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PLOS ONE  2014 

The Beet Cyst Nematode Heterodera schachtii Modulates the Expression of WRKY Transcription Factors in Syncytia to Favour Its Development in Arabidopsis Roots

DOI: 10.1371/journal.pone.0102360

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Abstract:

Cyst nematodes invade the roots of their host plants as second stage juveniles and induce a syncytium which is the only source of nutrients throughout their life. A recent transcriptome analysis of syncytia induced by the beet cyst nematode Heterodera schachtii in Arabidopsis roots has shown that thousands of genes are up-regulated or down-regulated in syncytia as compared to root segments from uninfected plants. Among the down-regulated genes are many which code for WRKY transcription factors. Arabidopsis contains 66 WRKY genes with 59 represented by the ATH1 GeneChip. Of these, 28 were significantly down-regulated and 6 up-regulated in syncytia as compared to control root segments. We have studied here the down-regulated genes WRKY6, WRKY11, WRKY17 and WRKY33 in detail. We confirmed the down-regulation in syncytia with promoter::GUS lines. Using various overexpression lines and mutants it was shown that the down-regulation of these WRKY genes is important for nematode development, probably through interfering with plant defense reactions. In case of WRKY33, this might involve the production of the phytoalexin camalexin.

References

[1]  Abad P, Gouzy J, Aury JM, Castagnone-Sereno P, Danchin EGJ, et al. (2008) Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nature Biotechnol 26: 909–915. doi: 10.1038/nbt.1482
[2]  Sobczak M, Golinowski W (2011) Cyst Nematodes and Syncytia. In: Jones J, Gheysen G, Fenoll C, editors. Genomics and Molecular Genetics of Plant-Nematode Interactions. Dordrecht, Heidelberg, London, New York: Springer Science+Business Media. 61–82.
[3]  Sijmons PC, Grundler FMW, Vonmende N, Burrows PR, Wyss U (1991) Arabidopsis thaliana as a New Model Host for Plant-Parasitic Nematodes. Plant J 1: 245–254. doi: 10.1046/j.1365-313x.1991.00245.x
[4]  Szakasits D, Heinen P, Wieczorek K, Hofmann J, Wagner F, et al. (2009) The transcriptome of syncytia induced by the cyst nematode Heterodera schachtii in Arabidopsis roots. Plant J 57: 771–784. doi: 10.1111/j.1365-313x.2008.03727.x
[5]  Puthoff DP, Nettleton D, Rodermel SR, Baum TJ (2003) Arabidopsis gene expression changes during cyst nematode parasitism revealed by statistical analyses of microarray expression profiles. Plant J 33: 911–921. doi: 10.1046/j.1365-313x.2003.01677.x
[6]  Bar-Or C, Kapulnik Y, Koltai H (2005) A broad characterization of the transcriptional profile of the compatible tomato response to the plant parasitic root knot nematode Meloidogyne javanica. European J Plant Pathol 111: 181–192. doi: 10.1007/s10658-004-2134-z
[7]  Hammes UZ, Schachtman DP, Berg RH, Nielsen E, Koch W, et al. (2005) Nematode-induced changes of transporter gene expression in Arabidopsis roots. Mol Plant-Microbe Interact 18: 1247–1257. doi: 10.1094/mpmi-18-1247
[8]  Jammes F, Lecomte P, de Almeida-Engler J, Bitton F, Martin-Magniette ML, et al. (2005) Genome-wide expression profiling of the host response to root-knot nematode infection in Arabidopsis. Plant J 44: 447–458. doi: 10.1111/j.1365-313x.2005.02532.x
[9]  Barcala M, Garcia A, Cabrera J, Casson S, Lindsey K, et al. (2010) Early transcriptomic events in microdissected Arabidopsis nematode-induced giant cells. Plant J 61: 698–712. doi: 10.1111/j.1365-313x.2009.04098.x
