Biologia plantarum 59:581-590, 2015 | DOI: 10.1007/s10535-015-0513-2

Identification of phospholipase D genes in Brassica napus and their transcription after phytohormone treatment and pathogen infection

M. Janda1,2, L. Ježková1,2, M. Nováková1,2, O. Valentová2, L. Burketová1, V. Šašek1,*
1 Laboratory of Pathological Plant Physiology, Institute of Experimental Botany AS CR, Prague, Czech Republic
2 Department of Biochemistry and Microbiology, Institute of Chemical Technology Prague, Prague, Czech Republic

Phospholipase D (PLD) and its product phosphatidic acid are now considered to be one of the key elements of numerous physiological processes in plants including the salicylic acid signalling pathway. The presented study investigates the transcriptional regulation of Brassica napus PLDs following treatments with defense-related stimuli. We cloned eight B. napus genes encoding members of PLDβ, γ, and δ isoforms and performed phylogenetic analysis with its ancestor species Brassica rapa and Brassica oleracea, and with the model plant Arabidopsis thaliana. Transcription of the identified genes was monitored after treatment with benzothiadiazole (BTH), methyl jasmonate (MeJA), bacterial elicitor flg22, wounding, and after infection with fungal pathogens Sclerotinia sclerotiorum and Leptosphaeria maculans. Most of the genes responded specifically to a particular treatment. Remarkably the genes encoding the PLDγ and PLDβ isoforms were up-regulated by stimuli associated with the salicylic acid signalling pathway. The generality of this finding was confirmed by the analysis of public transcriptional data from Arabidopsis thaliana.

Keywords: benzothiadiazole; Leptosphaeria maculans; methyl jasmonate; microarray; oilseed rape; salicylic acid; Sclerotinia sclerotiorum; transcriptomics
Subjects: phospholipase D; gene expression; benzothiadiazole; methyl jasmonate; salicylic acid; phylogenetic tree; oilseed rape

Received: October 20, 2014; Revised: January 15, 2015; Accepted: January 23, 2015; Published: September 1, 2015Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Janda, M., Ježková, L., Nováková, M., Valentová, O., Burketová, L., & Šašek, V. (2015). Identification of phospholipase D genes in Brassica napus and their transcription after phytohormone treatment and pathogen infection. Biologia plantarum, 59(3), 581-590. doi: 10.1007/s10535-015-0513-2.
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    Supplementary files

