Nitrate reductase activity (NRA) in the invasive alien Fallopia japonica: seasonal variation, differences among habitats types, and comparison with native species

Damian Chmura, Marek Krywult, Janusz Leszek Kozak

Abstract


Nitrate reductase activity (NRA) was studied in the invasive alien plant F. japonica (Japanese knotweed) during the vegetation season and among natural, semi-natural, and human-made habitats and compared with NRA in selected native species. NRA was measured directly in the field from the beginning of May until the beginning of October. NRA was much higher than in the plant’s native range, i.e., East Asia, and showed a high degree of variation over time with the highest values being reached at the stage of fast vegetative growth and at the beginning of fruiting. NRA was highest on dumping sites probably due to the high nitrogen input into soils and near traffic and the emission of NOx by vehicles. A comparison of the enzyme activity in four selected native plant species indicated that NRA in F. japonica was the highest with the exception of Urtica dioica, which exhibited a similar activity of the enzyme. A detailed comparison with this species showed that differences between these species on particular dates were influenced by differences in the phenology of both plants. The initial results that were obtained suggest that nitrogen pollution in an environment can contribute to habitat invasibility and a high level of NRA, which in addition to the many plant traits that are commonly accepted as characteristic of invasiveness features, may be an important factor that enhances invasion success.

Keywords


nitrogen assimilation; plant invasiveness; Reynoutria japonica; knotweed

Full Text:

PDF

References


Rejmánek M. Invasive plants: approaches and predictions. Austral Ecol. 2000;25:497–506. http://dx.doi.org/10.1046/j.1442-9993.2000.01080.x

Mälkönen E. Estimation of nitrogen saturation on the basis of long-term fertilization experiments. Plant Soil. 1990;128:75–82. http://dx.doi.org/10.1007/BF00009398

Nilsson LO, Wiklund K. Nutrient balance and P, K, Ca, Mg, S and B accumulation in a Norway spruce stand following ammonium sulphate application fertigation, irrigation, drought and N-free-fertilisation. Plant Soil. 1995;168–169:437–446. http://dx.doi.org/10.1007/BF00029357

Kumar A, Kumar HD. Nitrogen fixation by blue-green algae. In: Sen SP, editor. Proceedings of the plant physiology research, Society of Plant and Biochemistry, 1st International Congress of the Plant Physiology; 1988 Feb 15–20; New Delhi, India. New Delhi: Society of Plant and Biochemistry; 1988. p. 85–103.

Sinha RP, Kumar A. Screening of blue green algae for biofertilizer, In: Path PS, editor. Proceedings of the National Seminar on Organic Farming; 1992 Apr 18–19; Pune, India. Pune: College of Agriculture; 1992. p. 95–97.

Norby RJ, Weerasuriya Y, Hanson PJ. Induction of nitrate reductase activity in red spruce needles by NO2 and HNO3 vapor. Can J For Res. 1989;19:889–896. http://dx.doi.org/10.1139/x89-135

Perez-Soba M, van Deer Eerden LJM. Nitrogen uptake in needles of Scots pine (Pinus sylvestris L.) when exposed to gaseous ammonia and ammonium fertilizer in the soil, Plant Soil. 1993;153:231–242. http://dx.doi.org/10.1007/BF00012996

Wingsle GT, Nasholm T, Lundmark T, Ericsson A. Induction of nitrate reductase in needles of scots pine seedlings by NOx and NO3−. Physiol Plant. 1987;70:399–403. http://dx.doi.org/10.1111/j.1399-3054.1987.tb02835.x

Krywult M, Karolak A, Bytnerowicz A. Nitrate reductase activity as an indicator of ponderosa pine response to atmospheric nitrogen deposition in the San Bernardino Mountains. Environ Pollut. 1986;93:141–146. http://dx.doi.org/10.1016/0269-7491(96)00033-4

Krywult M, Bytnerowicz A. Induction of nitrate reductase activity by nitric acid vapor in California black oak (Quercus kellogii), canyon live oak (Quercus chrysolepis) and ponderosa pine (Pinus ponderosa) seedlings. Can J For Res. 1997;27:2101–2104. http://dx.doi.org/10.1139/x97-145

Vitousek PM, Mooney HA, Lubchenco J, Melillo JM. Human domination of Earth’s ecosystems. Science. 1997;5325(277):494–499. http://dx.doi.org/10.1007/978-0-387-73412-5_1

Mooney HA, Hobbs RJ. Invasive species in a changing world. Washington, DC: Island Press; 2000.

