Advertisement

Planta

, Volume 250, Issue 1, pp 347–366 | Cite as

Characterization of LuWRKY36, a flax transcription factor promoting secoisolariciresinol biosynthesis in response to Fusarium oxysporum elicitors in Linum usitatissimum L. hairy roots

  • Lucija Markulin
  • Cyrielle Corbin
  • Sullivan Renouard
  • Samantha Drouet
  • Charlène Durpoix
  • Charlotte Mathieu
  • Tatiana Lopez
  • Daniel Auguin
  • Christophe Hano
  • Éric LainéEmail author
Original Article
  • 270 Downloads

Abstract

Main conclusion

The involvement of a WRKY transcription factor in the regulation of lignan biosynthesis in flax using a hairy root system is described.

Abstract

Secoisolariciresinol is the main flax lignan synthesized by action of LuPLR1 (pinoresinol–lariciresinol reductase 1). LuPLR1 gene promoter deletion experiments have revealed a promoter region containing W boxes potentially responsible for the response to Fusarium oxysporum. W boxes are bound by WRKY transcription factors that play a role in the response to stress. A candidate WRKY transcription factor, LuWRKY36, was isolated from both abscisic acid and Fusarium elicitor-treated flax cell cDNA libraries. This transcription factors contains two WRKY DNA-binding domains and is a homolog of AtWRKY33. Different approaches confirmed LuWRKY36 binding to a W box located in the LuPLR1 promoter occurring through a unique direct interaction mediated by its N-terminal WRKY domain. Our results propose that the positive regulator action of LuWRKY36 on the LuPLR1 gene regulation and lignan biosynthesis in response to biotic stress is positively mediated by abscisic acid and inhibited by ethylene. Additionally, we demonstrate a differential Fusarium elicitor response in susceptible and resistant flax cultivars, seen as a faster and stronger LuPLR1 gene expression response accompanied with higher secoisolariciresinol accumulation in HR of the resistant cultivar.

Keywords

Abscisic acid Biotic stress Lignan Linum usitatissimum L. Pinoresinol–lariciresinol reductase Promoter WRKY 

Abbreviations

DPI

DNA–protein-interaction

EMSA

Electrophoretic mobility shift assay

FUSA

Fusarium oxysporum

HR

Hairy roots

SECO

(+)-Secoisolariciresinol

TF

Transcription factor

Notes

Acknowledgements

Lucija Markulin received a grant from the French Ministry of Research and Higher Education.

Compliance with ethical standard

Conflict of interest

The authors declare that they have no competing interest.

Supplementary material

425_2019_3172_MOESM1_ESM.docx (1.2 mb)
Supplementary material 1 (DOCX 1180 kb)

