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Integrated signaling networks in plant responses to sedentary endoparasitic nematodes: a perspective

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Abstract

Sedentary plant endoparasitic nematodes can cause detrimental yield losses in crop plants making the study of detailed cellular, molecular, and whole plant responses to them a subject of importance. In response to invading nematodes and nematode-secreted effectors, plant susceptibility/resistance is mainly determined by the coordination of different signaling pathways including specific plant resistance genes or proteins, plant hormone synthesis and signaling pathways, as well as reactive oxygen signals that are generated in response to nematode attack. Crosstalk between various nematode resistance-related elements can be seen as an integrated signaling network regulated by transcription factors and small RNAs at the transcriptional, posttranscriptional, and/or translational levels. Ultimately, the outcome of this highly controlled signaling network determines the host plant susceptibility/resistance to nematodes.

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References

  • Absmanner B, Stadler R, Hammes UZ (2013) Phloem development in nematode-induced feeding sites: the implications of auxin and cytokinin. Front Plant Sci 4:241

    PubMed Central  PubMed  Google Scholar 

  • Ali MA, Wieczorek K, Kreil DP, Bohlmann H (2014) The beet cyst nematode heterodera schachtii modulates the expression of WRKY transcription factors in syncytia to favour its development in arabidopsis roots. PLoS One 9:e102360

    PubMed Central  PubMed  Google Scholar 

  • Ammiraju JSS, Veremis JC, Huang X, Roberts PA, Kaloshian I (2003) The heat-stable root-knot nematode resistance gene Mi-9 from Lycopersicon peruvianum is localized on the short arm of chromosome 6. Theor Appl Genet 106:478–484

    CAS  PubMed  Google Scholar 

  • Atamian HS, Eulgem T, Kaloshian I (2012) SlWRKY70 is required for Mi-1-mediated resistance to aphids and nematodes in tomato. Planta 235:299–309

    CAS  PubMed  Google Scholar 

  • Axtell MJ (2013) Classification and comparison of small RNAs from plants. Annu Rev Plant Biol 64:137–159

    CAS  PubMed  Google Scholar 

  • Bakker E, Achenbach U, Bakker J, van Vliet J, Peleman J, Segers B, van der Heijden S, van der Linde P, Graveland R, Hutten R, van Eck H, Coppoolse E, van der Vossen E, Bakker J, Goverse A (2004) A high-resolution map of the H1 locus harbouring resistance to the potato cyst nematode Globodera rostochiensis. Theor Appl Genet 109:146–152

    CAS  PubMed  Google Scholar 

  • Barcala M, Garcia A, Cabrera J, Casson S, Lindsey K, Favery B, Garcia-Casado G, Solano R, Fenoll C, Escobar C (2010) Early transcriptomic events in microdissected Arabidopsis nematode-induced giant cells. Plant J Cell Mol Biol 61:698–712

    CAS  Google Scholar 

  • Baxter A, Mittler R, Suzuki N (2014) ROS as key players in plant stress signalling. J Exp Bot 65:1229–1240

    CAS  PubMed  Google Scholar 

  • Bellin D, Asai S, Delledonne M, Yoshioka H (2013) Nitric oxide as a mediator for defense responses. Mol Plant-Microbe Interact MPMI 26:271–277

    CAS  Google Scholar 

  • Bhattarai KK, Li Q, Liu Y, Dinesh-Kumar SP, Kaloshian I (2007) The MI-1-mediated pest resistance requires Hsp90 and Sgt1. Plant Physiol 144:312–323

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bhattarai KK, Xie QG, Mantelin S, Bishnoi U, Girke T, Navarre DA, Kaloshian I (2008) Tomato susceptibility to root-knot nematodes requires an intact jasmonic acid signaling pathway. Mol Plant-Microbe InteractMPMI 21:1205–1214

    CAS  Google Scholar 

  • Bhattarai KK, Atamian HS, Kaloshian I, Eulgem T (2010) WRKY72-type transcription factors contribute to basal immunity in tomato and Arabidopsis as well as gene-for-gene resistance mediated by the tomato R gene Mi-1. Plant J Cell Mol Biol 63:229–240

    CAS  Google Scholar 

  • Bleve-Zacheo T, Bongiovanni M, Melillo MT, Castagnone-Sereno P (1998) The pepper resistance genes Me1 and Me3 induce differential penetration rates and temporal sequences of root cell ultrastructural changes upon nematode infection. Plant Sci 133:79–90

    CAS  Google Scholar 

  • Branch C, Hwang CF, Navarre DA, Williamson VM (2004) Salicylic acid is part of the Mi-1-mediated defense response to root-knot nematode in tomato. Mol Plant-Microbe Interact MPMI 17:351–356

    CAS  Google Scholar 

  • Budahn H, Peterka H, Mousa MAA, Ding YH, Zhang SS, Li JB (2009) Molecular mapping in oil radish (Raphanus sativus L.) and QTL analysis of resistance against beet cyst nematode (Heterodera schachtii). Theor Appl Genet 118:775–782

