Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Nitrogen and oxygen isotope effects of tissue nitrate associated with nitrate acquisition and utilisation in the moss Hypnum plumaeforme

Xue-Yan Liu A B , Keisuke Koba B C , Muneoki Yoh B and Cong-Qiang Liu A
+ Author Affiliations
- Author Affiliations

A State Key Laboratory of Environmental Geochemistry, Institute of Geochemistry, Chinese Academy of Sciences, Guiyang 550002, China.

B Faculty of Agriculture, Tokyo University of Agriculture and Technology, Saiwai-cho 3-5-8, Fuchu City, Tokyo 183-8509, Japan.

C Corresponding author. Email: keikoba@cc.tuat.ac.jp

Functional Plant Biology 39(7) 598-608 https://doi.org/10.1071/FP12014
Submitted: 19 January 2012  Accepted: 15 May 2012   Published: 29 June 2012

Abstract

Mosses are effective accumulators and indicators of N deposition, but the mechanisms of moss N utilisation remain unclear. This study monitored nitrate concentrations ([NO3]) in solutions supplied to Hypnum plumaeforme Wils. to characterise NO3 uptake from rain events. Concentrations and isotopic ratios (δ15N and δ18O) of residual NO3 in moss tissues were measured to interpret induced NO3 reduction. Noninduced NO3 reduction was inferred from endogenous [NO3] and isotopic variations that occurred during 65 days of N deprivation. H. plumaeforme scavenges NO3 effectively from supplied solutions. The uptake rate increased with substrate [NO3] (0.4−3.9 mg N L–1) and generally obeyed saturation (Michaelis–Menten) kinetics. The uptake rate was maximised within 60 min after receiving NO3, irrespective of the initial substrate [NO3]. Lower tissue [NO3] and greater isotopic enrichment verified the inducibility of nitrate reductase activity (NRA) by NO3 availability, but short-term darkness did not markedly influence moss NO3 uptake or reduction. Significant reduction and isotopic enrichment were detected in moss NO3 reserves during N deprivation, showing 15ε of 12.1‰ and 18ε of 14.4‰. The Δδ15N : Δδ18O ratios of ~1 : 1 implied that NRA is the single process driving 15N and 18O fractionations. These results provide new isotopic insights into the nitrate reductase dynamics of the moss.

Additional keywords: denitrifier method, nitrate reduction, nitrate uptake, nitrogen deposition.


References

Aerts R (1996) Nutrient resorption from senescing leaves of perennials: are there general patterns? Journal of Ecology 84, 597–608.
Nutrient resorption from senescing leaves of perennials: are there general patterns?Crossref | GoogleScholarGoogle Scholar |

Aerts R, Wallén B, Malmer N (1992) Growth-limiting nutrients in Sphagnum-dominated bogs subject to low and high atmospheric nitrogen supply. Journal of Ecology 80, 131–140.
Growth-limiting nutrients in Sphagnum-dominated bogs subject to low and high atmospheric nitrogen supply.Crossref | GoogleScholarGoogle Scholar |

Aldous AR (2002) Nitrogen translocation in Sphagnum mosses: effects of atmospheric nitrogen deposition. New Phytologist 156, 241–253.
Nitrogen translocation in Sphagnum mosses: effects of atmospheric nitrogen deposition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovFGqsr8%3D&md5=c22739a29c625ca9e2723b62b45ede3dCAS |

Alghamdi AA (2003) The effect of inorganic and organic nitrogen sources and their combination on growth and metabolism of Vesicularia dubyana. PhD Thesis, Michigan Technological University, Houghton.