References

  1. Abraham MJ, Murtola T, Schulz R et al (2015) Gromacs: high performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX 1–2:19–25.  https://doi.org/10.1016/j.softx.2015.06.001 CrossRefGoogle Scholar
  2. Audenaert K, Callewaert E, Hofte M, De Saeger S, Haesaert G (2010) Hydrogen peroxide induced by the fungicide prothioconazole triggers deoxynivalenol (DON) production by Fusarium graminearum. BMC Microbiol 10:112CrossRefGoogle Scholar
  3. Bae H, Kim MS, Sicher RC et al (2006) Necrosis- and ethylene-inducing peptide from Fusarium oxysporum induces a complex cascade of transcripts associated with signal transduction and cell death in Arabidopsis. Plant Physiol 141:1056–1067.  https://doi.org/10.1104/pp.106.076869 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Baker NA, Sept D, Joseph S et al (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci USA 98:10037–10041.  https://doi.org/10.1073/pnas.181342398 CrossRefPubMedGoogle Scholar
  5. Borrone JW, Kuhn DN, Schnell RJ (2004) Isolation, characterization, and development of WRKY genes as useful genetic markers in Theobroma cacao. Theor Appl Genet 109:495–507.  https://doi.org/10.1007/s00122-004-1662-4 CrossRefPubMedGoogle Scholar
  6. Brand LH, Kirchler T, Hummel S et al (2010) DPI-ELISA: a fast and versatile method to specify the binding of plant transcription factors to DNA in vitro. Plant Methods 6:25.  https://doi.org/10.1186/1746-4811-6-25 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Brand LH, Fischer NM, Harter K et al (2013) Elucidating the evolutionary conserved DNA-binding specificities of WRKY transcription factors by molecular dynamics and in vitro binding assays. Nucleic Acids Res 41:9764–9778.  https://doi.org/10.1093/nar/gkt732 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Céspedes CL, Avila JG, García AM et al (2006) Antifungal and antibacterial activities of Araucaria araucana (Mol.) K. Koch heartwood lignans. Zeitschrift fur Naturforsch Sect C J Biosci 61:35–43.  https://doi.org/10.1515/znc-2006-1-207 CrossRefGoogle Scholar
  9. Chen X, Steed A, Travella S et al (2009) Fusarium graminearum exploits ethylene signalling to colonize dicotyledonous and monocotyledonous plants. New Phytol 182:975–983.  https://doi.org/10.1111/j.1469-8137.2009.02821.x CrossRefPubMedGoogle Scholar
  10. Chen R, Li Q, Tan H, Chen J, Xiao Y, Ma R, Gao S, Zerbe P, Chen W, Zhang L (2015) Gene-to-metabolite network for biosynthesis of lignans in MeJA-elicited Isatis indigotica hairy root cultures. Front Plant Sci 6:952.  https://doi.org/10.3389/fpls.2015.00952 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Chow C-N, Zheng H-Q, Wu N-Y et al (2016) PlantPAN 2.0: an update of plant promoter analysis navigator for reconstructing transcriptional regulatory networks in plants. Nucleic Acids Res 44:1154–1160.  https://doi.org/10.1093/nar/gkv1035 CrossRefGoogle Scholar
  12. Ciolkowski I, Wanke D, Birkenbihl RP, Somssich IE (2008) Studies on DNA-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function. Plant Mol Biol 68:81–92.  https://doi.org/10.1007/s11103-008-9353-1 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Corbin C, Decourtil C, Marosevic D et al (2013a) Role of protein farnesylation events in the ABA-mediated regulation of the Pinoresinol-Lariciresinol Reductase 1 (LuPLR1) gene expression and lignan biosynthesis in flax (Linum usitatissimum L.). Plant Physiol Biochem 72:96–111.  https://doi.org/10.1016/j.plaphy.2013.06.001 CrossRefPubMedGoogle Scholar
  14. Corbin C, Renouard S, Lopez T et al (2013b) Identification and characterization of cis-acting elements involved in the regulation of ABA- and/or GA-mediated LuPLR1 gene expression and lignan biosynthesis in flax (Linum usitatissimum L.) cell cultures. J Plant Physiol 170:516–522.  https://doi.org/10.1016/j.jplph.2012.11.003 CrossRefPubMedGoogle Scholar