    Download filebpl-201503-0022_S1.pdf

    File size: 86.18 kB

    References

    1. Abascal, F., Zardoya, R., Telford, M.J.: TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. - Nucl. Acids Res. 38: W7-13, 2010. Go to original source...
    2. Bargmann, B.O., Laxalt, A.M., Ter Riet, B., Testerink, C., Merquiol, E., Mosblech, A., Leon-Reyes, A., Pieterse, C.M., Haring, M.A., Heilmann, I., Bartels, D., Munnik, T.: Reassessing the role of phospholipase D in the Arabidopsis wounding response. - Plant Cell Environ. 32: 837-850, 2009. Go to original source...
    3. Bargmann, B.O., Munnik, T.: The role of phospholipase D in plant stress responses. - Curr. Opin. Plant Biol. 9: 515-522, 2006. Go to original source...
    4. Boratyn, G.M., Camacho, C., Cooper, P.S., Coulouris, G., Fong, A., Ma, N., Madden, T.L., Matten, W.T., McGinnis, S.D., Merezhuk, Y., Raytselis, Y., Sayers, E.W., Tao, T., Ye, J., Zaretskaya, I.: BLAST: a more efficient report with usability improvements. - Nucl. Acids Res. 41: W29-33, 2013. Go to original source...
    5. Cheng, F., Liu, S., Wu, J., Fang, L., Sun, S., Liu, B., Li, P., Hua, W., Wang, X.: BRAD, the genetics and genomics database for Brassica plants. - BMC Plant Biol. 11: 136, 2011. Go to original source...
    6. Cheung, F., Trick, M., Drou, N., Lim, Y.P., Park, J.Y., Kwon, S.J., Kim, J.A., Scott, R., Pires, J.C., Paterson, A.H., Town, C., Bancroft, I.: Comparative analysis between homoeologous genome segments of Brassica napus and its progenitor species reveals extensive sequence-level divergence. - Plant Cell 21: 1912-1928, 2009.
    7. Das, M., Reichman, J.R., Haberer, G., Welzl, G., Aceituno, F.F., Mader, M.T., Watrud, L.S., Pfleeger, T.G., Gutierrez, R.A., Schaffner, A.R., Olszyk, D.M.: A composite transcriptional signature differentiates responses towards closely related herbicides in Arabidopsis thaliana and Brassica napus. - Plant mol. Biol. 72: 545-556, 2010. Go to original source...
    8. De Torres Zabela, M., Fernandez-Delmond, I., Niittyla, T., Sanchez, P., Grant, M.: Differential expression of genes encoding Arabidopsis phospholipases after challenge with virulent or avirulent Pseudomonas isolates. - Mol. Plant Microbe Interact. 15: 808-816, 2002. Go to original source...
    9. Elias, M., Potocky, M., Cvrckova, F., Zarsky, V.: Molecular diversity of phospholipase D in angiosperms. - BMC Genomics 3: 2, 2002. Go to original source...
    10. Gomez-Gomez, L., Boller, T.: Flagellin perception: a paradigm for innate immunity. - Trends Plant Sci. 7: 251-256, 2002. Go to original source...
    11. Greeff, C., Roux, M., Mundy, J., Petersen, M.: Receptor-like kinase complexes in plant innate immunity. - Front. Plant Sci. 3: 209, 2012. Go to original source...
    12. Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W., Gascuel, O.: New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. - Syst. Biol. 59: 307-321, 2010. Go to original source...
    13. Janda, M., Planchais, S., Djafi, N., Martinec, J., Burketova, L., Valentova, O., Zachowski, A., Ruelland, E.: Phosphoglycerolipids are master players in plant hormone signal transduction. - Plant Cell Rep. 32: 839-851, 2013. Go to original source...
    14. Kalachova, T.A., Iakovenko, O.M., Kretinin, S.V., Kravets, V.S.: Effects of salicylic and jasmonic acid on phospholipase D activity and the level of active oxygen species in soybean seedlings. - Biol. Membr. 29: 169-176, 2012. Go to original source...
    15. Kilian, J., Whitehead, D., Horak, J., Wanke, D., Weinl, S., Batistic, O., D'Angelo, C., Bornberg-Bauer, E., Kudla, J., Harter, K.: The AtGene express global stress expression data set: protocols, evaluation and model data analysis of UV-B light, drought and cold stress responses. - Plant J. 50: 347-363, 2007. Go to original source...
    16. Krinke, O., Flemr, M., Vergnolle, C., Collin, S., Renou, J.P., Taconnat, L., Yu, A., Burketova, L., Valentova, O., Zachowski, A., Ruelland, E.: Phospholipase D activation is an early component of the salicylic acid signaling pathway in Arabidopsis cell suspensions. - Plant Physiol. 150: 424-436, 2009. Go to original source...
    17. Lamesch, P., Berardini, T.Z., Li, D.H., Swarbreck, D., Wilks, C., Sasidharan, R., Muller, R., Dreher, K., Alexander, D.L., Garcia-Hernandez, M., Karthikeyan, A.S., Lee, CH., Nelson, W.D., Ploetz, L., Singh, S., Wensel, A., Huala, E.: The Arabidopsis information resource (TAIR): improved gene annotation and new tools. - Nucl. Acids Res. 40: D1202-1210, 2012. Go to original source...
