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Mechanisms of Extracellular NO and Ca2+ Regulating the Growth of Wheat Seedling Roots

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Abstract

Our previous studies suggested the cross talk of nitric oxide (NO) with Ca2+ in regulating stomatal movement. However, its mechanism of action is not well defined in plant roots. In this study, sodium nitroprusside (SNP, a NO donor) showed an inhibitory effect on the growth of wheat seedling roots in a dose-dependent manner, which was alleviated through reducing extracellular Ca2+ concentration. Analyzing the content of Ca2+ and K+ in wheat seedling roots showed that SNP significantly promoted Ca2+ accumulation and inhibited K+ accumulation at a higher concentration of extracellular Ca2+, but SNP promoted K+ accumulation in the absence of extracellular Ca2+. To gain further insights into Ca2+ function in the NO-regulated growth of wheat seedling roots, we conducted the patch-clamped protoplasts of wheat seedling roots in a whole cell configuration. In the absence of extracellular Ca2+, NO activated inward-rectifying K+ channels, but had little effects on outward-rectifying K+ channels. In the presence of 2 mmol L−1 CaCl2 in the bath solution, NO significantly activated outward-rectifying K+ channels, which was partially alleviated by LaCl3 (a Ca2+ channel inhibitor). In contrast, 2 mmol L−1 CaCl2 alone had little effect on inward or outward-rectifying K+ channels. Thus, NO inhibits the growth of wheat seedling roots likely by promoting extracellular Ca2+ influx excessively. The increase in cytosolic Ca2+ appears to inhibit K+ influx, promotes K+ outflux across the plasma membrane, and finally reduces the content of K+ in root cells.

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References

  • Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signaling. Nat Rev Mol Cell Biol 1(1):11–21

    Article  CAS  PubMed  Google Scholar 

  • Besson-Barda AL, Courtoisa C, Gauthiera A, Dahana J, Dobrowolska G, Jeandrozc S, Pugina A, Wendehennea D (2008) Nitric oxide in plants: production and cross-talk with Ca2+ signaling. Mol Plant 1(2):218–228

    Article  Google Scholar 

  • Chen CW, Yang YW, Lur HS, Tski YG, Chang MC (2006) A novel function of abscisic acid in the regulation of rice (Oryza sativa L.) root growth and development. Plant Cell Physiol 47:1–13

    Article  PubMed  Google Scholar 

  • Clarkson DT, Hanson JB (1980) The mineral nutrition of higher plants. Annu Rev Plant Physiol 31:239–298

    Article  CAS  Google Scholar 

  • Clementi E (1998) Role of nitric oxide and its intracellular signaling pathways in the control of Ca2+ homeostasis. Biochem Pharmacol 55:713–718

    Article  CAS  PubMed  Google Scholar 

  • Correa-aragunde N, Graziano M, Lacattina L (2004) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218:900–905

    Article  CAS  PubMed  Google Scholar 

  • Cram WJ (1973) Chloride fluxes in cells of the isolated root cortex of Zea mays. Aust J Biol Sci 26:757–759

    CAS  Google Scholar 

  • Delledonne M, Xia Y, Dixon RA, Lamb C (1998) Nitric oxide functions as a signal in plant disease resistance. Nature 394:585–588

    Article  CAS  PubMed  Google Scholar 

  • Durner J, Wendehenne D, Klessig DF (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP2 ribose. Proc Natl Acad Sci USA 95(17):10328–10333

    Article  CAS  PubMed  Google Scholar 

  • Findlay GP, Tyerman SD, Garrill A, Skerrett M (1994) Pump and K+ inward rectifiers in the plasmalemma of wheat root protoplasts. J Membr Biol 139:103–116

    CAS  PubMed  Google Scholar 

  • Furchgott RF (1995) Special topic: nitric oxide. Annu Rev Physiol 57:695–682

    Google Scholar 

  • Gabriele BM, Tatiana NB, Manfred HW, Simon G (2009) Ca2+ regulates reactive oxygen species production and pH changes in Arabidopsis roots. Plant Cell 21:2341–2356

    Article  Google Scholar 

  • Garcia-Mata C, Gay R, Sokolvski S, Hills A, Lamattina L, Blatt MR (2003) Nitric oxide regulate K+ and Cl channels in guard cells through a subset of abscisic scid-evoked signaling pathways. Proc Natl Acad Sci 100:1116–1121

    Article  Google Scholar 

  • Gould KS, Lamotte O, Klinguer A, Pugin A, Wendehenne D (2003) Nitric oxide production in tobacco leaf cells: a generalized stress response? Plant Cell Environ 26:1851–1862

    Article  CAS  Google Scholar 

  • Hamill OP, Marty A, Neher E, Sakmann B, Sigworth FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 391:85–100

    Article  CAS  PubMed  Google Scholar 

  • Kiegle E, Gillihan M, Haseloff J, Tester M (2000) Hyperpolarisation-activated calcium currents found only in cells from the elongation zone of Arabidopsis thaliana roots. Plant J 21:225–229