  15. Corbin C, Drouet S, Mateljak I et al (2017) Functional characterization of the pinoresinol–lariciresinol reductase-2 gene reveals its roles in yatein biosynthesis and flax defense response. Planta 243:405–420.  https://doi.org/10.1007/s00425-017-2701-0 CrossRefGoogle Scholar
  16. Corbin C, Drouet S, Markulin L et al (2018) A genome-wide analysis of the flax (Linum usitatissimum L.) dirigent protein family: from gene identification and evolution to differential regulation. Plant Mol Biol 97:73.  https://doi.org/10.1007/s11103-018-0725-x CrossRefPubMedGoogle Scholar
  17. DeLano (2002) The PyMOL molecular graphics system. DeLano Scientific, Palo Alto, CAGoogle Scholar
  18. Dellagi A, Heilbronn J, Avrova AO et al (2000) A Potato Gene Encoding a WRKY-like transcription factor is induced in interactions with Erwinia carotovora subsp. atroseptica and Phytophthora infestans and is coregulated with class I endochitinase expression. Mol Plant-Microbe Interact MPMI 13:1092–1101.  https://doi.org/10.1094/MPMI.2000.13.10.1092 CrossRefPubMedGoogle Scholar
  19. Dong J, Chen C, Chen Z (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol Biol 51:21–37CrossRefGoogle Scholar
  20. Duan M-R, Nan J, Liang Y-H et al (2007) DNA binding mechanism revealed by high resolution crystal structure of Arabidopsis thaliana WRKY1 protein. Nucleic Acids Res 35:1145–1154.  https://doi.org/10.1093/nar/gkm001 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206CrossRefGoogle Scholar
  22. Fang J, Ramsay A, Renouard S et al (2016) Laser microdissection and spatiotemporal pinoresinol-lariciresinol reductase gene expression assign the cell layer-specific accumulation of secoisolariciresinol diglucoside in flaxseed coats. Front Plant Sci 7:1743.  https://doi.org/10.3389/fpls.2016.01743 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Gabr AMM, Mabrok HB, Kadry Z, Ghanem KZ, Blaut M, Smetanska I (2016) Lignan accumulation in callus and Agrobacterium rhizogenes mediated hairy root cultures of flax (Linum usitatissimum). Plant Cell Tiss Organ Cult 126:255–267.  https://doi.org/10.1007/s11240-016-0995-4 CrossRefGoogle Scholar
  24. Gabr AMM, Mabrok HB, Abdel-Rahim EA, El-Bahr MK, Smetanska I (2018) Determination of lignans, phenolic acids and antioxidant capacity in transformed hairy root culture of Linum usitatissimum. Nat Product Res 32:1867–1871.  https://doi.org/10.1080/14786419.2017.1405405 CrossRefGoogle Scholar
  25. Galindo-González L, Deyholos MK (2016) RNA-seq transcriptome response of flax (Linum usitatissimum L.) to the pathogenic fungus Fusarium oxysporum f. sp. lini. Front Plant Sci 7:1766.  https://doi.org/10.3389/fpls.2016.01766 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Gao X, He P (2013) Nuclear dynamics of Arabidopsis calcium-dependent protein kinases in effector-triggered immunity. Plant Signal Behav 8:23868.  https://doi.org/10.4161/psb.23868 CrossRefGoogle Scholar
  27. Gill US, Uppalapati SR, Gallego-Giraldo L et al (2017) Metabolic flux towards the (iso)flavonoid pathway in lignin modified alfalfa lines induces resistance against Fusarium oxysporum f. sp. medicaginis. Plant Cell Environ 41:1997–2007.  https://doi.org/10.1111/pce.13093 CrossRefPubMedGoogle Scholar
  28. Grunewald W, De Smet I, Lewis DR et al (2012) Transcription factor WRKY23 assists auxin distribution patterns during Arabidopsis root development through local control on flavonol biosynthesis. Proc Natl Acad Sci 109:1554–1559.  https://doi.org/10.1073/pnas.1121134109 CrossRefPubMedGoogle Scholar
  29. Guillaumie S, Mzid R, Méchin V et al (2010) The grapevine transcription factor WRKY2 influences the lignin pathway and xylem development in tobacco. Plant Mol Biol 72:215–234.  https://doi.org/10.1007/s11103-009-9563-1 CrossRefPubMedGoogle Scholar