[10]  Goellner M, Wang XH, Davis EL (2001) Endo-beta-1,4-glucanase expression in compatible plant-nematode interactions. Plant Cell 13: 2241–2255. doi: 10.1105/tpc.13.10.2241
[11]  Wieczorek K, Golecki B, Gerdes L, Heinen P, Szakasits D, et al. (2006) Expansins are involved in the formation of nematode-induced syncytia in roots of Arabidopsis thaliana. Plant J 48: 98–112. doi: 10.1111/j.1365-313x.2006.02856.x
[12]  Wieczorek K, Hofmann J, Blochl A, Szakasits D, Bohlmann H, et al. (2008) Arabidopsis endo-1,4-beta-glucanases are involved in the formation of root syncytia induced by Heterodera schachtii. Plant J 53: 336–351. doi: 10.1111/j.1365-313x.2007.03340.x
[13]  Siddique S, Endres S, Atkins JM, Szakasits D, Wieczorek K, et al. (2009) Myo-inositol oxygenase genes are involved in the development of syncytia induced by Heterodera schachtii in Arabidopsis roots. New Phytol 184: 457–472. doi: 10.1111/j.1469-8137.2009.02981.x
[14]  Ali MA, Plattner S, Radakovic Z, Wieczorek K, Elashry A, et al. (2013) An Arabidopsis ATPase gene involved in nematode-induced syncytium development and abiotic stress responses. Plant J. 74: 852–866. doi: 10.1111/tpj.12170
[15]  Ali MA, Abbas A, Kreil DP, Bohlmann H (2013) Overexpression of the transcription factor RAP2.6 leads to enhanced callose deposition in syncytia and enhanced resistance against the beet cyst nematode Heterodera schachtii in Arabidopsis roots. BMC Plant Biol 13: 47. doi: 10.1186/1471-2229-13-47
[16]  Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15: 247–258. doi: 10.1016/j.tplants.2010.02.006
[17]  Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10: 366–371. doi: 10.1016/j.pbi.2007.04.020
[18]  Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150: 1648–1655. doi: 10.1104/pp.109.138990
[19]  Yamasaki K, Kigawa T, Inoue M, Tateno M, Yamasaki T, et al. (2005) Solution structure of an Arabidopsis WRKY DNA binding domain. Plant Cell 17: 944–956. doi: 10.1105/tpc.104.026435
[20]  Popescu SC, Popescu GV, Bachan S, Zhang Z, Gerstein M, et al. (2009) MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes Dev 23: 80–92. doi: 10.1101/gad.1740009
[21]  Grunewald W, Karimi M, Wieczorek K, Van de Cappelle E, Wischnitzki E, et al. (2008) A role for AtWRKY23 in feeding site establishment of plant-parasitic nematodes. Plant Physiol 148: 358–368. doi: 10.1104/pp.108.119131
[22]  Petersen K, Fiil BK, Mundy J, Petersen M (2008) Downstream targets of WRKY33. Plant Signal Behav 3: 1033–1034.
[23]  Andreasson E, Jenkins T, Brodersen P, Thorgrimsen S, Petersen NHT, et al. (2005) The MAP kinase substrate MKS1 is a regulator of plant defense responses. Embo J 24: 2579–2589. doi: 10.1038/sj.emboj.7600737
[24]  Qiu JL, Fiil BK, Petersen K, Nielsen HB, Botanga CJ, et al. (2008) Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J 27: 2214–2221. doi: 10.1038/emboj.2008.147
[25]  Nafisi M, Goregaoker S, Botanga CJ, Glawischnig E, Olsen CE, et al. (2007) Arabidopsis Cytochrome P450 Monooxygenase 71A13 Catalyzes the Conversion of Indole-3-Acetaldoxime in Camalexin Synthesis. Plant Cell 19: 2039–2052. doi: 10.1105/tpc.107.051383
[26]  Mao G, Meng X, Liu Y, Zheng Z, Chen Z, et al. (2011) Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23: 1639–1653. doi: 10.1105/tpc.111.084996
[27]  Zheng Z, Qamar SA, Chen Z, Mengiste T (2006) Arabidopsis WRKY33 transcription factor is required for resistance to necrotrophic fungal pathogens. Plant J 48: 592–605. doi: 10.1111/j.1365-313x.2006.02901.x
