Skip to main content
Log in

Nitrogen addition has a stronger effect on stoichiometries of non-structural carbohydrates, nitrogen and phosphorus in Bothriochloa ischaemum than elevated CO2

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The nutrient concentrations and carbon:nitrogen:phosphorus stoichiometries of plants have been greatly altered by elevated CO2 concentrations and nitrogen (N) deposition. Studies of these changes, however, are mostly limited to tropical and subtropical forests. In this study, a C4 herbaceous grass (Bothriochloa ischaemum) was grown in a pot experiment at two CO2 concentrations (400 and 800 μmol mol−1) and three levels of N fertilization (0, 2.5 and 5 g N m−2 y−1) in a full factorial design. Plant biomass and the concentrations of non-structural carbohydrates (NSCs), N and phosphorus (P) in the shoots and roots were determined. The elevated CO2 concentration and N addition significantly increased total biomass, starch and NSC concentrations and root:shoot, starch:N, NSC:N, starch:P and NSC:P ratios in whole plants and roots. N addition alone decreased the soluble sugar (SS) concentration in whole plants and increased N concentration and decreased P concentration in whole plants and roots and thus decreased the SS:N ratio and increased the SS:P and N:P ratios. Our results suggested that SS, N and P concentrations and their stoichiometries responded more strongly to N addition than elevated CO2 concentration. Plant growth in this region suffers more from P than N limitation, and N addition would exacerbate the P limitation on plant growth.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alderman PD, Boote KJ, Sollenberger LE, Coleman S (2011) Carbohydrate and nitrogen reserves relative to regrowth dynamics of ‘Tifton 8’ bermudagrass as affected by nitrogen fertilization. Crop Sci 51:1727–1738

    Article  Google Scholar 

  • An Z, Niu DC, Wen HY, Yang Y, Zhang HR, Fu H (2011) Effects of N addition on nutrient resorption efficiency and C:N:P stoichiometric characteristics in Stipa bungeana of steppe grasslands in the Loess Plateau, China. Chin J Plant Ecol 38:801–807

    Article  Google Scholar 

  • Bao SD (2000) Soil and agricultural chemistry analysis, 3rd edn. China Agriculture Press, Beijing, pp 268–270

    Google Scholar 

  • Chen BB, Zou DH, Ma JH (2016) Interactive effects of elevated CO2 and nitrogen-phosphorus supply in the physiological properties of Pyropia haitanensis (Bangiales, Rhodophyta). J Appl Phycol 28:1235–1243

    Article  CAS  Google Scholar 

  • de Souza AP, Arundale RA, Dohleman FG, Long SP, Buckeridge MS (2013) Will the exceptional productivity of Miscanthus x giganteus increase further under rising atmospheric CO2? Agric Forest Meteorol 171–172: 82–92

    Article  Google Scholar 

  • Deng Q, Cheng XL, Zhou GY, Liu JX, Liu SZ, Zhang QF, Zhang DQ (2013) Seasonal responses of soil respiration to elevated CO2 and N addition in young subtropical forest ecosystems in southern China. Ecol Eng 61:65–73

    Article  Google Scholar 

  • Deng Q, Hui DF, Luo YQ, Elser J, Wang YP, Loladze I, Zhang QF, Dennis S (2015) Down-regulation of tissue N:P ratios in terrestrial plants to elevated CO2. Ecology 96:3354–3362

    Article  PubMed  Google Scholar 

  • Dong JL, Li X, Duan ZQ (2016) Biomass allocation and organs growth of cucumber (Cucumis sativus L.) under elevated CO2 and different N supply. Arch Agron Soil Sci 62:277–288

    Article  CAS  Google Scholar 

  • Farrer EC, Herman DJ, Franzova E, Pham T, Suding KN (2013) Nitrogen deposition, plant carbon allocation, and soil microbes: changing interactions due to enrichment. Am J Bot 100:1458–1470

    Article  CAS  PubMed  Google Scholar 

  • Fujita Y, Robroek BJM, de Ruiter PC, Heil GW, Wassen MJ (2010) Increased N affects P uptake of eight grassland species: the role of root surface phosphatase activity. Oikos 119:1665–1673

    Article  CAS  Google Scholar 

  • Galloway JN, Dentener FJ, Capone DG, Boyer EW, Howarth RW, Seitzinger SP, Asner GP, Cleveland CC, Green PA, Holland EA, Karl DM, Michaels AF, Porter JH, Townsend AR, Vöosmarty CJ (2004) Nitrogen cycles: past, present, and future. Biogeochemistry 70:153–226

    Article  CAS  Google Scholar 

  • Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–892

    Article  CAS  PubMed  Google Scholar 

  • Gruber N, Galloway JN (2008) An earth-system perspective of the global nitrogen cycle. Nature 451:293–296

    Article  CAS  PubMed  Google Scholar 

  • Guo ZW, Hu JJ, Yang QP, Li YC, Chen SL, Chen WJ (2015) Influence of mulching management on the relationships between foliar non-structural carbohydrates and N, P concentrations in Phyllostachys violascens stand. Chinese. J Appl Ecol 26:1064–1070

    CAS  Google Scholar 

  • Han WX, Fang JY, Reich PB, Woodward FI, Wang ZH (2011) Biogeography and variability of eleven mineral elements in plant leaves across gradients of climate, soil and plant functional type in China. Ecol Lett 14:788–796

