Abstract
Key message
Nitrate served as an important nitrogen source for dominant deciduous tree species, especially during their leaf expansion period, even in boreal forests, where nitrate availability was assumed to be low.
Abstract
Temporal changes in leaf nitrate assimilation with leaf growth were intensively investigated in boreal tree species to demonstrate the contribution of nitrate as a N source and to determine temporal changes in the contribution of nitrate during leaf ontogeny. Leaf area, mass, nitrate reductase activity (NRA), N concentration, and δ15N were repeatedly measured in developing leaves of naturally grown Alnus crispa, Betula neoalaskana, and Populus tremuloides during their leaf expansion period. Alnus crispa and B. neoalaskana showed distinct peaks in NRA during leaf expansion, whereas P. tremuloides did not. The highest peak in NRA occurred for A. crispa, whereas it had low NRA during the summer. Peak NRA in B. neoalaskana was lower than that of A. crispa (p < 0.01, ANOVA), although it showed higher NRA during summer (p < 0.01, ANOVA). All species showed clear decrease in N concentration through the leaf expansion period, but total N content per leaf increased. Only the N-fixing species A. crispa showed a rapid change in δ15N during the leaf expansion, and the decline indicated the changes in N source during the leaf development. The results indicate leaves of target species assimilated nitrate during the leaf expansion period, consuming immense energy, although leaves were considered a carbon sink during the early leaf expansion period. We suggest the early onset of leaf growth due to climate warming could influence plant nutrition via asynchrony between supply and demand for energy during spring.
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References
Andrews M (1986) The partitioning of nitrate assimilation between root and shoot of higher plants. Plant Cell Environ 9:511–519. https://doi.org/10.1111/1365-3040.ep11616228
Chapin FS, Van Cleve K, Tryon P (1986) Relationship of ion absorption to growth rate in taiga trees. Oecologia 69:238–242. https://doi.org/10.1007/BF00377628
Craine JM, Brookshire ENJ, Cramer MD, Hasselquist NJ, Koba K, Marin-Spiotta E, Wang L (2015) Ecological interpretations of nitrogen isotope ratios of terrestrial plants and soils. Plant Soil 396:1–26. https://doi.org/10.1007/s11104-015-2542-1
Deng X, Weinbaum SA, DeJong TM, Muraoka TT (1989) Utilization of nitrogen from storage and current-year uptake in walnut spurs during the spring flush of growth. Physiol Plant 75:492–498
Feigenbaum S, Bielorai H, Erner Y, Dasberg S (1987) The fate of 15N labeled nitrogen applied to mature citrus trees. Plant Soil 97:179–187
Frak E, Millard P, Le Roux X, Guillaumie S, Wendler R (2002) Coupling sap flow velocity and amino acid concentrations as an alternative method to 15N labeling for quantifying nitrogen remobilization by walnut trees. Plant Physiol 130:1043–1053. https://doi.org/10.1104/pp.002139
Gebauer G, Rehder H, Wollenweber B (1988) Nitrate, nitrate reduction and organic nitrogen in plants from different ecological and taxonomic groups of Central Europe. Oecologia 75:371–385. https://doi.org/10.1007/BF00376940
Gebauer G, Hahn G, Rodenkirchen H, Zuleger M (1998) Effects of acid irrigation and liming on nitrate reduction and nitrate content of Picea abies (L.) Karst. and Oxalis acetosella L. Plant Soil 199:59–70. https://doi.org/10.1023/A:1004263223917
