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Populus deltoides females are more selective in nitrogen assimilation than males under different nitrogen forms supply

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Female cuttings of Populus deltoides were sensitive to inorganic nitrogen forms and biased for NO − 3 –N, whereas males exhibited no obvious preference for nitrogen form in nitrogen fertilizations.

Abstract

We investigated the effects of different inorganic nitrogen forms (NO3 −–N and NH4 +–N) on the morphology, physiology, and carbohydrate accumulation of male and female Populus deltoides. Results showed that both NO3 −–N and NH4 +–N supply forms significantly increased plant growth, C and N contents of all plant organs, chlorophyll pigment contents, net photosynthesis rates (P n), and instantaneous photosynthetic N-use efficiencies (PNUE) in the leaves of both male and female P. deltoides. Females exhibited high total plant dry mass accumulation, P n, PNUE, and N contents in leaves but lower non-structure carbohydrate accumulation than males under nitrate treatment. However, males showed significantly higher P n, PNUE, and 15NH4 + in the leaves, free amino acid content, and nitrate reductase (NR) activities than females under each nitrogen form supply treatment. These results suggested that male and female P. deltoides used different adaptive strategies in dry mass accumulation, allocation, and exhibited different interactions between nitrogen and carbon metabolism. Males exhibited higher nitrogen assimilation ability and N-use efficiency than females under nitrogen fertilizations, whereas females showed more sensitivity to inorganic nitrogen forms of treatments and distinct preference for NO3 −–N. Male P. deltoides showed no obvious bias to the two different N forms. Therefore, the different preferences of male and female P. deltoides of N supplied forms can serve as an important strategy for minimizing intraspecific competition between the two genders.

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References

  • Allen GA, Antos JA (1988) Relative reproductive effort in males and females of the dioecious shrub Oemleria cerasiformis. Oecologia 76:111–118. doi:10.1007/BF00379608

    Article  Google Scholar 

  • Andrews M (1986) The partitioning of nitrate assimilation between root and shoot of higher plants. Plant Cell Environ 9:511–519. doi:10.1111/1365-3040

    CAS  Google Scholar 

  • Arnozis PA, Findenegg GR (1986) Electrical charge balance in the xylem sap of beet and sorghum plants grown with either NO3 or NH4 nitrogen. J Plant Physiol 125:441–449

    Article  CAS  Google Scholar 

  • Barrett SCH, Hough J (2012) Sexual dimorphism in flowering plants. J Exp Bot 64:67–82. doi:10.1093/jxb/ers308

    Article  PubMed  Google Scholar 

  • Bloom AJ, Caldwell RM, Finazzo J, Warner RL, Weissbart J (1989) Oxygen and carbon dioxide fluxes from barley shoots depend on nitrate assimilation. Plant Physiol 91:352–356. doi:10.1104/pp.91.1.352

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Britto DT, Siddiqi MY, Glass ADM, Kronzucker HJ (2001) Futile transmembrane NH4 + cycling: a cellular hypothesis to explain ammonium toxicity in plants. Proc Natl Acad Sci USA 98:4255–4258. doi:10.1073/pnas.061034698

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen L, Han Y, Jiang H, Korpelainen H, Li C (2011) Nitrogen nutrient status induces sexual differences in responses to cadmium in Populus yunnanensis. J Exp Bot 62:5037–5050. doi:10.1093/jxb/err203

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chen J, Duan B, Wang M, Korpelainen H, Li C (2014) Intra- and inter-sexual competition of Populus cathayana under different watering regimes. Funct Ecol 28:124–136. doi:10.1111/1365-2435.12180

    Article  Google Scholar 

  • Choi WJ, Chang SX, Hao X (2005) Soil retention, tree uptake, and tree resorption of 15NH4NO3 and NH 154 NO3 applied to trembling and hybrid aspens at planting. Can J Res 35:823–831. doi:10.1139/x05-011

    Article  CAS  Google Scholar 

  • Claussen W, Lenz F (1999) Effect of ammonium or nitrate nutrition on net photosynthesis, growth, and activity of the enzymes nitrate reductase and glutamine synthetase in blueberry, raspberry and strawberry. Plant Soil 208:95–102. doi:10.1023/A:1004543128899

