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Changes in membrane fluidity and phospholipase D activity are required for heat activation of PyMBF1 in Pyropia yezoensis (Rhodophyta)

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Abstract

Multiprotein bridging factor 1 (MBF1) is a highly conserved transcriptional co-activator involved in the regulation of diverse processes, such as environmental stress responses. We recently identified a novel MBF1 gene, PyMBF1, from the marine red alga Pyropia yezoensis. In this study, quantitative real-time PCR analysis revealed that PyMBF1 transcripts were upregulated in P. yezoensis cells during exposure to oxidative and heat stresses. We also examined heat signaling in P. yezoensis cells by monitoring the accumulation of PyMBF1 transcripts. Heat activation of PyMBF1 was inhibited by the membrane rigidifier dimethylsulfoxide, whereas it was induced without heat stress by the membrane fluidizer benzyl alcohol (BA). Induction of PyMBF1 transcripts by heat and BA was inhibited by 1-butanol, an inhibitor of phospholipase D (PLD). The results suggest that the heat activation of PyMBF1 requires membrane fluidization and activation of PLD. These findings provide an initial step toward understanding heat signaling in marine red algae.

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References

  • Asamizu E, Nagajima M, Kitade Y, Saga N, Nakamura Y, Tabata S (2003) Comparison of RNA expression profiles between the two generations of Porphyra yezoensis (Rhodophyta), based on expressed sequence tag frequency analysis. J Phycol 39:923–930

    Article  Google Scholar 

  • Brendel C, Gelman L, Auwerx J (2002) Multiprotein bridging factor-1 (MBF-1) is a cofactor for nuclear receptors that regulate lipid metabolism. Mol Endocrinol 16:1367–1377

    Article  PubMed  CAS  Google Scholar 

  • Contreras-Porcia L, Thomas D, Flores V, Correa JA (2011) Tolerance to oxidative stress induced by desiccation in Porphyra columbina (Bangiales, Rhodophyta). J Exp Bot 62:1815–1829

    Article  PubMed  CAS  Google Scholar 

  • Fukuda S, Mikami K, Uji T, Park EJ, Ohba T, Asada K, Kitade Y, Endo H, Kato I, Saga N (2008) Factors influencing efficiency of transient gene expression in the red macrophyte Porphyra yezoensis. Plant Sci 174:329–339

    Article  CAS  Google Scholar 

  • Gardiner J, Collings DA, Harper JDI, Marc J (2003) The effects of the phospholipase D-antagonist 1-butanol on seedling development and microtubule organisation in Arabidopsis. Plant Cell Physiol 44:687–696

    Article  PubMed  CAS  Google Scholar 

  • Huang GT, Ma SL, Bai LP, Zhang L, Ma H, Jia P, Liu J, Zhong M, Guo ZF (2012) Signal transduction during cold, salt, and drought stresses in plants. Mol Biol Rep 39:969–987

    Article  PubMed  Google Scholar 

  • Inaba M, Suzuki I, Szalontai B, Kanesaki Y, Los DA, Hayashi H, Murata N (2003) Gene-engineered rigidification of membrane lipids enhances the cold inducibility of gene expression in Synechocystis. J Biol Chem 278:12191–12198

    Article  PubMed  CAS  Google Scholar 

  • Knight H, Knight MR (2000) Imaging spatial and cellular characteristics of low temperature calcium signature after cold acclimation in Arabidopsis. J Exp Bot 51:1679–1686

    Article  PubMed  CAS  Google Scholar 

  • Knight H, Trewavas AJ, Knight MR (1996) Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 8:489–503

    PubMed  CAS  Google Scholar 

  • Li L, Saga N, Mikami K (2009) Ca2+ influx and phosphoinositide signalling are essential for the establishment and maintenance of cell polarity in monospores from the red alga Porphyra yezoensis. J Exp Bot 60:3477–3489

    Article  PubMed  CAS  Google Scholar 

  • Li XC, Xing YZ, Jiang X, Qiao J, Tan HL, Tian Y, Zhou B (2012) Identification and characterization of the catalase gene PyCAT from the red alga Pyropia yezoensis (Bangiales, Rhodophyta). J Phycol 48:664–669

