Nitrogen resorption and fractionation during leaf senescence in typical tree species in Japan

Abstract

In northeastern Japan, an area of high precipitation and mountains, beech (Fagus creanata Blume), larch (Larix kaempferi Lamb.), cedar (Cryptomeria japonica D. Don) and black locust (Robinia pseudoacacia L.) were evaluated for N resorption and N isotope fractionation in pre- and post-abscission leaves in comparison to green leaves. The highest leaf N concentration in summer corresponded to the N-fixing black locust, followed in decreasing order by the deciduous beech and larch and evergreen cedar. On the other hand, the lowest N resorption efficiency corresponded to black locust and the highest to beech, in increasing order by larch and cedar. All tree species returned significant amounts of N before leaf abscission; however, N isotope fractionation during leaf N resorption was only found for beech, with a depleted N isotope value from green to pre-abscission leaf. The most N, however, was resorbed from pre-abscission to post-abscission. This result may indicate that δ¹⁵N fractionation took place during N transformation processes, such as protein hydrolysis, when the concentration of free amino acids increased sharply. The difference in the type of amino acid produced by each species could have influenced the N isotope ratio in beech but not in the other tree species. The results of this study showed that it is possible to infer the type and timing of processes relevant to N resorption by analyzing leaf δ¹⁵N variation during senescence.

Keywords

Amino acids / Cool temperate forest / Fresh litter / N resorption / δ¹⁵N

References

[1] Adriaenssens S, Hansen K, Staelens J, Wuyts K, De Schrijver A, Baeten L, Boeckx P, Samson R, Verheyen K. Throughfall deposition and canopy exchange processes along a vertical gradient within the canopy of beech (Fagus sylvatica L.) and Norway spruce (Picea abies (L.) Karst). Sci Total Environ, 2012, 420: 168-182.

[2] Aerts R. Nutrient resorption from senescing leaves of perennials: are there general patterns?. J Ecol, 1996, 84(4): 597-608.

[3] Amundson R, Austin AT, Schuur EA, Yoo K, Matzek V, Kendall C, Baisden WT. Global patterns of the isotopic composition of soil and plant nitrogen. Glob Biogeochem Cycles, 2003 17 1 1031

[4] Aranibar JN, Otter L, Macko SA, Feral CJW, Epstein HE, Dowty PR, Eckardt FD, Shugart HH, Swap RJ. Nitrogen cycling in he soil-plant system along a precipitation gradient in the Kalahari Sands. Glob Change Biol, 2004, 10(3): 359-373.

[5] Babst BA, Coleman GD. Seasonal nitrogen cycling in temperate trees: transport and regulatory mechanisms are key missing links. Plant Sci, 2018, 270: 268-277.

[6] Chapin FS, Kedrowski RA. Seasonal changes in nitrogen and phosphorus fractions and autumn retranslocation in evergreen and deciduous taiga trees. Ecology, 1983, 64(2): 376-391.

[7] Chavez-Vergara B, Merino A, Vázquez-Marrufo G, García-Oliva F. Organic matter dynamics and microbial activity during decomposition of forest floor under two native neotropical oak species in a temperate deciduous forest in Mexico. Geoderma, 2014, 235: 133-145.

[8] Chavez-Vergara BM, González-Rodríguez A, Etchevers JD, Oyama K, García-Oliva F. Foliar nutrient resorption constrains soil nutrient transformations under two native oak species in a temperate deciduous forest in Mexico. Eur J For Res, 2015, 134(5): 803-817.

[9] Codron J, Codron D, Lee-Thorp JA, Sponheimer M, Bond WJ, de Ruiter D, Grant R. Taxonomic, anatomical, and spatio-temporal variations in the stable carbon and nitrogen isotopic compositions of plants from an African savanna. J Archaeol Sci, 2005, 32(12): 1757-1772.

[10] Craine JM, Elmore AJ, Aidar MP, Bustamante M, Dawson TE, Hobbie EA, Nardoto GB. Global patterns of foliar nitrogen isotopes and their relationships with climate, mycorrhizal fungi, foliar nutrient concentrations, and nitrogen availability. New Phytol, 2009, 183(4): 980-992.

[11] Fotelli MN, Rennenberg H, Gessler A. Effects of drought on the competitive interference of an early successional (Rubus fruticosus) on fagus sylvatica L. seedlings: 15N uptake and partitioning. Responses of amino acids and other N compounds. Plant Biol, 2002, 4: 311-320.