    Article  CAS  Google Scholar 

  • Coleman MD, Dickson RE (1998) Isebrands JG (1998) Growth and physiology of aspen supplied with different fertilizer addition rates. Physiol Plant 103:513–526. doi:10.1034/j.1399-3054.1998410.x

    Article  CAS  Google Scholar 

  • Cooke JEK, Martin TA, Davis JM (2005) Short-term physiological and developmental responses to nitrogen availability in hybrid poplar. New Phytol 167:41–52. doi:10.1111/j.1469-8137.2005.01435.x

    Article  CAS  PubMed  Google Scholar 

  • Cooper DT (1990) Populus deltoides Bartr. Ex Marsh. var. deltoides Eastern Cottonwood. In: Silvics of North America, Vol. 2, Hardwoods (Burns RM, Honkala BH, Technical coords.), Agriculture Handbook 654, Washington DC: USDA Forest Service, pp 530–535

  • Coplen TB (2008) Explanatory glossary of terms used in expression of relative isotope ratios and gas ratios. IUPAC Provisional Recommendations. Inorganic Chemistry Division. Commission on Isotopic Abundances and Atomic Weights. http://old.iupac.org/reports/provisional/abstract08/coplen_310508.html/

  • Correia I, Nunes A, Duarte IF, Barros A, Delgadillo I (2005) Sorghum fermentation followed by spectroscopic techniques. Food Chem 90:853–859. doi:10.1016/j.foodchem.2004.05.060

    Article  CAS  Google Scholar 

  • Dailey FA, Kuo T, Warner RL (1982) Pyridine nucleotide specificity of barley nitrate reductase. Plant Physiol 69:1196–1199. doi:10.1104/pp.69.5.1196

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Darwin C (1877) The different forms of flowers on plants of the same species. John Murray, Albemarle Street

    Book  Google Scholar 

  • Dawson TE, Bliss LC (1989) Patterns of water use and the tissue water relations in the dioecious shrub, Salix arctica: the physiological basis for habitat partitioning between the sexes. Oecologia 79:332–343. doi:10.1007/BF00384312

    Article  CAS  PubMed  Google Scholar 

  • Dawson TE, Ehleringer JR (1993) Gender-specific physiology, carbon isotope discrimination, and habitat distribution in boxelder, Acer negundo. Ecology 74:798–815

    Article  Google Scholar 

  • Dawson TE, Ward JK, Ehleringer JR (2004) Temporal scaling of physiological responses from gas exchange to tree rings: a gender-specific study of Acer negundo (Boxelder) growing under different conditions. Funct Ecol 18:212–222. doi:10.1111/j.0269-8463.2004.00838.x

    Article  Google Scholar 

  • DesRochers A, Van den Driessche R, Thomas BR (2003) Nitrogen fertilization of trembling aspen seedlings grown on soils of different pH. Can J For Res 33:552–560. doi:10.1139/X02-191

    Article  CAS  Google Scholar 

  • Di HJ, Cameron KC, Sherlock RR (2007) Comparison of the effectiveness of a nitrification inhibitor, dicyandiamide, in reducing nitrous oxide emissions in four different soils under different climatic and management conditions. Soil Use Manag 23:1–9. doi:10.1111/j.1475-2743.2006.00057.x

    Article  Google Scholar 

  • Dluzniewska P, Gessler A, Dietrich H, Schnitzler JP, Teuber M, Rennenberg H (2007) Nitrogen uptake and metabolism in Populus × canescens as affected by salinity. New Phytol 173:279–293. doi:10.1111/j.1469-8137.2006.01908.x

    Article  CAS  PubMed  Google Scholar 

  • Errebhi M, Wilcox GE (1990) Plant species response to ammonium-nitrate concentration ratios. J Plant Nutr 13:1017–1029. doi:10.1080/01904169009364132

    Article  CAS  Google Scholar 

  • Fangmeier A, Hadwiger-Fangmeier A, Van der Eerden L, Jäger HJ (1994) Effects of atmospheric ammonia on vegetation—a review. Environ Pollut 86:43–82. doi:10.1016/0269-7491(94)90008-6

