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Overexpression of a Zea mays phospholipase C1 gene enhances drought tolerance in tobacco in part by maintaining stability in the membrane lipid composition

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Abstract

Phosphatidylinositol-specific phospholipase C (PI-PLC: EC 3.1.4.11) plays key roles in a variety of physiological processes in plants. We previously reported that the putative PLC genes from maize (Zea mays L.) are transcriptionally upregulated in response to drought (Sui et al. in Gene 426:47–56, 2008). In this paper, we report the further characterization of ZmPLC1. First, the expression of ZmPLC1 successfully complemented the yeast plc1 mutant BY4742 and restored its growth defects with regard to galactose utilization. The determination of PLC activity in the transformed yeast strain further demonstrated the enzymatic properties of ZmPLC1. Second, we obtained drought stress-tolerant transgenic tobacco plants by overexpressing the maize PLC1 gene under the control of the CaMV 35S promoter. To determine whether ZmPLC1 regulates plants’ response to drought stress by regulating phospholipid and galactolipid levels, we analyzed the lipid species in ZmPLC1 transgenic and wild-type tobacco plants before and after drought treatment using an ESI–MS/MS approach. The results show that, under drought stress conditions, the overexpression of ZmPLC1 in tobacco maintained the stability of the unsaturated lipid species PtdIns, MGDG, DGDG, PE, and PC in leaves, whereas their levels in wild-type tobacco decreased dramatically. These results not only demonstrate the conserved function of ZmPLC1 and its practical applications in dicots, but also elucidate the molecular mechanism of the role PI-PLC plays in plant responses to drought stress.

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References

  • Athenstaedt K, Daum G (2001) Phosphatidic acid, a key intermediate in lipid metabolism. Eur J Biochem 266(1):1–16

    Article  Google Scholar 

  • Bargmann BOR, Laxalt AM, Riet B, Van Schooten B, Merquiol E, Testerink C, Haring MA, Bartels D, Munnik T (2009) Multiple PLDs required for high salinity and water deficit tolerance in plants. Plant Cell Physiol 50(1):78–89

    Article  PubMed  CAS  Google Scholar 

  • Benhassaine-Kesri G, Aid F, Demandre C, Kader JC, Mazliak P (2002) Drought stress affects chloroplast lipid metabolism in rape (Brassica napus) leaves. Physiol Plant 115(2):221–227

    Article  PubMed  CAS  Google Scholar 

  • Campos PS, Pham Thi AT (1997) Effects of an abscisic acid pretreatment on membrane leakage and lipid composition of Vigna unguiculata leaf discs subjected to osmotic stress. Plant Sci 130(1):11–18

    Article  CAS  Google Scholar 

  • De Paula FM, Thi A, De Silva JV, Justin A, Demandre C, Mazliak P (1990) Effects of water stress on the molecular species composition of polar lipids from Vigna unguiculata L. leaves. Plant Sci 66(2):185–193

    Article  Google Scholar 

  • Dubots E, Audry M, Yamaryo Y, Bastien O, Ohta H, Breton C, Maréchal E, Block MA (2010) Activation of the chloroplast monogalactosyldiacylglycerol synthase MGD1 by phosphatidic acid and phosphatidylglycerol. J Biol Chem 285(9):6003–6011

    Article  PubMed  CAS  Google Scholar 

  • Gaxiola RA, Li J, Undurraga S, Dang LM, Allen GJ, Alper SL, Fink GR (2001) Drought-and salt-tolerant plants result from overexpression of the AVP1 H+-pump. Proc Natl Acad Sci 98(20):11444–11449

    Article  PubMed  CAS  Google Scholar 

  • Georges F, Das S, Ray H, Bock C, Nokhrina K, Kolla VA, Keller W (2009) Over-expression of Brassica napus phosphatidylinositol-phospholipase C2 in canola induces significant changes in gene expression and phytohormone distribution patterns, enhances drought tolerance and promotes early flowering and maturation. Plant Cell Environ 32(12):1664–1681

    Article  PubMed  CAS  Google Scholar 

  • Gigon A, Matos AR, Laffray D, Zuily-Fodil Y, Pham-Thi AT (2004) Effect of drought stress on lipid metabolism in the leaves of Arabidopsis thaliana (ecotype Columbia). Ann Bot 94(3):345–351

    Article  PubMed  CAS  Google Scholar 

  • Guerfel M, Baccouri O, Boujnah D, Zarrouk M (2008) Changes in lipid composition, water relations and gas exchange in leaves of two young ‘Chemlali’and ‘Chetoui’olive trees in response to water stress. Plant Soil 311(1):121–129