Armitage HF, Britton AJ, van der Wal R, Pearce IK, Thompson DBA, Woodin SJ (2012) Nitrogen deposition enhances moss growth, but leads to an overall decline in habitat condition of mountain moss-edge heath. Global Change Biology 18, 290–300.
Nitrogen deposition enhances moss growth, but leads to an overall decline in habitat condition of mountain moss-edge heath.Crossref | GoogleScholarGoogle Scholar |

Aslam M, Huffaker RC, Rains DW, Rao KP (1979) Influence of light and ambient carbon dioxide concentration on nitrate assimilation by intact barley seedlings. Plant Physiology 63, 1205–1209.
Influence of light and ambient carbon dioxide concentration on nitrate assimilation by intact barley seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXkslWkt7Y%3D&md5=5ca5d0db9081f5a73120dab52f4f4e5aCAS |

Ayres E, van der Wal R, Sommerkorn M, Bardgett RD (2006) Direct uptake of soil nitrogen by mosses. Biology Letters 2, 286–288.
Direct uptake of soil nitrogen by mosses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XnsFSqsLw%3D&md5=56362cd568480e7b07606c74c550510cCAS |

Bates JW (2000) Mineral nutrition, substratum ecology, and pollution. In ‘Bryophyte biology’. (Eds AJ Shaw, B Goffinet) pp. 248–311 (Cambridge University Press, Cambridge, UK)

Bayley SE, Vitt DH, Newbury RW, Beaty KG, Behr R, Miller C (1987) Experimental acidification of a Sphagnum-dominated peatland: first year results. Canadian Journal of Fisheries and Aquatic Sciences 44, s194–s205.
Experimental acidification of a Sphagnum-dominated peatland: first year results.Crossref | GoogleScholarGoogle Scholar |

Blevins DG, Barnett NM, Frost WB (1978) Role of potassium and malate in nitrate uptake and translocation by wheat seedlings. Plant Physiology 62, 784–788.
Role of potassium and malate in nitrate uptake and translocation by wheat seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXltlygsQ%3D%3D&md5=d99e9b225b6d86493ca6cb30516f9404CAS |

Bobbink R, Hicks K, Galloway J, Spranger T, Alkemade R, Ashmore M, Bustamante M, Cinderby S, Davidson E, Dentener F, Emmett B, Erisman JW, Fenn M, Gilliam F, Nordin A, Pardo L, de Vries W (2010) Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis. Ecological Applications 20, 30–59.
Global assessment of nitrogen deposition effects on terrestrial plant diversity: a synthesis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3c3itVWlug%3D%3D&md5=2fd1a5d80349c534189d4d8381b28882CAS |

Bowden RD (1991) Inputs, outputs, and accumulation of nitrogen in an early successional moss (Polytrichum) ecosystem. Ecological Monographs 61, 207–223.
Inputs, outputs, and accumulation of nitrogen in an early successional moss (Polytrichum) ecosystem.Crossref | GoogleScholarGoogle Scholar |

Bragazza L, Limpens J, Gerdol R, Grosvernier P, Hájek M, Hájek T, Hajkova P, Hansen I, Iacumin P, Kutnar L, Rydin H, Tahvanainen T (2005) Nitrogen concentration and δ15N signature of ombrotrophic Sphagnum mosses at different N deposition levels in Europe. Global Change Biology 11, 106–114.
Nitrogen concentration and δ15N signature of ombrotrophic Sphagnum mosses at different N deposition levels in Europe.Crossref | GoogleScholarGoogle Scholar |

Buchwald C, Casciotti KL (2010) Oxygen isotopic fractionation and exchange during bacterial nitrite oxidation. Limnology and Oceanography 55, 1064–1074.
Oxygen isotopic fractionation and exchange during bacterial nitrite oxidation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotVWgtbY%3D&md5=21cfe1c745a3fdbfd690b80c248e771fCAS |

Casciotti KL, Sigman DM, Hasting GM, Böhlke JK, Hilkert A (2002) Measurement of the oxygen isotopic composition of nitrate in seawater and freshwater using the denitrifier method. Analytical Chemistry 74, 4905–4912.
Measurement of the oxygen isotopic composition of nitrate in seawater and freshwater using the denitrifier method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmslGgu70%3D&md5=0281fb55f1c43a4d21555ad59061e4eaCAS |

Comstock J (2001) Steady-state isotopic fractionation in branched pathways using plant uptake of NO3 – as an example. Planta 214, 220–234.
Steady-state isotopic fractionation in branched pathways using plant uptake of NO3 as an example.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXovFKns7s%3D&md5=ca72e29b18f9932ef092d21e69531a85CAS |

Coplen TB (2011) Guidelines and recommended terms for expression of stable-isotope-ratio and gas-ratio measurement results. Rapid Communications in Mass Spectrometry 25, 2538–2560.