[12] Gauthier NP, Soufi B, Walkowicz WE, Pedicord VA, Mavrakis KJ, Macek B, Miller ML. Cell-selective labeling using amino acid precursors for proteomic studies of multicellular environments. Nat Methods, 2013 10 8 768

[13] González-Zurdo P, Escudero A, Mediavilla S. N resorption efficiency and proficiency in response to winter cold in three evergreen species. Plant Soil, 2015, 394(1–2): 87-98.

[14] Handley LL, Austin AT, Stewart GR, Robinson D, Scrimgeour CM, Raven JA, Schmidt S. The ¹⁵N natural abundance (δ¹⁵N) of ecosystem samples reflects measures of water availability. Funct Plant Biol, 1999, 26(2): 185-199.

[15] Hayashi M, Lopez MCL, Nobori Y, Byambasuren M, Boy J. Nitrogen isotope pattern in Mongolian larch stands at the southern Eurasian boreal forest boundary. Isot Environ Health Stud, 2018, 45(6): 608-621.

[16] Hobbie EA, Jumpponen A, Trappe J. Foliar and fungal ¹⁵N: ¹⁴N ratios reflect development of mycorrhizae and nitrogen supply during primary succession—testing analytical models. Oecologia, 2005, 146(2): 258-268.

[17] Kahmen A, Wanek W, Buchmann N. Foliar δ¹⁵N values characterize soil N cycling and reflect nitrate or ammonium preference of plants along a temperate grassland gradient. Oecologia, 2008, 156(4): 861-870.

[18] Killingbeck KT. Nutrient resorption. Plant cell death processes, 2004, Cambridge: Academic Press 215 226

[19] Kobayashi H, Tashiro N. Temporal variation in leaf nitrogen content in a Cryptomeria japonica canopy. J Forest Environ (Jpn), 2003, 45(2): 99-102.

[20] Kolb KJ, Evans RD. Implications of leaf nitrogen recycling on the nitrogen isotope composition of deciduous plant tissues. New Phytol, 2002, 156(1): 57-64.

[21] Lima ALDS, Zanella F, Schiavianto MA, Haddad CRB. N availability and mechanisms of N conservation in deciduous and semideciduous tropical forest legume trees. Acta Bot Bras, 2006, 20(3): 625-632.

[22] Lopez CML, Mizota C, Nobori Y, Sasaki T, Yamanaka T. Temporal changes in nitrogen acquisition of Japanese black pine (Pinus thunbergii) associated with black locust (Robinia pseudoacacia). J For Res, 2014, 25(3): 585-589.

[23] Mae T. Leaf senescence and nitrogen metabolism. Plant cell death processes, 2004, Cambridge: Academic Press 157 168

[24] Malagoli M, Dal Canal A, Quaggioti S, Pegoraro P, Botacin A. Differences in nitrate and ammonium uptake between Scots pine and European larch. Plant Soil, 2000, 221(1): 1-3.

[25] Michelsen A, Schmidt IK, Jonasson S, Quarmby C, Sleep D. Leaf ¹⁵ N abundance of subarctic plants provides field evidence that ericoid, ectomycorrhizal and non-and arbuscular mycorrhizal species access different sources of soil nitrogen. Oecologia, 1996, 105(1): 53-63.

[26] Millard P. Measurement of the remobilization of nitrogen for spring leaf growth of trees under field conditions. Tree Physiol, 1994, 14(7-8-9): 1049-1054.

[27] Näsholm T. Removal of nitrogen during needle senescence in Scots pine (Pinus sylvestris L.). Oecologia, 1994, 99(3–4): 290-296.

[28] Negi GCS, Singh SP. Leaf nitrogen dynamics with particular reference to retranslocation in evergreen and deciduous tree species of Kumaun Himalaya. Can J For Res, 1993, 23(3): 349-357.

[29] Oikawa A, Ostuka T, Nakabayashi R, Jikumaru Y, Isuzugawa K, Murayama H, Saito K, Shiratake K. Metabolic profiling of developing pear fruits reveals dynamic variation in primary and secondary metabolites, including plant hormones. PLoS ONE, 2015 10 7 e0131408

[30] Özbucak TB, Kutbay HG, Kilic D, Korkmaz H, Bilgin A, Yalcin E, Apaydin Z. Foliar resorption of nutrients in selected sympatric tree species in gallery forest Black Sea region. Pol J Ecol, 2008, 56(2): 227-237.

[31] Pardo LH, Templer PH, Goodale CL, Duke S, Groffman PM, Adams MB, Compton J. Regional assessment of N saturation using foliar and root δ¹⁵N. Biogeochemistry, 2006, 80(2): 143-171.

