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SlWRKY70 is required for Mi-1-mediated resistance to aphids and nematodes in tomato

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Abstract

Plant resistance (R) gene-mediated defense responses against biotic stresses include vast transcriptional reprogramming. In several plant-pathogen systems, members of the WRKY family of transcription factors have been demonstrated to act as both positive and negative regulators of plant defense transcriptional networks. To identify the possible roles of tomato (Solanum lycopersicum) WRKY transcription factors in defense mediated by the R gene Mi-1 against potato aphid, Macrosiphum euphorbiae, and root-knot nematode (RKN), Meloidogyne javanica, we used tobacco rattle virus (TRV)-based virus-induced gene silencing and transcriptionally suppressed SlWRKY70, a tomato ortholog of the Arabidopsis thaliana WRKY70 gene. Silencing SlWRKY70 attenuated Mi-1-mediated resistance against both potato aphid and RKN showing that SlWRKY70 is required for Mi-1 function. Furthermore, we found SlWRKY70 transcripts to be inducible in response to aphid infestation and RKN inoculation. Mi-1-mediated recognition of these pests modulates this transcriptional response. As previously described for AtWRKY70, we found SlWRKY70 transcript levels to be up-regulated by salicylic acid and suppressed by methyl jasmonate. This indicates that some aspects of WRKY70 regulation are conserved among distantly related eudicots.

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Abbreviations

Avr:

Avirulence

ETI:

Effector-triggered immunity

Hat:

Hours after treatment

JA:

Jasmonic acid

MeJA:

Methyl jasmonate

PAMPs:

Pathogen associated molecular patterns

PRRs:

Pattern recognition receptors

PTI:

PAMP-triggered immunity

R:

Resistance

RKN:

Root-knot nematodes

SA:

Salicylic acid

TFs:

Transcriptions factors

TRV:

Tobacco rattle virus

VIGS:

Virus-induced gene silencing

References

  • Abramovitch RB, Anderson JC, Martin GB (2006) Bacterial elicitation and evasion of plant innate immunity. Nature Rev Mol Cell Biol 7:601–611

    Article  CAS  Google Scholar 

  • Abuqamar S, Chen X, Dhawan R, Bluhm B, Salmeron J, Lam S, Dietrich RA, Mengiste T (2006) Expression profiling and mutant analysis reveals complex regulatory networks involved in Arabidopsis response to Botrytis infection. Plant J 48:28–44

    Article  PubMed  CAS  Google Scholar 

  • Ahmad S, Gordon-Weeks R, Pickett J, Ton J (2010) Natural variation in priming of basal resistance: from evolutionary origin to agricultural exploitation. Mol Plant Pathol 11:817–827

    PubMed  Google Scholar 

  • BenMamoun M (2006) FPRANK: Stata module to compute Two-Sample Fligner-Policello Robust Rank Order Test. Statistical Software Components, S456739. Boston: Department of Economics, Boston College

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

    Article  PubMed  CAS  Google Scholar 

  • Bhattarai KK, Xie QG, Pourshalimi D, Younglove T, Kaloshian I (2007b) Coi1-dependent signaling pathway is not required for Mi-1-mediated potato aphid resistance. Mol Plant Microbe Interact 20:276–282

    Article  PubMed  CAS  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 Interact 21:1205–1214

    Article  PubMed  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 63:229–240

    Article  PubMed  CAS  Google Scholar 

  • Chen C, Chen Z (2000) Isolation and characterization of two pathogen- and salicylic acid-induced genes encoding WRKY DNA-binding proteins from tobacco. Plant Mol Biol 42:387–396

    Article  PubMed  CAS  Google Scholar 

  • Cheng YT, Germain H, Wiermer M, Bi D, Xu F, Garcia AV, Wirthmueller L, Despres C, Parker JE, Zhang Y, Li X (2009) Nuclear pore complex component MOS7/Nup88 is required for innate immunity and nuclear accumulation of defense regulators in Arabidopsis. Plant Cell 21:2503–2516

    Article  PubMed  CAS  Google Scholar 

  • Conrath U, Beckers GJM, Flors V, Garcia-Agustin P, Jakab G, Mauch F, Newman MA, Pieterse CMJ, Poinssot B, Pozo MJ, Pugin A, Schaffrath U, Ton J, Wendehenne D, Zimmerli L, Mauch-Mani B (2006) Priming: getting ready for battle. Mol Plant Microbe Interact 19:1062–1071

    Article  PubMed  CAS  Google Scholar 

  • Ekengren SK, Liu Y, Schiff M, Dinesh-Kumar SP, Martin GB (2003) Two MAPK cascades, NPR1, and TGA transcription factors play a role in Pto-mediated disease resistance in tomato. Plant J 36:905–917