  30. Hafez YM, Bacsó R, Király Z, Künstler A, Király L (2012) Upregulation of antioxidants in tobacco by low concentrations of H2O2 suppresses necrotic disease symptoms. Phytopathology 102:848–856CrossRefGoogle Scholar
  31. Haile ZM, Pilati S, Sonego P et al (2017) Molecular analysis of the early interaction between the grapevine flower and Botrytis cinerea reveals that prompt activation of specific host pathways leads to fungus quiescence. Plant Cell Environ 40:1409–1428.  https://doi.org/10.1111/pce.12937 CrossRefPubMedGoogle Scholar
  32. Hano C, Addi M, Bensaddek L et al (2006a) Differential accumulation of monolignol-derived compounds in elicited flax (Linum usitatissimum) cell suspension cultures. Planta 223:975–989.  https://doi.org/10.1007/s00425-005-0156-1 CrossRefPubMedGoogle Scholar
  33. Hano C, Martin I, Fliniaux O et al (2006b) Pinoresinol-lariciresinol reductase gene expression and secoisolariciresinol diglucoside accumulation in developing flax (Linum usitatissimum) seeds. Planta 224:1291–1301.  https://doi.org/10.1007/s00425-006-0308-y CrossRefPubMedGoogle Scholar
  34. Hano C, Renouard S, Molinié R et al (2013) Flaxseed (Linum usitatissimum L.) extract as well as (+)-secoisolariciresinol diglucoside and its mammalian derivatives are potent inhibitors of Î ± -amylase activity. Bioorg Med Chem Lett 23:3007–3012.  https://doi.org/10.1016/j.bmcl.2013.03.029 CrossRefPubMedGoogle Scholar
  35. Horton P, Park K-J, Obayashi T et al (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:585–587.  https://doi.org/10.1093/nar/gkm259 CrossRefGoogle Scholar
  36. Huang J, MacKerell ADJ (2013) CHARMM36 all-atom additive protein force field: validation based on comparison to NMR data. J Comput Chem 34:2135–2145.  https://doi.org/10.1002/jcc.23354 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Huis R, Hawkins S, Neutelings G (2010) Selection of reference genes for quantitative gene expression normalization in flax (Linum usitatissimum L.). BMC Plant Biol 10:71.  https://doi.org/10.1186/1471-2229-10-71 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907CrossRefGoogle Scholar
  39. Jennings JC, Apel-Birkhold PC, Bailey BA, Anderson JD (2000) Induction of ethylene biosynthesis and necrosis in weed leaves by a Fusarium oxysporum. Weed Sci 48:7–14.  https://doi.org/10.1614/0043-1745(2000)048%5b0007:IOEBAN%5d2.0.CO;2 CrossRefGoogle Scholar
  40. Johnson CS, Kolevski B, Smyth DR (2002) TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor. Plant Cell 14:1359–1375CrossRefGoogle Scholar
  41. Karimi M, Inzé D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7:193–195CrossRefGoogle Scholar
  42. Kato N, Dubouzet E, Kokabu Y et al (2007) Identification of a WRKY protein as a transcriptional regulator of benzylisoquinoline alkaloid biosynthesis in Coptis japonica. Plant Cell Physiol 48:8–18.  https://doi.org/10.1093/pcp/pcl041 CrossRefPubMedGoogle Scholar
  43. Koch MA, Haubold B, Mitchell-Olds T (2000) Comparative evolutionary analysis of chalcone synthase and alcohol dehydrogenase loci in Arabidopsis, Arabis, and related genera (Brassicaceae). Mol Biol Evol 17:1483–1498CrossRefGoogle Scholar
  44. Kostyn K, Czemplik M, Kulma A, Bortniczuk M, Skała J, Szopa J (2012) Genes of phenylpropanoid pathway are activated in early response to Fusarium attack in flax plants. Plant Sci 190:103–115.  https://doi.org/10.1016/j.plantsci.2012.03.011 CrossRefPubMedGoogle Scholar
  45. Kulik T, Buśko M, Pszczółkowska A et al (2014) Plant lignans inhibit growth and trichothecene biosynthesis in Fusarium graminearum. Lett Appl Microbiol 59:99–107.  https://doi.org/10.1111/lam.12250 CrossRefPubMedGoogle Scholar