    Article  CAS  Google Scholar 

  • Liu B, Yao L, Wang WG, Gao JH, Chen F, Wang SH, Xu Y, Tang L, Jia YJ (2010) Molecular cloning and characterization of phospholipase D from Jatropha curcas. Mol Biol Rep 37:939–946

    Article  PubMed  CAS  Google Scholar 

  • Liu QX, Jindra M, Ueda H, Hiromi Y, Hirose S (2003) Drosophila MBF1 is a co-activator for tracheae defective and contributes to the formation of tracheal and nervous systems. Development 130:719–728

    Article  PubMed  CAS  Google Scholar 

  • Los DA, Murata N (2004) Membrane fluidity and its roles in the perception of environmental signals. Biochim Biophys Acta 1666:142–157

    Article  PubMed  CAS  Google Scholar 

  • Lu IF, Sung MS, Lee TM (2006) Salinity stress and hydrogen peroxide regulation of antioxidant defense system in Ulva fasciata. Mar Biol 150:1–15

    Article  CAS  Google Scholar 

  • Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158

    Article  PubMed  CAS  Google Scholar 

  • Mikami K, Uji T, Li L, Takahashi M, Yasui H, Saga N (2009) Visualization of phosphoinositides via the development of the transient expression system of a cyan fluorescent protein in the red alga Porphyra yezoensis. Mar Biotechnol 11:563–569

    Article  PubMed  CAS  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  PubMed  CAS  Google Scholar 

  • Mishkind M, Vermeer JEM, Darwish E, Munnik T (2009) Heat stress activates phospholipase D and triggers PIP2 accumulation at the plasma membrane and nucleus. Plant J 60:10–21

    Article  PubMed  CAS  Google Scholar 

  • Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:86–96

    Article  PubMed  CAS  Google Scholar 

  • Monroy AF, Dhindsa RS (1995) Low-temperature signal transduction: induction of cold acclimation-specific genes of alfalfa by calcium at 25 °C. Plant Cell 7:321–331

    PubMed  CAS  Google Scholar 

  • Munnik T, Arisz SA, deVrije T, Musgrave A (1995) G protein activation stimulates phospholipase D signaling in plants. Plant Cell 7:2197–2210

    PubMed  CAS  Google Scholar 

  • Näär AM, Lemon BD, Tjian R (2001) Transcriptional coactivator complexes. Annu Rev Biochem 70:475–501

    Article  PubMed  Google Scholar 

  • Nikaido I, Asamizu E, Nakajima M, Nakamura Y, Saga N, Tabata S (2000) Generation of 10,154 expressed sequence tags from a leafy gametophyte of a marine red alga, Porphyra yezoensis. DNA Res 7:223–227

    Article  PubMed  Google Scholar 

  • Örvar BL, Sangwan V, Omann F, Dhindsa RS (2000) Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. Plant J 23:785–794

    Article  PubMed  Google Scholar 

  • Pnueli L, Hallak-Herr E, Rozenberg M, Cohen M, Goloubinoff P, Kaplan A, Mittler R (2002) Molecular and biochemical mechanisms associated with dormancy and drought tolerance in the desert legume Retama raetam. Plant J 31:319–330

    Article  PubMed  CAS  Google Scholar 

  • Qin C, Wang X (2002) The Arabidopsis phospholipase D family. Characterization of a calcium-independent and phosphatidylcholine-selective PLDζ1 with distinct regulatory domains. Plant Physiol 128:1057–1068

    Article  PubMed  CAS  Google Scholar 

  • Rizhsky L, Liang HJ, Mittler R (2002) The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol 130:1143–1151

    Article  PubMed  CAS  Google Scholar 

  • Saga N, Kitade Y (2002) Porphyra: a model plant in marine sciences. Fish Sci 68(Suppl):1075–1078

    Google Scholar 

  • Sangwan V, Foulds I, Singh J, Dhindsa RS (2001) Cold-activation of Brassica napus BN115 promoter is mediated by structural changes in membranes and cytoskeleton, and requires Ca2+ influx. Plant J 27:1–12

