Acta Physiologiae Plantarum

, Volume 26, Issue 4, pp 459–473

The role of nitric oxide in plant growth regulation and responses to abiotic stresses

Review

Abstract

Nitric oxide (NO) has received much attention in the recent two decades, equally from human, animal and plant biologists. It was found to play a crucial role in human and animal physiology, immunological reactions and signal transduction. Its ubiquity and versatile properties caught the attention of plant physiologists and biochemists. This work presents an extensive review on the NO presence and action in plants. Various modes of NO synthesis are discussed and the most novel approaches to the elucidation of plant nitric oxide synthase (NOS) structure are presented. This review focuses on the physiological role of NO in regulation of plant growth and development, as well as in the process of gene expression. Special attention is given to the action of NO during abiotic stress and the antioxidant properties of the molecule.

Key words

antioxidant enzymes heavy metals plant growth rhizogenesis stomatal closure signaling nitric oxide synthase 

List of abbreviations

AFLP

cDNA-amplification fragment length polymorphism

AOX

alternative oxidase

APOD

ascorbate peroxidase

APR2

5′-adenylylphosphosulfate reductase

cADPR

cyclic ADP Ribose

CAT

catalase

DAF-2DA

4,5-diaminofluorescein diacetate

GA

gibberellic acid

GDC

glycine decarboxylase

GR

glutathione reductase

kDa

kilodaltons

GST

glutathione-S-transferase

Hb

hemoglobin

IAA

indole-3-acetic acid

IPO

ipomoelin

Lhca

Lhcb-light-harvesting chlorophyll a/b binding proteins

MAPK

mitogen activated protein kinase

MDA

malondialdehyde

Ni:NOR

nitrite: NO-reductase

NMMA

NG-monomethyl-L-arginine

NO

nitric oxide

NOS

nitric oxide synthase

NR

nitrate reductase

OGA

oligogalacturonic acid

PAD4

phytoalexin-deficient 4 protein

PAL

phenylalanine ammonia lyase

PCD

programmed cell death

phyA

phytochrome A

phyB

phytochrome B

POX

general peroxidase

PQ

paraquat

PR-1

pathogenesis related protein 1

PTIO

2-(4-carboxy-2-phenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide

ROS

reactive oxygen species

RWC

relative water content

SIN-1

3-morpholinosydnonimine

SNAP

S-nitroso-N-acetylpenicillamine

SNP

sodium nitroprusside

SOD

superoxide dismutase

XOR

xanthine reductase

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References

  1. Arteel G.E., Briviba K., Sies H. 1999. Protection against peroxynitrite. FEBS Let. 445: 226–230.CrossRefGoogle Scholar
  2. Barroso J.B., Corpas F.J., Carreras A., Sandalio L.M., Valderrama R., Palma J.M., Lupianez J.A., del Rio L. 1999. Localization of nitric oxide synthase in plant peroxisomes. The Journal of Biol. Chem. 274: 36729–36733.CrossRefGoogle Scholar
  3. Batak I., Devi M., Giba Z., Grubisi A., Poff K.L., Konjevi R. 2002. The effects of potassium nitrate and NO-donors on phytochrome A- and phytochrome B-induced germination of Arabidopsis thaliana seeds. Seed Sci. Res. 12: 253–257.CrossRefGoogle Scholar
  4. Beligni M.V., Lamattina L. 1999. Nitric oxide counteracts cytotoxic processes mediated by reactive oxygen species in plant tissues, Planta 208: 337–344.CrossRefGoogle Scholar
  5. Beligni M.V., Lamattina L. 2000. Nitric oxide stimulates seed germination, de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants. Planta 210: 215–221.PubMedCrossRefGoogle Scholar
  6. Beligni M.V., Lamattina L. 2001. Nitric oxide in plants: the history is just beginning. Plant Cell Environ. 24: 267–278.CrossRefGoogle Scholar