    Article  CAS  PubMed  Google Scholar 

  • Fodor F, Gáspár L, Morales F, Gogorcena Y, Lucena JJ, Cseh E, Kröpfl K, Abadía J, Sárvári É (2005) Effects of two iron sources on iron and cadmium allocation in poplar (Populus alba) plants exposed to cadmium. Tree Physiol 25:1173–1180. doi:10.1093/treephys/25.9.1173

    Article  CAS  PubMed  Google Scholar 

  • Freeman DC, Klikoff LG, Harper KT (1976) Differential resource utilization by the sexes of dioecious plants. Science 193:597–599. doi:10.1126/science.193.4253.597

    Article  CAS  PubMed  Google Scholar 

  • Gambrell RP, Delaune RD, Patrick WH Jr (1991) Redox processes in soils following oxygen depletion. In: Jackson MB, Davies DD, Lambers H (eds) Plant life under oxygen deprivation: ecology, physiology, and biochemistry. SPB Academic Publishing, The Hague, pp 101–117

    Google Scholar 

  • Gerendás J, Zhu Z, Bendixen R, Ratcliffe RG, Sattelmacher B (1997) Physiological and biochemical processes related to ammonium toxicity in higher plants. Z Pflanzenernähr Bodenkund 160:239–251. doi:10.1002/jpln.19971600218

    Article  Google Scholar 

  • Gessler A, Schneider S, Von Sengbusch D, Weber P, Hanemann U, Huber C, Rothe A, Kreutzer K, Rennenberg H (1998) Field and laboratory experiments on net uptake of nitrate and ammonium by the roots of spruce (Picea abies) and beech (Fagus sylvatica) trees. New Phytol 138:275–285. doi:10.1046/j.1469-8137.1998.00107.x

    Article  CAS  Google Scholar 

  • Gojon A, Plassard C, Bussi C (1994) Root/shoot distribution of NO3 − assimilation in herbaceous and woody species. SPB Academic Publishing, The Hague

    Google Scholar 

  • Guo S, Brück H, Sattelmacher B (2002) Effects of supplied nitrogen form on growth and water uptake of French bean (Phaseolus vulgaris L.) plants. Plant Soil 239:267–275. doi:10.1023/A:1015014417018

    Article  CAS  Google Scholar 

  • Guo S, Zhou Y, Shen Q, Zhang F (2007) Effect of ammonium and nitrate nutrition on some physiological processes in higher plants-growth, photosynthesis, photorespiration, and water relations. Plant Biol 9:21–29. doi:10.1055/s-2006-924541

    Article  CAS  PubMed  Google Scholar 

  • Heldt HW (1997) Plant Biochemistry and Molecular Biology. Oxford University Press, Oxford

    Google Scholar 

  • Hidaka A, Kitayama K (2009) Divergent patterns of photosynthetic phosphorus-use efficiency versus nitrogen–use efficiency of tree leaves along nutrient-availability gradients. J Ecol 97:984–991. doi:10.1111/j.1365-2745.01540.x

    Article  CAS  Google Scholar 

  • Holtgrieve GW, Jewett PK, Matson PA (2006) Variations in soil N cycling and trace gas emissions in wet tropical forests. Oecologia 146:584–594. doi:10.1007/s00442-005-0222-1

    Article  PubMed  Google Scholar 

  • Host GE, Rauscher HM, Isebrands JG, Michael DA (1990) Validation of photosynthate production in ECOPHYS, an ecophysiological growth process model of Populus. Tree Physiol 7:283–296. doi:10.1093/treephys/7.1-2-3-4.283

    Article  PubMed  Google Scholar 

  • Huber SC (1983) Relation between photosynthetic starch formation and dry-weight partitioning between the shoot and root. Can J Bot 61:2709–2716. doi:10.1139/b83-298

    Article  Google Scholar 

  • Huber SC, Kaiser KM (1996) Regulation of C/N interactions in higher plants by protein phosphorylation. In: Verma DPS (ed) Signal transduction in plant growth and development. Springer, Wien, New York, pp 87–112

