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Modulation of nitrate reductase activity by photosynthetic electron transport chain and nitric oxide balance in the red macroalga Gracilaria chilensis (Gracilariales, Rhodophyta)

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Abstract

Nitrate reductase (NR), a key enzyme in nitrogen metabolism, has been implicated in the production of nitric oxide (NO) in plants. The effect of photosynthetic electron transport chain inhibitors and NO scavengers or donors on NR activity of Gracilaria chilensis was studied under experimental laboratory conditions. Effective quantum yield (Φ PSII) and NR activity were significantly diminished by 3-(3,4-dichlorophenyl)-1,1-dimethylurea and 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone, two photosynthetic electron flux inhibitors of photosystem (PS) II and PSI, respectively, but not by diphenyleneiodonium, a NADPH oxidase inhibitor, indicating a direct dependence of NR activity on the PSII and PSI electron flux. Nitrate reductase activity was sensitive to a decrease or increase of NO levels when NO scavenger (2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide) and NO donor (sodium nitroprusside) were added. Moreover, the addition of 8Br-cGMP, a secondary signal molecule, stimulated NR activity. These results evidence a modulation of the photosynthetic electron transport chain and NO balance on G. chilensis NR activity. This association could be linked to the crucial tight modulation of nitrogen assimilation and carbon metabolism to guarantee nitrite incorporation into organic compounds and to avoid toxicity by nitrite, reactive oxygen species, or nitric oxide in the cells. Nitric oxide showed to be an important signaling molecule regulating NR activity and cGMP could participate as secondary messenger on this regulation by phosphorylation and desphosphorylation processes.

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References

  • Basra A, Dhawan AK, Goyal SS (2002) DCMU inhibits in vivo nitrate reduction in illuminated barley (C3) leaves but not in maize (C4): a new mechanism for the role of light? Planta 215:855–861

    Article  CAS  PubMed  Google Scholar 

  • Bassham JA, Larsen PO, Cornwell AL (1981) Relationships between nitrogen metabolism and photosynthesis. In: Bewley JD (ed) Nitrogen and carbon metabolism. Development in plant and soil science. Dr. W. Junk, London, pp 135–163

    Chapter  Google Scholar 

  • Beligni MV, Lamattina L (2001) Nitric oxide in plants: the history is just beginning. Plant Cell Environ 24:267–278

    Article  CAS  Google Scholar 

  • Buschmann AH, Westermeier R, Retamales CA (1995) Cultivation of Gracilaria on the sea-bottom in southern Chile: a review. J Appl Phycol 7:291–301

    Article  Google Scholar 

  • Chow F, Oliveira MC, Pédersem M (2004) In vitro assay and light regulation of nitrate reductase in red alga Gracilaria chilensis. J Plant Physiol 161:769–776

    Article  CAS  PubMed  Google Scholar 

  • Cooney RV, Harwood PJ, Custer LJ, Franke AA (1994) Light-mediated conversion of nitrogen-dioxide to nitric-oxide by carotenoids. Environ Health Persp 102:460–462

    Article  CAS  Google Scholar 

  • Crawford NM (2006) Mechanisms for nitric oxide synthesis in plants. J Exp Bot 57:471–478

    Article  CAS  PubMed  Google Scholar 

  • Dean JV, Harper JE (1988) The conversion of nitrite to nitrogen oxide(s) by the constitutive NAD(P)H-nitrate reductase enzyme from soybean. Plant Physiol 88:389–395

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Desikan R, Cheung M-K, Bright J, Henson D, Hancock JT, Neill SJ (2002) ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. J Exp Bot 55:205–212

    Article  Google Scholar 

  • Du S, Zhang Y, Lin X, Wang Y, Tang C (2008) Regulation of nitrate reductase by nitric oxide in Chinese cabbage pakchoi (Brassica chinensis L.). Plant Cell Environ 31:195–204

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Edwards P (1970) Illustrated guide to the seaweeds and sea grasses in the vicinity of Porto Aransas, Texas. Contr Mar Sci Austin 15:1–228

    Google Scholar 

  • García-Mata C, Lamattina L (2003) Abscisic acid, nitric oxide and stomatal closure. Is nitrate reductase one of the missing links? Trends Plant Sci 8:20–26