    PubMed  Google Scholar 

  • Cabrera J, Diaz-Manzano FE, Sanchez M, Rosso MN, Melillo T, Goh T, Fukaki H, Cabello S, Hofmann J, Fenoll C, Escobar C (2014) A role for LATERAL ORGAN BOUNDARIES-DOMAIN 16 during the interaction Arabidopsis-Meloidogyne spp. provides a molecular link between lateral root and root-knot nematode feeding site development. New Phytol 203:632–645

    CAS  PubMed  Google Scholar 

  • Cai D (1997) Positional cloning of a gene for nematode resistance in sugar beet. Science 275:832–834

    CAS  PubMed  Google Scholar 

  • Charlton WL, Harel HY, Bakhetia M, Hibbard JK, Atkinson HJ, McPherson MJ (2010) Additive effects of plant expressed double-stranded RNAs on root-knot nematode development. Int J Parasitol 40:855–864

    CAS  PubMed  Google Scholar 

  • Chen R, Li H, Zhang L, Zhang J, Xiao J, Ye Z (2007) CaMi, a root-knot nematode resistance gene from hot pepper (Capsium annuum L.) confers nematode resistance in tomato. Plant Cell Rep 26:895–905

    CAS  PubMed  Google Scholar 

  • Claverie M, Dirlewanger E, Bosselut N, Van Ghelder C, Voisin R, Kleinhentz M, Lafargue B, Abad P, Rosso MN, Chalhoub B, Esmenjaud D (2011) The Ma gene for complete-spectrum resistance to Meloidogyne species in Prunus is a TNL with a huge repeated C-terminal post-LRR region. Plant Physiol 156:779–792

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cook DE, Lee TG, Guo X, Melito S, Wang K, Bayless AM, Wang J, Hughes TJ, Willis DK, Clemente TE, Diers BW, Jiang J, Hudson ME, Bent AF (2012) Copy number variation of multiple genes at Rhg1 mediates nematode resistance in soybean. Science 338:1206–1209

    CAS  PubMed  Google Scholar 

  • Cook DE, Bayless AM, Wang K, Guo X, Song Q, Jiang J, Bent AF (2014) Distinct copy number, coding sequence, and locus methylation patterns underlie Rhg1-mediated soybean resistance to soybean cyst nematode. Plant Physiol 165:630–647

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cooper WR, Jia L, Goggin L (2005) Effects of jasmonate-induced defenses on root-knot nematode infection of resistant and susceptible tomato cultivars. J Chem Ecol 31:1953–1967

    CAS  PubMed  Google Scholar 

  • Dalzell JJ, Warnock ND, Stevenson MA, Mousley A, Fleming CC, Maule AG (2010) Short interfering RNA-mediated knockdown of drosha and pasha in undifferentiated Meloidogyne incognita eggs leads to irregular growth and embryonic lethality. Int J Parasitol 40:1303–1310

    CAS  PubMed  Google Scholar 

  • de Majnik J, Ogbonnaya FC, Moullet O, Lagudah ES (2003) The Cre1 and Cre3 nematode resistance genes are located at homeologous loci in the wheat genome. Mol Plant Microbe Interact 16:1129–1134

    PubMed  Google Scholar 

  • Dighe ND, Robinson AF, Bell AA, Menz MA, Cantrell RG, Stelly DM (2009) Linkage mapping of resistance to reniform nematode in cotton following introgression from gossypium longicalyx (Hutch. & Lee). Crop Sci 49:1151–1164

    CAS  Google Scholar 

  • Djian-Caporalino C, Pijarowski L, Fazari A, Samson M, Gaveau L, O’Byrne C, Lefebvre V, Caranta C, Palloix A, Abad P (2001) High-resolution genetic mapping of the pepper (Capsicum annuum L.) resistance loci Me-3 and Me-4 conferring heat-stable resistance to root-knot nematodes (Meloidogyne spp.). Theor Appl Genet 103:592–600

    CAS  Google Scholar 

  • Djian-Caporalino C, Fazari A, Arguel MJ, Vernie T, VandeCasteele C, Faure I, Brunoud G, Pijarowski L, Palloix A, Lefebvre V, Abad P (2007) Root-knot nematode (Meloidogyne spp.) Me resistance genes in pepper (Capsicum annuum L.) are clustered on the P9 chromosome. Theor Appl Genet 114:473–486

    CAS  PubMed  Google Scholar 

  • 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. Int J Parasitol 41:385–396

    CAS  PubMed  Google Scholar 

  • Ernst K, Kumar A, Kriseleit D, Kloos DU, Phillips MS, Ganal MW (2002) The broad-spectrum potato cyst nematode resistance gene (Hero) from tomato is the only member of a large gene family of NBS-LRR genes with an unusual amino acid repeat in the LRR region. Plant J Cell Mol Biol 31:127–136

    CAS  Google Scholar 

  • Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10:366–371

    CAS  PubMed  Google Scholar 

  • Fahlgren N, Montgomery TA, Howell MD, Allen E, Dvorak SK, Alexander AL, Carrington JC (2006) Regulation of AUXIN RESPONSE FACTOR3 by TAS3 ta-siRNA affects developmental timing and patterning in Arabidopsis. Curr Biol CB 16:939–944

