Seasonal dynamics of stem N2O exchange follow the physiological activity of boreal trees

. 2019 Nov 01 ; 10 (1) : 4989. [epub] 20191101

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid31676776
Odkazy

PubMed 31676776
PubMed Central PMC6825224
DOI 10.1038/s41467-019-12976-y
PII: 10.1038/s41467-019-12976-y
Knihovny.cz E-zdroje

The role of trees in the nitrous oxide (N2O) balance of boreal forests has been neglected despite evidence suggesting their substantial contribution. We measured seasonal changes in N2O fluxes from soil and stems of boreal trees in Finland, showing clear seasonality in stem N2O flux following tree physiological activity, particularly processes of CO2 uptake and release. Stem N2O emissions peak during the vegetation season, decrease rapidly in October, and remain low but significant to the annual totals during winter dormancy. Trees growing on dry soils even turn to consumption of N2O from the atmosphere during dormancy, thereby reducing their overall N2O emissions. At an annual scale, pine, spruce and birch are net N2O sources, with spruce being the strongest emitter. Boreal trees thus markedly contribute to the seasonal dynamics of ecosystem N2O exchange, and their species-specific contribution should be included into forest emission inventories.

Zobrazit více v PubMed

Kuusela K. The boreal forests: an overview. Unasylva. 1992;170:3–13.

Dalal RC, Allen DE. Turner Review No. 18: Greenhouse gas fluxes from natural ecosystems. Aust. J. Bot. 2008;56:369–407. doi: 10.1071/BT07128. DOI

Korhonen, K. T. et al. Suomen metsät 2004–2008 ja niiden kehitys 1921–2008. Metsätieteen aikakauskirja 3/2013, 269–608 (2013).

IPCC. in Climate Change 2013: The Physical Science Basis. (eds Stocker, T. F. et al.) (IPCC: Intergovernmental Panel on Climate Change, Cambridge University Press, 2013).

Wrage N, Velthof GL, van Beusichem ML, Oenema O. Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol. Biochem. 2001;33:1723–1732. doi: 10.1016/S0038-0717(01)00096-7. DOI

Smith KA, et al. Exchange of greenhouse gases between soil and atmosphere: interactions of soil physical factors and biological processes. Eur. J. Soil. Sci. 2003;54:779–791. doi: 10.1046/j.1351-0754.2003.0567.x. DOI

Rütting T, Boeckx P, Müller C, Klemedtsson L. Assessment of the importance of dissimilatory nitrate reduction to ammonium for the terrestrial nitrogen cycle. Biogeosciences. 2011;8:1779–1791. doi: 10.5194/bg-8-1779-2011. DOI

Pihlatie M, Ambus P, Rinne J, Pilegaard K, Vesala T. Plant-mediated nitrous oxide emissions from beech (Fagus sylvatica) leaves. New Phytol. 2005;168:93–98. doi: 10.1111/j.1469-8137.2005.01542.x. PubMed DOI

Machacova K, Papen H, Kreuzwieser J, Rennenberg H. Inundation strongly stimulates nitrous oxide emissions from stems of the upland tree Fagus sylvatica and the riparian tree Alnus glutinosa. Plant Soil. 2013;364:287–301. doi: 10.1007/s11104-012-1359-4. DOI

Smart DR, Bloom AJ. Wheat leaves emit nitrous oxide during nitrate assimilation. Proc. Natl. Acad. Sci. USA. 2001;98:7875–7878. doi: 10.1073/pnas.131572798. PubMed DOI PMC

Machacova K, Maier M, Svobodova K, Lang F, Urban O. Cryptogamic stem covers may contribute to nitrous oxide consumption by mature beech trees. Sci. Rep. 2017;7:13243. doi: 10.1038/s41598-017-13781-7. PubMed DOI PMC

Yu, K. & Chen, G. in Nitrous Oxide Emissions Research Progress (eds Sheldon, A. I. & Barnhart, E. P.) 85–104 (Nova Science Publishers, Hauppauge, NY, USA, 2009).