[28]  Jiang Y, Deyholos MK (2009) Functional characterization of Arabidopsis NaCl-inducible WRKY25 and WRKY33 transcription factors in abiotic stresses. Plant Mol Biol 69: 91–105. doi: 10.1007/s11103-008-9408-3
[29]  Lippok B, Birkenbihl RP, Rivory G, Brummer J, Schmelzer E, et al. (2007) Expression of AtWRKY33 encoding a pathogen- or PAMP-responsive WRKY transcription factor is regulated by a composite DNA motif containing W box elements. Mol Plant-Microbe Interact 20: 420–429. doi: 10.1094/mpmi-20-4-0420
[30]  Robatzek S, Somssich IE (2001) A new member of the Arabidopsis WRKY transcription factor family, AtWRKY6, is associated with both senescence- and defence-related processes. Plant J 28: 123–133. doi: 10.1046/j.1365-313x.2001.01131.x
[31]  Yu D, Chen C, Chen Z (2001) Evidence for an important role of WRKY DNA binding proteins in the regulation of NPR1 gene expression. Plant Cell 13: 1527–1540. doi: 10.1105/tpc.13.7.1527
[32]  Robatzek S, Somssich IE (2002) Targets of AtWRKY6 regulation during plant senescence and pathogen defense. Genes Dev 16: 1139–1149. doi: 10.1101/gad.222702
[33]  Epple P, Apel K, Bohlmann H (1995) An Arabidopsis thaliana Thionin Gene Is Inducible Via a Signal-Transduction Pathway Different from That for Pathogenesis-Related Proteins. Plant Physiol 109: 813–820. doi: 10.1104/pp.109.3.813
[34]  Logemann E, Birkenbihl RP, Ulker B, Somssich IE (2006) An improved method for preparing Agrobacterium cells that simplifies the Arabidopsis transformation protocol. Plant Methods 2: 16. doi: 10.1186/1746-4811-2-16
[35]  Szakasits D, Siddique S, Bohlmann H (2007) An improved pPZP vector for Agrobacterium-mediated plant transformation. Plant Mol Biol Reporter 25: 115–120. doi: 10.1007/s11105-007-0013-4
[36]  Ali MA, Shah KH, Bohlmann H (2012) pMAA-Red: a new pPZP-derived vector for fast visual screening of transgenic Arabidopsis plants at the seed stage. BMC Biotechnol 12: 37. doi: 10.1186/1472-6750-12-37
[37]  Holtorf S, Apel K, Bohlmann H (1995) Comparison of different constitutive and inducible promoters for the overexpression of transgenes in Arabidopsis thaliana. Plant Mol Biol 29: 637–646. doi: 10.1007/bf00041155
[38]  Siddique S, Wieczorek K, Szakasits D, Kreil DP, Bohlmann H (2011) The promoter of a plant defensin gene directs specific expression in nematode-induced syncytia in Arabidopsis roots. Plant Physiol Biochem 49: 1100–1107. doi: 10.1016/j.plaphy.2011.07.005
[39]  Takemoto D, Hardham AR, Jones DA (2005) Differences in cell death induction by Phytophthora Elicitins are determined by signal components downstream of MAP kinase kinase in different species of Nicotiana and cultivars of Brassica rapa and Raphanus sativus. Plant Physiol 138: 1491–1504. doi: 10.1104/pp.104.058388
[40]  Ren D, Yang H, Zhang S (2002) Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. J Biol Chem 277: 559–565. doi: 10.1074/jbc.m109495200
[41]  Journot-Catalino N, Somssich IE, Roby D, Kroj T (2006) The transcription factors WRKY11 and WRKY17 act as negative regulators of basal resistance in Arabidopsis thaliana. Plant Cell 18: 3289–3302. doi: 10.1105/tpc.106.044149
[42]  Jürgensen K (2001) Untersuchungen zum Assimilat- und Wassertransfer in der Interaktion zwischen Arabidopsis thaliana und Heterodera schachtii. Kiel, Germany: Christian-Albrechts Universit?t.
[43]  Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901–3907.
[44]  Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25: 402–408. doi: 10.1006/meth.2001.1262
[45]  Wang Q, Wang M, Zhang X, Hao B, Kaushik SK, et al. (2011) WRKY gene family evolution in Arabidopsis thaliana. Genetica 139: 973–983. doi: 10.1007/s10709-011-9599-4