  7. Bellligni M.V., Lamattina L. 2002. Nitric oxide interferes with plant photo-oxidative stress by detoxifying reactive oxygen species. Plant Cell Environ. 25: 737–743.CrossRefGoogle Scholar
  8. Beligni M.V., Fath A., Bethke P.C., Lamattina L., Jones R.L. 2002. Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers. Plant Physiol. 129: 1642–1650.PubMedCrossRefGoogle Scholar
  9. Brannan R.G., Connolly B.J., Decker E.A. 2001. Peroxynitrite: a potential initiator of lipid oxidation in food. Trends in Food Sci & Technol. 12: 164–173.CrossRefGoogle Scholar
  10. Capone R., Tiwari B.S., Levine A. 2004. Rapid transmission of oxidative and nitrosative stress signals from roots to shoots in Arabidopsis. Plant Physiol. Biochem. 42: 425–428.PubMedCrossRefGoogle Scholar
  11. Caro A., Puntarulo S. 1998. Nitric oxide decreases superoxide anion generation by microsomes from soybean embryonic axes. Physiol. Plant. 104: 357–364.CrossRefGoogle Scholar
  12. Clarke A., Desikan R., Hurst R.D., Hancock J.T, Neill S.J. 2000. NO way back: nitric oxide and programmed cell death in Arabidopsis thaliana suspension cultures. The Plant J. 24: 667–677.CrossRefGoogle Scholar
  13. Correa-Aragunde N., Graziano M., Lamattina L. 2004. Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218: 900–905.PubMedCrossRefGoogle Scholar
  14. Cueto M., Hernandez-Perera O., Martin R., Bentura M.L., Rodrigo J., Lamas S., Golvano M.P. 1996. Presence of nitric oxide synthase activity in roots and nodules of Lupinus albus. FEBS Let. 398: 159–164.CrossRefGoogle Scholar
  15. Delledonne M., Xia Y., Dixon R.A., Lamb C. 1998. Nitric oxide functions as a signal in plant disease resistance, Nature 394: 585–588.PubMedCrossRefGoogle Scholar
  16. Delledonne M., Zeier J., Marocco A., Lamb C. 2001. Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. PNAS 98: 13454–13459.PubMedCrossRefGoogle Scholar
  17. Delledonne M., Murgia I., Ederle D., Sbicego P.F., Biondani A., Polverari A., Lamb C. 2002. Reactive oxygen intermediates modulate nitric oxide signaling in the plant hypersensitive disease-resistance response. Plant Physiol. Biochem. 40: 605–610.CrossRefGoogle Scholar
  18. Desikan R., Griffiths R., Hancock J., Neill S. 2002. A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. PNAS 99:16314–16318.PubMedCrossRefGoogle Scholar
  19. Desikan R., Cheung M.K., Bright J., Henson D., Hancock J.T., Neill S.J. 2004. ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. J.Exp.Bot. 55: 205–212.PubMedCrossRefGoogle Scholar
  20. Dordas C., Rivoal J., Hill R.D. 2003a. Plant haemoglobins, nitric oxide and hypoxic stress. Annals of Bot. 91: 173–178.CrossRefGoogle Scholar
  21. Dordas C., Hasinoff B.B., Igamberdiev A.U., Manach N., Rivoal J., Hill R.D. 2003b. Expression of a stress-induced hemoglobin affects NO levels produced by alfalfa root cultures under hypoxic stress. The Plant J. 35: 763–770.CrossRefGoogle Scholar
  22. Durner J., Wendehenne D., Klessig D.F. 1998. Defense gene induction in tobacco by nitric oxide, cyclic GMP and cyclic ADP-ribose. PNAS 95: 10328–10333.PubMedCrossRefGoogle Scholar
  23. Foissner I., Wendehenne D., Langebartels C., Durner J. 2000. In vivo imaging of an elicitor-induced nitric oxide burst in tobacco. Plant Journal 23: 817–824.PubMedCrossRefGoogle Scholar
  24. Garces H., Durzan D., Pedroso M.C. 2001. Mechanical stress elicits nitric oxide formation and DNA fragmentation in Arabidopsis thaliana. Annals of Bot. 87: 567–574.CrossRefGoogle Scholar
  25. Garcia-Mata C., Lamattina L. 2001. Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol. 126: 1196–1204.CrossRefGoogle Scholar