    Article  PubMed  CAS  Google Scholar 

  • Eulgem T (2005) Regulation of the Arabidopsis defense transcriptome. Trends Plant Sci 10:71–78

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206

    Article  PubMed  CAS  Google Scholar 

  • Flor HH (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 9:275–296

    Article  Google Scholar 

  • Fu WJ, Hu J, Spencer T, Carroll R, Wu G (2006) Statistical models in assessing fold change of gene expression in real-time RT-PCR experiments. Comput Biol Chem 30:21–26

    Article  PubMed  CAS  Google Scholar 

  • Glazebrook J, Chen W, Estes B, Chang HS, Nawrath C, Metraux JP, Zhu T, Katagiri F (2003) Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. Plant J 34:217–228

    Article  PubMed  CAS  Google Scholar 

  • Hayward A, Padmanabhan M, Dinesh-Kumar SP (2011) Virus-induced gene silencing in Nicotiana benthamiana and other plant species. Methods Mol Biol 678:55–63

    Article  PubMed  CAS  Google Scholar 

  • Hussey KL (1973) Effects of microsporidan infection on larval trematodes: infection with Nosema strigeoideae or N. echinostomi. J Invertebr Pathol 22:193–198

    Article  PubMed  CAS  Google Scholar 

  • Jaskiewicz M, Conrath U, Peterhansel C (2011) Chromatin modification acts as a memory for systemic acquired resistance in the plant stress response. EMBO Rep 12:50–55

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Knoth C, Ringler J, Dangl JL, Eulgem T (2007) Arabidopsis WRKY70 is required for full RPP4-mediated disease resistance and basal defense against Hyaloperonospora parasitica. Mol Plant Microbe Interact 20:120–128

    Article  PubMed  CAS  Google Scholar 

  • Lambert K, Ferrie B, Nombela G, Brenner E, Williamson V (1999) Identification of genes whose transcripts accumulate rapidly in tomato after root-knot nematode infection. Physiol Mol Plant Pathol 55:341–348

    Article  CAS  Google Scholar 

  • Li J, Brader G, Palva ET (2004) The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 16:319–331

    Article  PubMed  CAS  Google Scholar 

  • Li J, Brader G, Kariola T, Palva ET (2006a) WRKY70 modulates the selection of signaling pathways in plant defense. Plant J 46:477–491

    Article  PubMed  CAS  Google Scholar 

  • Li Q, Xie QG, Smith-Becker J, Navarre DA, Kaloshian I (2006b) Mi-1-Mediated aphid resistance involves salicylic acid and mitogen-activated protein kinase signaling cascades. Mol Plant Microbe Interact 19:655–664

    Article  PubMed  CAS  Google Scholar 

  • Mantelin S, Peng HC, Li B, Atamian HS, Takken FL, Kaloshian I (2011) The receptor-like kinase SlSERK1 is required for Mi-1-mediated resistance to potato aphids in tomato. Plant J 67:459–471

    Article  PubMed  CAS  Google Scholar 

  • Martinez-de IIarduya O, Moore AE, Kaloshian I (2001) The tomato Rme1 locus is required for Mi-mediated resistance to root knot nematodes and the potato aphid. Plant J 27:417–425

    Article  Google Scholar 

  • Mur LA, Kenton P, Atzorn R, Miersch O, Wasternack C (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol 140:249–262

    Article  PubMed  CAS  Google Scholar 

  • Nimchuk Z, Eulgem T, Holt IB, Dangl JL (2003) Recognition and response in the plant immune system. Annu Rev Genet 37:579–609

    Article  PubMed  CAS  Google Scholar 

  • Pan YJ, Cho CC, Kao YY, Sun CH (2009) A novel WRKY-like protein involved in transcriptional activation of cyst wall protein genes in Giardia lamblia. J Biol Chem 284:17975–17988

    Article  PubMed  CAS  Google Scholar 

  • Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150:1648–1655

    Article  PubMed  CAS  Google Scholar 

  • Ramamoorthy R, Jiang SY, Kumar N, Venkatesh PN, Ramachandran S (2008) A comprehensive transcriptional profiling of the WRKY gene family in rice under various abiotic and phytohormone treatments. Plant Cell Physiol 49:865–879

    Article  PubMed  CAS  Google Scholar 

  • Ren CM, Zhu Q, Gao BD, Ke SY, Yu WC, Xie DX, Peng W (2008) Transcription factor WRKY70 displays important but no indispensable roles in jasmonate and salicylic acid signaling. J Integr Plant Biol 50:630–637

    Article  PubMed  CAS  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Ross CA, Liu Y, Shen QJ (2007) The WRKY gene family in rice (Oryza sativa). J Integr Plant Biol 49:827–842