    Article  CAS  Google Scholar 

  • Hirayama T, Ohto C, Mizoguchi T, Shinozaki K (1995) A gene encoding a phosphatidylinositol-specific phospholipase C is induced by dehydration and salt stress in Arabidopsis thaliana. Proc Natl Acad Sci 92(9):3903–3907

    Article  PubMed  CAS  Google Scholar 

  • Hirayama T, Mitsukawa N, Shibata D, Shinozaki K (1997) AtPLC2, a gene encoding phosphoinositide-specific phospholipase C, is constitutively expressed in vegetative and floral tissues in Arabidopsis thaliana. Plant Mol Biol 34(1):175–180

    Article  PubMed  CAS  Google Scholar 

  • Hofgen R, Willmitzer L (1988) Storage of competent cells for Agrobacterium transformation. Nucleic Acids Res 16(20):9877

    Article  PubMed  CAS  Google Scholar 

  • Hunt L, Mills LN, Pical C, Leckie CP, Aitken FL, Kopka J, Mueller-Roeber B, McAinsh MR, Hetherington AM, Gray JE (2003) Phospholipase C is required for the control of stomatal aperture by ABA. Plant J 34(1):47–55

    Article  PubMed  CAS  Google Scholar 

  • Ito H, Fukuda Y, Murata K, Kimura A (1983) Transformation of intact yeast cells treated with alkali cations. J Bacteriol 153(1):163–168

    PubMed  CAS  Google Scholar 

  • Kim YJ, Kim JE, Lee JH, Lee MH, Jung HW, Bahk YY, Hwang BK, Hwang I, Kim WT (2004) The Vr-PLC3 gene encodes a putative plasma membrane-localized phosphoinositide-specific phospholipase C whose expression is induced by abiotic stress in mung bean (Vigna radiata L.). FEBS Lett 556(1):127–136

    Article  PubMed  CAS  Google Scholar 

  • Kinnunen PKJ (2000) Lipid bilayers as osmotic response elements. Cell Physiol Biochem 10(5–6):243–250

    Article  PubMed  CAS  Google Scholar 

  • König S, Mosblech A, Heilmann I (2007) Stress-inducible and constitutive phosphoinositide pools have distinctive fatty acid patterns in Arabidopsis thaliana. FASEB J 21(9):1958–1967

    Article  PubMed  Google Scholar 

  • Larsson KE, Nyström B, Liljenberg C (2006) A phosphatidylserine decarboxylase activity in root cells of oat (Avena sativa) is involved in altering membrane phospholipid composition during drought stress acclimation. Plant Physiol Biochem 44(4):211–219

    Article  PubMed  CAS  Google Scholar 

  • Li W, Wang R, Li M, Li L, Wang C, Welti R, Wang X (2008) Differential degradation of extraplastidic and plastidic lipids during freezing and post-freezing recovery in Arabidopsis thaliana. J Biol Chem 283(1):461–468

    Article  PubMed  CAS  Google Scholar 

  • Mills LN, Hunt L, Leckie CP, Aitken FL, Wentworth M, McAinsh MR, Gray JE, Hetherington AM (2004) The effects of manipulating phospholipase C on guard cell ABA-signalling. J Exp Bot 55(395):199–204

    Article  PubMed  CAS  Google Scholar 

  • Moellering ER, Benning C (2011) Galactoglycerolipid metabolism under stress: a time for remodeling. Trends Plant Sci 16(2):98–107

    Article  PubMed  CAS  Google Scholar 

  • Monteiro de Paula F, THI A, Zuily-Fodil Y, Ferrari-Iliou R, Vieira da Silva J, Mazliak P (1993) Effects of water stress on the biosynthesis and degradation of polyunsaturated lipid molecular species in leaves of Vigna unguiculata. Plant Physiol Biochem 31(5):707–715

    CAS  Google Scholar 

  • Munnik T, Vermeer JEM (2009) Osmotic stress-induced phosphoinositide and inositol phosphate signalling in plants. Plant Cell Environ 33(4):655–669

    Article  Google Scholar 

  • Ohlroggeav J, Browseb J (1995) Lipid biosynthesis. Plant cell 7:957–970

    Google Scholar 

  • Sanchez JP, Chua NH (2001) Arabidopsis PLC1 is required for secondary responses to abscisic acid signals. Plant Cell 13(5):1143–1154