Grassi G, Millard P, Wendler R, Minotta G, Tagliavini M (2002) Measurement of xylem sap amino acid concentrations in conjunction with whole tree transpiration estimates spring N remobilization by cherry (Prunus avium L.) trees. Plant Cell Environ 25:1689–1699. https://doi.org/10.1046/j.1365-3040.2002.00949.x
Guak S, Neilsen D, Millard P, Wendler R, Neilsen GH (2003) Determining the role of N remobilization for growth of apple (Malus domestica Borkh) trees by measuring xylem-sap N flux. J Exp Bot 54:2121–2131. https://doi.org/10.1093/jxb/erg228
Hänninen H (2006) Climate warming and the risk of frost damage to boreal forest trees: identification of critical ecophysiological traits. Tree Physiol 26:889–898. https://doi.org/10.1093/treephys/26.7.889
Högberg P, Granström A, Johansson T, Lundmark-Thelin A, Näsholm T (1986) Plant nitrate reductase activity as an indicator of availability of nitrate in forest soils. Can J for Res 16:1165–1169. https://doi.org/10.1139/x86-207
Jaworski E (1971) Nitrate reductase assay in intact plant tissues. Biochem Biophys Res Commun 43:1274–1279. https://doi.org/10.1016/S0006-291X(71)80010-4
Keeney DR, Nelson DW (1982) Nitrogen—inorganic forms. In: Page AL, Miller RH, Keeney DR (eds) Methods of soil analysis. Part 2. ASA and SSSA, Madison, pp 643–698. https://doi.org/10.2134/agronmonogr9.2.2ed.c33
Kielland K, Barnet B, Schell D (1998) Intraseasonal variation in the δ15N signature of taiga trees and shrubs. Can J for Res 28:485–488. https://doi.org/10.1139/x98-007
Kielland K, Ruess RW, Olson K, Boone RD (2006) Contribution of winter processes to soil nitrogen flux in taiga forest ecosystems. Biogeochemistry 81:340–360. https://doi.org/10.1007/s10533-006-9045-3
Koba K, Hirobe M, Koyama L, Kohzu A, Tokuchi N, Nadelhoffer K, Wada E, Takeda H (2003) Natural 15N abundance of plants and soil N in a temperate coniferous forest. Ecosystems 6:457–469. https://doi.org/10.1007/s10021-002-0132-6
Koyama L, Kielland K (2011) Plant physiological responses to hydrologically mediated changes in nitrogen supply on a boreal forest floodplain: a mechanism explaining the discrepancy in nitrogen demand and supply. Plant Soil 342:129–139. https://doi.org/10.1007/s11104-010-0676-8
Koyama LA, Kielland K (2018) Black spruce assimilates nitrate in boreal winter. Tree Physiol 39:536–543. https://doi.org/10.1093/treephys/tpy109
Koyama L, Tokuchi N (2003) Effects of NO3− availability on NO3− use in seedlings of three woody shrub species. Tree Physiol 23:281–288. https://doi.org/10.1093/treephys/23.4.281
Koyama L, Tokuchi N, Fukushima K, Terai M, Yamamoto Y (2008) Seasonal changes in nitrate use by three woody species: the importance of the leaf-expansion period. Trees 22:851–859. https://doi.org/10.1007/s00468-008-0246-3
Koyama L, Hirobe M, Koba K, Tokuchi N (2013) Nitrate-use traits of understory plants as potential regulators of vegetation distribution on a slope in a Japanese cedar plantation. Plant Soil 362:119–134. https://doi.org/10.1007/s11104-012-1257-9
Koyama LA, Terai M, Tokuchi N (2020) Nitrate reductase activities in plants from different ecological and taxonomic groups grown in Japan. Ecol Res 35:708–712. https://doi.org/10.1111/1440-1703.12083
Kudo G, Cooper EJ (2019) When spring ephemerals fail to meet pollinators: mechanism of phenological mismatch and its impact on plant reproduction. Proc Biol Sci 286:20190573. https://doi.org/10.1098/rspb.2019.0573
Kudo G, Ida TY, Tani T (2008) Linkages between phenology, pollination, photosynthesis, and reproduction in deciduous forest understory plants. Ecology 89:321–331. https://doi.org/10.1890/06-2131.1