Machacova K, et al. Pinus sylvestris as a missing source of nitrous oxide and methane in boreal forest. Sci. Rep. 2016;6:23410. doi: 10.1038/srep23410. PubMed DOI PMC

Wen Y, Corre MD, Rachow C, Chen L, Veldkamp E. Nitrous oxide emissions from stems of alder, beech and spruce in a temperate forest. Plant Soil. 2017;420:423–434. doi: 10.1007/s11104-017-3416-5. DOI

Rusch H, Rennenberg H. Black alder (Alnus glutinosa (L.) Gaertn.) trees mediate methane and nitrous oxide emission from the soil to the atmosphere. Plant Soil. 1998;201:1–7. doi: 10.1023/A:1004331521059. DOI

McBain MC, Warland JS, McBride RA, Wagner-Riddle C. Laboratory-scale measurements of N2O and CH4 emissions from hybrid poplars (Populus deltoides x Populus nigra) Waste Manag. Res. 2004;22:454–465. doi: 10.1177/0734242X04048832. PubMed DOI

Díaz-Pinés E, et al. Nitrous oxide emissions from stems of ash (Fraxinus angustifolia Vahl) and European beech (Fagus sylvatica L.) Plant Soil. 2015;398:35–45. doi: 10.1007/s11104-015-2629-8. DOI

Sevanto S, et al. Wintertime photosynthesis and water uptake in a boreal forest. Tree Physiol. 2006;26:749–757. doi: 10.1093/treephys/26.6.749. PubMed DOI

Kolari P, et al. CO2 exchange and component CO2 fluxes of a boreal Scots pine forest. Boreal Environ. Res. 2009;14:761–783.

Chang C, Janzen HH, Cho CM, Nakonechny EM. Nitrous oxide emission through plants. Soil Sci. Soc. Am. J. 1998;62:35–38. doi: 10.2136/sssaj1998.03615995006200010005x. DOI

Goshima N, et al. Emission of nitrous oxide (N2O) from transgenic tobacco expressing antisense NiR mRNA. Plant J. 1999;19:75–80. doi: 10.1046/j.1365-313X.1999.00494.x. PubMed DOI

Hakata M, Takahashi M, Zumft W, Sakamoto A, Morikawa H. Conversion of the nitrate nitrogen and nitrogen dioxide to nitrous oxides in plants. Acta Biotechnol. 2003;23:249–257. doi: 10.1002/abio.200390032. DOI

Albert KR, Bruhn A, Ambus P. Nitrous oxide emission from Ulva lactuca incubated in batch cultures is stimulated by nitrite, nitrate and light. J. Exp. Mar. Biol. Ecol. 2013;448:37–45. doi: 10.1016/j.jembe.2013.06.010. DOI

Lenhart K, et al. Nitrous oxide and methane emissions from cryptogamic covers. Glob. Change Biol. 2015;21:3889–3900. doi: 10.1111/gcb.12995. PubMed DOI

Lenhart K, et al. Nitrous oxide effluxes from plants as a potentially important source to the atmosphere. New Phytol. 2019;221:1398–1408. doi: 10.1111/nph.15455. PubMed DOI

Yu KW, Wang ZP, Chen GX. Nitrous oxide and methane transport through rice plants. Biol. Fert. Soils. 1997;24:341–343. doi: 10.1007/s003740050254. DOI

Davidson EA, Keller M, Erickson HE, Verchot LV, Veldkamp E. Testing a conceptual model of soil emissions of nitrous and nitric oxides. BioScience. 2000;50:667–680. doi: 10.1641/0006-3568(2000)050[0667:TACMOS]2.0.CO;2. DOI

Papen, H. et al. in Tree Species Effects on Soils: Implications for Global Change (eds Binkley, D. & Menyailo, O.) 165–172 (NATO Science Series IV-Earth and Environmental Sciences, Springer Netherlands, 2005).

Menyailo OV, Hungate BA, Zech W. The effect of single tree species on soil microbial activities related to C and N cycling in the Siberian artificial afforestation experiment—tree species and soil microbial activities. Plant Soil. 2002;242:183–196. doi: 10.1023/A:1016245619357. DOI

Menyailo, O. V. & Hungate, B. A. in Tree Species Effects on Soils: Implications for Global Change (eds Binkley, D. & Menyailo, O. V.) 293–305 (NATO Science Series, Kluwer Academic Publishers, Dordrecht, 2005).

