.MaroisE.HauseG.BonasU. (2007). A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science 318, 648-651. DOI: 10.1126/science.1144956

KikuchiT.AikawaT.KosakaH.PritchardL.OguraN.JonesJ.T. (2007). Expressed sequence tag (EST) analysis of the pine wood nematode Bursaphelenchus xylophilus and B. mucronatus. Molecular and Biochemical Parasitology 155, 9-17. DOI: 10.1016/j.molbiopara.2007.05.002

KingS.R.F.McLellanH.BoevinkP.C.ArmstrongM.R.BukharovaT.SukartaO.WinJ.KamounS.BirchP.R.J.BanfieldM.J. (2014). Phytophthora infestans RXLR effector PexRD2 interacts with host MAPKKKε to suppress plant immune signaling. Plant Cell 26, 1345-1359. DOI: 10.1105/tpc.113.120055

KumarS.SchifferP.H.BlaxterM. (2012). 959 Nematode Genomes: a semantic wiki for coordinating sequencing projects. Nucleic Acids Research 40, D1295-D1300. DOI: 10.1093/nar/gkr826

KyndtT.JiH.VanholmeB.GheysenG. (2013). Transcriptional silencing of RNAi constructs against nematode genes in Arabidopsis. Nematology 15, 519-528. DOI: 10.1163/15685411-00002698

LacombeS.Rougon-CardosoA.SherwoodE.PeetersN.DahlbeckD.van EsseH.P.SmokerM.RallapalliG.ThommaB.P.H.J.StaskawiczB. (2010). Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nature Biotechnology 28, 365-369. DOI: 10.1038/nbt.1613

LeeA.H.-Y.MiddletonM.A.GuttmanD.S.DesveauxD. (2013). Phytopathogen type III effectors as probes of biological systems. Microbial Biotechnology 6, 230-240. DOI: 10.1111/1751-7915.12042

LeeC.ChronisD.KenningC.PeretB.HeweziT.DavisE.L.BaumT.J.HusseyR.S.BennettM.MitchumM.G. (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. DOI: 10.1104/pp.110.167197

LeeS.HuttonS.WhitakerV. (2016). Mini review: potential applications of nonhost resistance for crop improvement. Frontiers in Plant Science 7, 997. DOI: 10.3389/fpls.2016.00997

LenmanM.AliA.MühlenbockP.Carlson-NilssonU.LiljerothE.ChampouretN.VleeshouwersV.G.A.A.AndreassonE. (2016). Effector-driven marker development and cloning of resistance genes against Phytophthora infestans in potato breeding clone SW93-1015. Theoretical and Applied Genetics 129, 105-115. DOI: 10.1007/s00122-015-2613-y

LiG.HuangS.GuoX.LiY.YangY.GuoZ.KuangH.RietmanH.BergervoetM.VleeshouwersV.G.A.A. (2011). Cloning and characterization of R3b; members of the R3 superfamily of late blight resistance genes show sequence and functional divergence. Molecular Plant-Microbe Interactions 24, 1132-1142. DOI: 10.1094/MPMI-11-10-0276

Lozano-TorresJ.L.WilbersR.H.P.WarmerdamS.Finkers-TomczakA.Diaz-GranadosA.van SchaikC.C.HelderJ.BakkerJ.GoverseA.SchotsA. (2014). Apoplastic venom allergen-like proteins of cyst nematodes modulate the activation of basal plant innate immunity by cell surface receptors. PLoS Pathogens 10, e1004569. DOI: 10.1371/journal.ppat.1004569

MahfouzM.M.PiatekA.StewartC.N. (2014). Genome engineering via TALENs and CRISPR/Cas9 systems: challenges and perspectives. Plant Biotechnology Journal 12, 1006-1014. DOI: 10.1111/pbi.12256

MaierT.R.HeweziT.PengJ.BaumT.J. (2013). Isolation of whole esophageal gland cells from plant-parasitic nematodes for transcriptome analyses and effector identification. Molecular Plant-Microbe Interactions 26, 31-35. DOI: 10.1094/mpmi-05-12-0121-fi

ManosalvaP.ManoharM.von ReussS.H.ChenS.KochA.KaplanF.ChoeA.MicikasR.J.WangX.KogelK.-H. (2015). Conserved nematode signalling molecules elicit plant defenses and pathogen resistance. Nature Communications 6, 7795. DOI: 10.1038/ncomms8795

MantelinS.ThorpeP.JonesJ.T. (2015). Suppression of plant defences by plant-parasitic nematodes. In: EscobarC.FenollC. (Eds). Advances in botanical research. Oxford, UK, Elsevier, pp.  325-337. DOI: 10.1016/bs.abr.2014.12.011