    CAS  Google Scholar 

  • Fairbairn DJ, Cavallaro AS, Bernard M, Mahalinga-Iyer J, Graham MW, Botella JR (2007) Host-delivered RNAi: an effective strategy to silence genes in plant parasitic nematodes. Planta 226:1525–1533

    CAS  PubMed  Google Scholar 

  • Fei Q, Xia R, Meyers BC (2013) Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks. Plant Cell 25:2400–2415

    CAS  PubMed Central  PubMed  Google Scholar 

  • Feng B, Shan L (2014) ROS open roads to roundworm infection. Sci Signal 7:pe10

    PubMed  Google Scholar 

  • Finkers-Tomczak A, Danan S, van Dijk T, Beyene A, Bouwman L, Overmars H, van Eck H, Goverse A, Bakker J, Bakker E (2009) A high-resolution map of the Grp1 locus on chromosome V of potato harbouring broad-spectrum resistance to the cyst nematode species Globodera pallida and Globodera rostochiensis. Theor Appl Genet 119:165–173

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fudali SL, Wang C, Williamson VM (2013) Ethylene signaling pathway modulates attractiveness of host roots to the root-knot nematode Meloidogyne hapla. Mol Plant-Microbe Interact MPMI 26:75–86

    CAS  Google Scholar 

  • Fujimoto T, Tomitaka Y, Abe H, Tsuda S, Futai K, Mizukubo T (2011) Expression profile of jasmonic acid-induced genes and the induced resistance against the root-knot nematode (Meloidogyne incognita) in tomato plants (Solanum lycopersicum) after foliar treatment with methyl jasmonate. J Plant Physiol 168:1084–1097

    CAS  PubMed  Google Scholar 

  • Fuller VL, Lilley CJ, Urwin PE (2008) Nematode resistance. New Phytol 180:27–44

    CAS  PubMed  Google Scholar 

  • Gao X, Starr J, Gobel C, Engelberth J, Feussner I, Tumlinson J, Kolomiets M (2008) Maize 9-lipoxygenase ZmLOX3 controls development, root-specific expression of defense genes, and resistance to root-knot nematodes. Mol Plant-Microbe Interact MPMI 21:98–109

    CAS  Google Scholar 

  • Gleason CA, Liu QL, Williamson VM (2008) Silencing a candidate nematode effector gene corresponding to the tomato resistance gene Mi-1 leads to acquisition of virulence. Mol Plant-Microbe Interact MPMI 21:576–585

    CAS  Google Scholar 

  • Glowacki S, Macioszek VK, Kononowicz AK (2011) R proteins as fundamentals of plant innate immunity. Cell Mol Biol Lett 16:1–24

    CAS  PubMed  Google Scholar 

  • Goverse A, Smant G (2013) The activation and suppression of plant innate immunity by parasitic nematodes. Annu Rev Phytopathol 52:243–265

  • 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 MPMI 13:1121–1129

    CAS  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

    CAS  PubMed Central  PubMed  Google Scholar 

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

    PubMed Central  PubMed  Google Scholar 

  • Gutierrez OA, Robinson AF, Jenkins JN, McCarty JC, Wubben MJ, Callahan FE, Nichols RL (2011) Identification of QTL regions and SSR markers associated with resistance to reniform nematode in Gossypium barbadense L. accession GB713. Theor Appl Genet 122:271–280

    PubMed  Google Scholar 

  • Hauge BM, Wang Ming L, Parsons Jeremy D, Parnell Laurence D (2001) Soybean cyst nematode (SCN) resistance loci RHG1 AND RHG4. In. Monsanto Technology LLC, St. Louis

    Google Scholar 

  • He P, Shan L, Sheen J (2007) Elicitation and suppression of microbe-associated molecular pattern-triggered immunity in plant-microbe interactions. Cell Microbiol 9:1385–1396

    CAS  PubMed  Google Scholar 

  • Hewezi T, Baum TJ (2013) Manipulation of plant cells by cyst and root-knot nematode effectors. Mol Plant-Microbe Interact MPMI 26:9–16

    CAS  Google Scholar 

  • Hewezi T, Howe P, Maier TR, Baum TJ (2008) Arabidopsis small RNAs and their targets during cyst nematode parasitism. Mol Plant-Microbe Interact MPMI 21:1622–1634

    CAS  Google Scholar 

  • Hewezi T, Howe PJ, Maier TR, Hussey RS, Mitchum MG, Davis EL, Baum TJ (2010) Arabidopsis spermidine synthase is targeted by an effector protein of the cyst nematode Heterodera schachtii. Plant Physiol 152:968–984

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hewezi T, Maier TR, Nettleton D, Baum TJ (2012) The Arabidopsis microRNA396-GRF1/GRF3 regulatory module acts as a developmental regulator in the reprogramming of root cells during cyst nematode infection. Plant Physiol 159:321–335

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hewezi T, Piya S, Richard G, Rice JH (2014) Spatial and temporal expression patterns of auxin response transcription factors in the syncytium induced by the beet cyst nematode Heterodera schachtii in Arabidopsis. Molecular plant pathology