    18. Lee, S.M., Suh, S., Kim, S., Crain, R.C., Kwak, J.M., Nam, H.G., Lee, Y.S.: Systemic elevation of phosphatidic acid and lysophospholipid levels in wounded plants. - Plant J. 12: 547-556, 1997. Go to original source...
    19. Li, G., Lin, F., Xue, H.W.: Genome-wide analysis of the phospholipase D family in Oryza sativa and functional characterization of PLD beta 1 in seed germination. - Cell Res. 17: 881-894, 2007. Go to original source...
    20. Liu, Q., Zhang, C., Yang, Y., Hu, X.: Genome-wide and molecular evolution analyses of the phospholipase D gene family in poplar and grape. - BMC Plant Biol. 10: 117, 2010. Go to original source...
    21. Madrid, E., Corchete, P.: Silymarin secretion and its elicitation by methyl jasmonate in cell cultures of Silybum marianum is mediated by phospholipase D-phosphatidic acid. - J. exp. Bot. 61: 747-754, 2010. Go to original source...
    22. Marshall, O.J.: PerlPrimer: cross-platform, graphical primer design for standard, bisulphite and real-time PCR. - Bioinformatics 20: 2471-2472, 2004. Go to original source...
    23. Novakova, M., Sasek, V., Dobrev, P.I., Valentova, O., Burketova, L.: Plant hormones in defense response of Brassica napus to Sclerotinia sclerotiorum - reassessing the role of salicylic acid in the interaction with a necrotroph. - Plant Physiol. Biochem. 80: 308-317, 2014. Go to original source...
    24. Obermeier, C., Hosseini, B., Friedt, W., Snowdon, R.: Gene expression profiling via LongSAGE in a non-model plant species: a case study in seeds of Brassica napus. - BMC Genomics 10: 295, 2009. Go to original source...
    25. Ostergaard, L., King, G.J.: Standardized gene nomenclature for the Brassica genus. - Plant Methods 4: 10, 2008. Go to original source...
    26. Pieterse, C.M., Van der Does, D., Zamioudis, C., Leon-Reyes, A., Van Wees, S.C.: Hormonal modulation of plant immunity. - Annu. Rev. cell. dev. Biol. 28: 489-521, 2012. Go to original source...
    27. Pleskot, R., Pejchar, P., Bezvoda, R., Lichtscheidl, I.K., Wolters Arts, M., Marc, J., Zarsky, V., Potocky, M.: Turnover of phosphatidic acid through distinct signaling pathways affects multiple aspects of pollen tube growth in tobacco. - Front. Plant. Sci. 3: 54, 2012. Go to original source...
    28. Pozo, M.J., Van Der Ent, S., Van Loon, L.C., Pieterse, C.M.: Transcription factor MYC2 is involved in priming for enhanced defense during rhizobacteria-induced systemic resistance in Arabidopsis thaliana. - New Phytol. 180: 511-523, 2008. Go to original source...
    29. Profotova, B., Burketova, L., Novotna, Z., Martinec, J., Valentova, O.: Involvement of phospholipases C and D in early response to SAR and ISR inducers in Brassica napus plants. - Plant Physiol. Biochem. 44: 143-151, 2006. Go to original source...
    30. Qutob, D., Kemmerling, B., Brunner, F., Kufner, I., Engelhardt, S., Gust, A.A., Luberacki, B., Seitz, H.U., Stahl, D., Rauhut, T., Glawischnig, E., Schween, G., Lacombe, B., Watanabe, N., Lam, E., Schlichting, R., Scheel, D., Nau, K., Dodt, G., Hubert, D., Gijzen, M., Nurnberger, T.: Phytotoxicity and innate immune responses induced by Nep1-like proteins. - Plant Cell 18: 3721-3744, 2006. Go to original source...
    31. Raho, N., Ramirez, L., Lanteri, M.L., Gonorazky, G., Lamattina, L., Ten Have, A., Laxalt, A.M.: Phosphatidic acid production in chitosan-elicited tomato cells, via both phospholipase D and phospholipase C/diacylglycerol kinase, requires nitric oxide. - J. Plant Physiol. 168: 534-539, 2011. Go to original source...
    32. Rainteau, D., Humbert, L., Delage, E., Vergnolle, C., Cantrel, C., Maubert, M.A., Lanfranchi, S., Maldiney, R., Collin, S., Wolf, C., Zachowski, A., Ruelland, E.: Acyl chains of phospholipase D transphosphatidylation products in Arabidopsis cells: a study using multiple reaction monitoring mass spectrometry. - PLoS One 7: e41985, 2012. Go to original source...
    33. Sasek, V., Novakova, M., Jindrichova, B., Boka, K., Valentova, O., Burketova, L.: Recognition of avirulence gene AvrLm1 from hemibiotrophic ascomycete Leptosphaeria maculans triggers salicylic acid and ethylene signaling in Brassica napus. - Mol. Plant Microbe Interact. 25: 1238-1250, 2012. Go to original source...
    34. Steiner, A.A.: Influence of chemical composition of a nutrient solution on production of tomato plants. - Plant Soil 24: 454, 1966. Go to original source...
    35. Tsuda, K., Sato, M., Glazebrook, J., Cohen, J.D., Katagiri, F.: Interplay between MAMP-triggered and SA-mediated defense responses. - Plant J. 53: 763-775, 2008. Go to original source...