Bąba, W, Kurowska M, Kompała-Bąba A, Wilczek A, Długosz J, Szarejko I. Genetic diversity of populations of Brachypodium pinnatum (L.) P. Beauv.: expansive grass in a fragmented landscape. Pol J Ecol. 2012;60(1):31–40.

Bidwell S, Attiwill PM, Adams MA. Nitrogen availability and weed invasion in a remnant native woodland in urban Melbourne. Austral Ecol. 2006;31:262–270. http://dx.doi.org/10.1111/j.1442-9993.2006.01575.x

Baker HG. Characteristics and modes of origin of weeds. In: Baker HG, Stebbins CL, editors. The genetics of colonizing species. New York, NY: Academic Press; 1965. p. 147–169.

Richardson DM, Pyšek P. Naturalization of introduced plants: ecological drivers of biogeographic pattern. New Phytol. 2012;196:383–396. http://dx.doi.org/10.1111/j.1469-8137.2012.04292.x

Lowe S, Browne M, Boudjelas S, de Poorter M. 100 of the world’s worst invasive alien species. A selection from the Global Invasive Species Database. Auckland: The Invasive Species Specialist Group (ISSG); 2000.

Tateno M, Hirose T. Nitrification and nitrogen accumulation in early stages of primary succession on Mt. Fuji. Ecol Res. 1987;2:113–120. http://dx.doi.org/10.1007/BF02346920

Norby RJ. Foliar nitrate reductase: a marker for assimilation of atmospheric nitrogen oxides. In: Grosblatt N, editor. Biological markers of air-pollution stress and damage in forests. Washington, DC: National Academy Press; 1989. p. 245–250.

Krywult M, Bielec D. Measurement of nitrate reductase activity in a field conditions – methodology. J Ecol Eng. 2013;32:115–121. http://dx.doi.org/10.12912/23920629/373

Diekmann M, Falkengren-Grerup U. Prediction of species response to atmospheric nitrogen deposition by means of ecological measures and life history traits. J Ecol. 2002;90(1):108–120. http://dx.doi.org/10.1046/j.0022-0477.2001.00639.x

Tokarska-Guzik B. The establishment and spread of alien plant species (kenophytes) in the flora of Poland. Katowice: Wydawnictwo Uniwersytetu Śląskiego; 2005.

Bzdęga K, Janiak A, Tarlowska S, Kurowska M, Tokarska-Guzik B, Szarejko I. Unexpected genetic diversity of Fallopia japonica from Central Europe revealed after AFLP analysis. Flora. 2012;207(9):636–645. http://dx.doi.org/10.1016/j.flora.2012.05.002

Tokarska-Guzik B, Dajdok Z, Zając M, Zając A, Urbisz A, Danielewicz W. Rośliny obcego pochodzenia w Polsce ze szczególnym uwzględnieniem gatunków inwazyjnych. Warszawa: Generalna Dyrekcja Ochrony Środowiska; 2012.

Chmura D, Nejfeld P, Borowska M, Woźniak G, Nowak T, Tokarska-Guzik B. The importance of land use type in Fallopia (Reynoutria) japonica invasion in the suburban environment. Pol J Ecol. 2013;61(2):205–210.

Jaworski EG. Nitrate reductase assay in intact plant tissue. Biochem Biophys Res Commun. 1971;43:1274–1279. http://dx.doi.org/10.1016/S0006-291X(71)80010-4

Krywult M, Turunen M, Sutinen ML, Derome K, Norokorpi Y. Nitrate reductase activity in some subarctic species and UV in influence in the foliage of Betula pendula Roth seedlings. Sci Total Environ. 2002;284(1–3):149–153. http://dx.doi.org/10.1016/S0048-9697(01)00875-0

Amaya K, Sugiura K. A simple, inexpensive and reliable method of measuring nitrogen dioxide concentration in ambient air. Environment Protection Engineering. 1983;9:5–9.