  26. Garcia-Mata C., Lamattina L. 2002. Nitric oxide and abscisic acid cross talk in guard cells. Plant Physiol. 128: 790–792.PubMedCrossRefGoogle Scholar
  27. Garcia-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.PubMedCrossRefGoogle Scholar
  28. Giba Z., Grubisic D., Todorovic S., Sajc L., Stojakovic D., Konjevic T. 1998. Effect of nitric oxide-releasing compounds on phytochrome-controlled germination of Empress tree seeds. Plant Growth Reg. 26: 175–181.CrossRefGoogle Scholar
  29. Gould K.S., Klinguer A., Pugin A., Wendehenne D. 2003. Nitric oxide production in tobacco leaf cells: a generalized stress response? Plant Cell Environ. 26: 1851–1862.CrossRefGoogle Scholar
  30. Gouvea C.M.C.P. 1997. NO-releasing substances that induce growth elongation in maize root segments. Plant Growth Regul. 21: 183–187.CrossRefGoogle Scholar
  31. Graziano M., Beligni M.V., Lamattina L. 2002. Nitric oxide improves internal iron availability in plants. Plant Physiol. 130: 1852–1859.PubMedCrossRefGoogle Scholar
  32. Guo F-Q., Okamoto M., Crawford N.M. 2003. Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302: 100–103.PubMedCrossRefGoogle Scholar
  33. Haba P., Agüera E., Benitez L., Maldonado J.M. 2001. Modulation of nitrate reductase activity in cucumber (Cucumis sativus) roots. Plant Sci. 161: 231–237.CrossRefPubMedGoogle Scholar
  34. Herbette S., Lenne C., Tourvieille D., Drevet J., Roeckel-Drevet P. 2003. Transcripts of sunflower antioxidant scavengers of the SOD and GPX families accumulate differentially in response to downy mildew infection, phytohormones, reactive oxygen species, nitric oxide, protein kinase and phosphatase inhibitors. Physiol. Plant. 119: 418–428.CrossRefGoogle Scholar
  35. Hu X., Neill S.J., Cai W., Tang Z. 2003. Nitric oxide mediates elicitor-induced saponin synthesis in cell cultures of Panax ginseng. Funct. Plant Biol. 30: 901–907.CrossRefGoogle Scholar
  36. Huang X., Rad U., Durner J. 2002a. Nitric oxide induces transcriptional activation of the nitric oxide-tolerant alternative oxidase in Arabidopsis suspension cells. Planta 215: 914–923.PubMedCrossRefGoogle Scholar
  37. Huang X., Kiefer E., Rad U., Ernst D., Foissner I., Durner J. 2002b. Nitric oxide burst and nitric oxide-dependent gene induction in plants. Plant Physiol. Biochem. 40: 625–631.CrossRefGoogle Scholar
  38. Huang X., Stettmaier K., Michel C., Hutzler P., Mueller M.J., Durner J. 2004. Nitric oxide is induced by wounding and influences jasmonic acid signaling in Arabidopsis thaliana. Planta 218: 938–946.PubMedCrossRefGoogle Scholar
  39. Hung K.T., Chang C.J., Kao C.H. 2002. Paraquat toxicity is reduced by nitric oxide in rice leaves. J. Plant. Physiol. 159: 159–166.CrossRefGoogle Scholar
  40. Hung K.T., Kao C.H. 2003. Nitric oxide counteracts the senescence of rice leaves induced by abscisic acid. J. Plant Physiol. 160: 871–879.PubMedCrossRefGoogle Scholar
  41. Jih P.-J., Chen Y.-C., Jeng S.-T. 2003. Involvement of hydrogen peroxide and nitric oxide in expression of the ipomoelin gene from sweet potato. Plant Physiol. 132: 381–389.PubMedCrossRefGoogle Scholar
  42. Klessig D.F., Durner J., Noad R., Navarre D.A., Wendehenne D., Kumar D., Zhou J., Shah J., Zhang S., Kachroo P., Trifa Y., Pontier D., Lam E., Silva H. 2000. Nitric oxide and salicylic acid signaling in plant defense — defense gene induction in tobacco by nitric oxide, cyclic GMP and cyclic ADP-ribose, PNAS 95: 8849–8855.CrossRefGoogle Scholar