  46. Lanubile A, Ferrarini A, Maschietto V et al (2014) Functional genomic analysis of constitutive and inducible defense responses to Fusarium verticillioides infection in maize genotypes with contrasting ear rot resistance. BMC Genomics 15:710.  https://doi.org/10.1186/1471-2164-15-710 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Levée V, Major I, Levasseur C et al (2009) Expression profiling and functional analysis of Populus WRKY23 reveals a regulatory role in defense. New Phytol 184:48–70.  https://doi.org/10.1111/j.1469-8137.2009.02955.x CrossRefPubMedGoogle Scholar
  48. Li C-Y, Deng G-M, Yang J et al (2012) Transcriptome profiling of resistant and susceptible Cavendish banana roots following inoculation with Fusarium oxysporum f. sp. cubense tropical race 4. BMC Genomics 13:374.  https://doi.org/10.1186/1471-2164-13-374 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Liu S, Ziegler J, Zeier J et al (2017) Botrytis cinerea B05.10 promotes disease development in Arabidopsis by suppressing WRKY33-mediated host immunity. Plant Cell Environ 40:2189–2206.  https://doi.org/10.1111/pce.13022 CrossRefPubMedGoogle Scholar
  50. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408.  https://doi.org/10.1006/meth.2001.1262 CrossRefGoogle Scholar
  51. Logemann E, Birkenbihl RP, Rawat V et al (2013) Functional dissection of the PROPEP2 and PROPEP3 promoters reveals the importance of WRKY factors in mediating microbe-associated molecular pattern-induced expression. New Phytol 198:1165–1177.  https://doi.org/10.1111/nph.12233 CrossRefPubMedGoogle Scholar
  52. Lorenc-Kukula K, Zuk M, Kulma A, Czemplik M, Kostyn K, Skala J et al (2009) Engineering flax with the GT family 1 Solanum sogarandinum glycosyltransferase SsGT1 confers increased resistance to Fusarium infection. J Agric Food Chem 57:6698–6705.  https://doi.org/10.1021/jf900833k CrossRefPubMedGoogle Scholar
  53. Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155CrossRefGoogle Scholar
  54. Ma R, Xiao Y, Lv Z, Tan H, Chen R, Li Q, Chen J, Wang Y, Yin J, Zhang L, Chen W (2017) Transcription factor, Ii049, positively regulates lignan biosynthesis in Isatis indigotica through activating salicylic acid signaling and lignan/lignin pathway genes. Front Plant Sci 8:1361.  https://doi.org/10.3389/fpls.2017.01361 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Mao G, Meng X, Liu Y et al (2011) Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23:1639–1653.  https://doi.org/10.1105/tpc.111.084996 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Markulin L, Corbin C, Renouard S, Drouet S, Gutierrez L, Mateljak I, Auguin D, Hano C, Fuss E, Lainé E (2019a) Pinoresinol lariciresinol reductases, key to the lignan synthesis in plants. Planta  https://doi.org/10.1007/s00425-019-03137-y CrossRefGoogle Scholar
  57. Markulin L, Drouet S, Corbin C, Decourtil C, Garros L, Renouard S, Lopez T, Mongelard G, Gutierrez L, Auguin D, Laine E, Hano C (2019b) The control exerted by ABA on lignan biosynthesis in flax (Linum usitatissimum L.) is modulated by a Ca2+ signal transduction involving the calmodulin-like LuCML15b. J Plant Physiol 236:74–87.  https://doi.org/10.1016/j.jplph.2019.03.005 CrossRefPubMedGoogle Scholar
  58. Matić S, Bagnaresi P, Biselli C et al (2016) Comparative transcriptome profiling of resistant and susceptible rice genotypes in response to the seedborne pathogen Fusarium fujikuroi. BMC Genomics 17:608.  https://doi.org/10.1186/s12864-016-2925-6 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Matoušek J, Kocábek T, Patzak J et al (2016) The “putative” role of transcription factors from HlWRKY family in the regulation of the final steps of prenylflavonid and bitter acids biosynthesis in hop (Humulus lupulus L.). Plant Mol Biol 92:263–277.  https://doi.org/10.1007/s11103-016-0510-7 CrossRefPubMedGoogle Scholar
  60. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497.  https://doi.org/10.1111/j.1399-3054.1962.tb08052.x CrossRefGoogle Scholar
  61. Nei M, Gojoborit T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426PubMedGoogle Scholar