  • Hogenhout SA, Van der Hoorn RA, Terauchi R, Kamoun S (2009) Emerging concepts in effector biology of plant-associated organisms. Molecular plant-microbe interactions : MPMI 22:115–122

    CAS  PubMed  Google Scholar 

  • Hwang CF, Williamson VM (2003) Leucine-rich repeat-mediated intramolecular interactions in nematode recognition and cell death signaling by the tomato resistance protein Mi. The Plant journal : for cell and molecular biology 34:585–593

    CAS  Google Scholar 

  • Hwang CF, Bhakta AV, Truesdell GM, Pudlo WM, Williamson VM (2000) Evidence for a role of the N terminus and leucine-rich repeat region of the Mi gene product in regulation of localized cell death. Plant Cell 12:1319–1329

    CAS  PubMed Central  PubMed  Google Scholar 

  • Iberkleid I, Vieira P, de Almeida Engler J, Firester K, Spiegel Y, Horowitz SB (2013) Fatty acid-and retinol-binding protein, Mj-FAR-1 induces tomato host susceptibility to root-knot nematodes. PLoS ONE 8:e64586

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ithal N, Recknor J, Nettleton D, Maier T, Baum TJ, Mitchum MG (2007) Developmental transcript profiling of cyst nematode feeding cells in soybean roots. Molecular plant-microbe interactions : MPMI 20:510–525

    CAS  PubMed  Google Scholar 

  • Ji H, Gheysen G, Denil S, Lindsey K, Topping JF, Nahar K, Haegeman A, De Vos WH, Trooskens G, Van Criekinge W, De Meyer T, Kyndt T (2013) Transcriptional analysis through RNA sequencing of giant cells induced by Meloidogyne graminicola in rice roots. J Exp Bot 64:3885–3898

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    CAS  PubMed  Google Scholar 

  • Kandoth PK, Ithal N, Recknor J, Maier T, Nettleton D, Baum TJ, Mitchum MG (2011) The Soybean Rhg1 locus for resistance to the soybean cyst nematode Heterodera glycines regulates the expression of a large number of stress- and defense-related genes in degenerating feeding cells. Plant Physiol 155:1960–1975

    CAS  PubMed Central  PubMed  Google Scholar 

  • Karczmarek A, Overmars H, Helder J, Goverse A (2004) Feeding cell development by cyst and root-knot nematodes involves a similar early, local and transient activation of a specific auxin-inducible promoter element. Molecular plant pathology 5:343–346

    CAS  PubMed  Google Scholar 

  • Katiyar-Agarwal S, Jin H (2010) Role of small RNAs in host-microbe interactions. Annu Rev Phytopathol 48:225–246

    CAS  PubMed Central  PubMed  Google Scholar 

  • Khallouk S, Voisin R, Van Ghelder C, Engler G, Amiri S, Esmenjaud D (2011) Histological mechanisms of the resistance conferred by the Ma gene against Meloidogyne incognita in Prunus spp. Phytopathology 101:945–951

    CAS  PubMed  Google Scholar 

  • Klink VP, Overall CC, Alkharouf NW, MacDonald MH, Matthews BF (2007) Laser capture microdissection (LCM) and comparative microarray expression analysis of syncytial cells isolated from incompatible and compatible soybean (Glycine max) roots infected by the soybean cyst nematode (Heterodera glycines). Planta 226:1389–1409

    CAS  PubMed  Google Scholar 

  • Klink VP, Kim KH, Martins V, Macdonald MH, Beard HS, Alkharouf NW, Lee SK, Park SC, Matthews BF (2009) A correlation between host-mediated expression of parasite genes as tandem inverted repeats and abrogation of development of female Heterodera glycines cyst formation during infection of Glycine max. Planta 230:53–71

    CAS  PubMed  Google Scholar 

  • Kyndt T, Nahar K, Haegeman A, De Vleesschauwer D, Hofte M, Gheysen G (2012) Comparing systemic defence-related gene expression changes upon migratory and sedentary nematode attack in rice. Plant biology 14(Suppl 1):73–82

    CAS  PubMed  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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li J, Todd TC, Oakley TR, Lee J, Trick HN (2010) Host-derived suppression of nematode reproductive and fitness genes decreases fecundity of Heterodera glycines Ichinohe. Planta 232:775–785

    CAS  PubMed  Google Scholar 

  • Li F, Pignatta D, Bendix C, Brunkard JO, Cohn MM, Tung J, Sun H, Kumar P, Baker B (2012a) MicroRNA regulation of plant innate immune receptors. Proc Natl Acad Sci USA 109:1790–1795

    CAS  PubMed Central  PubMed  Google Scholar 

  • Li X, Wang X, Zhang S, Liu D, Duan Y, Dong W (2012b) Identification of soybean microRNAs involved in soybean cyst nematode infection by deep sequencing. PLoS ONE 7:e39650

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lin J, Mazarei M, Zhao N, Zhu JJ, Zhuang X, Liu W, Pantalone VR, Arelli PR, Stewart CN Jr, Chen F (2013) Overexpression of a soybean salicylic acid methyltransferase gene confers resistance to soybean cyst nematode. Plant Biotechnol J 11:1135–1145

