Abstract
Main conclusion
Hypoxia leads to NO formation in poplar roots. Additionally, either NO or a NO derivative is transported from the roots to the shoot causing NO emission from aboveground plant organs.
Nitric oxide (NO) is involved in the response of plants to various forms of stress including hypoxia. It also seems to play an important role in stomatal closure during stress exposure. In this study, we investigated the formation of NO in roots of intact poplar (Populus × canescens) plants in response to hypoxia, as well as its dependence on nitrate availability. We further addressed the question if root hypoxia triggers NO emission from aboveground plant parts, i.e., stems and leaves of young poplar trees. Our results indicate that NO is formed in poplar roots in response to hypoxia and that this production depends on the availability of nitrate and its conversion product nitrite. As long as nitrate was available in the nutrient solution, NO emission of roots occurred; in the range of the nitrate concentrations (10–100 µM) tested, NO emission was widely independent on nitrate concentration. However, the time period in which NO was emitted and the total amount of NO emitted strongly depended on the nitrate concentration of the solution. Hypoxia also led to increased NO emissions from the leaves and stems of the trees. There was a tight correlation between leaf and stem NO emission of hypoxia-treated plants. We propose that NO is produced by nitrate reductase in the roots and either NO itself, a metabolic NO precursor, or a NO derivative is transported in the xylem sap of the trees from the roots to the shoot thereby mediating NO emission from aboveground parts of the plant.
Similar content being viewed by others
Abbreviations
- ROS:
-
Reactive oxygen species
- PMSF:
-
Phenazinemethosulfate
- NED:
-
N-(1-naphthyl)-ethylene-diamine dihydrochloride
- PPFD:
-
Photosynthetically active photon flux density
- nsHb:
-
Non-symbiotic hemoglobin
References
Benamar A, Rolletschek H, Borisjuk L, Avelange-Macherel MH, Curien G, Mostefai HA, Andriantsitohaina R, Macherel D (2008) Nitrite-nitric oxide control of mitochondrial respiration at the frontier of anoxia. Biochim Biophys Acta 1777:1268–1275
Black BL, Fuchigami LH, Coleman GD (2002) Partitioning of nitrate assimilation among leaves, stems and roots of poplar. Tree Physiol 22:717–724
Botrel A, Magne C, Kaiser W (1996) Nitrate reduction, nitrite reduction and ammonium assimilation in barley roots in response to anoxia. Plant Physiol Biochem 34:645–652
Brandão AD, Sodek L (2009) Nitrate uptake and metabolism by roots of soybean plants under oxygen deficiency. Braz J Plant Physiol 21:13–23
Brunswick P, Cresswell CF (1988) Nitrite uptake into intact pea chloroplasts I. Kinetics and relationship with nitrite assimilation. Plant Physiol 86:378–383
Chen J, Xiao Q, Wu F, Pei Z, Wang J, Wu Y, Zheng H (2010) Nitric oxide emission from barley seedlings and detached leaves and roots treated with nitrate and nitrite. Plant Soil Environ 56:201–208
Chen J, Xiong D-Y, Wang W-H, Hu W-J, Simon M et al (2013) Nitric oxide mediates root K+/Na+ balance in a mangrove plant, Kandelia obovata, by enhancing the expression of AKT1-type K+ channel and Na+/H+ antiporter under high salinity. PLoS One. doi:10.1371/journal.pone.0071543
Copolovici L, Niinemets Ü (2010) Flooding induced emissions of volatile signalling compounds in three tree species with differing waterlogging tolerance. Plant, Cell Environ 33:1582–1594
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. Proc Natl Acad Sci USA 99:16314–16318
Dordas C, Hasinoff BB, Igamberdiev AU, Manac’h N, Rivoal J, Hill RD (2003) Expression of a stress-induced hemoglobin affects NO levels produced by alfalfa root cultures under hypoxic stress. Plant J 35:763–770
Dordas C, Hasinoff BB, Rivoal J, Hill RD (2004) Class-1 hemoglobins, nitrate and NO levels in anoxic maize cell-suspension cultures. Planta 219:66–72