Ladwig LM, Chandler JL, Guiden PW, Henn JJ (2019) Extreme winter warm event causes exceptionally early bud break for many woody species. Ecosphere 10:e02542
Lillo C (2008) Signalling cascades integrating light-enhanced nitrate metabolism. Biochem J 415:11–19. https://doi.org/10.1042/BJ20081115
Linkosalo T, Carter TR, Hakkinen R, Hari P (2000) Predicting spring phenology and frost damage risk of Betula spp. under climatic warming: a comparison of two models. Tree Physiol 20:1175–1182. https://doi.org/10.1093/treephys/20.17.1175
Linkosalo T, Häkkinen R, Terhivuo J, Tuomenvirta H, Hari P (2009) The time series of flowering and leaf bud burst of boreal trees (1846–2005) support the direct temperature observations of climatic warming. Agric for Meteorol 149:453–461. https://doi.org/10.1016/j.agrformet.2008.09.006
Liu XY, Koba K, Koyama LA, Hobbie SE, Weiss MS, Inagaki Y, Shaver GR, Giblin AE, Hobara S, Nadelhoffer KJ, Sommerkorn M, Rastetter EB, Kling GW, Laundre JA, Yano Y, Makabe A, Yano M, Liu CQ (2018) Nitrate is an important nitrogen source for Arctic tundra plants. Proc Natl Acad Sci USA 115:3398–3403. https://doi.org/10.1073/pnas.1715382115
Makoto K, Kajimoto T, Koyama L, Kudo G, Shibata H, Yanai Y, Cornelissen JHC (2014) Winter climate change in plant–soil systems: summary of recent findings and future perspectives. Ecol Res 29:593–606. https://doi.org/10.1007/s11284-013-1115-0
Menzel A, Sparks TH, Estrella N, Koch E, Aasa A, Ahas R, Alm-Kübler K, Bissolli P, Braslavská OG, Briede A, Chmielewski FM, Crepinsek Z, Curnel Y, Dahl Å, Defila C, Donnelly A, Filella Y, Jatczak K, Måge F, Mestre A, Nordli Ø, Peñuelas J, Pirinen P, Remišová V, Scheifinger H, Striz M, Susnik A, Van Vliet AJH, Wielgolaski F-E, Zach S, Zust ANA (2006) European phenological response to climate change matches the warming pattern. Glob Change Biol 12:1969–1976. https://doi.org/10.1111/j.1365-2486.2006.01193.x
Millard P (1994) Measurement of the remobilization of nitrogen for spring leaf growth of trees under field conditions. Tree Physiol 14:1049–1054. https://doi.org/10.1093/treephys/14.7-8-9.1049
Millard P, Grelet G-A (2010) Nitrogen storage and remobilization by trees: ecophysiological relevance in a changing world. Tree Physiol 30:1083–1095. https://doi.org/10.1093/treephys/tpq042
Millard P, Wendler R, Hepburn A, Smith A (1998) Variations in the amino acid composition of xylem sap of Betula pendula Roth. trees due to remobilization of stored N in the spring. Plant Cell Environ 21:715–722. https://doi.org/10.1046/j.1365-3040.1998.00313.x
Neilsen D, Millard P, Neilsen GH, Hogue EJ (1997) Sources of N for leaf growth in a high-density apple (Malus domestica) orchard irrigated with ammonium nitrate solution. Tree Physiol 17:733–739
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Meth 9:671–675. https://doi.org/10.1038/nmeth.2089
Šesták Z, Tichá I, Čatský F, Solárová J, Pospišilová J, Hodáňová D (1985) Integration of photosynthetic characteristics during leaf development. In: Sesták Z (ed) Photosynthesis during leaf development. Springer Science & Business Media, Berlin, pp 263–286. https://doi.org/10.1007/978-94-009-5530-1_11
Smirnoff N, Todd P, Stewart G (1984) The occurrence of nitrate reduction in the leaves of woody plants. Ann Bot 54:363–374. https://doi.org/10.1093/oxfordjournals.aob.a086806
Solomonson L, Barber M (1990) Assimilatory nitrate reductase: functional properties and regulation. Annu Rev Plant Physiol Plant Mol Biol 41:225–253. https://doi.org/10.1146/annurev.pp.41.060190.001301