Menyailo OV, Hungate BA. Tree species and moisture effects on soil sources of N2O: Quantifying contributions from nitrification and denitrification with 18O isotopes. J. Geophys. Res. 2006;111:G02022. doi: 10.1029/2005JG000058. DOI

Kieloaho AJ, et al. Stimulation of soil organic nitrogen pool: The effect of plant and soil organic matter degrading enzymes. Soil Biol. Biochem. 2016;96:97–106. doi: 10.1016/j.soilbio.2016.01.013. DOI

Walker TS, Bais HP, Grotewold E, Vivanco JM. Root exudation and rhizosphere biology. Plant Physiol. 2003;132:44–51. doi: 10.1104/pp.102.019661. PubMed DOI PMC

Colmer TD. Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant Cell Environ. 2003;26:17–36. doi: 10.1046/j.1365-3040.2003.00846.x. DOI

Wassmann R, Aulakh MS. The role of rice plants in regulating mechanisms of methane emissions. Biol. Fert. Soils. 2000;31:20–29. doi: 10.1007/s003740050619. DOI

Prendergast-Miller MT, Baggs EM, Johnson D. Nitrous oxide production by the ectomycorrhizal fungi Paxillus involutus and Tylospora fibrillosa. FEMS Microbiol. Lett. 2011;316:31–35. doi: 10.1111/j.1574-6968.2010.02187.x. PubMed DOI

Okiobe ST, Augustin J, Mansour I, Veresoglou SD. Disentangling direct and indirect effects of mycorrhiza on nitrous oxide activity and denitrification. Soil Biol. Biochem. 2019;134:142–151. doi: 10.1016/j.soilbio.2019.03.025. DOI

Bender SF, et al. Symbiotic relationships between soil fungi and plants reduce N2O emissions from soil. ISME J. 2014;8:1336–1345. doi: 10.1038/ismej.2013.224. PubMed DOI PMC

Bender SF, Conen F, Van der Heijden MGA. Mycorrhizal effects on nutrient cycling, nutrient leaching and N2O production in experimental grassland. Soil Biol. Biochem. 2015;80:283–292. doi: 10.1016/j.soilbio.2014.10.016. DOI

Bruhn D, Albert KR, Mikkelsen TN, Ambus P. UV-induced N2O emission from plants. Atmos. Environ. 2014;99:206–214. doi: 10.1016/j.atmosenv.2014.09.077. DOI

Thornley JHM. Plant growth and respiration re-visited: maintenance respiration defined—it is an emergent property of, not a separate process within, the system—and why the respiration: photosynthesis ratio is conservative. Ann. Bot. 2011;108:1365–1380. doi: 10.1093/aob/mcr238. PubMed DOI PMC

Lintunen A, et al. Bursts of CO2 released during freezing offer a new perspective on avoidance of winter embolism in trees. Ann. Bot. 2014;114:1711–1718. doi: 10.1093/aob/mcu190. PubMed DOI PMC

Evans DE. Aerenchyma formation. New Phytol. 2003;161:35–49. doi: 10.1046/j.1469-8137.2003.00907.x. DOI

Arbellay E, Stoffel M, Bollschweiler M. Wood anatomical analysis of Alnus incana and Betula pendula injured by a debris-flow event. Tree Physiol. 2010;30:1290–1298. doi: 10.1093/treephys/tpq065. PubMed DOI

Sorz J, Hietz P. Gas diffusion through wood: implications for oxygen supply. Trees. 2006;20:34–41. doi: 10.1007/s00468-005-0010-x. DOI

Chapuis-Lardy L, Wrage N, Metay A, Chotte JL, Bernoux M. Soils, a sink for N2O? A review. Glob. Change Biol. 2007;13:1–17. doi: 10.1111/j.1365-2486.2006.01280.x. DOI

Lendzian KJ. Survival strategies of plants during secondary growth: barrier properties of phellems and lenticels towards water, oxygen, and carbon dioxide. J. Exp. Bot. 2006;57:2535–2546. doi: 10.1093/jxb/erl014. PubMed DOI

Pihlatie M, et al. Gas concentration driven fluxes of nitrous oxide and carbon dioxide in boreal forest soil. Tellus. 2007;59B:458–469. doi: 10.1111/j.1600-0889.2007.00278.x. DOI

Mäkisara, K., Katila, M., Peräsaari, J. & Tomppo, E. in Natural Resources and Bioeconomy Studies 10/2016 (Natural Resources Institute Finland, 2016).