    CAS  PubMed  Google Scholar 

  • Liu Q, Chen YQ (2009) Insights into the mechanism of plant development: interactions of miRNAs pathway with phytohormone response. Biochemical and biophysical research communications 384:1–5

    CAS  PubMed  Google Scholar 

  • Liu S, Kandoth PK, Warren SD, Yeckel G, Heinz R, Alden J, Yang C, Jamai A, El-Mellouki T, Juvale PS, Hill J, Baum TJ, Cianzio S, Whitham SA, Korkin D, Mitchum MG, Meksem K (2012) A soybean cyst nematode resistance gene points to a new mechanism of plant resistance to pathogens. Nature 492:256–260

    CAS  PubMed  Google Scholar 

  • 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 : for cell and molecular biology 38:203–214

    CAS  Google Scholar 

  • Lorieux M, Reversat G, Diaz SXG, Denance C, Jouvenet N, Orieux Y, Bourger N, Pando-Bahuon A, Ghesquiere A (2003) Linkage mapping of Hsa-1(Og), a resistance gene of African rice to the cyst nematode, Heterodera sacchari. Theor Appl Genet 107:691–696

    CAS  PubMed  Google Scholar 

  • Lukasik-Shreepaathy E, Slootweg E, Richter H, Goverse A, Cornelissen BJ, Takken FL (2012) Dual regulatory roles of the extended N terminus for activation of the tomato MI-1.2 resistance protein. Molecular plant-microbe interactionsq: MPMI 25:1045–1057

    CAS  PubMed  Google Scholar 

  • Luzzi BM, Boerma HR, Hussey RS (1994) A GENE FOR RESISTANCE TO THE SOUTHERN ROOT-KNOT NEMATODE IN SOYBEAN. J Hered 85:484–486

    Google Scholar 

  • Mantelin S, Bhattarai KK, Jhaveri TZ, Kaloshian I (2013) Mi-1-mediated resistance to Meloidogyne incognita in tomato may not rely on ethylene but hormone perception through ETR3 participates in limiting nematode infection in a susceptible host. PLoS ONE 8:e63281

    CAS  PubMed Central  PubMed  Google Scholar 

  • Marin E, Jouannet V, Herz A, Lokerse AS, Weijers D, Vaucheret H, Nussaume L, Crespi MD, Maizel A (2010) miR390, Arabidopsis TAS3 tasiRNAs, and their AUXIN RESPONSE FACTOR targets define an autoregulatory network quantitatively regulating lateral root growth. Plant Cell 22:1104–1117

    CAS  PubMed Central  PubMed  Google Scholar 

  • Martinez de Ilarduya O, Nombela G, Hwang CF, Williamson VM, Muniz M, Kaloshian I (2004) Rme1 is necessary for Mi-1-mediated resistance and acts early in the resistance pathway. Molecular plant-microbe interactions : MPMI 17:55–61

    PubMed  Google Scholar 

  • Matthews BF, Beard H, MacDonald MH, Kabir S, Youssef RM, Hosseini P, Brewer E (2013) Engineered resistance and hypersusceptibility through functional metabolic studies of 100 genes in soybean to its major pathogen, the soybean cyst nematode. Planta 237:1337–1357

    CAS  PubMed Central  PubMed  Google Scholar 

  • Matthews BF, Beard H, Brewer E, Kabir S, MacDonald MH, Youssef RM (2014) Arabidopsis genes, AtNPR1, AtTGA2 and AtPR-5, confer partial resistance to soybean cyst nematode (Heterodera glycines) when overexpressed in transgenic soybean roots. BMC Plant Biol 14:96

    PubMed Central  PubMed  Google Scholar 

  • Mazarei M, Puthoff DP, Hart JK, Rodermel SR, Baum TJ (2002) Identification and characterization of a soybean ethylene-responsive element-binding protein gene whose mRNA expression changes during soybean cyst nematode infection. Molecular plant-microbe interactions : MPMI 15:577–586

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Mazarei M, Elling AA, Maier TR, Puthoff DP, Baum TJ (2007) GmEREBP1 is a transcription factor activating defense genes in soybean and Arabidopsis. Molecular plant-microbe interactions : MPMI 20:107–119

    CAS  PubMed  Google Scholar 

  • Mazarei M, Liu W, Al-Ahmad H, Arelli PR, Pantalone VR, Stewart CN Jr (2011) Gene expression profiling of resistant and susceptible soybean lines infected with soybean cyst nematode. TAG Theoretical and applied genetics Theoretische und angewandte Genetik 123:1193–1206

    CAS  PubMed  Google Scholar 

  • 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. The New phytologist 170:501–512

    CAS  PubMed  Google Scholar 

  • Melillo MT, Leonetti P, Leone A, Veronico P, Bleve-Zacheo T (2011) ROS and NO production in compatible and incompatible tomato-Meloidogyne incognita interactions. Eur J Plant Pathol 130:489–502