  43. Kopyra M., Gwó d E.A. 2003. Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiol. Biochem. 41: 1011–1017.CrossRefGoogle Scholar
  44. Kumar D., Klessig D.F. 2000. Differential induction of tobacco MAP kinases by the defence signals nitric oxide, salicylic acid, ethylene and jasmonic acid, Mol. Plant Microbe Interact. 13: 347–351.PubMedCrossRefGoogle Scholar
  45. Kuo W.N., Ku T.W., Jones D.L., Jn-Baptiste J. 1995. Nitric oxide synthase immunoreactivity in baker’s yeasts, lobster and wheat germ. Biochem. Arch. 11: 73–78.Google Scholar
  46. Lamattina L., Garcia-Mata C., Graziano M., Pagnussat G. 2003. Nitric Oxide: The versatility of an extensive signal molecule. Annu.Rev.Plant Biol. 54: 109–136.PubMedCrossRefGoogle Scholar
  47. Lamotte O., Gould K., Lecourieux D., Sequeira-Legrand A., Lebrun-Garcia A., Durner J., Pugin A., Wendehenne D. 2004. Analysis of nitric oxide signalling functins in tobacco cells challenged by the elicitor cryptogein. Plant Physiol. 135: 516–530.PubMedCrossRefGoogle Scholar
  48. Laxalt A.M., Beligni M.V., Zamattena X. 1997. Nitric oxide preserves the level of chlorophyll in potato leaves infected with Phytophthora infestans. Eur. J. Plant Pathol. 103: 643–651.CrossRefGoogle Scholar
  49. Leshem Y.Y., Haramaty E. 1996. The characterization and contrasting effects of the nitric oxide free radical in vegatative stress and senescence of Pisum sativum Linn. foliage. J. Plant Physiol. 148: 258–263.Google Scholar
  50. Leshem Y.Y., Haramaty E., Iluz D., Malik Z., Sofer Y., Roitman L., Lesem Y. 1997. Effect of stress nitric oxide (NO): Interaction between chlorophyll fluorescence, galactolipid fluidity and lipoxygenese activity. Plant Physiol. Biochem. 35: 573–579.Google Scholar
  51. Leshem Y.Y., Wills R.B.H., Ku V.V.V. 1998. Evidence for the function of the free radical gas — nitric oxide (NO) — as an endogenous maturation and senescence regulating factor in higher plants. Plant Physiol. Biochem. 36: 825–833.CrossRefGoogle Scholar
  52. Leshem Y.Y. 2000. Nitric oxide in plants, Kluwer Academic Publishers, Dordrecht.Google Scholar
  53. Lum H.K., Butt Y.K.C., Lo S.C.L. 2001. Hydrogen peroxide induces a rapid production of nitric oxide in mung bean (Phaseolus aureus). Nitric Oxide 6: 205–213.CrossRefGoogle Scholar
  54. Mackerness S. A. H., John C.F., Jordan B., Thomas B. 2001. Early signaling components in ultraviolet-B responses: distinct roles for different reactive oxygen species and nitric oxide. FEBS Let. 489: 237–242.CrossRefGoogle Scholar
  55. Magalhaes J.R., Monte D.C., Durzan D. 2000. Nitric oxide and ethylene emission in Arabidopsis thaliana. Physiol. Mol. Biol. Plants. 2: 117–127.Google Scholar
  56. McDonald L.J., and Murad F. 1995. Nitric oxide and cGMP signaling. Adv. Pharmacol. 34: 263–275.PubMedCrossRefGoogle Scholar
  57. Millar A.H., Day D.A. 1996. Nitric oxide inhibits the cytochrome oxidase but not the alternative oxidase of plant mitochondria. FEBS Let. 398: 155–158.CrossRefGoogle Scholar
  58. Mittler R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends in Plant Sci. 7: 405–410.CrossRefGoogle Scholar
  59. Modolo L.V., Cunha F.Q., Braga M.R., Salgado I. 2002. Nitric oxide synthase-mediated phytoalexin accumulation in soybean cotyledons in response to the Diaporthe phaseolorum f. sp. eridionalis elicitor. Plant Physiol. 130: 1288–1297.PubMedCrossRefGoogle Scholar
  60. Murgia I, Delledonne M., Soave C. 2002. Nitric oxide mediates iron-induced ferritin accumulation in Arabidopsis. Plant Journal 30: 521–528.PubMedCrossRefGoogle Scholar