    Google Scholar 

  • Hultine KR, Bush SE, West AG, Ehleringer JR (2007) Population structure, physiology and ecohydrological impacts of dioecious riparian tree species of western North America. Oecologia 154:85–93. doi:10.1007/s00442-007-0813-0

    Article  CAS  PubMed  Google Scholar 

  • Huppe HC, Turpin DH (1994) Integration of carbon and nitrogen metabolism in plant and algal cells. Annu Rev Plant Biol 45:577–607. doi:10.1146/annurev.pp.45.060194.003045

    Article  CAS  Google Scholar 

  • Ibrahim L, Proe MF, Cameron AD (1997) Main effects of nitrogen supply and drought stress upon whole-plant carbon allocation in poplar. Can J Res 27:1413–1419

    Article  Google Scholar 

  • Imsande J, Touraine B (1994) N demand and the regulation of nitrate uptake. Plant Physiol 105:3–7

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kreuzwieser J, Herschbach C, Stulen I, Wiersema P, Vaalburg W, Rennenberg H (1997) Interactions of NH4 + and L-glutamate with NO3 − transport processes of non-mycorrhizal Fagus sylvatica roots. J Exp Bot 48:1431–1438. doi:10.1093/jxb/48.7.1431

    Article  CAS  Google Scholar 

  • Kronzucker HJ, Siddiqi MY, Glass ADM (1997) Conifer root discrimination against soil nitrate and the ecology of forest succession. Nature 385:59–61. doi:10.1038/385059a0

    Article  CAS  Google Scholar 

  • Krupa SV (2003) Effects of atmospheric ammonia (NH3) on terrestrial vegetation: a review. Environ Pollut 24:179–221. doi:10.1016/S0269-7491(02)00434-7

    Article  Google Scholar 

  • Laporte MM, Delph LF (1996) Sex-specific physiology and source-sink relations in the dioecious plant Silene latifolia. Oecologia 106:63–72. doi:10.1007/BF00334408

    Article  Google Scholar 

  • Lee RB, Purves JV, Ratcliffe RG, Saker LR (1992) Nitrogen assimilation and the control of ammonium and nitrate absorption by maize roots. J Exp Bot 43:1385–1396. doi:10.1093/jxb/43.11.1385

    Article  CAS  Google Scholar 

  • Li C, Xu G, Zang R, Korpelainen H, Berninger F (2007) Sex-related differences in leaf morphological and physiological responses in Hippophae rhamnoides along an altitudinal gradient. Tree Physiol 27:399–406. doi:10.1093/treephys/27.3.399

    Article  CAS  PubMed  Google Scholar 

  • Li H, Li M, Luo J, Cao X, Qu L, Gai Y, Jiang X, Liu T, Bai H, Janz D, Polle A, Peng C, Luo ZB (2012) N-fertilization has different effects on the growth, carbon and nitrogen physiology, and wood properties of slow- and fast-growing Populus species. J Exp Bot 63:6173–6185. doi:10.1093/jxb/ers271

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Liu Z, Dickmann DI (1992) Responses of two hybrid Populus clones to flooding, drought, and nitrogen availability. I Morphology and growth. Can J Bot 70:2265–2270. doi:10.1139/b92-281

    Article  Google Scholar 

  • Livingston NJ, Guy RD, Sun ZJ, Ethier GJ (1999) The effects of nitrogen stress on the stable carbon isotope composition, productivity and water use efficiency of white spruce (Picea glauca (Moench) Voss) seedlings. Plant Cell Environ 22:281–289. doi:10.1046/j.1365-3040.1999.00400.x

    Article  Google Scholar 

  • Luo J, Li H, Liu T, Polle A, Peng C, Luo ZB (2013a) Nitrogen metabolism of two contrasting poplar species during acclimation to limiting nitrogen availability. J Exp Bot 64:4207–4224. doi:10.1093/jxb/ert234

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Luo J, Qin J, He F, Li H, Liu T, Polle A, Peng C, Luo ZB (2013b) Net fluxes of ammonium and nitrate in association with H+ fluxes in fine roots of Populus popularis. Planta 237:919–931. doi:10.1007/s00425-012-7-1807-7