McCallumC.M.ComaiL.GreeneE.A.HenikoffS. (2000). Targeting induced local lesions in genomes (TILLING) for plant functional genomics. Plant Physiology 123, 439-442. DOI: 10.1104/pp.123.2.439

MeiY.ThorpeP.GuzhaA.HaegemanA.BlokV.C.MacKenzieK.GheysenG.JonesJ.T.MantelinS. (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. DOI: 10.1163/15685411-00002875

MejlhedeN.KyjovskaZ.BackesG.BurhenneK.RasmussenS.K.JahoorA. (2006). EcoTILLING for the identification of allelic variation in the powdery mildew resistance genes mlo and Mla of barley. Plant Breeding 125, 461-467. DOI: 10.1111/j.1439-0523.2006.01226.x

MitchumM.G.HusseyR.S.BaumT.J.WangX.EllingA.A.WubbenM.J.DavisE.L. (2013). Nematode effector proteins: an emerging paradigm of parasitism. New Phytologist 199, 879-894. DOI: 10.1111/nph.12323

NiuJ.LiuP.LiuQ.ChenC.GuoQ.YinJ.YangG.JianH. (2016). Msp40 effector of root-knot nematode manipulates plant immunity to facilitate parasitism. Scientific Reports 6, 19443. DOI: 10.1038/srep19443

NoonJ.B.HeweziT.MaierT.R.SimmonsC.WeiJ.-Z.WuG.LlacaV.DeschampsS.DavisE.L.MitchumM.G. (2015). Eighteen new candidate effectors of the phytonematode Heterodera glycines produced specifically in the secretory esophageal gland cells during parasitism. Phytopathology 105, 1362-1372. DOI: 10.1094/PHYTO-02-15-0049-R

PetitotA.-S.DereeperA.AgbessiM.Da SilvaC.GuyJ.ArdissonM.FernandezD. (2016). Dual RNA-seq reveals Meloidogyne graminicola transcriptome and candidate effectors during the interaction with rice plants. Molecular Plant Pathology 17, 860-874. DOI: 10.1111/mpp.12334

PostmaW.J.SlootwegE.J.RehmanS.Finkers-TomczakA.TytgatT.O.G.van GelderenK.Lozano-TorresJ.L.RoosienJ.PompR.van SchaikC.C. (2012). The effector SPRYSEC-19 of Globodera rostochiensis suppresses CC-NB-LRR-mediated disease resistance in plants. Plant Physiology 160, 944-954. DOI: 10.1104/pp.112.200188

RehmanS.PostmaW.J.TytgatT.O.G.PrinsP.QinL.OvermarsH.VossenJ.H.SpiridonL.-N.PetrescuA.-J.GoverseA. (2009). A secreted SPRY domain-containing protein (SPRYSEC) from the plant-parasitic nematode Globodera rostochiensis interacts with a CC-NB-LRR protein from a susceptible tomato. Molecular Plant-Microbe Interactions 22, 330-340. DOI: 10.1094/MPMI-22-3-0330

SaccoM.A.KoropackaK.GrenierE.JaubertM.J.BlanchardA.GoverseA.SmantG.MoffettP. (2009). The cyst nematode SPRYSEC protein RBP-1 elicits Gpa2- and RanGAP2-dependent plant cell death. PLoS Pathogens 5, e1000564. DOI: 10.1371/journal.ppat.1000564

SchoonbeekH.J.WangH.H.StefanatoF.L.CrazeM.BowdenS.WallingtonE.ZipfelC.RidoutC.J. (2015). Arabidopsis EF-Tu receptor enhances bacterial disease resistance in transgenic wheat. New Phytologist 206, 606-613. DOI: 10.1111/nph.13356

Schulze-LefertP.PanstrugaR. (2011). A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends in Plant Science 16, 117-125. DOI: 10.1016/j.tplants.2011.01.001

SchwessingerB.BaharO.ThomasN.HoltonN.NekrasovV.RuanD.CanlasP.E.DaudiA.PetzoldC.J.SinganV.R. (2015). Transgenic expression of the dicotyledonous pattern recognition receptor EFR in rice leads to ligand-dependent activation of defense responses. PLoS Pathogens 11, e1004809. DOI: 10.1371/journal.ppat.1004809

SegretinM.E.PaisM.FranceschettiM.Chaparro-GarciaA.BosJ.I.B.BanfieldM.J.KamounS. (2014). Single amino acid mutations in the potato immune receptor R3a expand response to Phytophthora effectors. Molecular Plant-Microbe Interactions 27, 624-637. DOI: 10.1094/MPMI-02-14-0040-R

SmantG.JonesJ.T. (2011). Suppression of plant defences by nematodes. In: JonesJ.T.GheysenG.FenollC. (Eds). Genomics and molecular genetics of plant-nematode interactions. Berlin, Germany, Springer, pp.  273-286.