  61. Navarre D., Wendehenne D., Durner J., Noad R., Klessig D.F. 2000. Nitric oxide modulates the activity of tobacco aconitase. Plant Physiol. 122: 573–582.PubMedCrossRefGoogle Scholar
  62. Neill S.J., Desikan R., Clarke A., Hancock J.T. 2002. Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol. 128: 13–16.PubMedCrossRefGoogle Scholar
  63. Neill S.J., Desikan R., Hancock J.T. 2003. Nitric oxide signalling in plants. New Phytologist 159: 11–35.CrossRefGoogle Scholar
  64. Noritake T., Kawakita K., Doke N. 1996. Nitric oxide induces phytoalexin accumulation in potato tuber tissues. Plant Cell Physiol. 37: 113–116.Google Scholar
  65. Pagnussat G.C., Simontacchi M., Puntarulo S., Lamattina L. 2002. Nitric oxide is required for root organogenesis. Plant Physiol. 129: 954–956.PubMedCrossRefGoogle Scholar
  66. Pagnussat G.C., Lanteri M.L., Lamattina L. 2003. Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol. 132: 1241–1248.PubMedCrossRefGoogle Scholar
  67. Pagnussat G.C., Lanteri M.L., Lombardo M.C., 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.PubMedCrossRefGoogle Scholar
  68. Parani M., Rudrabhatla S., Myers R., Weirich H., Smith B., Leaman D.W., Goldman S.L. 2004. Microarray analysis of nitric oxide responsive transcripts in Arabidopsis. Plant Biotech. J. 2: 359–366.CrossRefGoogle Scholar
  69. Pedroso M.C., Magalhaes J.R., Durzan D. 2000. Nitric oxide induces cell death in Taxus cells. Plant Sci. 157: 173–180.CrossRefPubMedGoogle Scholar
  70. Pinto M.C., Tommasi F., De Gara L. 2002. Changes in the antioxidant systems as part of the signaling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in tobacco bright-yellow 2 cells. Plant Physiol. 130: 698–708.PubMedCrossRefGoogle Scholar
  71. Polverari A., Molesini B., Pezzotti M., Buonaurio R., Marte M., Delledonne M. 2003. Nitric oxide-mediated transcriptional changes in Arabidopsis thaliana. MPMI 16: 1094–1105.PubMedGoogle Scholar
  72. Prado A.M., Porterfield D.M., Feijó J.A. 2004. Nitric oxide is involved in growth regulation and re-orientation of pollen tubes. Development 131: 2707–2715.PubMedCrossRefGoogle Scholar
  73. Rausch T., Kirsch M., Löw R., Lehr A., Vierck R., Zhigang A. 1996. Salt stress response of higher plants: the role of proton pumps and Na+/H+ antiporters. J. Plant Physiol. 148: 425–433.Google Scholar
  74. Ribeiro E.A., Cunha F.Q., Tamashiro W.M.S.C., Martins I.S. 1999. Growth phase-dependent subcellular localization of nitric oxide synthase in maize cells. FEBS Let. 445: 283–286.CrossRefGoogle Scholar
  75. Del Rio L.A., Corpas F.J., Barroso J.B. 2004. Nitric oxide and nitric oxide synthase activity in plants. Phytochemistry 65: 783–792.PubMedCrossRefGoogle Scholar
  76. Rockel P., Strube F., Rockel A., Wildt J., Kaiser W.M. 2002. Regulation of nitric oxide (NO) production by plant nitrate reductase in vivo and in vitro. J. Exp. Bot. 53: 103–110.PubMedCrossRefGoogle Scholar
  77. Romero-Puertas M.C., Delledonne M. 2003. Nitric oxide signaling in plant-pathogen interactions. IUBMB Life 55: 579–583.PubMedGoogle Scholar
  78. 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.PubMedCrossRefGoogle Scholar
  79. Scherer G.F.E. 2000. NO donors mimic and NO inhibitors inhibit cytokinin action in betalaine accumulation in Amaranthus caudatus. Plant Growth Reg. 32: 345–350.CrossRefGoogle Scholar
  80. Schmidt H.H.W.H., Walter U. 1994. NO at work, Cell 78: 919–925.CrossRefGoogle Scholar
  81. Sen S., Cheema I.R. 1995. Nitric oxide synthase and calmodulin reactivity in plant embryonic tissue. Biochem. Arch. 11: 221–27.Google Scholar