    Article  CAS  PubMed  Google Scholar 

  • Marschner H (1995) Mineral nutrition of higher plants, 2nd edn. Academic Press, London

    Google Scholar 

  • McGarvey RC, Martin TA, White TL (2004) Integrating within-crown variation in net photosynthesis in loblolly and slash pine families. Tree Physiol 24:1209–1220. doi:10.1093/treephys/24.11.1209

    Article  PubMed  Google Scholar 

  • Min X, Siddiqi MY, Guy RD, Glass ADM, Kronzucker HJ (1998) Induction of nitrate uptake and nitrate reductase activity in trembling aspen and lodgepole pine. Plant Cell Environ 21:1039–1046. doi:10.1046/j.1365-3040.1998.00340.x

    Article  CAS  Google Scholar 

  • Mitchell AK (1998) Acclimation of Pacific yew (Taxus brevifolia) foliage to sun and shade. Tree Physiol 18:749–757. doi:10.1093/treephys/18.11.749

    Article  PubMed  Google Scholar 

  • Monaghan RM, Smith LC, Ledgard SF (2009) The effectiveness of a granular formulation of dicyandiamide (DCD) in limiting nitrate leaching from a grazed dairy pasture. New Zeal J Agr Res 52:145–159. doi:10.1080/00288230909510499

    Article  CAS  Google Scholar 

  • Montesinos D, Villar-Salvador P, García-Fayos P, Verdú M (2012) Genders in Juniperus thurifera have different functional responses to variations in nutrient availability. New Phytol 193:705–712. doi:10.1111/j.1469-8137.2011.03982.x

    Article  CAS  PubMed  Google Scholar 

  • Munzarova E, Lorenzen B, Brix H, Vojtiskova L, Votrubova O (2006) Effect of NH4 +/NO3 − availability on nitrate reductase activity and nitrogen accumulation in wetland helophytes Phragmites australis and Glyceria maxima. Environ Exp Bot 55:49–60. doi:10.1016/j.envexpbot.2004.09.011

    Article  CAS  Google Scholar 

  • Murata T, Akazawa T, Fukuchi S (1968) Enzymic Mechanism of Starch Breakdown in Germinating Rice Seeds’ I. An Analytical Study. Plant Physiol 43:1899–1905. doi:10.1104/pp.43.12.1899

    Article  CAS  Google Scholar 

  • Nelson DW, Sommers LE (1982) Total carbon, organic carbon, organic matter. In: Dinauer RC (ed) Methods of soil analysis. Part 2, American Society of Agronomy, Inc. and Soil Science Society of America, Inc., Madison, WI, pp 539–579

  • Nunes-Nesi A, Fernie AR, Stitt M (2010) Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Mol Plant 3:973–996. doi:10.1093/mp/ssq049

    Article  CAS  PubMed  Google Scholar 

  • O’Callaghan M, Gerard EM, Carter PE, Lardner R, Sarathchandra U, Burch G, Ghani A, Bell N (2010) Effect of the nitrification inhibitor dicyandiamide (DCD) on microbial communities in a pasture soil amended with bovine urine. Soil Biol Biochem 42:1425–1436. doi:10.1016/j.soilbio.2010.05.003

    Article  Google Scholar 

  • Paul MJ, Driscoll SP (1997) Sugar repression of photosynthesis: the role of carbohydrates in signalling nitrogen deficiency through source: sink imbalance. Plant Cell Environ 20:110–116. doi:10.1046/j.1365-3040.1997.d01-17.x

    Article  CAS  Google Scholar 

  • Paul MJ, Stitt M (1993) Effects of nitrogen and phosphorus deficiencies on levels of carbohydrates, respiratory enzymes and metabolites in seedlings of tobacco and their response to exogenous sucrose. Plant Cell Environ 16:1047–1057. doi:10.1111/j.1365-3040.1996.tb02062.x

    Article  CAS  Google Scholar 

  • Porra RJ, Thompson WA, Kriedemann PE (1989) Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. BBA Bioenerg 975:384–394. doi:10.1016/S0005-2728(89)80347-0