    CAS  Google Scholar 

  • Melito S, Heuberger AL, Cook D, Diers BW, MacGuidwin AE, Bent AF (2010) A nematode demographics assay in transgenic roots reveals no significant impacts of the Rhg1 locus LRR-Kinase on soybean cyst nematode resistance. BMC Plant Biol 10:104

    PubMed Central  PubMed  Google Scholar 

  • Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM (1998) The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10:1307–1319

    CAS  PubMed Central  PubMed  Google Scholar 

  • Mitchum MG, Hussey RS, Baum TJ, Wang X, Elling AA, Wubben M, Davis EL (2013) Nematode effector proteins: an emerging paradigm of parasitism. The New phytologist 199:879–894

    PubMed  Google Scholar 

  • Molinari S, Fanelli E, Leonetti P (2013) Expression of tomato salicylic acid (SA)-responsive pathogenesis-related genes in Mi-1-mediated and SA-induced resistance to root-knot nematodes. Molecular plant pathology

  • Mosblech A, Feussner I, Heilmann I (2009) Oxylipins: structurally diverse metabolites from fatty acid oxidation. Plant physiology and biochemistry: PPB/Societe francaise de physiologie vegetale 47:511–517

    CAS  Google Scholar 

  • Nahar K, Kyndt T, De Vleesschauwer D, Hofte M, Gheysen G (2011) The jasmonate pathway is a key player in systemically induced defense against root knot nematodes in rice. Plant Physiol 157:305–316

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nombela G, Williamson VM, Muniz M (2003) The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Molecular plant-microbe interactions: MPMI 16:645–649

    CAS  PubMed  Google Scholar 

  • Ozalvo R, Cabrera J, Escobar C, Christensen SA, Borrego EJ, Kolomiets MV, Castresana C, Iberkleid I, Brown Horowitz S (2013) Two closely related members of Arabidopsis 13-lipoxygenases (13-LOXs), LOX3 and LOX4, reveal distinct functions in response to plant-parasitic nematode infection. Molecular plant pathology

  • Paal J, Henselewski H, Muth J, Meksem K, Menendez CM, Salamini F, Ballvora A, Gebhardt C (2004) Molecular cloning of the potato Gro1-4 gene conferring resistance to pathotype Ro1 of the root cyst nematode Globodera rostochiensis, based on a candidate gene approach. The Plant journal : for cell and molecular biology 38:285–297

    CAS  Google Scholar 

  • Park SW, Kaimoyo E, Kumar D, Mosher S, Klessig DF (2007) Methyl salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318:113–116

    CAS  PubMed  Google Scholar 

  • Parkhi V, Kumar V, Campbell LM, Bell AA, Shah J, Rathore KS (2010) Resistance against various fungal pathogens and reniform nematode in transgenic cotton plants expressing Arabidopsis NPR1. Transgenic Res 19:959–975

    CAS  PubMed  Google Scholar 

  • Portillo M, Cabrera J, Lindsey K, Topping J, Andres MF, Emiliozzi M, Oliveros JC, Garcia-Casado G, Solano R, Koltai H, Resnick N, Fenoll C, Escobar C (2013) Distinct and conserved transcriptomic changes during nematode-induced giant cell development in tomato compared with Arabidopsis: a functional role for gene repression. The New phytologist 197:1276–1290

    CAS  PubMed  Google Scholar 

  • Priya DB, Somasekhar N, Prasad J, Kirti P (2011) Transgenic tobacco plants constitutively expressing Arabidopsis NPR1 show enhanced resistance to root-knot nematode. Meloidogyne incognita. BMC research notes 4:231

    Google Scholar 

  • Qiao Y, Liu L, Xiong Q, Flores C, Wong J, Shi J, Wang X, Liu X, Xiang Q, Jiang S, Zhang F, Wang Y, Judelson HS, Chen X, Ma W (2013) Oomycete pathogens encode RNA silencing suppressors. Nat Genet 45:330–333

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ray PD, Huang BW, Tsuji Y (2012) Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 24:981–990

    CAS  PubMed Central  PubMed  Google Scholar 

  • Robinson AF (2007) Reniform in U.S. cotton: when, where, why, and some remedies. Annu Rev Phytopathol 45:263–288

    CAS  PubMed  Google Scholar 

  • Romano GB, Sacks EJ, Stetina SR, Robinson AF, Fang DD, Gutierrez OA, Scheffler JA (2009) Identification and genomic location of a reniform nematode (Rotylenchulus reniformis) resistance locus (Ren (ari)) introgressed from Gossypium aridum into upland cotton (G. hirsutum). Theor Appl Genet 120:139–150

    PubMed Central  PubMed  Google Scholar 

  • Ruiz-Ferrer V, Voinnet O (2009) Roles of plant small RNAs in biotic stress responses. Annu Rev Plant Biol 60:485–510

    CAS  PubMed  Google Scholar 

  • Sacco MA, Koropacka K, Grenier E, Jaubert MJ, Blanchard A, Goverse A, Smant G, Moffett P (2009) The cyst nematode SPRYSEC protein RBP-1 elicits Gpa2- and RanGAP2-dependent plant cell death. PLoS Pathog 5:e1000564