Deising H, Rudolph H (1987) Nitrate-induced de novo synthesis and regulation of NAD(P)H nitrate reductase from Sphagnum. Physiologia Plantarum 71, 477–482.
Nitrate-induced de novo synthesis and regulation of NAD(P)H nitrate reductase from Sphagnum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXptFOksw%3D%3D&md5=b203086020de3c5d5fcabb464727fd50CAS |

Delhon P, Gojon A, Tillard P, Passama L (1995) Diurnal regulation of NO3 – uptake in soybean plants. I. Changes in NO3 – influx, efflux, and N utilization in the plant during the day/night cycle. Journal of Experimental Botany 46, 1585–1594.
Diurnal regulation of NO3 uptake in soybean plants. I. Changes in NO3 influx, efflux, and N utilization in the plant during the day/night cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXptVymsrw%3D&md5=1936f99a055df691593ea004d65393a8CAS |

Eckstein RL, Karlsson PS (1999) Recycling of nitrogen among segments of Hylocomium splendens as compared with Polytrichum commune: implications for clonal integration in an ectohydric bryophyte. Oikos 86, 87–96.

Evans RD (2001) Physiological mechanisms influencing plant nitrogen isotope composition. Trends in Plant Science 6, 121–126.
Physiological mechanisms influencing plant nitrogen isotope composition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsFGrsr4%3D&md5=586a411b8d3254f096cb5acbfe98a2b5CAS |

Evans RD, Bloom AJ, Sukrapanna SS, Ehleringer JR (1996) Nitrogen isotope composition of tomato (Lycopersicon esculentum Mill. cv. T-5) grown under ammonium or nitrate nutrition. Plant, Cell & Environment 19, 1317–1323.
Nitrogen isotope composition of tomato (Lycopersicon esculentum Mill. cv. T-5) grown under ammonium or nitrate nutrition.Crossref | GoogleScholarGoogle Scholar |

Gebauer G, Melzer A, Rehder H (1984) Nitrate content and nitrate reductase activity in Rumex obtusifolius L. I. Differences in organs and diurnal changes. Oecologia 63, 136–142.
Nitrate content and nitrate reductase activity in Rumex obtusifolius L. I. Differences in organs and diurnal changes.Crossref | GoogleScholarGoogle Scholar |

Gebauer G, Schuhmacher MI, Krstic B, Rehder H, Ziegler H (1987) Biomass production and nitrate metabolism of Atriplex hortensis L. (C3 plant) and Amaranthus retroflexus L. (C4 plant) in cultures at different levels of nitrogen supply. Oecologia 72, 303–314.
Biomass production and nitrate metabolism of Atriplex hortensis L. (C3 plant) and Amaranthus retroflexus L. (C4 plant) in cultures at different levels of nitrogen supply.Crossref | GoogleScholarGoogle Scholar |

Glass ADM, Shaff JE, Kochian LV (1992) Studies of the uptake of nitrate in barley. IV. Electrophysiology. Plant Physiology 99, 456–463.
Studies of the uptake of nitrate in barley. IV. Electrophysiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XltlSntLw%3D&md5=7dfbf891a35c98d87267204e4ca69542CAS |

Glass ADM, Britto DT, Kaiser BN, Kinghorn JR, Kronzucker HJ, Kumar A, Okamoto M, Rawat S, Siddiqi MY, Unkles SE, Vidmar JJ (2002) The regulation of nitrate and ammonium transport systems in plants. Journal of Experimental Botany 53, 855–864.
The regulation of nitrate and ammonium transport systems in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XivFSntLc%3D&md5=c5e0cb19eee53dac944ddae94db1d671CAS |

Glime JM (2007) ‘Bryophyte ecology, Vol. 1. Physiological ecology.’ (Michigan Technological University and the International Association of Bryologists). Available at http://www.bryoecol.mtu.edu

Gordon C, Wynn JM, Woodin SJ (2001) Impacts of increased nitrogen supply on high Arctic heath: the importance of bryophytes and phosphorus availability. New Phytologist 149, 461–471.
Impacts of increased nitrogen supply on high Arctic heath: the importance of bryophytes and phosphorus availability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXis1ans70%3D&md5=b2c74a2b56e74ceb0c2c131b0a6a3adaCAS |

Granger J (2006) Coupled nitrogen and oxygen isotope fractionation of nitrate imparted during its assimilation and dissimilatory reduction by unicellular plankton. PhD Thesis, The University of British Columbia, Vancouver.