    Article  CAS  Google Scholar 

  • Rushton PJ, Somssich IE (1998) Transcriptonal control of plant genes responsive to pathogens. Curr Opin Plant Biol 1:311–315

    Article  PubMed  CAS  Google Scholar 

  • Ryals JL, Neuenschwander UH, Willits MC, Molina A, Steiner H-Y, Hunt MD (1996) Systemic acquired resistance. Plant Cell 8:1809–1819

    Article  PubMed  CAS  Google Scholar 

  • Shen H, Gold SE, Tamaki SJ, Keen NT (1992) Construction of a Tn7-lux system for gene expression studies in gram-negative bacteria. Gene 122:27–34

    Article  PubMed  CAS  Google Scholar 

  • Singh K, Foley RC, Onate-Sanchez L (2002) Transcription factors in plant defense and stress responses. Curr Opin Plant Biol 5:430–436

    Article  PubMed  CAS  Google Scholar 

  • Skibbe M, Qu N, Galis I, Baldwin IT (2008) Induced plant defenses in the natural environment: Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory. Plant Cell 20:1984–2000

    Article  PubMed  CAS  Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  PubMed  CAS  Google Scholar 

  • Tao Y, Xie Z, Chen W, Glazebrook J, Chang HS, Han B, Zhu T, Zou G, Katagiri F (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:317–330

    Article  PubMed  CAS  Google Scholar 

  • Thomma BPHJ, Eggermont K, Penninckx IAMA, Mauch-Mani B, Vogelsang R, Cammue BPA, Broekaert WF (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA 95:15107–15111

    Article  PubMed  CAS  Google Scholar 

  • Tsuda K, Sato M, Stoddard T, Glazebrook J, Katagiri F (2009) Network properties of robust immunity in plants. PLoS Genet 5:e1000772

    Article  PubMed  Google Scholar 

  • Van Eck L, Schultz T, Leach JE, Scofield SR, Peairs FB, Botha AM, Lapitan NL (2010) Virus-induced gene silencing of WRKY53 and an inducible phenylalanine ammonia-lyase in wheat reduces aphid resistance. Plant Biotechnol J 8:1023–1032

    Article  PubMed  Google Scholar 

  • van Esse HP, Fradin EF, de Groot PJ, de Wit PJ, Thomma BP (2009) Tomato transcriptional responses to a foliar and a vascular fungal pathogen are distinct. Mol Plant Microbe Interact 22:245–258

    Article  PubMed  Google Scholar 

  • Wirthmueller L, Zhang Y, Jones JD, Parker JE (2007) Nuclear accumulation of the Arabidopsis immune receptor RPS4 is necessary for triggering EDS1-dependent defense. Curr Biol 17:2023–2029

    Article  PubMed  CAS  Google Scholar 

  • Yang B, Jiang Y, Rahman MH, Deyholos MK, Kav NN (2009) Identification and expression analysis of WRKY transcription factor genes in canola (Brassica napus L.) in response to fungal pathogens and hormone treatments. BMC Plant Biol 9:68

    Article  PubMed  Google Scholar 

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Acknowledgments

We thank Qi Li for help with VIGS experiments; Dr. Jason Stajich, James Starrett, and Dr. Cheryl Hayashi for help with the phylogenetic analysis; and Dr. S. P. Dinesh-Kumar, University of California Davis, for the TRV-WRKY constructs. This work was supported by grants from the National Science Foundation (grant no. IOB-0543937) and University of California Agricultural Experiment Station to I.K., as well as the National Research Initiative of the USDA Cooperative State Research, Education and Extension Service (grant no. 2008-01098) to T.E. and I.K.

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Authors and Affiliations

  1. Department of Nematology, University of California, 2107A Genomics Building, Riverside, CA, 92521, USA

    Hagop S. Atamian & Isgouhi Kaloshian

  2. Graduate Program in Genetics, Genomics and Bioinformatics, University of California, Riverside, CA, 92521, USA

    Hagop S. Atamian, Thomas Eulgem & Isgouhi Kaloshian

  3. Institute for Integrative Genome Biology, Center for Plant Cell Biology, University of California, Riverside, CA, 92521, USA

    Thomas Eulgem & Isgouhi Kaloshian

  4. Department of Botany and Plant Sciences, University of California, Riverside, CA, 92521, USA

    Thomas Eulgem

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  1. Hagop S. Atamian
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Correspondence to Isgouhi Kaloshian.

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Atamian, H.S., Eulgem, T. & Kaloshian, I. SlWRKY70 is required for Mi-1-mediated resistance to aphids and nematodes in tomato. Planta 235, 299–309 (2012). https://doi.org/10.1007/s00425-011-1509-6

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  • DOI: https://doi.org/10.1007/s00425-011-1509-6

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