    PubMed  CAS  Google Scholar 

  • Shou H, Bordallo P, Fan J-B, Yeakley JM, Bibikova M, Sheen J, Wang K (2004) Expression of an active tobacco mitogen-activated protein kinase kinase kinase enhances freezing tolerance in transgenic maize. Proc Natl Acad Sci USA 101(9):3298–3303

    Article  PubMed  CAS  Google Scholar 

  • Sui Z, Niu L, Yue G, Yang A, Zhang J (2008) Cloning and expression analysis of some genes involved in the phosphoinositide and phospholipid signaling pathways from maize (Zea mays L.). Gene 426(1):47–56

    Article  PubMed  CAS  Google Scholar 

  • Testerink C, Munnik T (2005) Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci 10(8):368–375

    Article  PubMed  CAS  Google Scholar 

  • Testerink C, Munnik T (2011) Molecular, cellular, and physiological responses to phosphatidic acid formation in plants. J Exp Bot 62(7):2349–2361

    Article  PubMed  CAS  Google Scholar 

  • Torres-Franklin ML, Gigon A, De Melo DF, Zuily-Fodil Y, Pham-Thi AT (2007) Drought stress and rehydration affect the balance between MGDG and DGDG synthesis in cowpea leaves. Physiol Plant 131(2):201–210

    PubMed  CAS  Google Scholar 

  • Voelker T, Sturm A, Chrispeels MJ (1987) Differences in expression between two seed lectin alleles obtained from normal and lectin-deficient beans are maintained in transgenic tobacco. EMBO J 6(12):3571

    PubMed  CAS  Google Scholar 

  • Wada H, Murata N (2007) The essential role of phosphatidylglycerol in photosynthesis. Photosynth Res 92(2):205–215

    Article  PubMed  CAS  Google Scholar 

  • Wang CR, Yang AF, Yue GD, Gao Q, Yin HY, Zhang JR (2008) Enhanced expression of phospholipase C 1 (ZmPLC1) improves drought tolerance in transgenic maize. Planta 227(5):1127–1140

    Article  PubMed  CAS  Google Scholar 

  • Welti R, Li W, Li M, Sang Y, Biesiada H, Zhou HE, Rajashekar C, Williams TD, Wang X (2002) Profiling membrane lipids in plant stress responses. J Biol Chem 277(35):31994–32002

    Article  PubMed  CAS  Google Scholar 

  • Xu C, Härtel H, Wada H, Hagio M, Yu B, Eakin C, Benning C (2002) The pgp1 mutant locus of Arabidopsis encodes a phosphatidylglycerolphosphate synthase with impaired activity. Plant Physiol 129(2):594–604

    Article  PubMed  CAS  Google Scholar 

  • Xue HW, Chen X, Mei Y (2009) Function and regulation of phospholipid signalling in plants. Biochem J 421(Pt 2):145

    Article  PubMed  CAS  Google Scholar 

  • Zhai SM, Gao Q, Xue HW, Sui ZH, Yue GD, Yang AF, Zhang JR (2012) Overexpression of the phosphatidylinositol synthase gene from Zea mays in tobacco plants alters the membrane lipids composition and improves drought stress tolerance. Planta 235(1):69–84

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank the Kansas Lipidomics Research Center Analytical Laboratory for lipid analysis. The laboratory is supported by the National Science Foundation’s EPSCoR program under grant no. EPS-0236913 with matching support from the State of Kansas through Kansas Technology Enterprise Corporation and Kansas State University. This work was supported by Hi-Tech Research and Development (863) Program of China (2012AA10A306), the National Basic Research Program of China (973 Program, 2009CB118400), the National Science Foundation of China (20902054) and the Independent Innovation Foundation of Shandong University (2010TS093).

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Authors and Affiliations

  1. School of Chemistry and Chemical Engineering, Shandong University, Jinan, 250100, People’s Republic of China

    Shumei Zhai

  2. School of Life Science, Shandong University, 27 Shanda South Road, Jinan, 250100, People’s Republic of China

    Shumei Zhai, Qiang Gao, Xiuxia Liu, Zhenhua Sui & Juren Zhang

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  1. Shumei Zhai
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  2. Qiang Gao
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  3. Xiuxia Liu
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  4. Zhenhua Sui
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  5. Juren Zhang
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Correspondence to Juren Zhang.

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Zhai, S., Gao, Q., Liu, X. et al. Overexpression of a Zea mays phospholipase C1 gene enhances drought tolerance in tobacco in part by maintaining stability in the membrane lipid composition. Plant Cell Tiss Organ Cult 115, 253–262 (2013). https://doi.org/10.1007/s11240-013-0358-3

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