Granger J, Sigman DM, Needoba JA, Harrison PJ (2004) Coupled nitrogen and oxygen isotope fractionation of nitrate during assimilation by cultures of marine phytoplankton. Limnology and Oceanography 49, 1763–1773.
Coupled nitrogen and oxygen isotope fractionation of nitrate during assimilation by cultures of marine phytoplankton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovVWqsbY%3D&md5=7bec431f7ea28f6086dead921193ca0eCAS |

Granger J, Sigman DM, Rohde MM, Maldonado MT, Tortell PD (2010) N and O isotope effects during nitrate assimilation by unicellular prokaryotic and eukaryotic plankton cultures. Geochimica et Cosmochimica Acta 74, 1030–1040.
N and O isotope effects during nitrate assimilation by unicellular prokaryotic and eukaryotic plankton cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1SlsLfP&md5=9169a86021354e8152dbc608239ad5d3CAS |

Gundale M, Deluca TH, Nordin A (2011) Bryophytes attenuate anthropogenic nitrogen inputs in boreal forests. Global Change Biology 17, 2743–2753.
Bryophytes attenuate anthropogenic nitrogen inputs in boreal forests.Crossref | GoogleScholarGoogle Scholar |

Koranda M, Kerschbaum S, Wanek W, Zechmeister H, Richter A (2007) Physiological responses of bryophytes Thuidium tamariscinum and Hylocomium splendens to increased nitrogen deposition. Annals of Botany 99, 161–169.
Physiological responses of bryophytes Thuidium tamariscinum and Hylocomium splendens to increased nitrogen deposition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXisVOhtrY%3D&md5=56dd998283cbc4beae50d887259385ecCAS |

Ledgard SF, Woo KC, Bergersen FJ (1985) Isotopic fractionation during reduction of nitrate and nitrite by extracts of spinach leaves. Functional Plant Biology 12, 631–640.

Leskovac V (2003) ‘Comprehensive enzyme kinetics.’ (Springer-Verlag: Netherlands).

Li Y, Vitt DH (1997) Patterns of retention and utilization of aerially deposited nitrogen in boreal peatlands. Ecoscience 4, 106–116.

Liu XY, Koba K, Takebayashi Y, Liu CQ, Fang YT, Yoh M (2012a) Preliminary insights into δ15N and δ18O of nitrate in natural mosses: a new application of the denitrifier method. Environmental Pollution 162, 48–55.
Preliminary insights into δ15N and δ18O of nitrate in natural mosses: a new application of the denitrifier method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xps1Wgsg%3D%3D&md5=320797350e39d32df5fe507a3e2766c3CAS |

Liu XY, Koba K, Takebayashi Y, Liu CQ, Fang YT, Yoh M (2012b) Dual N and O isotopes of nitrate in natural plants: first insights into individual variability and organ-specific pattern. Biogeochemistry
Dual N and O isotopes of nitrate in natural plants: first insights into individual variability and organ-specific pattern.Crossref | GoogleScholarGoogle Scholar | in press.

MacKown CT (1987) Nitrate uptake and assimilation following nitrate deprivation. Journal of Experimental Botany 38, 1079–1090.
Nitrate uptake and assimilation following nitrate deprivation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXlt1yltA%3D%3D&md5=02ed5aa4bcf8ff2008b7033104104a3fCAS |

Mäkipää R (1995) Sensitivity of forest floor mosses in boreal forests to nitrogen and sulphur deposition. Water, Air, and Soil Pollution 85, 1239–1244.
Sensitivity of forest floor mosses in boreal forests to nitrogen and sulphur deposition.Crossref | GoogleScholarGoogle Scholar |

Marion GM, Miller PC, Black CH (1987) Competition for tracer 15N in tussock tundra ecosystems. Holarctic Ecology 10, 230–234.