    PubMed Central  PubMed  Google Scholar 

  • Sahu PP, Pandey G, Sharma N, Puranik S, Muthamilarasan M, Prasad M (2013) Epigenetic mechanisms of plant stress responses and adaptation. Plant Cell Rep 32:1151–1159

    CAS  PubMed  Google Scholar 

  • Schwessinger B, Zipfel C (2008) News from the frontline: recent insights into PAMP-triggered immunity in plants. Curr Opin Plant Biol 11:389–395

    CAS  PubMed  Google Scholar 

  • Seifi A, Kaloshian I, Vossen J, Che DD, Bhattarai KK, Fan JM, Naher Z, Goverse A, Tjallingii WF, Lindhout P, Visser RGF, Bai YL (2011) Linked, if Not the Same, Mi-1 Homologues Confer Resistance to Tomato Powdery Mildew and Root-Knot Nematodes. Mol Plant Microbe Interact 24:441–450

    CAS  PubMed  Google Scholar 

  • Semblat JP, Rosso MN, Hussey RS, Abad P, Castagnone-Sereno P (2001) Molecular cloning of a cDNA encoding an amphid-secreted putative avirulence protein from the root-knot nematode Meloidogyne incognita. Molecular plant-microbe interactions: MPMI 14:72–79

    CAS  PubMed  Google Scholar 

  • Shen XL, Van Becelaere G, Kumar P, Davis RF, May OL, Chee P (2006) QTL mapping for resistance to root-knot nematodes in the M-120 RNR Upland cotton line (Gossypium hirsutum L.) of the Auburn 623 RNR source. Theor Appl Genet 113:1539–1549

    CAS  PubMed  Google Scholar 

  • Shirasu K (2009) The HSP90-SGT1 chaperone complex for NLR immune sensors. Annu Rev Plant Biol 60:139–164

    CAS  PubMed  Google Scholar 

  • Shivaprasad PV, Chen HM, Patel K, Bond DM, Santos BA, Baulcombe DC (2012) A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell 24:859–874

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shukla LI, Chinnusamy V, Sunkar R (2008) The role of microRNAs and other endogenous small RNAs in plant stress responses. Biochim Biophys Acta 1779:743–748

    CAS  PubMed  Google Scholar 

  • Siddique S, Matera C, Radakovic ZS, Hasan MS, Gutbrod P, Rozanska E, Sobczak M, Torres MA, Grundler FM (2014) Parasitic worms stimulate host NADPH oxidases to produce reactive oxygen species that limit plant cell death and promote infection. Science signaling 7:ra33

  • Sobczak M, Avrova A, Jupowicz J, Phillips MS, Ernst K, Kumar A (2005) Characterization of susceptibility and resistance responses to potato cyst nematode (Globodera spp.) infection of tomato lines in the absence and presence of the broad-spectrum nematode resistance Hero gene. Molecular plant-microbe interactions: MPMI 18:158–168

    CAS  PubMed  Google Scholar 

  • Tameling WI, Elzinga SD, Darmin PS, Vossen JH, Takken FL, Haring MA, Cornelissen BJ (2002) The tomato R gene products I-2 and MI-1 are functional ATP binding proteins with ATPase activity. Plant Cell 14:2929–2939

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tripathy BC, Oelmuller R (2012) Reactive oxygen species generation and signaling in plants. Plant signaling & behavior 7:1621–1633

    CAS  Google Scholar 

  • Tucker ML, Xue P, Yang R (2010) 1-Aminocyclopropane-1-carboxylic acid (ACC) concentration and ACC synthase expression in soybean roots, root tips, and soybean cyst nematode (Heterodera glycines)-infected roots. J Exp Bot 61:463–472

    CAS  PubMed Central  PubMed  Google Scholar 

  • Uehara T, Sugiyama S, Matsuura H, Arie T, Masuta C (2010) Resistant and susceptible responses in tomato to cyst nematode are differentially regulated by salicylic acid. Plant Cell Physiol 51:1524–1536

    CAS  PubMed  Google Scholar 

  • van der Voort J, Janssen GJW, Overmars H, van Zandvoort PM, van Norel A, Scholten OE, Janssen R, Bakker J (1999) Development of a PCR-based selection assay for root-knot nematode resistance (Rmc1) by a comparative analysis of the Solanum bulbocastanum and S-tuberosum genome. Euphytica 106:187–195

    Google Scholar 

  • van der Vossen EA, van der Voort JN, Kanyuka K, Bendahmane A, Sandbrink H, Baulcombe DC, Bakker J, Stiekema WJ, Klein-Lankhorst RM (2000) Homologues of a single resistance-gene cluster in potato confer resistance to distinct pathogens: a virus and a nematode. The Plant journal: for cell and molecular biology 23:567–576

    Google Scholar 

  • Vlot AC, Dempsey DA, Klessig DF (2009) Salicylic Acid, a multifaceted hormone to combat disease. Annu Rev Phytopathol 47:177–206