Krochmal D, Gorski L. Modification of Amaya–Sugiura passive sampling spectrophotometric method of nitrogen dioxide determination in ambient air. Fresenius J Anal Chem. 1991;340(4):220–222. http://dx.doi.org/10.1007/BF00321772

R Core Team. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2015.

Krywult M, Smykla J, Kinnunen H, Martz F, Sutinen ML, Lakkala K. et al. Influence of solar UV radiation on the nitrogen metabolism in needles of Scots pine (Pinus sylvestris L.). Environ Pollut. 2008;156:1105–1111. http://dx.doi.org/10.1016/j.envpol.2008.04.009

Gharbi A, Hipkin CR. Studies on nitrate reductase in British angiosperms. New Phytol. 1984;97(4):629–639. http://dx.doi.org/10.1111/j.1469-8137.1984.tb03627.x

Bímová K, Mandák B, Kasparová I. How does Reynoutria invasion fit the various theories of invasibility? J Veg Sci. 2004;15:495–504. http://dx.doi.org/10.1111/j.1654-1103.2004.tb02288.x

Tokarska-Guzik B, Bzdęga K, Knapik D, Jenczała G. Changes in plant species richness in some riparian plant communities as a result of their colonisation by taxa of Reynoutria (Fallopia). Biodiversity: Research and Conservation. 2006;1–2:123–130.

Chmura D, Tokarska-Guzik B, Nowak T, Woźniak G, Bzdęga K, Koszela K, et al. The influence of invasive Fallopia taxa on resident plant species in two river valleys (southern Poland). Acta Soc Bot Pol. 2015;84(1):23–33. http://dx.doi.org/10.5586/asbp.2015.008

Andrews M. The partitioning of nitrate assimilation between root and shoot of higher plants. Plant Cell Environ. 1986;9:511–519. http://dx.doi.org/10.1111/1365-3040.ep11616228

Tang MH, Porder S, Lovett GM. Species differences in nitrate reductase activity are unaffected by nitrogen enrichment in northeastern US forests. For Ecol Manage. 2012;275:52–59. http://dx.doi.org/10.1016/j.foreco.2012.03.006

Cape JN, Tang YS, van Dijk N, Love L, Sutton MA, Palmer SCF. Concentrations of ammonia and nitrogen dioxide at roadside verges, and their contribution to nitrogen deposition. Environ Pollut. 2004;132:469–478. http://dx.doi.org/10.1016/j.envpol.2004.05.009

Krywult M, Klich M. Nitrate reductase activity as an indicator of nitrate fixation and assimilation by tropical forest species on St. Thomas Island. Fragmenta Floristica et Geobotanica. 2000;45(1–2):213–220.

Hill PW, Farrar J, Roberts P, Farrell M, Grant H, Newsham KK, et al. Vascular plant success in a warming Antarctic may be due to efficient nitrogen acquisition. Nat Clim Chang. 2011;1(1):50–53. http://dx.doi.org/10.1038/nclimate1060

Krywult M, Smykla J, Wincenciak A. The presence of nitrates and the impact of ultraviolet radiation as factors that determine nitrate reductase activity and nitrogen concentrations in Deschampsia antarctica Desv. around penguin rookeries on King George Island, Maritime Antarctica. Water Air Soil Pollut. 2013;224:1–12. http://dx.doi.org/10.1007/s11270-013-1563-8

Davis MA, Grime JP, Thompson K. Fluctuating resources in plant communities: a general theory of invasibility. J Ecol. 2000;88:528–534. http://dx.doi.org/10.1046/j.1365-2745.2000.00473.x




DOI: https://doi.org/10.5586/asbp.3514

Journal ISSN:
  • 2083-9480 (online)
  • 0001-6977 (print; ceased since 2016)
This is an Open Access journal, which distributes its content under the terms of the Creative Commons Attribution License, which permits redistribution, commercial and non-commercial, provided that the content is properly cited.
The journal is a member of the Committee on Publication Ethics (COPE) and aims to follow the COPE’s principles.
The journal publisher is a member of the Open Access Scholarly Publishers Association.
The journal content is indexed in Similarity Check, the Crossref initiative to prevent scholarly and professional plagiarism.
Publisher
Polish Botanical Society