[46]  Li G, Meng X, Wang R, Mao G, Han L, et al. (2012) Dual-level regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLoS Genet 8: e1002767. doi: 10.1371/journal.pgen.1002767
[47]  Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, et al. (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415: 977–983. doi: 10.1038/415977a
[48]  Bottcher C, Westphal L, Schmotz C, Prade E, Scheel D, et al. (2009) The multifunctional enzyme CYP71B15 (PHYTOALEXIN DEFICIENT3) converts cysteine-indole-3-acetonitrile to camalexin in the indole-3-acetonitrile metabolic network of Arabidopsis thaliana. Plant Cell 21: 1830–1845. doi: 10.1105/tpc.109.066670
[49]  Schuhegger R, Nafisi M, Mansourova M, Petersen BL, Olsen CE, et al. (2006) CYP71B15 (PAD3) catalyzes the final step in camalexin biosynthesis. Plant Physiol 141: 1248–1254. doi: 10.1104/pp.106.082024
[50]  Besseau S, Li J, Palva ET (2012) WRKY54 and WRKY70 co-operate as negative regulators of leaf senescence in Arabidopsis thaliana. J Experimental Bot 63: 2667–2679. doi: 10.1093/jxb/err450
[51]  Babitha KC, Ramu SV, Pruthvi V, Mahesh P, Nataraja KN, et al. (2012) Co-expression of AtbHLH17 and AtWRKY28 confers resistance to abiotic stress in Arabidopsis. Transgenic Res 22: 327–341. doi: 10.1007/s11248-012-9645-8
[52]  Xing DH, Lai ZB, Zheng ZY, Vinod KM, Fan BF, et al. (2008) Stress- and Pathogen-Induced Arabidopsis WRKY48 is a Transcriptional Activator that Represses Plant Basal Defense. Mol Plant 1: 459–470. doi: 10.1093/mp/ssn020
[53]  Sch?n M, T?ller A, Diezel C, Roth C, Westphal L, et al. (2013) Analyses of wrky18wrky40 Plants Reveal Critical Roles of SA/EDS1 Signaling and Indole-Glucosinolate Biosynthesis for Golovinomyces orontii Resistance and a Loss-of Resistance Towards Pseudomonas syringae pv.tomato AvrRPS4. Mol Plant-Microbe Interact 26: 758–767. doi: 10.1094/mpmi-11-12-0265-r
[54]  Kasajima I, Ide Y, Yokota Hirai M, Fujiwara T (2010) WRKY6 is involved in the response to boron deficiency in Arabidopsis thaliana. Physiol Plant 139: 80–92. doi: 10.1111/j.1399-3054.2010.01349.x
[55]  Chen YF, Li LQ, Xu Q, Kong YH, Wang H, et al. (2009) The WRKY6 transcription factor modulates PHOSPHATE1 expression in response to low Pi stress in Arabidopsis. Plant Cell 21: 3554–3566. doi: 10.1105/tpc.108.064980
[56]  Matthews BF, Beard H, Brewer E, Kabir S, Macdonald MH, et al. (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. doi: 10.1186/1471-2229-14-96
[57]  Geng X, Cheng J, Gangadharan A, Mackey D (2012) The Coronatine Toxin of Pseudomonas syringae Is a Multifunctional Suppressor of Arabidopsis Defense. Plant Cell 24: 4763–4774. doi: 10.1105/tpc.112.105312
[58]  Ithal N, Recknor J, Nettleton D, Maier T, Baum TJ, et al. (2007) Developmental transcript profiling of cyst nematode feeding cells in soybean roots. Mol Plant-Microbe Interact 20: 510–525. doi: 10.1094/mpmi-20-5-0510
[59]  Birkenbihl RP, Diezel C, Somssich IE (2012) Arabidopsis WRKY33 Is a Key Transcriptional Regulator of Hormonal and Metabolic Responses toward Botrytis cinerea Infection. Plant Physiol 159: 266–285. doi: 10.1104/pp.111.192641
[60]  Veech JA (1982) Phytoalexins and their Role in the Resistance of Plants to Nematodes. J Nematology 14: 2–9.
[61]  Huang JS, Barker KR (1991) Glyceollin I in soybean-cyst nematode interactions : spatial and temporal distribution in roots of resistant and susceptible soybeans. Plant Physiol 96: 1302–1307. doi: 10.1104/pp.96.4.1302

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