  62. Olivain C, Trouvelot S, Binet M-NM-N et al (2003) Colonization of flax roots and early physiological responses of flax cells inoculated with pathogenic and nonpathogenic strains of Fusarium oxysporum. Appl Environ Microbiol 69:5453–5462.  https://doi.org/10.1128/AEM.69.9.5453-5462.2003 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Plasencia A, Soler M, Dupas A et al (2016) Eucalyptus hairy roots, a fast, efficient and versatile tool to explore function and expression of genes involved in wood formation. Plant Biotechnol J 14:1381–1393.  https://doi.org/10.1111/pbi.12502 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Renouard S, Corbin C, Lopez T et al (2012) Abscisic acid regulates pinoresinol-lariciresinol reductase gene expression and secoisolariciresinol accumulation in developing flax (Linum usitatissimum L.) seeds. Planta 235:85–98.  https://doi.org/10.1007/s00425-011-1492-y CrossRefPubMedGoogle Scholar
  65. Renouard S, Tribalatc M-A, Lamblin F et al (2014) RNAi-mediated pinoresinol lariciresinol reductase gene silencing in flax (Linum usitatissimum L.) seed coat: consequences on lignans and neolignans accumulation. J Plant Physiol 171:1372–1377.  https://doi.org/10.1016/j.jplph.2014.06.005 CrossRefPubMedGoogle Scholar
  66. Rushton PJ, Torres JT, Parniske M et al (1996) Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO J 15:5690–5700CrossRefGoogle Scholar
  67. Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247–258.  https://doi.org/10.1016/j.tplants.2010.02.006 CrossRefPubMedGoogle Scholar
  68. Rushton DL, Tripathi P, Rabara RC et al (2012) WRKY transcription factors: key components in abscisic acid signalling. Plant Biotechnol J 10:2–11.  https://doi.org/10.1111/j.1467-7652.2011.00634.x CrossRefPubMedPubMedCentralGoogle Scholar
  69. Schluttenhofer C, Pattanaik S, Patra B, Yuan L (2014) Analyses of Catharanthus roseus and Arabidopsis thaliana WRKY transcription factors reveal involvement in jasmonate signaling. BMC Genomics 15:502.  https://doi.org/10.1186/1471-2164-15-502 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Shen H-B, Chou K-C (2007) Nuc-PLoc: a new web-server for predicting protein subnuclear localization by fusing PseAA composition and PsePSSM. Protein Eng Des Sel 20:561–567.  https://doi.org/10.1093/protein/gzm057 CrossRefPubMedGoogle Scholar
  71. Svetaz LA, Bustamante CA, Goldy C et al (2017) Unravelling early events in the Taphrina deformansPrunus persica interaction: an insight into the differential responses in resistant and susceptible genotypes. Plant, Cell Environ 40:1456–1473.  https://doi.org/10.1111/pce.12942 CrossRefGoogle Scholar
  72. Tamura K, Stecher G, Peterson D et al (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729.  https://doi.org/10.1093/molbev/mst197 CrossRefPubMedPubMedCentralGoogle Scholar
  73. Tanaka Y, Sano T, Tamaoki M et al (2005) Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol 138:2337–2343.  https://doi.org/10.1104/pp.105.063503 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefGoogle Scholar
  75. Venglat P, Xiang D, Qiu S et al (2011) Gene expression analysis of flax seed development. BMC Plant Biol 11:74.  https://doi.org/10.1186/1471-2229-11-74 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Wang Z, Hobson N, Galindo L et al (2012) The genome of flax (Linum usitatissimum) assembled de novo from short shotgun sequence reads. Plant J 72:461–473.  https://doi.org/10.1111/j.1365-313X.2012.05093.x CrossRefPubMedGoogle Scholar
  77. Wang Z, Fang H, Chen Y et al (2014) Overexpression of BnWRKY33 in oilseed rape enhances resistance to Sclerotinia sclerotiorum. Mol Plant Pathol 15:677–689.  https://doi.org/10.1111/mpp.12123 CrossRefPubMedPubMedCentralGoogle Scholar