Mariotti A, Germon JC, Hubert P, Kaiser P, Letolle R, Tardieux A, Tardieux P (1981) Experimental determination of nitrogen kinetic isotope fractionation: some principles; illustration for the denitrification and nitrification processes. Plant and Soil 62, 413–430.
Experimental determination of nitrogen kinetic isotope fractionation: some principles; illustration for the denitrification and nitrification processes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XmslOjtQ%3D%3D&md5=5755b06efb487cd407d70efd0a90a22eCAS |

Mariotti A, Mariotti F, Champigny ML, Amarger N, Moyse A (1982) Nitrogen isotope fractionation associated with nitrate reductase-activity and uptake of NO3 – by pearl millet. Plant Physiology 69, 880–884.
Nitrogen isotope fractionation associated with nitrate reductase-activity and uptake of NO3 by pearl millet.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38Xhslyiu7Y%3D&md5=c3b1c654f0eaf763d842e843b4d0cb50CAS |

Needoba JA, Harrison PJ (2004) Influence of low light and a light : dark cycle on NO3 – uptake, intracellular NO3 –, and nitrogen isotope fractionation by marine phytoplankton. Journal of Phycology 40, 505–516.
Influence of low light and a light : dark cycle on NO3 uptake, intracellular NO3 , and nitrogen isotope fractionation by marine phytoplankton.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXls1Sltbk%3D&md5=e20044027c576214c02fb93422b19515CAS |

Needoba JA, Waser NA, Harrison PJ, Calvert SE (2003) Nitrogen isotope fractionation in 12 species of marine phytoplankton during growth on nitrate. Marine Ecology Progress Series 255, 81–91.
Nitrogen isotope fractionation in 12 species of marine phytoplankton during growth on nitrate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXosFCns7o%3D&md5=187585d1aa5fe23f400b370cf2063ddcCAS |

Oaks A, Wallace W, Stevens D (1972) Synthesis and turnover of nitrate reductase in corn roots. Plant Physiology 56, 692–695.

Olleros-Izard T (1983) Kinetische Isotopeneffekte der Arginase und Nitratreduktase Reaktion: ein Betrag zur Aufklärung der entsprechenden Reaktionmechanismen. PhD thesis, Technischen Universität München, Freising-Weihenstephan.

Paulissen MPCP, van der Ven PJM, Dees AJ, Bobbink R (2004) Differential effects of nitrate and ammonium on three fen bryophyte species in relation to pollution nitrogen input. New Phytologist 164, 451–458.
Differential effects of nitrate and ammonium on three fen bryophyte species in relation to pollution nitrogen input.Crossref | GoogleScholarGoogle Scholar |

Pearce ISK, Woodin SJ, Van der Wal R (2003) Physiological and growth responses of the montane bryophyte Racomitrium lanuginosum to atmospheric nitrogen deposition. New Phytologist 160, 145–155.
Physiological and growth responses of the montane bryophyte Racomitrium lanuginosum to atmospheric nitrogen deposition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXot1Witbo%3D&md5=9a1dfd2e7e4a227ae530b08ba0cc8609CAS |

Pennock JR, Velinsky DJ, Sharp JH, Ludlam J, Fogel ML (1996) Isotope fractionation of ammonium and nitrate during their uptake by Skeletonema costatum: implications for the δ15N dynamics under bloom conditions. Limnology and Oceanography 41, 451–459.
Isotope fractionation of ammonium and nitrate during their uptake by Skeletonema costatum: implications for the δ15N dynamics under bloom conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XkvFKht7o%3D&md5=2726a9a4feb419e67b6412ad30801682CAS |

Peuke AD, Jeschke WD (1998) The effects of light on induction, time courses and kinetic patterns of net nitrate uptake in barley. Plant, Cell & Environment 21, 765–774.
The effects of light on induction, time courses and kinetic patterns of net nitrate uptake in barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmsVertLc%3D&md5=87f307281e379afc8a0a52677bffe9b1CAS |