  82. Seregélyes C., Barna B., Hennig J., Konopka D., Pasternak T.P., Lukács N., Fehér A., Horváth G.V., Dudits D. 2003. Phytoglobins can interfere with nitric oxide functions during plant growth and pathogenic responses: a transgenic approach. Plant Sci. 165: 541–550.CrossRefGoogle Scholar
  83. Seregélyes C., Igamberdiev A.U., Maassen A., Hennig J., Dudits D., Hill R.D. 2004. NO-degradation by alfaalfa class 1 hemoglobin (Mhb1): a possible link to PR-1a gene expression in Mhb1-overproducing tobacco plants. FEBS Let. 571: 61–66.CrossRefGoogle Scholar
  84. Singh A.K., Sharma L., Mallick N. 2004. Antioxidative role of nitric oxide on copper toxicity to a chlorophycean alga, Chlorella. Ecotoxicology and Environ. Safety 59: 223–227.Google Scholar
  85. Stöhr C., Ullrich W.R. 2002. Generation and possible roles of NO in plant roots and their apoplastic space. J. Exp. Bot. 53: 2293–2303.PubMedCrossRefGoogle Scholar
  86. Tun N.N., Holk A., Scherer F.E. 2001. Rapid increase of NO release in plant cell cultures induced by cytokinin. FEBS Let. 509: 174–176.CrossRefGoogle Scholar
  87. Uchida A., Jagendorf A.T., Hibino T., Takabe T., Takabe T. 2002. Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Sci. 163: 515–523.CrossRefGoogle Scholar
  88. Van Camp W., Inzé D., Van Montagu M. 1998. H2O2 and NO: redox signals in disease resistance, Trends Plant Sci. 3: 330–334.CrossRefGoogle Scholar
  89. Wendehenne D., Pugin A., Klessig D., Durner J. 2001. Nitric oxide: comparative synthesis and signaling in animal and plant cells. Trends Plant Sci. 6: 177–183.PubMedCrossRefGoogle Scholar
  90. Wendehenne D., Durner J., Klessig D.F. 2004. Nitric oxide: a new player in plant signalling and defence response. Current Opinion in Plant Biol. 7: 449–455.CrossRefGoogle Scholar
  91. Wojtaszek P. 2000. Nitric oxide in plants. To NO or not to NO. Phytochemistry 54: 1–4.PubMedCrossRefGoogle Scholar
  92. Xing H., Tan L., An L., Zhao Z., Wang S., Zhang C. 2004. Evidence for the involvement of nitric oxide and reactive oxygen species in osmotic stress tolerance of wheat seedlings: inverse correlation between leaf abscisic acid accumulation and leaf water loss. Plant Growth Reg. 42: 61068.Google Scholar
  93. Xu Y.C., Zhao B.L. 2003. The main origin of endogenous NO in higher non-leguminous plants. Plant Physiol. Biochem. 41: 833–838.CrossRefGoogle Scholar
  94. Yamasaki H., Sakihama Y. 2000. Simultaneous production of nitric oxide and peroxynitrite by plant nitrate reductase: in vitro evidence for the NR-dependent formation of active nitrogen species. FEBS Let. 468: 89–92.CrossRefGoogle Scholar
  95. Zemojtel T., Penzkofer T., Dandekar T., Schultz J. 2004. A novel conserved family of nitric oxide synthase? Trends Biochem Sci. 29: 224–226.PubMedCrossRefGoogle Scholar
  96. Zhao Z., Chen G., Zhang C. 2001. Interaction between reactive oxygen species and nitric oxide in drought-induced abscisic acid synthesis in root tips of wheat seedlings. Aust. J. Plant Physiol. 28: 1055–1061.Google Scholar
  97. Zhao Z., Zhang F., Guo J., Yang Y., Li B., Zhang L. 2004. Nitric oxide functions as a signal in salt resistance in the calluses from two ecotypes of reed. Plant Physiol. 134: 849–857.PubMedCrossRefGoogle Scholar
  98. Zottini M., Formentin E., Scattolin M., Carimi F., Lo Schiavo F., Terzi M. 2002. Nitric oxide affects plant mitochondrial functionality in vivo. FEBS Let. 515: 75–78.CrossRefGoogle Scholar

Copyright information

© Department of Plant Physiology 2004

Authors and Affiliations

  1. 1.Laboratory of Plant EcophysiologyAdam Mickiewicz UniversityPoznaPoland

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