Ehlting B, Dluznieska P, Dietrich H, Selle A, Teuber M, Hänsch R, Nehls U, Polle A, Schnitzler J-P, Rennenberg H, Gessler A (2007) Interaction of nitrogen nutrition and salinity in Grey poplar (Populus tremula × alba). Plant, Cell Environ 30:796–811
García-Mata C, Lamattina L (2001) Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiol 126:1196–1204
Gould K, 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
Gupta KJ, Kaiser WM (2010) Production and scavenging of nitric oxide by barley root mitochondria. Plant Cell Physiol 51:576–584
Gupta KJ, Fernie AR, Kaiser WM, van Dongen JT (2011a) On the origins of nitric oxide. Trends Plant Sci 16:160–168
Gupta KJ, Hebelstrup KH, Mur LA, Igamberdiev AU (2011b) Plant hemoglobins: important players at the crossroads between oxygen and nitric oxide. FEBS Lett 585:3843–3849
Gupta KJ, Shah JK, Brotman Y, Jahnke K, Willmitzer L, Kaiser WM, Bauwe H, Igamberdiev AU (2012) Inhibition of aconitase by nitric oxide leads to induction of the alternative oxidase and to a shift of metabolism towards biosynthesis of amino acids. J Exp Bot 63:1773–1784
Hebelstrup KH, van Zanten M, Mandon J, Voesenek LA, Harren FJ, Cristescu SM, Moller IM, Mur LA (2012) Haemoglobin modulates NO emission and hyponasty under hypoxia-related stress in Arabidopsis thaliana. J Exp Bot 3:5581–5591
Heizmann U, Kreuzwieser J, Schnitzler J-P, Brüggemann N, Rennenberg H (2001) Assimilate transport in the xylem sap of Pedunculate oak (Quercus robur) saplings. Plant Biol 3:132–138
Hill RD (2012) Non-symbiotic haemoglobins—what’s happening beyond nitric oxide scavenging? AoB Plants. doi:10.1093/aobpla/pls004
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. College of Agriculture, University of California, California, Berkeley
Igamberdiev AU, Hill RD (2009) Plant mitochondrial function during anaerobiosis. Ann Bot 103:259–268
Igamberdiev AU, Seregelyes C, Manac N, Hill RD (2004) NADH-dependent metabolism of nitric oxide in alfalfa root cultures expressing barley hemoglobin. Planta 219:95–102
Jia L, Bonaventura C, Bonaventura J, Stamler JS (1996) S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature 380:221–226
Kreuzwieser J, Rennenberg H (2014) Molecular and physiological responses of trees to waterlogging stress. Plant, Cell Environ 37:2245–2259
Kreuzwieser J, Scheerer U, Rennenberg H (1999) Metabolic origin of acetaldehyde emitted by poplar (Populus tremula × P. alba) trees. J Exp Bot 50:757–765
Kreuzwieser J, Fürniss S, Rennenberg H (2002) Impact of waterlogging on the N-metabolism of flood tolerant and non-tolerant tree species. Plant, Cell Environ 25:1039–1049
Kreuzwieser J, Papadopoulou E, Rennenberg H (2004) Interaction of flooding with carbon metabolism of forest trees. Plant Biol 6:299–306
Kreuzwieser J, Hauberg J, Howell KA, Carroll A, Rennenberg H, Millar AH, Whelan J (2009) Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiol 149:461–473
Lamattina L, García-Mata C, Graziano M, Pagnussat G (2003) Nitric oxide: the versatility of an extensive signal molecule. Annu Rev Plant Biol 54:109–136
Millard P, Wendler R, Grassi G, Grelet G-A, Tagliavini M (2006) Translocation of nitrogen in the xylem of field-grown cherry and poplar trees during remobilization. Tree Physiol 26:527–536
Morard P, Silvestre J, Lacoste L, Caumes E, Lamaze T (2004) Nitrate uptake and nitrite release by tomato roots in response to anoxia. J Plant Physiol 161:855–865
Mur LAJ, Sivakumaran A, Mandon J, Cristescu SM, Harren FJ, Hebelstrup KH (2012) Haemoglobin modulates salicylate and jasmonate/ethylene-mediated resistance mechanisms against pathogens. J Exp Bot 63:4375–4387
Neill SJ, Desikan R, Clarke A, Hancock JT (2002) Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiol 128:13–16
Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signaling in plants. New Phytol 159:11–35
Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Morris P, Ribeiro D, Wilson I (2008) Nitric oxide, stomatal closure, and abiotic stress. J Exp Bot 59:165–176
Oliveira HC, Salgado I, Sodek L (2013a) Involvement of nitrite in the nitrate-mediated modulation of fermentative metabolism and nitric oxide production of soybean roots during hypoxia. Planta 237:255–264
Oliveira HC, Salgado I, Sodek L (2013b) Nitrite decreases ethanol production by intact soybean roots submitted to oxygen deficiency—a role for mitochondrial nitric oxide synthesis? Plant Signal Behav. doi:10.4161/psb.23578
Papen H, Geβler A, Zumbusch E, Rennenberg H (2002) Chemolithoautotrophic nitrifiers in the phyllosphere of a spruce ecosystem receiving high atmospheric nitrogen input. Curr Microbiol 44:56–60
Parent C, Berger A, Folzer H, Dat J, Crevècoeur M, Badot PM, Capelli N (2008) A novel nonsymbiotic hemoglobin from oak: cellular and tissue specificity of gene expression. New Phytol 177:142–154
Planchet E, Kaiser WM (2006) Nitric oxide production in plants: facts and fictions. Plant Signal Behav 1:46–51
Planchet E, Jagadis Gupta K, Sonoda M, Kaiser WM (2005) Nitric oxide emission from tobacco leaves and cell suspensions: rate limiting factors and evidence for the involvement of mitochondrial electron transport. Plant J 41:732–743
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
Sander R (1999) Compilation of Henry’s Law constants for inorganic and organic species of potential importance in environmental chemistry (Version 3) http://www.henrys-law.org
Schneider A, Kreuzwieser J, Schupp R, Sauter JJ, Rennenberg H (1994) Thiol and amino acid composition of the xylem sap of poplar trees (Populus × canadensis ‘robusta’). Can J Bot 72:347–351
Scholander PF, Hammel HT, Bradstreet ED, Hemmingsen EA (1965) Sap pressure in vascular plants. Science 148:339–346
Shingles R, Roh MH, McCarty RE (1996) Nitrite transport in chloroplast inner envelope vesicles. I. Direct measurement of proton-linked transport. Plant Physiol 112:1375–1381
Siebrecht S, Tischner R (1999) Changes in the xylem exudate composition of poplar (Populus tremula × P. alba)—dependent on the nitrogen and potassium supply. J Exp Bot 50:1797–1806
Simon J, Stoelken G, Rienks M, Rennenberg H (2009) Rhizospheric NO affects N uptake and gene expression patterns in Fagus sylvatica. FEBS Lett 583:2907–2910
Simon J, Dong F, Buegger F, Rennenberg H (2013) Rhizospheric NO affects N uptake and metabolism in Scots pine (Pinus sylvestris L.) seedlings depending on soil N availability and N source. Plant, Cell Environ 36:1019–1026
Stoimenova M, Kaiser W (2004) the role of nitrate reduction in plant flooding survival. Progress in botany. Springer, Berlin, pp 357–371
Strohm M, Jouanin L, Kunert KJ, Pruvost C, Polle A, Foyer CH, Rennenberg H (1995) Regulation of glutathione synthesis in leaves of transgenic poplar (Populus tremula × P. alba) overexpressing glutathione synthetase. Plant J 7:141–145
Vanin AF, Svistunenko DA, Mikoyan VD, Serezhenkov VA, Fryer MJ, Baker NR, Cooper CE (2004) Endogenous superoxide production and the nitrite/nitrate ratio control the concentration of bioavailable free nitric oxide in leaves. J Biol Chem 279:24100–24107
Zhao M-G, Chen L, Zhang L-L, Zhang W-H (2009) Nitric reductase-dependent nitric oxide production is involved in cold acclimation and freezing tolerance in Arabidopsis. Plant Physiol 151:755–767
Acknowledgments
We are most grateful to Prof Werner Kaiser and Prof Rainer Hedrich (both University of Würzburg, Germany) for introduction into NO measurements and for providing the NO analyzers. Bin Liu was supported by a grant of the China Scholarship Council (Grant # 2010630072).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Liu, B., Rennenberg, H. & Kreuzwieser, J. Hypoxia induces stem and leaf nitric oxide (NO) emission from poplar seedlings. Planta 241, 579–589 (2015). https://doi.org/10.1007/s00425-014-2198-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-014-2198-8