Press MC, Lee JA (1982) Nitrate reductase activity of Sphagnum species in the S. Pennines. New Phytologist 92, 487–494.
Nitrate reductase activity of Sphagnum species in the S. Pennines.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXntV2kug%3D%3D&md5=fb07687dd4fe6b2a2389436080e1c86cCAS |

Proctor MCF, Oliver MJ, Wood AJ, Alpert P, Stark LR, Cleavitt NL, Mishler BD (2007) Desiccation-tolerance in bryophytes: a review. The Bryologist 110, 595–621.
Desiccation-tolerance in bryophytes: a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpvVCmsA%3D%3D&md5=e39dd2ac86ed01d90efbfdae67dccab8CAS |

Raven JA, Griffiths H, Smith EC, Vaughn KC (1998) New perspectives in the biophysics and physiology of bryophytes. In ‘Bryology in the twenty-first century’. (Eds JW Bates, NW Ashton, JG Duckett ) pp. 261–275. (Maney Publishing and the British Bryological Society: Leeds, UK).

Robinson D, Handley LL, Scrimgeour CM (1998) A theory for 15N/14N fractionation in nitrate-grown vascular plants. Planta 205, 397–406.
A theory for 15N/14N fractionation in nitrate-grown vascular plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjvVKrs7Y%3D&md5=81ebe3c93788c9839dc62d15fe33252eCAS |

Rudolph HJ, Voigt JU (1986) Effects of NH4 +-N and NO3 –-N on growth and metabolism of Sphagnum magellanicum. Physiologia Plantarum 66, 339–343.
Effects of NH4 +-N and NO3 -N on growth and metabolism of Sphagnum magellanicum.Crossref | GoogleScholarGoogle Scholar |

Ruiz JM, Romero L (2002) Relationship between potassium fertilization and nitrate assimilation in leaves and fruits of cucumber (Cucumis sativus) plants. The Annals of Applied Biology 140, 241–245.
Relationship between potassium fertilization and nitrate assimilation in leaves and fruits of cucumber (Cucumis sativus) plants.Crossref | GoogleScholarGoogle Scholar |

Salemaa M, Mäkipää R, Oksanen J (2008) Differences in the growth response of three bryophyte species to nitrogen. Environmental Pollution 152, 82–91.
Differences in the growth response of three bryophyte species to nitrogen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXivVOrt78%3D&md5=ccb592e72fff2fbe55d68a31339b239cCAS |

Schwoerbel J, Tillmanns GC (1974) Assimilation of nitrogen from the medium and nitrate reductase activity in submerged macrophytes: Fontinalis antipyretica L. Archiv fuer Hydrobiologie 2, 282–294. [In German\]

Soares A, Pearson J (1997) Short-term physiological responses of mosses to atmospheric ammonium and nitrate. Water, Air, and Soil Pollution 93, 225–242.
Short-term physiological responses of mosses to atmospheric ammonium and nitrate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhs12ksr0%3D&md5=f15463f010a11275a426c6bb641dcf5dCAS |

Stevens CJ, Manning P, van den Berg LJL, de Graaf MCC, Wamelink GWW, Boxman AW, Bleeker A, Vergeer P, Arroniz-Crespo M, Limpens J, Lamers LPM, Bobbink R, Dorland E (2011) Ecosystem responses to reduced and oxidised nitrogen inputs in European terrestrial habitats. Environmental Pollution 159, 665–676.
Ecosystem responses to reduced and oxidised nitrogen inputs in European terrestrial habitats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsFWksw%3D%3D&md5=e2d68a454bb8b5f6f68e730e4089ddd5CAS |

Stewart GR, Pate GS, Unkovich M (1993) Characteristics of inorganic nitrogen assimilation of plants in fire-prone Mediterranean-type vegetation. Plant, Cell & Environment 16, 351–363.
Characteristics of inorganic nitrogen assimilation of plants in fire-prone Mediterranean-type vegetation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlsF2hsL0%3D&md5=723457f62eb87bc76cf2e9d161933c6eCAS |