    CAS  PubMed  Google Scholar 

  • Vos P, Simons G, Jesse T, Wijbrandi J, Heinen L, Hogers R, Frijters A, Groenendijk J, Diergaarde P, Reijans M, Fierens-Onstenk J, de Both M, Peleman J, Liharska T, Hontelez J, Zabeau M (1998) The tomato Mi-1 gene confers resistance to both root-knot nematodes and potato aphids. Nat Biotechnol 16:1365–1369

    CAS  PubMed  Google Scholar 

  • Wang KL, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14(Suppl):S131–S151

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang C, Ulloa M, Roberts PA (2006) Identification and mapping of microsatellite markers linked to a root-knot nematode resistance gene (rkn1) in Acala NemX cotton (Gossypium hirsutum L.). Theor Appl Genet 112:770–777

    CAS  PubMed  Google Scholar 

  • Wang X, Replogle A, Davis EL, Mitchum MG (2007) The tobacco Cel7 gene promoter is auxin-responsive and locally induced in nematode feeding sites of heterologous plants. Molecular plant pathology 8:423–436

    CAS  PubMed  Google Scholar 

  • Williamson VM (1999) Plant nematode resistance genes. Curr Opin Plant Biol 2:327–331

    CAS  PubMed  Google Scholar 

  • Williamson VM, Gleason CA (2003) Plant–nematode interactions. Curr Opin Plant Biol 6:327–333

    CAS  PubMed  Google Scholar 

  • Williamson VM, Kumar A (2006) Nematode resistance in plants: the battle underground. Trends in genetics : TIG 22:396–403

    CAS  PubMed  Google Scholar 

  • Wu Y, Zhang D, Chu JY, Boyle P, Wang Y, Brindle ID, De Luca V, Despres C (2012) The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid. Cell reports 1:639–647

    CAS  PubMed  Google Scholar 

  • Wubben MJ 2nd, Su H, Rodermel SR, Baum TJ (2001) Susceptibility to the sugar beet cyst nematode is modulated by ethylene signal transduction in Arabidopsis thaliana. Molecular plant-microbe interactions: MPMI 14:1206–1212

    CAS  PubMed  Google Scholar 

  • Wubben MJ 2nd, Rodermel SR, Baum TJ (2004) Mutation of a UDP-glucose-4-epimerase alters nematode susceptibility and ethylene responses in Arabidopsis roots. The Plant journal : for cell and molecular biology 40:712–724

    CAS  Google Scholar 

  • Wubben MJ, Jin J, Baum TJ (2008) Cyst nematode parasitism of Arabidopsis thaliana is inhibited by salicylic acid (SA) and elicits uncoupled SA-independent pathogenesis-related gene expression in roots. Molecular plant-microbe interactions : MPMI 21:424–432

    CAS  PubMed  Google Scholar 

  • Yaghoobi J, Yates JL, Williamson VM (2005) Fine mapping of the nematode resistance gene Mi-3 in Solanum peruvianum and construction of a S-lycopersicum DNA contig spanning the locus. Mol Genet Genomics 274:60–69

    CAS  PubMed  Google Scholar 

  • Yoon EK, Yang JH, Lim J, Kim SH, Kim SK, Lee WS (2010) Auxin regulation of the microRNA390-dependent transacting small interfering RNA pathway in Arabidopsis lateral root development. Nucleic Acids Res 38:1382–1391

    CAS  PubMed Central  PubMed  Google Scholar 

  • Youssef RM, MacDonald MH, Brewer EP, Bauchan GR, Kim KH, Matthews BF (2013) Ectopic expression of AtPAD4 broadens resistance of soybean to soybean cyst and root-knot nematodes. BMC Plant Biol 13:67

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yu LZ, Wu XQ, Ye JR, Zhang SN, Wang C (2012) NOS-like-mediated nitric oxide is involved in Pinus thunbergii response to the invasion of Bursaphelenchus xylophilus. Plant Cell Rep 31:1813–1821

    CAS  PubMed  Google Scholar 

  • Zhai J, Jeong DH, De Paoli E, Park S, Rosen BD, Li Y, Gonzalez AJ, Yan Z, Kitto SL, Grusak MA, Jackson SA, Stacey G, Cook DR, Green PJ, Sherrier DJ, Meyers BC (2011) MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev 25:2540–2553

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhu QH, Fan L, Liu Y, Xu H, Llewellyn D, Wilson I (2013) miR482 regulation of NBS-LRR defense genes during fungal pathogen infection in cotton. PLoS ONE 8:e84390

    PubMed Central  PubMed  Google Scholar 

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Acknowledgments

The authors would like to thank Alabama Cotton Commission, Cotton Inc,, and the Alabama Agricultural Experimental Station for research support for this work. Additionally, the financial support from the Auburn University Department of Biological Sciences and the Auburn University Cellular and Molecular Biosciences Program to Ruijuan Li during her graduate program is gratefully acknowledged.

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The authors declare that they have no conflict of interest.

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Communicated by Neal Stewart.

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Li, R., Rashotte, A.M., Singh, N.K. et al. Integrated signaling networks in plant responses to sedentary endoparasitic nematodes: a perspective. Plant Cell Rep 34, 5–22 (2015). https://doi.org/10.1007/s00299-014-1676-6

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