[32] Pardo LH, Semaoune P, Schaberg PG, EagarC SM. Patterns in ^{δ 15} N in roots, stems, and leaves of sugar maple and American beech seedlings, saplings, and mature trees. Biogeochemistry, 2013, 112(1–3): 275-291.

[33] Santa Regina I, Tarazona T. Nutrient cycling in a natural beech forest and adjacent planted pine in northern Spain. Forestry, 2001, 74(1): 11-28.

[34] Schmidt S, Stewart GR. δ¹⁵N values of tropical savanna and monsoon forest species reflect root specializations and soil nitrogen status. Oecologia, 2003, 134(4): 569-577.

[35] Seidel F, Lopez CML, Guggenberger G, Nobori Y. Impact of low severity fire on soil organic carbon and nitrogen characteristics in Japanese cedar forest, Yamagata Prefecture, Japan. Open J For, 2017, 7: 270-284.

[36] Shearer G, Kohl DH. Natural ¹⁵N abundance of NH₄ ⁺, amide N, and total N in various fractions of nodules of peas, soybeans and lupins. Funct Plant Biol, 1989, 16(4): 305-313.

[37] Singh A. Nitrogen and phosphorus resorption efficiency in some, native tropical trees planted on a mine spoil in Singrauli Coalfields, India. Int J Environ Bioenergy, 2014, 9(3): 161-170.

[38] Singh A. Nitrogen and phosphorus resorption efficiency in some leguminous and non-leguminous tropical tree species planted on coal mine spoil in a tropical dry environment. Ambit J Educ Res Rev, 2015, 1: 1-7.

[39] Sun X, Kang H, Chen HY, Björn B, Samuel BF, Liu C. Biogeographic patterns of nutrient resorption from Quercus variabilis Blume leaves across China. Plant Biol, 2016, 18(3): 505-513.

[40] Tateno R, Takeda H. Nitrogen uptake and nitrogen use efficiency above and below ground along a topographic gradient of soil nitrogen availability. Oecologia, 2010, 163(3): 793-804.

[41] Templer PH, Arthur MA, Lovett GM, Weathers KC. Plant and soil natural abundance ^{δ 15} N: indicators of relative rates of nitrogen cycling in temperate forest ecosystems. Oecologia, 2007, 153(2): 399-406.

[42] Ueda MU, Mizumachi E, Tokuchi N. Foliage nitrogen turnover: differences among nitrogen absorbed at different times by Quercus serrata saplings. Annals of Botany, 2011, 108(1): 169-175.

[43] van Heerwaarden LM, Toet S, Aerts R. Current measures of nutrient resorption efficiency lead to a substantial underestimation of real resorption efficiency: facts and solutions. Oikos, 2003, 101(3): 664-669.

[44] Vergutz L, Manzoni S, Porporato A, Novais RF, Jackson RB. Global resorption efficiencies and concentrations of carbon and nutrients in leaves of terrestrial plants. Ecol Monogr, 2012, 82(2): 205-220.

[45] Vitousek P, Matson PA, Van Cleve K. Nitrogen availability and nitrification during succession: primary, secondary, and old-field seres. Plant Soil, 1989, 115(2): 229-239.

[46] Wang L, Ibrom A, Korhonen JFJ, Frumau KF, Wu J, Pihlatie M, Schjoerring JK. Interactions between leaf nitrogen status and longevity in relation to N cycling in three contrasting European forest canopies. Biogeosciences, 2013, 10: 999-1011.

[47] Wright IJ, Westoby M. Nutrient concentration, resorption and lifespan: leaf traits of Australian sclerophyll species. Funct Ecol, 2003, 17(1): 10-19.

[48] Yasumura Y, Onoda Y, Hikosaka K, Hirose T. Nitrogen resorption from leaves under different growth irradiance in three deciduous woody species. Plant Ecol, 2005, 178(1): 29-37.

[49] Yoneyama T, Muraoka T, Murakami T, Boonkerd N. Natural abundance of ¹⁵N in tropical plants with emphasis on tree legumes. Plant Soil, 1993, 153(2): 295-304.

[50] Yuan Z, Chen HY. Global trends in senesced-leaf nitrogen and phosphorus. Glob Ecol Biogeogr, 2009, 18(5): 532-542.

[51] Yuan ZY, Li LH, Han XG, Huang JH, Jiang GM, Wan SQ, Zhang WH, Chen QS. Nitrogen resorption from senescing leaves in 28 plant species in a semi-arid region of northern China. J Arid Environ, 2005, 63(1): 191-202.