Tcherkez G, Farquhar GD (2006) Viewpoint: isotopic fractionation by plant nitrate reductase, twenty years later. Functional Plant Biology 33, 531–537.
Viewpoint: isotopic fractionation by plant nitrate reductase, twenty years later.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltFGhs78%3D&md5=e16b2d573292294c81c0b416a0b7f95aCAS |

Tischner R (2000) Nitrate uptake and reduction in higher and lower plants. Plant, Cell & Environment 23, 1005–1024.
Nitrate uptake and reduction in higher and lower plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnslWgtL8%3D&md5=f193319b199e967c4cc34eb46b52fd75CAS |

van der Leij M, Smith SJ, Miller AJ (1998) Remobilization of vacuolar stored nitrate in barley root cells. Planta 205, 64–72.
Remobilization of vacuolar stored nitrate in barley root cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXislGitrY%3D&md5=f3a6a1e6ff6b51a8e40301b67f00530bCAS |

Wallace W (1974) Purification and properties of a nitrate reductase-inactivating enzyme. Biochimica et Biophysica Acta 341, 267–276.

Wanek W, Pörtl K (2008) Short-term 15N uptake kinetics and nitrogen nutrition of bryophytes in a lowland rainforest, Costa Rica. Functional Plant Biology 35, 51–62.
Short-term 15N uptake kinetics and nitrogen nutrition of bryophytes in a lowland rainforest, Costa Rica.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFeksrc%3D&md5=1ff8bb5dc8d7a88a3e345ec72b82305dCAS |

Wanek W, Zotz G (2011) Are vascular epiphytes nitrogen or phosphorus limited? A study of plant 15N fractionation and foliar N : P stoichiometry with the tank bromeliad Vriesea sanguinolenta. New Phytologist 192, 462–470.
Are vascular epiphytes nitrogen or phosphorus limited? A study of plant 15N fractionation and foliar N : P stoichiometry with the tank bromeliad Vriesea sanguinolenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsV2itLbO&md5=c2f9e053c4c9dcacda7f3e31ee65758cCAS |

Wania R, Hietz P, Wanek W (2002) Natural 15N abundance of epiphytes depends on the position within the forest canopy: source signals and isotope fractionation. Plant, Cell & Environment 25, 581–589.
Natural 15N abundance of epiphytes depends on the position within the forest canopy: source signals and isotope fractionation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtFOks78%3D&md5=a7bec348da54dea3b8053bed8ee4f7c8CAS |

Waser NA, Yu ZM, Yin KD, Nielsen B, Harrison PJ, Turpin DH, Calvert SE (1999) Nitrogen isotopic fractionation during a simulated diatom spring bloom: importance of N-starvation in controlling fractionation. Marine Ecology Progress Series 179, 291–296.
Nitrogen isotopic fractionation during a simulated diatom spring bloom: importance of N-starvation in controlling fractionation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhs1ersw%3D%3D&md5=6be8efc273fd87be6d2d079d3e576163CAS |

Woodin SJ, Lee JA (1987) The effects of nitrate, ammonium and temperature on nitrate reductase activity in Sphagnum species. New Phytologist 105, 103–115.
The effects of nitrate, ammonium and temperature on nitrate reductase activity in Sphagnum species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXhsFeitLs%3D&md5=6b4961173584d587555d2edcdda3e1a4CAS |

Woodin SJ, Press MC, Lee JA (1985) Nitrate reductase activity in Sphagnum fuscum in relation to wet deposition of nitrate from the atmosphere. New Phytologist 99, 381–388.
Nitrate reductase activity in Sphagnum fuscum in relation to wet deposition of nitrate from the atmosphere.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXitVehsrc%3D&md5=3b7cb88b9cd489747b1f04bec8cc25e9CAS |

Yoneyama T, Kaneko A (1989) Variations in the natural abundance of 15N in nitrogenous fractions of komatsuna plants supplied with nitrate. Plant & Cell Physiology 30, 957–962.

Zielke HR, Filner P (1971) Synthesis and turnover of nitrate induced by nitrate in cultured tobacco cells. The Journal of Biological Chemistry 246, 1772–1779.