    Article  CAS  Google Scholar 

  • Raab TK, Terry N (1995) Carbon, nitrogen, and nutrient interactions in Beta vulgaris L. as influenced by nitrogen source, NO3 − versus NH4 +. Plant Physiol 107:575–585. doi:10.1104/pp.107.2.575

    CAS  PubMed Central  PubMed  Google Scholar 

  • Raven JA (1985) Tansley review No. 2. New Phytol 101:25–77

    Article  CAS  Google Scholar 

  • Rennenberg H, Wildhagen H, Ehlting B (2010) Nitrogen nutrition of poplar trees. Plant Biol 12:275–291. doi:10.1111/j.1438-8677.2009.00309.x

    Article  CAS  PubMed  Google Scholar 

  • Renner SS, Ricklefs RE (1995) Dioecy and its correlates in the flowering plants. Am J Bot 82:596–606

    Article  Google Scholar 

  • Rowland DL, Johnson NC (2001) Sexual demographics of riparian populations of Populus deltoides: can mortality be predicted from a change in reproductive status? Can J Bot 79:702–710. doi:10.1139/b01-049

    Google Scholar 

  • Rufty TW, Huber SC, Volk RJ (1988) Alterations in leaf carbohydrate metabolism in response to nitrogen stress. Plant Physiol 88:725–730. doi:10.1104/pp.88.3.725

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Salsac L, Chaillou S, Morot Gaudry JF, Lesaint C, Jolivet E (1987) Nitrate and ammonium nutrition in plants [organic anion, ion accumulation, osmolarity]. Plant Physiol Biochem 25:805–812

    Google Scholar 

  • Scheible WR, Lauerer M, Schulze ED, Caboche M, Stitt M (1997) Accumulation of nitrate in the shoot acts as a signal to regulate shoot-root allocation in tobacco. Plant J 11:671–691. doi:10.1046/j.1365-313X.1997.11040671.x

    Article  CAS  Google Scholar 

  • Serna MD, Borras R, Legaz F, Primo-Millo E (1992) The influence of nitrogen concentration and ammonium/nitrate ratio on N-uptake, mineral composition and yield of citrus. Plant Soil 147:13–23. doi:10.1007/BF00009366

    Article  CAS  Google Scholar 

  • Shelp BJ (1987) The composition of phloem exudate and xylem sap from broccoli (Brassica oleracea var. italica) supplied with NH4 +, NO3 − or NH4NO3. J Exp Bot 38:1619–1636. doi:10.1093/jxb/38.10.1619

    Article  CAS  Google Scholar 

  • Strojny Z (1999) Effect of nutrient solution concentration and NH4: NO3 ratio on Maranta growth. Sci Hortic 80:105–112. doi:10.1016/S0304-4238(98)00225-8

    Article  CAS  Google Scholar 

  • Vitousek PM, Gosz JR, Grier CC, Melillo JM, Reiners WA, Todd RL (1979) Nitrate losses from disturbed ecosystems. Science 204:469–474. doi:10.1126/science.204.4392.469

    Article  CAS  PubMed  Google Scholar 

  • Walch-Liu P, Neumann G, Bangerth F, Engels C (2000) Rapid effects of nitrogen form on leaf morphogenesis in tobacco. J Exp Bot 51:227–237. doi:10.1093/jexbot/51.343.227

    Article  CAS  PubMed  Google Scholar 

  • Wang X, Curtis PS (2001) Gender-specific responses of Populus tremuloides to atmospheric CO2 enrichment. New Phytol 150:675–684. doi:10.1046/j.1469-8137.2001.00138.x

    Article  CAS  Google Scholar 

  • Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, Bongers F, Cavender-Bares J, Chapin T, Cornelissen JHC, Diemer M, Flexas J, Garnier E, Groom PK, Gulias J, Hikosaka K, Lamont BB, Lee T, Lee W, Lusk C, Midgley JJ, Navas M, Niinemets Ü, Oleksyn J, Osada N, Poorter H, Poot P, Prior L, Pyankov VI, Roumet C, Thomas SC, Tjoelker MG, Veneklaas EJ, Villar R (2004) The worldwide leaf economics spectrum. Nature 428:821–827. doi:10.1038/nature02403