Dobrovolny L. Density and spatial distribution of beech (Fagus sylvatica L.) regeneration in Norway spruce (Picea abies (L.) Karsten) stands in the central part of the Czech Republic. IForest-Biogeosciences Forestry. 2016;9:666–672. doi: 10.3832/ifor1581-008. DOI

Ge ZM, et al. Impacts of changing climate on the productivity of Norway spruce dominant stands with a mixture of Scots pine and birch in relation to water availability in southern and northern Finland. Tree Physiol. 2011;31:323–338. doi: 10.1093/treephys/tpr001. PubMed DOI

Bowatte S, et al. Emissions of nitrous oxide from the leaves of grasses. Plant Soil. 2014;374:275–283. doi: 10.1007/s11104-013-1879-6. DOI

Simpson IJ, Edwards GC, Thurtell GW. Micrometeorological measurements of methane and nitrous oxide exchange above a boreal aspen forest. J. Geophys. R. 1997;102:29331–29341. doi: 10.1029/97JD03181. DOI

Eugster W, et al. Methodical study of nitrous oxide eddy covariance measurements using quantum cascade laser spectrometery over a Swiss forest. Biogeosciences. 2007;4:927–939. doi: 10.5194/bg-4-927-2007. DOI

Nicolini G, Castaldi S, Fratini G, Valentini R. A literature overview of micrometeorological CH4 and N2O flux measurements in terrestrial ecosystems. Atmos. Environ. 2013;81:311–319. doi: 10.1016/j.atmosenv.2013.09.030. DOI

Högberg P, Näsholm T, Franklin O, Högberg MN. Tamm review: on the nature of the nitrogen limitation to plant growth in Fennoscandian boreal forests. For. Ecol. Manag. 2017;403:161–185. doi: 10.1016/j.foreco.2017.04.045. DOI

Aber J, et al. Nitrogen saturation in temperate forest ecosystems—hypotheses revisited. Bioscience. 1998;48:921–934. doi: 10.2307/1313296. DOI

Butterbach-Bahl K, Gasche R, Willibald G, Papen H. Exchange of N-gases at the Hoglwald Forest—a summary. Plant Soil. 2002;240:117–123. doi: 10.1023/A:1015825615309. DOI

Kreutzer K, Butterbach-Bahl K, Rennenberg H, Papen H. The complete nitrogen cycle of an N-saturated spruce forest ecosystem. Plant Biol. 2009;11:643–649. doi: 10.1111/j.1438-8677.2009.00236.x. PubMed DOI

Pirinen, P. et al. Tilastoja Suomen Ilmastosta 1981–2010 (Climatological Statistics of Finland 1981–2010) 1–96 (Finnish Meteorological Institute Reports 2012/1, Helsinki, 2012).

Maier M, Machacova K, Lang F, Svobodova K, Urban O. Combining soil and tree-stem flux measurements and soil gas profiles to understand CH4 pathways in Fagus sylvatica forests. J. Plant Nutr. Soil Sci. 2018;181:31–35. doi: 10.1002/jpln.201600405. DOI

Pihlatie M, et al. Comparison of static chambers to measure CH4 emissions from soils. Agr. For. Meteorol. 2013;171–172:124–136. doi: 10.1016/j.agrformet.2012.11.008. DOI

Pumpanen J, et al. Respiration in boreal forest soil as determined from carbon dioxide concentration profile. Soil Sci. Soc. Am. J. 2008;72:1187–1196. doi: 10.2136/sssaj2007.0199. DOI

Ilvesniemi H, et al. Water balance of a boreal Scots pine forest. Boreal Environ. Res. 2010;15:375–396.

Hari, P. et al. in Physical and Physiological Forest Ecology (eds Hari, P., Heliövaara, K. & Kulmala, L.) 471–487 (Springer Science, 2013).

Rannik Ü, Keronen P, Hari P, Vesala T. Estimation of forest–atmosphere CO2 exchange by eddy covariance and profile techniques. Agr. For. Meteorol. 2004;126:141–155. doi: 10.1016/j.agrformet.2004.06.010. DOI

Mammarella I, et al. Relative humidity effect on the high-frequency attenuation of water vapor flux measured by a closed-path eddy covariance system. J. Atmos. Ocean. Tech. 2009;26:1856–1866. doi: 10.1175/2009JTECHA1179.1. DOI

Machacova, K. et al. Summer fluxes of nitrous oxide from boreal forest. In Global Change: A Complex Challenge, Conference Proceedings, 78–81 (Global Change Research Center, Brno, 2015).

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...