    Article  PubMed  CAS  Google Scholar 

  • Sangwan V, Orvar BL, Beyerly J, Hirt H, Dhindsa RS (2002) Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J 31:629–638

    Article  PubMed  CAS  Google Scholar 

  • Suri SS, Dhindsa RS (2008) A heat-activated MAP kinase (HAMK) as a mediator of heat shock response in tobacco cells. Plant Cell Environ 31:218–226

    Article  PubMed  CAS  Google Scholar 

  • Sutherland JE, Lindstrom SC, Nelson WA, Brodie J, Lynch MDJ, Hwang MS, Choi HG, Miyata M, Kikuchi N, Oliveira MC, Farr T, Neefus C, Mols-Mortensen A, Milstein D, Müller KM (2011) A new look at an ancient order: generic revision of the Bangiales (Rhodophyta). J Phycol 47:1131–1151

    Article  Google Scholar 

  • Suzuki N, Rizhsky L, Liang HJ, Shuman J, Shulaev V, Mittler R (2005) Enhanced tolerance to environmental stress in transgenic plants expressing the transcriptional coactivator multiprotein bridging factor 1c. Plant Physiol 139:1313–1322

    Article  PubMed  CAS  Google Scholar 

  • Takemaru K, Harashima S, Ueda H, Hirose S (1998) Yeast coactivator MBF1 mediates GCN4-dependent transcriptional activation. Mol Cell Biol 18:4971–4976

    PubMed  CAS  Google Scholar 

  • Takemaru K, Li FQ, Ueda H, Hirose S (1997) Multiprotein bridging factor 1 (MBF1) is an evolutionarily conserved transcriptional coactivator that connects a regulatory factor and TATA element-binding protein. Proc Natl Acad Sci U S A 94:7251–7256

    Article  PubMed  CAS  Google Scholar 

  • Testerink C, Munnik T (2005) Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci 10:368–375

    Article  PubMed  CAS  Google Scholar 

  • Tsuda K, Yamazaki K (2004) Structure and expression analysis of three subtypes of Arabidopsis MBF1 genes. Biochim Biophys Acta 1680:1–10

    Article  PubMed  CAS  Google Scholar 

  • Uji T, Hirata R, Mikami K, Mizuta H, Saga N (2012a) Molecular characterization and expression analysis of sodium pump genes in the marine red alga Porphyra yezoensis. Mol Biol Rep 39:7973–7980

    Article  PubMed  CAS  Google Scholar 

  • Uji T, Monma R, Mizuta H, Saga N (2012b) Molecular characterization and expression analysis of two Na+/H+ antiporter genes in the marine red alga Porphyra yezoensis. Fish Sci 78:985–991

    Article  CAS  Google Scholar 

  • Uji T, Takahashi M, Saga N, Mikami K (2010) Visualization of nuclear localization of transcription factors with cyan and green fluorescent proteins in the red alga Porphyra yezoensis. Mar Biotechnol 12:150–159

    Article  PubMed  CAS  Google Scholar 

  • Wan SB, Wang W, Wen PF, Chen JY, Kong WF, Pan QH, Zhan JC, Tian L, Liu HT, Huang WD (2007) Cloning of phospholipase D from grape berry and its expression under heat acclimation. J Biochem Mol Biol 40:595–603

    Article  PubMed  CAS  Google Scholar 

  • Zonia L, Munnik T (2006) Cracking the green paradigm: functional coding of phosphoinositide signals in plant stress responses. Subcell Biochem 39:207–237

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported in part by a grant from the Regional Innovation Cluster Program (Global Type) of the Ministry of Education, Culture, Sports, Science and Technology of Japan to N.S.

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Correspondence to Naotsune Saga.

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Uji, T., Sato, R., Mizuta, H. et al. Changes in membrane fluidity and phospholipase D activity are required for heat activation of PyMBF1 in Pyropia yezoensis (Rhodophyta). J Appl Phycol 25, 1887–1893 (2013). https://doi.org/10.1007/s10811-013-0006-7

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  • DOI: https://doi.org/10.1007/s10811-013-0006-7

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