Templer PH (2012) Changes in winter climate: soil frost, root injury, and fungal communities. Plant Soil 353:15–17. https://doi.org/10.1007/s11104-011-1064-8
Thomas F, Hilker C (2000) Nitrate reduction in leaves and roots of young pedunculate oaks (Quercus robur) growing on different nitrate concentrations. Environ Exp Bot 43:19–32. https://doi.org/10.1016/S0098-8472(99)00040-4
Valentine DW, Kielland K, Chapin FS III, McGuire AD, Van Cleve K (2006) Patterns of biogeochemistry in alaskan boreal forests. In: Chapin FS III, Oswood MW, van Cleve K, Viereck LA, Verbyla DL (eds) Alaska’s changing boreal forest. Oxford University Press, Oxford, pp 241–266. https://doi.org/10.1093/oso/9780195154313.003.0021
Yanagisawa S (2014) Transcription factors involved in controlling the expression of nitrate reductase genes in higher plants. Plant Sci 229:167–171. https://doi.org/10.1016/j.plantsci.2014.09.006
Yarie J, Bonanza Creek LTER (1998) Soil physical and chemical properties based on genetic horizon from 4 replicate pits placed around the replicate LTER control plots sampled in 1988 and 1989 Bonanza Creek LTER—University of Alaska Fairbanks. BNZ:134, http://www.lter.uaf.edu/data/data-detail/id/134. https://doi.org/10.6073/pasta/475a1825dfa264822ed53ca3574bb8e6
Acknowledgements
The stable isotope assay in the current study was conducted with the support of the Joint-Usage/Research Center: Stable Isotope Laboratory at the Center for Ecological Research, Kyoto University.
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This work was supported by JSPS KAKENHI Grant Number JP21780149 to LAK.
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468_2021_2259_MOESM1_ESM.pdf
Temporal changes in leaf traits regarding N acquisition and growth of Alnus crispa (left; (a), (d), (g), and (j)), Betula neoalaskana (middle; (b), (e), (h), and (k)), and Populus tremuloides (right; (c), (f), (i), and (l)) during the greening season 2010 in comparison with those of summer 2009. (a)-(c) N content per leaf; (d)-(f) NRA(+NO3) (closed square) and NRA(−NO3) (open square) per leaf; (g)-(i) leaf growth rate in area (broken line; left axis), leaf growth rate in mass (solid line; right axis) and LMA (leaf mass per area. cross; right axis); (j)-(l) leaf area (open diamond; left axis) and mass (closed diamond; right axis). Average ± s.d. are shown for five trees. Leaf growth rates were calculated as the difference of estimated leaf area on a day and the following day based on the growth curve. Note that the Y-axes are not identical among species to clearly show the intraspecies temporal changes (PDF 94 KB)
468_2021_2259_MOESM2_ESM.pdf
Relationship between leaf NRA(+NO3) and other leaf traits in individuals of Alnus crispa (left; (a), (d), (g), (j), (m) and (p)), Betula neoalaskana (middle; (b), (e), (h), (k), (n) and (q)), and Populus tremuloides (right; (c), (f), (i), (l), (o) and (r)) during the greening season 2010. (a)-(c) leaf δ15N; (d)-(f) leaf N content per leaf; and (g)-(i) leaf N content per area; (j)-(l) leaf N concentration; (m)-(o) NRA(−NO3) per leaf dry weight and (p)-(r) LMA (leaf mass per area). Different symbols indicate different individuals (PDF 150 KB)
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Koyama, L.A., Kielland, K. Seasonal changes in nitrate assimilation of boreal woody species: importance of the leaf-expansion period. Trees 36, 941–951 (2022). https://doi.org/10.1007/s00468-021-02259-9
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DOI: https://doi.org/10.1007/s00468-021-02259-9