    Article  CAS  PubMed  Google Scholar 

  • Knight H, Trewavas AJ, Knight MR (1997) Calcium signaling in Arabidopsis thaliana responding to drought and salinity. Plant J 12:1067–1078

    Article  CAS  PubMed  Google Scholar 

  • Kochian LV, Xin-Zhi J, Lucas WJ (1985) Potassium transport in corn roots. IV. Characterization of the linear component. Plant Physiol 79:771–776

    Article  CAS  PubMed  Google Scholar 

  • Lamotte O, Courtois C, DobrowolskaG BA, Pugin A, Wendehenne D (2006) Mechanisms of nitric-oxide-induced increase of free cytosolic Ca2+ concentration in Nicotiana plumbaginifolia cells. Free Radic Biol Med 40:1369–1376

    Article  CAS  PubMed  Google Scholar 

  • Lee HC (2001) Physiological functions of cyclic ADP ribose and NAAP as calcium messengers. Annu Rev Pharmacol Toxicol 41:317–345

    Article  PubMed  Google Scholar 

  • Mcainsh MR, Brownlee C, Hetherington AM (1990) Abscisic acid-induced elevation of guard cell cytoplasmic Ca2+ precedes stomatal closure. Nature 343:186–188

    Article  CAS  Google Scholar 

  • Mcainsh MR, Webb AAR, Taylor JE, Hetherington AM (1995) Stimulus-induced oscillations in guard cell cytoplasmic free calcium. Plant Cell 7:1207–1219

    Article  CAS  PubMed  Google Scholar 

  • McClung CR (2006) Plant circadian rhythms. Plant Cell 18:792–803

    Article  CAS  PubMed  Google Scholar 

  • Pagnussat GC, Simontacchi M, Puntarulo S, Lamattina L (2002) Nitric oxide is required for root organogenesis. Plant Physiol 129:954–956

    Article  CAS  PubMed  Google Scholar 

  • Pagnussat GC, Lanteri ML, Lombardo ML, Lamattina L (2004) Nitric oxide mediates the indole acetic acid induction activation of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiol 135:279–286

    Article  CAS  PubMed  Google Scholar 

  • Pei ZM, Murata Y, Benning G, Thomine S, Kluesener B, Allen GJ, Grill E, Schroeder JI (2000) Calcium channels activated by hydrogen peroxide mediate abscisic acid signaling in guard cells. Nature 406:731–734

    Article  CAS  PubMed  Google Scholar 

  • Schiefelbein JW, Shipley A, Rowse P (1992) Calcium influx at the tip of growing root-hair cells of Arabidopsis thaliana. Planta 187:455–459

    Article  CAS  Google Scholar 

  • Schroeder JI, Hagiwara S (1989) Cytosolic calcium regulates ion channels in the plasma membrane of Vicia faba guard cells. Nature 338:427–430

    Article  Google Scholar 

  • Sokolovski S, Blatt MR (2004) Nitric oxide block of outward-rectifying K+ channels indicates direct control by protein nitrosylation in guard cells. Plant Physiol 136:4275–4284

    Article  CAS  PubMed  Google Scholar 

  • Tang RH, Han SC, Zheng HL, Cook CW, Choi CS, Woerner TE, Jackson RB, Pei ZM (2007) Coupling diurnal cytosolic Ca2+ oscillations to the CAS-IP3 pathway in Arabidopsis. Science 315:1423–1426

    Article  CAS  PubMed  Google Scholar 

  • Very AA, Davies JM (2000) Hyperpolarization-activated calcium channels at the tip of Arabidopsis root hairs. Proc Natl Acad Sci USA 97:9801–9806

    Article  CAS  PubMed  Google Scholar 

  • Wen Y, Zhao X, Zhang X (2008) Effects of nitric oxide on root growth and absorption in wheat seedlings in response to water stress. Acta Agron Sin 34(2):344–348

    Article  CAS  Google Scholar 

  • Zhang L, Zhao X, Wang YJ, Zhang X (2009) Crosstalk of NO with Ca2+ in stomatal movement in Vicia faba guard cells. Acta Agron Sin 35(8):1491–1499

    CAS  Google Scholar 

  • Zhao FG, Song CP, He JQ, Zhu H (2007) Polyamines improve K+/Na+ homeostasis in barley seedlings by regulating root ion channel activities. Plant Physiol 145:1061–1072

    Article  CAS  PubMed  Google Scholar 

  • Zhao X, Wang YL, Wang YJ, Wang XL, Zhang X (2008) Effects of exogenous Ca2+ on stomatal movement and plasma membrane K+ channels of Vicia faba guard cell under salt stress. Acta Agron Sin 34(11):1970–1976

    Article  CAS  Google Scholar 

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Acknowledgments

Financial supports from National Natural Science Foundation of China (30871300) are acknowledged.

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Correspondence to Xiao Zhang.

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Zhao, X., Zhao, Xw., He, H. et al. Mechanisms of Extracellular NO and Ca2+ Regulating the Growth of Wheat Seedling Roots. J. Plant Biol. 53, 275–281 (2010). https://doi.org/10.1007/s12374-010-9114-y

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  • DOI: https://doi.org/10.1007/s12374-010-9114-y

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