SteuernagelB.PeriyannanS.K.Hernandez-PinzonI.WitekK.RouseM.N.YuG.HattaA.AyliffeM.BarianaH.JonesJ.D.G. (2016). Rapid cloning of disease-resistance genes in plants using mutagenesis and sequence capture. Nature Biotechnology 34, 652-655. DOI: 10.1038/nbt.3543

StreubelJ.PesceC.HutinM.KoebnikR.BochJ.SzurekB. (2013). Five phylogenetically close rice SWEET genes confer TAL effector-mediated susceptibility to Xanthomonas oryzae pv. oryzae. New Phytologist 200, 808-819. DOI: 10.1111/nph.12411

Thordal-ChristensenH. (2003). Fresh insights into processes of nonhost resistance. Current Opinion in Plant Biology 6, 351-357. DOI: 10.1016/S1369-5266(03)00063-3

ThorpeP.MantelinS.CockP.J.A.BlokV.C.CokeM.C.Eves van den AkkerS.GuzeevaE.A.LilleyC.J.SmantG.ReidA.J. (2014). Genomic characterisation of the effector complement of the potato cyst nematode Globodera pallida. BMC Genomics 15, 923. DOI: 10.1186/1471-2164-15-923

UrwinP.E.LilleyC.J.AtkinsonH.J. (2002). Ingestion of double-stranded RNA by preparasitic juvenile cyst nematodes leads to RNA interference. Molecular Plant-Microbe Interactions 15, 747-752. DOI: 10.1094/MPMI.2002.15.8.747

van SchieC.C.N.TakkenF.L.W. (2014). Susceptibility genes 101: how to be a good host. Annual Review of Phytopathology 52, 551-581. DOI: 10.1146/annurev-phyto-102313-045854

Van WeymersP.S.M.BakerK.ChenX.HarrowerB.CookeD.E.L.GilroyE.M.BirchP.R.J.ThilliezG.J.A.LeesA.K.LynottJ.S. (2016). Utilizing ‘Omic’ technologies to identify and prioritize novel sources of resistance to the oomycete pathogen Phytophthora infestans in potato germplasm collections. Frontiers in Plant Science 7, 672. DOI: 10.3389/fpls.2016.00672

Vega-ArreguínJ.C.JallohA.BosJ.I.B.MoffettP. (2014). Recognition of an Avr3a homologue plays a major role in mediating non-host resistance to Phytophthora capsici in Nicotiana species. Molecular Plant-Microbe Interactions 27, 770-780. DOI: 10.1094/MPMI-01-14-0014-R

VleeshouwersV.G.A.A.RietmanH.KrenekP.ChampouretN.YoungC.OhS.-K.WangM.BouwmeesterK.VosmanB.VisserR.G.F. (2008). Effector genomics accelerates discovery and functional profiling of potato disease resistance and Phytophthora Infestans avirulence genes. PLoS ONE 3, e2875. DOI: 10.1371/journal.pone.0002875

WeiC.-F.KvitkoB.H.ShimizuR.CrabillE.AlfanoJ.R.LinN.-C.MartinG.B.HuangH.-C.CollmerA. (2007). A Pseudomonas syringae pv. tomato DC3000 mutant lacking the type III effector HopQ1-1 is able to cause disease in the model plant Nicotiana benthamiana. The Plant Journal 51, 32-46. DOI: 10.1111/j.1365-313X.2007.03126.x

WubbenM.J.CallahanF.E.SchefflerB.S. (2010). Transcript analysis of parasitic females of the sedentary semi-endoparasitic nematode Rotylenchulus reniformis. Molecular and Biochemical Parasitology 172, 31-40. DOI: 10.1016/j.molbiopara.2010.03.011

WulffB.B.H.HorvathD.M.WardE.R. (2011). Improving immunity in crops: new tactics in an old game. Current Opinion in Plant Biology 14, 468-476. DOI: 10.1016/j.pbi.2011.04.002

XueB.HamamouchN.LiC.HuangG.HusseyR.S.BaumT.J.DavisE.L. (2013). The 8D05 parasitism gene of Meloidogyne incognita is required for successful infection of host roots. Phytopathology 103, 175-181. DOI: 10.1094/PHYTO-07-12-0173-R

YangY.JittayasothornY.ChronisD.WangX.CousinsP.ZhongG.-Y. (2013). Molecular characteristics and efficacy of 16D10 siRNAs in inhibiting root-knot nematode infection in transgenic grape hairy roots. PLoS ONE 8, e69463. DOI: 10.1371/journal.pone.0069463