    36. Van der Luit, A.H., Piatti, T., Van Doorn, A., Musgrave, A., Felix, G., Boller, T., Munnik, T.: Elicitation of suspensioncultured tomato cells triggers the formation of phosphatidic acid and diacylglycerol pyrophosphate. - Plant Physiol. 123: 1507-1516, 2000. Go to original source...
    37. Walley, J.W., Coughlan, S., Hudson, M.E., Covington, M.F., Kaspi, R., Banu, G., Harmer, S.L., Dehesh, K.: Mechanical stress induces biotic and abiotic stress responses via a novel cis-element. - PLoS Genet. 3: 1800-1812, 2007.
    38. Wang, C., Zien, C.A., Afitlhile, M., Welti, R., Hildebrand, D.F., Wang, X.: Involvement of phospholipase D in woundinduced accumulation of jasmonic acid in Arabidopsis. - Plant Cell 12: 2237-2246, 2000. Go to original source...
    39. Wang, D., Amornsiripanitch, N., Dong, X.: A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. - PLoS Pathog. 2: e123, 2006. Go to original source...
    40. Wang, X.: Phospholipase D in hormonal and stress signaling. - Curr. Opin. Plant Biol. 5: 408-414, 2002. Go to original source...
    41. Wang, X.: Regulatory functions of phospholipase D and phosphatidic acid in plant growth, development, and stress responses. - Plant Physiol. 139: 566-573, 2005. Go to original source...
    42. Wang, X., Wang, H.Z., Wang, J., Sun, R.F., Wu, J., Liu, S.Y., Bai, Y.Q., Mun, J.H., Bancroft, I., Cheng, F., Huang, S.W., Li, X.X., Hua, W., Wang, J.Y., Wang, X.Y., Freeling, M., Pires, J.C., Paterson, A.H., Chalhoub, B., Wang, B., Hayward, A., Sharpe, A.G., Park, B.S., Weisshaar, B., Liu, B.H., Li, B., Liu, B., Tong, C.B., Song, C., Duran, C., Peng, C.F., Geng, C.Y., Koh, C.S., Lin, C.Y., Edwards, D., Mu, D.S., Shen, D., Soumpourou, E., Li, F., Fraser, F., Conant, G., Lassalle, G., King, G.J., Bonnema, G., Tang, H.B., Wang, H.P., Belcram, H., Zhou, H.L., Hirakawa, H., Abe, H., Guo, H., Wang, H., Jin, H.Z., Parkin, I.A.P., Batley, J., Kim, J.S., Just, J., Li, J.W., Xu, J.H., Deng, J., Kim, J.A., Li, J.P., Yu, J.Y., Meng, J.L., Wang, J.P., Min, J.M., Poulain, J., Wang, J., Hatakeyama, K., Wu, K., Wang, L., Fang, L., Trick, M., Links, M.G., Zhao, M.X., Jin, M.N., Ramchiary, N., Drou, N., Berkman, P.J., Cai, Q.L., Huang, Q.F., Li, R.Q., Tabata, S., Cheng, S.F., Zhang, S., Zhang, S.J., Huang, S.M., Sato, S., Sun, S.L., Kwon, S.J., Choi, S.R., Lee, T.H., Fan, W., Zhao, X., Tan, X., Xu, X., Wang, Y., Qiu, Y., Yin, Y., Li, Y.R., Du, Y.C., Liao, Y.C., Lim, Y., Narusaka, Y., Wang, Y.P., Wang, Z.Y., Li, Z.Y., Wang, Z.W., Xiong, Z.Y., Zhang, Z.H: The genome of the mesopolyploid crop species Brassica rapa. - Nat. Genet. 43: 1035-1039, 2011. Go to original source...
    43. Yamaguchi, T., Kuroda, M., Yamakawa, H., Ashizawa, T., Hirayae, K., Kurimoto, L., Shinya, T., Shibuya, N.: Suppression of a phospholipase D gene, OsPLDbeta1, activates defense responses and increases disease resistance in rice. - Plant Physiol. 150: 308-319, 2009. Go to original source...
    44. Yang, B., Jiang, Y., Rahman, M.H., Deyholos, M.K., Kav, N.N.: 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, 2009. Go to original source...
    45. Yang, S., Lu, S.H., Yuan, Y.J.: Lipidomic analysis reveals differential defense responses of Taxus cuspidata cells to two elicitors, methyl jasmonate and cerium (Ce4+). - Biochim. biophys. Acta 1781: 123-134, 2008. Go to original source...
    46. Young, S.A., Wang, X., Leach, J.E.: Changes in the plasma membrane distribution of rice phospholipase D during resistant interactions with Xanthomonas oryzae pv. oryzae. - Plant Cell 8: 1079-1090, 1996. Go to original source...
    47. Yu, B.Y., Gruber, M., Khachatourians, G.G., Hegedus, D.D., Hannoufa, A.: Gene expression profiling of developing Brassica napus seed in relation to changes in major storage compounds. - Plant Sci. 178: 381-389, 2010. Go to original source...
    48. Yu, J., Zhao, M., Wang, X., Tong, C., Huang, S., Tehrim, S., Liu, Y., Hua, W., Liu, S.: Bolbase: a comprehensive genomics database for Brassica oleracea. - BMC Genomics 14: 664, 2013. Go to original source...
    49. Zhao, J., Devaiah, S.P., Wang, C., Li, M., Welti, R., Wang, X.: Arabidopsis phospholipase Dbeta1 modulates defense responses to bacterial and fungal pathogens. - New Phytol. 199: 228-240, 2013. Go to original source...
    50. Zhao, J., Zhou, D., Zhang, Q., Zhang, W.: Genomic analysis of phospholipase D family and characterization of GmPLDalphas in soybean (Glycine max). - J. Plant Res. 125: 569-578, 2012. Go to original source...

    Return to the content