    Article  PubMed  Google Scholar 

  • Givan CV, Joy KW, Kleczkoski LA (1988) A decade of photorespiratory nitrogen cycling. Trends Biochem Sci 13:433–437

    Article  CAS  PubMed  Google Scholar 

  • Huppe HC, Turpin DH (1994) Integration of carbon and nitrogen metabolism on plant and algal cells. Annu Rev Plant Physiol Mol Biol 45:577–607

    Article  CAS  Google Scholar 

  • Jansson EÅ, Huang L, Malkey R, Govoni M, Nihlén C, Olsson A, Stensdotter M, Petersson J, Holm L, Weitzberg E, Lundberg JO (2008) A mammalian functional nitrate reductase that regulates nitrite and nitric oxide homeostasis. Nat Chem Biol 4:411–417

    Article  CAS  PubMed  Google Scholar 

  • Jin CW, Du ST, Zhang YS, Lin XY, Tang CX (2009) Differential regulatory role of nitric oxide in mediating nitrate reductase activity in roots of tomato (Solanum lycocarpum). Ann Bot 104:9–17

    Article  CAS  PubMed  Google Scholar 

  • Kleczkowski LA (1994) Inhibitors of photosynthetic enzymes/carriers and metabolism. Annu Rev Plant Physiol Plant Mol Biol 45:339–367

    Article  CAS  Google Scholar 

  • Klepper L (1990) Comparison between NOx evolution mechanisms of wild-type and NR1 mutant soybean leaves. Plant Physiol 93:26–32

    Article  CAS  PubMed  Google Scholar 

  • Klepper L (1991) NOx evolution by soybean leaves treated with salicylic-acid and selected derivates. Pestic Biochem Phys 39:43–48

    Article  CAS  Google Scholar 

  • Lacza Z, Pankotai E, Csordás A, Gero D, Kiss L, Horváth EM, Kollai M, Busija DW, Szabó C (2006) Mitochondrial NO and reactive nitrogen species production: does mtNOS exist? Nitric Oxide 14:162–168

    Article  CAS  PubMed  Google Scholar 

  • Lea P, Blackwell RD (1992) The role of amino acid metabolism in photosynthesis. In: Singh BK, Shannon JC, Flores H (eds) Biosynthesis and molecular regulation of amino acids in plants. American Society of Plant Physiologists, Rockville, pp 98–110

    Google Scholar 

  • Leshesm YY (1996) Nitric oxide in biological systems. Plant Growth Regul 18:155–159

    Article  Google Scholar 

  • Li X, Oaks A (1994) Induction and turnover of nitrate reductase in Zea mays. Plant Physiol 106:1145–1149

    CAS  PubMed  Google Scholar 

  • Mallick N, Rai LC, Mohn FH, Soeder CJ (1999) Studies on nitric oxide (NO) formation by the green alga Scenedesmus obliquus and the diazotrophic cyanobacterium Anabena doliolum. Chemosphere 39:1601–1610

    Article  CAS  PubMed  Google Scholar 

  • Mazur BJ, Falco SC (1989) The development of herbicide resistant crops. Annu Rev Plant Physiol Plant Mol Biol 40:441–470

    Article  CAS  Google Scholar 

  • McDonald LJ, Murad F (1995) Nitric oxide and cGMP signaling. Adv Pharmacol 34:263–276

    Article  CAS  PubMed  Google Scholar 

  • Meyer C, Lea US, Provan F, Kaiser WM, Lillo C (2005) Is nitrate reductase a major player in the plant NO (nitric oxide) game? Photosynth Res 83:181–189

    Article  CAS  PubMed  Google Scholar 

  • Moreland DE (1980) Mechanisms of action of herbicides. Annu Rev Plant Physiol 31:597–638

    Article  CAS  Google Scholar 

  • Nishimura H, Hayamizu T, Yanagisawa Y (1986) Reduction of NO2 to NO by rush and other plants. Environ Sci Technol 20:413–416

    Article  CAS  PubMed  Google Scholar 

  • Provan F, Lillo C (1999) Photosynthetic post-translational activation of nitrate reductase. J Plant Physiol 154:605–609