ZhangL.DaviesL.J.EllingA.A. (2015). A Meloidogyne incognita effector is imported into the nucleus and exhibits transcriptional activation activity in planta. Molecular Plant Pathology 16, 48-60. DOI: 10.1111/mpp.12160


  • The zigzag model in context of plant-nematode interactions. In 2006, Jones & Dangl established the zigzag model to illustrate the quantitative output of the plant immune system in response to microbes but the concept has proven to be more broadly applicable to pests and pathogens. Components of the zigzag model that have been identified in plant-nematode interactions are shown in bold red type. The conceptual arms-race between host and pathogens can be depicted in four major phases. In phase I, conserved pathogen-associated molecular patterns (PAMPs; represented by the letter P in the pink forms) are recognised in plants by cell surface pattern-recognition receptors (PRRs) leading to induction of PAMP-triggered immunity (PTI). The only PAMP from plant-parasitic nematodes identified to date is a pheromone, the ascaroside 18 (Ascr#18; Manosalva et al., 2015), but its cognate PRR is not yet known. In phase II, adapted pathogens secrete effectors into the host that interfere with PTI, leading to effector-triggered susceptibility (ETS). Several nematode effectors (represented by the letter E in the blue clouds) have been characterised that can suppress PTI responses (see review by Mantelin et al., 2015). In phase III, particular effectors (represented in the blue clouds by the letter A for ‘Avirulence factors’) are detected by a second layer of plant resistance receptors (products of the R genes), activating effector-triggered immunity (ETI), which in most cases leads to the induction of a hypersensitive plant cell-death reaction (HR). Very few nematode R genes have been cloned (see review by Goverse & Smant, 2014) and only one avirulence effector has been identified so far, the Globodera pallida RBP-1 SPRYSEC effector AvrGpa2 (Sacco et al., 2009). In phase IV, as pathogen and host coevolve new effectors and R genes, susceptibility or resistance predominate in turn. Avirulence factors (A) maybe lost or modified to avoid recognition by cognate R proteins (as is the case for RBP-1) and perhaps new effectors are gained (B, C, D) that are able to suppress ETI. Such activity has been demonstrated for the ubiquitin carboxyl extension protein GrUBCEP12 and many SPRYSEC effectors (see review by Mantelin et al., 2015). Based on a figure in Smant & Jones (2011).

    View in gallery
  • Effector-mediated cell death in plants. A, B: A typical hypersensitive reaction is elicited by recognition of Globodera pallida effector Gp-RBP-1 (StGpa2-cognate avirulence factor) in Agrobacterium tumefaciens-based transient expression assay in potato accession Cara containing the StGpa2 resistance gene (A) or by transient co-expression of both StGpa2 and Gp-RBP-1 in Nicotiana benthamiana leaf (B). Conversely, eGFP control in potato and either StGpa2 or Gp-RBP-1 expressed alone in N. benthamiana do not induce a response in plants. Transient expressions were performed with untagged constructs for StGpa2, Gp-RBP-1 (Sacco et al., 2009) and eGFP control as described in Mei et al. (2015), by infiltration of A. tumefaciens strains at an OD600nm of 0.5. Symptoms observed under white light 7 days post infiltration. Infiltrated areas are indicated by dashed circles. C, D, E: Effectors also participate in non-host resistance. C: Wild-type Pseudomonas syringae pathovar tomato (Pst) strain DC3000 can barely infect N. benthamiana, whilst Pst mutant strain CUCPB5460 lacking the type-III effector HopQ1-1 is able to cause disease in the non-host plant (demonstrated by Wei et al., 2007). Necrotic disease symptoms observed 7 days after bacteria infiltration at OD600nm of 1.10−4 in 10 mM MgSO4 solution. Infiltrated areas are circled. D, E: Cell death is triggered specifically in non-host N. sylvestris (D) by a Phytophthora infestans RXLR effector (Pi-A) while transient expression of the same effector in the host plant N. benthamiana (E) does not induce symptoms in the leaf. Another effector (Pi-B) as well as the Td-Tomato construct used as control do not induce symptoms. Conversely, a typical hypersensitive reaction is elicited by recognition of P. infestans effector Pi-Avr3a in the presence of the potato resistance protein StR3a in N. benthamiana leaf (E). Effectors and controls in binary vector pGRAB were transformed in A. tumefaciens GV3101 and agro-infiltrated at an OD600nm of 0.1 in Nicotiana leaves (Mantelin & Hein, pers. comm.). Symptoms were observed under white light 7 days post inoculation. Infiltrated areas are indicated by dashed circles.

    View in gallery


Content Metrics

Content Metrics

All Time Past Year Past 30 Days
Abstract Views 18 18 11
Full Text Views 18 18 8
PDF Downloads 3 3 0
EPUB Downloads 2 2 2