    Article  CAS  PubMed  Google Scholar 

  • Xu X, Yang F, Xiao X, Zhang S, Korpelainen H, Li C (2008) Sex-specific responses of Populus cathayana to drought and elevated temperatures. Plant Cell Environ 31:850–860. doi:10.1111/j.1365-3040.2008.01799.x

    Article  CAS  PubMed  Google Scholar 

  • Yemm EW, Willis AJ (1954) The estimation of carbohydrates in plant extracts by anthrone. Biochem J 57:508–514

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yousfi S, Serret MD, Marquez AJ, Voltas J, Araus JL (2012) Combined use of δ13C, δ18O and δ15N tracks nitrogen metabolism and genotypic adaptation of durum wheat to salinity and water deficit. New Phytol 194:230–244. doi:10.1111/j.1469-8137.2011.04036.x

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Lu S, Xu X, Korpelainen H, Li C (2009) Changes in antioxidant enzyme activities and isozyme profiles in leaves of male and female Populus cathayana infected with Melampsora larici-populina. Tree Physiol 30:116–128. doi:10.1093/treephys/tpp094

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Jiang H, Peng S, Korpelainen H, Li C (2010) Sex-related differences in morphological, physiological, and ultrastructural responses of Populus cathayana to chilling. J Exp Bot 62:675–686. doi:10.1093/jxb/erq306

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhang S, Jiang H, Zhao H, Korpelainen H, Li C (2014) Sexually different physiological responses of Populus cathayana to nitrogen and phosphorus deficiencies. Tree Physiol 34:343–354. doi:10.1093/treephys/tpu025

    Article  CAS  PubMed  Google Scholar 

  • Zhao H, Li Y, Duan B, Korpelainen H, Li C (2009) Sex-related adaptive responses of Populus cathayana to photoperiod transitions. Plant Cell Environ 32:1401–1411. doi:10.1111/j.1365-3040.2009.02007.x

    Article  CAS  PubMed  Google Scholar 

  • Zhao H, Xu X, Zhang Y, Korpelainen H, Li C (2011) Nitrogen deposition limits photosynthetic response to elevated CO2 differentially in a dioecious species. Oecologia 165:41–54. doi:10.1007/s00442-010-1763-5

    Article  PubMed  Google Scholar 

  • Zhao H, Li Y, Zhang X, Korpelainen H, Li C (2012) Sex-related and stage-dependent source-to-sink transition in Populus cathayana grown at elevated CO2 and elevated temperature. Tree Physiol 32:1325–1338. doi:10.1093/treephys/tps074

    Article  CAS  PubMed  Google Scholar 

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Author contribution statement

Junyu Li, the chief executor of the paper, responsible for data collection, analysis and the thesis writing; Tingfa Dong, the major participant of the paper, responsible for data collection and analysis; Qingxue Guo, the major participant of the paper, responsible for data collection and analysis; Hongxia Zhao, the corresponding author of the paper, responsible for experimental design, planning budget, project organization and the thesis emendation.

Acknowledgments

The research was supported by the National Key Basic Research Program of China (No. 2012CB416901), the National Natural Science Foundation of China (No. 31100289), and Young Talent Team Program of the Institute of Mountain Hazards and Environment (SDSQB-2012-02).

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The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Chengdu Institute of Biology, Chinese Academy of Sciences, 610041, Chengdu, China

    Junyu Li & Tingfa Dong

  2. Key Laboratory of Mountain Surface Processes and Ecological Regulation, Institute of Mountain Hazards and Environment, Chinese Academy of Sciences, 610041, Chengdu, China

    Qingxue Guo & Hongxia Zhao

  3. University of Chinese Academy of Sciences, 100039, Beijing, China

    Junyu Li, Tingfa Dong & Qingxue Guo

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  1. Junyu Li
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Li, J., Dong, T., Guo, Q. et al. Populus deltoides females are more selective in nitrogen assimilation than males under different nitrogen forms supply. Trees 29, 143–159 (2015). https://doi.org/10.1007/s00468-014-1099-6

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  • DOI: https://doi.org/10.1007/s00468-014-1099-6

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