    Article  CAS  Google Scholar 

  • Rockel P, Strube F, Rockel A, Wildt J, Kaiser WM (2002) Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J Exp Bot 53:103–110

    Article  CAS  PubMed  Google Scholar 

  • Rosales EP, Iannone MF, Groppa MD, Benavides MP (2011) Nitric oxide inhibits nitrate reductase activity in wheat leaves. Plant Physiol Biochem 49:124–130

    Article  CAS  PubMed  Google Scholar 

  • Sakihama Y, Nakamura S, Yamasaki H (2002) Nitric oxide production mediated by nitrate reductase in the green alga Chlamydomonas reinhardtii: an alternative NO production pathway in photosynthetic organisms. Plant Cell Physiol 43:290–297

    Article  CAS  PubMed  Google Scholar 

  • Sandmann G, Böger P (1986) Sites of herbicide inhibition at the photosynthetic apparatus. In: Staehelin LA, Arntzen CJ (eds) Encyclopedia of plant physiology, vol 19. Springer, Berlin, pp 596–602

    Google Scholar 

  • Syrett PJ (1981) Nitrogen metabolism of microalgae. In: Platt T (ed) Physiological bases of phytoplankton ecology. Can Bull Fish Aquat Sci 210: 182–210

  • Turpin DH (1991) Effects of inorganic N availability on algal photosynthesis and carbon metabolism. J Phycol 27:14–20

    Article  CAS  Google Scholar 

  • Van Camp W, Van Montagu M, Inze D (1998) H2O2 and NO: redox signals in disease resistance. Trends Plant Sci 3:330–334

    Article  Google Scholar 

  • Van Rensen JJS (1989) Herbicides interacting with photosystem II. In: Dodge AD (ed) Herbicides and plant metabolism. Cambridge University Press, Cambridge, pp 21–36

    Google Scholar 

  • Yamamoto-Katou A, Katou S, Yoshioka H, Doke N, Kawakita K (2006) Nitrate reductase is responsible for elicitin-induced nitric oxide production in Nicotiana benthamiana. Plant Cell Physiol 47:726–735

    Article  CAS  PubMed  Google Scholar 

  • Yamasaki H, Sakihama Y (2000) Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vivo evidence for the NR-dependent formation of active nitrogen species. FEBS Lett 468:89–92

    Article  CAS  PubMed  Google Scholar 

  • Yamasaki H, Sakihama Y, Takahashi S (1999) An alternative pathway for nitric oxide production in plants: new features of an old enzyme. Trends Plant Sci 4:128–129

    Article  PubMed  Google Scholar 

  • Zar JH (1999) Biostatistical analysis, 4th edn. Prentice-Hall, Englewood Cliffs

    Google Scholar 

Download references

Acknowledgments

This investigation was supported by the National Council for Research and Development (CNPq, Brazil), State of São Paulo Research Foundation (FAPESP, Brazil), and Swedish Foundation for International Cooperation in Research and Higher Education (STINT). The authors thank Stanislaw Karpinski for laboratorial support with photosynthesis analysis.

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Authors and Affiliations

  1. Department of Botany, Institute of Bioscience, University of São Paulo, São Paulo, SP, Brazil

    Fungyi Chow & Mariana C. Oliveira

  2. Department of Botany, Stockholm University, Stockholm, Sweden

    Marianne Pedersén

  3. Departamento de Botânica, Instituto de Biociências, Universidade de São Paulo, Rua do Matão 277, 05508-090, São Paulo, SP, Brazil

    Fungyi Chow

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  1. Fungyi Chow
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  2. Marianne Pedersén
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  3. Mariana C. Oliveira
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Correspondence to Fungyi Chow.

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Chow, F., Pedersén, M. & Oliveira, M.C. Modulation of nitrate reductase activity by photosynthetic electron transport chain and nitric oxide balance in the red macroalga Gracilaria chilensis (Gracilariales, Rhodophyta). J Appl Phycol 25, 1847–1853 (2013). https://doi.org/10.1007/s10811-013-0005-8

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  • DOI: https://doi.org/10.1007/s10811-013-0005-8

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