  78. Waterhouse AM, Procter JB, Martin DMA et al (2009) Jalview version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:1189–1191.  https://doi.org/10.1093/bioinformatics/btp033 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Wei W, Cui M-Y, Hu Y et al (2018) Ectopic expression of FvWRKY42, a WRKY transcription factor from the diploid woodland strawberry (Fragaria vesca), enhances resistance to powdery mildew, improves osmotic stress resistance, and increases abscisic acid sensitivity in Arabidopsis. Plant Sci 275:60–74.  https://doi.org/10.1016/j.plantsci.2018.07.010 CrossRefPubMedGoogle Scholar
  80. Wróbel-Kwiatkowska M, Starzycki M, Zebrowski J et al (2007) Lignin deficiency in transgenic flax resulted in plants with improved mechanical properties. J Biotechnol 128:919–934.  https://doi.org/10.1016/j.jbiotec.2006.12.030 CrossRefPubMedGoogle Scholar
  81. Xiao Y, Ji Q, Gao S, Tan H, Chen R, Li Q, Chen J, Yang Y, Zhang L, Wang Z, Chen W, Hu Z (2015) Combined transcriptome and metabolite profiling reveals that IiPLR1 plays an important role in lariciresinol accumulation in Isatis indigotica. J Exp Bot 66:6259–6271.  https://doi.org/10.1093/jxb/erv333 CrossRefPubMedGoogle Scholar
  82. Yamasaki K, Kigawa T, Inoue M et al (2005) Solution structure of the major DNA-binding domain of Arabidopsis thaliana ethylene-insensitive3-like3. J Mol Biol 348:253–264.  https://doi.org/10.1016/j.jmb.2005.02.065 CrossRefPubMedGoogle Scholar
  83. Yang P, Chen C, Wang Z et al (1999) A pathogen- and salicylic acid-induced WRKY DNA-binding activity recognizes the elicitor response element of the tobacco class I chitinase gene promoter. Plant J 18:141–149.  https://doi.org/10.1046/j.1365-313X.1999.00437.x CrossRefGoogle Scholar
  84. Yang L, Ye C, Zhao Y et al (2018) An oilseed rape WRKY-type transcription factor regulates ROS accumulation and leaf senescence in Nicotiana benthamiana and Arabidopsis through modulating transcription of RbohD and RbohF. Planta 247:1323–1338.  https://doi.org/10.1007/s00425-018-2868-z CrossRefPubMedGoogle Scholar
  85. Yao Q, Bollinger C, Gao J et al (2012) P3DB: an integrated database for plant protein phosphorylation. Front Plant Sci 3:206.  https://doi.org/10.3389/fpls.2012.00206 CrossRefPubMedPubMedCentralGoogle Scholar
  86. Ye Y, Cheung DWL, Wang Y et al (2015) GLProbs: aligning multiple sequences adaptively. IEEE/ACM Trans Comput Biol Bioinforma 12:67–78.  https://doi.org/10.1109/TCBB.2014.2316820 CrossRefGoogle Scholar
  87. Yogendra KN, Dhokane D, Kushalappa AC et al (2017) StWRKY8 transcription factor regulates benzylisoquinoline alkaloid pathway in potato conferring resistance to late blight. Plant Sci 256:208–216.  https://doi.org/10.1016/j.plantsci.2016.12.014 CrossRefPubMedGoogle Scholar
  88. 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.  https://doi.org/10.1105/TPC.010115 CrossRefPubMedPubMedCentralGoogle Scholar
  89. Zhang Y (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9:40.  https://doi.org/10.1186/1471-2105-9-40 CrossRefPubMedPubMedCentralGoogle Scholar
  90. Zhang L, Chen J, Zhou X, Chen X, Li Q, Tan H, Dong X, Xiao Y, Chen L, Chen W (2016) Dynamic metabolic and transcriptomic profiling of methyl jasmonate-treated hairy roots reveals synthetic characters and regulators of lignan biosynthesis in Isatis indigotica Fort. Plant Biotechnol J 14:2217–2227.  https://doi.org/10.1111/pbi.12576 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Lucija Markulin
    • 1
  • Cyrielle Corbin
    • 1
  • Sullivan Renouard
    • 1
  • Samantha Drouet
    • 1
  • Charlène Durpoix
    • 1
  • Charlotte Mathieu
    • 1
  • Tatiana Lopez
    • 1
  • Daniel Auguin
    • 1
  • Christophe Hano
    • 1
  • Éric Lainé
    • 1
    Email author
  1. 1.Laboratoire de Biologie des Ligneux et des Grandes Cultures, EA 1207, INRA USC 1328, Université d’OrléansPôle Universitaire d’Eure et LoirChartresFrance

Personalised recommendations