    Article  CAS  PubMed  Google Scholar 

  • Han XW, Tsunekawa A, Tsubo M, Shao HB (2013) Responses of plant-soil properties to increasing N deposition and implications for large-scale eco-restoration in the semiarid grassland of the northern Loess Plateau, China. Ecol Eng 60:1–9

    Article  Google Scholar 

  • Hartmann H, Trumbore S (2016) Understanding the roles of nonstructural carbohydrates in forest trees-from what we can measure to what we want to know. New Phytol 211:386–403

    Article  CAS  PubMed  Google Scholar 

  • Heimann M, Reichstein M (2008) Terrestrial ecosystem carbon dynamics and climate feedbacks. Nature 451:289–292

    Article  CAS  PubMed  Google Scholar 

  • Huang WJ, Zhou GY, Liu JX, Zhang DQ, Xu ZH, Liu SZ (2012) Effects of elevated carbon dioxide and nitrogen addition on foliar stoichiometry of nitrogen and phosphorus of five tree species in subtropical model forest ecosystems. Environ Pollut 168:113–120

    Article  CAS  PubMed  Google Scholar 

  • Huang WJ, Zhou GY, Liu JX, Duan HL, Liu XZ, Fang X, Zhang DQ (2014) Shifts in soil phosphorus fractions under elevated CO2 and N addition in model forest ecosystems in subtropical China. Plant Ecol 215:1373–1384

    Article  Google Scholar 

  • Huang WJ, Houlton BZ, Marklein AR, Liu JX, Zhou GY (2015a) Plant stoichiometric responses to elevated CO2 vary with nitrogen and phosphorus inputs: evidence from a global-scale meta-analysis. Sci Rep 5:18225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang WJ, Zhou GY, Deng XF, Liu JX, Duan HL, Zhang DQ, Chu GW, Liu SZ (2015b) Nitrogen and phosphorus productivities of five subtropical tree species in response to elevated CO2 and N addition. Eur J Forest Res 134:845–856

    Article  CAS  Google Scholar 

  • Huang WJ, Zhou GY, Liu JX, Zhang DQ, Liu SZ, Chu GW, Fang X (2015c) Mineral elements of subtropical tree seedlings in response to elevated carbon dioxide and nitrogen addition. PLoS ONE 10:e0120190

    Article  PubMed  PubMed Central  Google Scholar 

  • Ibrahim MH, Jaafar HZE, Rahmat A, Rahman ZA (2011) The relationship between phenolics and flavonoids production with total non structural carbohydrate and photosynthetic rate in Labisia pumila Benth. under high CO2 and nitrogen fertilization. Molecules 16:162–174

    Article  CAS  Google Scholar 

  • Jiao F, Wen ZM, An SS, Yuan Z (2013) Successional changes in soil stoichiometry after land abandonment in Loess Plateau, China. Ecol Eng 58:249–254

    Article  Google Scholar 

  • Kakani VG, Vu JCV, Allen LH Jr, Boote KJ (2011) Leaf photosynthesis and carbohydrates of CO2 enriched maize and grain sorghum exposed to a short period of soil water deficit during vegetative development. J Plant Physiol 168:2169–2176

    Article  CAS  PubMed  Google Scholar 

  • Latt CR, Nair PKR, Kang BT (2001) Reserve carbohydrate levels in the boles and structural roots of five multipurpose tree species in a seasonally dry tropical climate. For Ecol Manag 146:145–158

    Article  Google Scholar 

  • Lee M, Manning P, Rist J (2010) A global comparison of grassland biomass responses to CO2 and nitrogen enrichment. Philos Trans R Soc B 365:2047–2056

    Article  CAS  Google Scholar 

  • Lee SH, Kim SH, Ding WX, Kang H (2015) Impact of elevated CO2 and N addition on bacteria, fungi, and archaea in a marsh ecosystem with various types of plants. Appl Microbiol Biotechnol 99:5295–5305

    Article  CAS  PubMed  Google Scholar 

  • Li MH, Xiao WF, Shi PL, Wang SG, Zhong YD, Liu XL, Wang XD, Cai XH, Shi ZM (2008a) Nitrogen and carbon source-sink relationships in trees at the Himalayan treelines compared with lower elevations. Plant Cell Environ 31:1377–1387

    Article  CAS  PubMed  Google Scholar 

  • Li MH, Xiao WF, Wang SG, Cheng GW, Cherubini P, Cai XH, Liu XL, Wang XD, Zhu WZ (2008b) Mobile carbohydrates in Himalayan treeline trees. I. Evidence for carbon gain limitation but not for growth limitation. Tree Physiol 28:1287–1296

    Article  CAS  PubMed  Google Scholar 

  • Liu JX, Zhang DQ, Zhou GY, Duang HL (2012) Changes in leaf nutrient traits and photosynthesis of four tree species: effects of elevated CO2, N fertilization and canopy positions. J Plant Ecol 5:376–390

    Article  Google Scholar 

  • Liu JX, Huang WJ, Zhou GY, Zhang DQ, Liu SZ, Li YY (2013a) Nitrogen to phosphorus ratios of tree species in response to elevated carbon dioxide and nitrogen addition in subtropical forests. Global Change Biol 19:208–216

    Article  Google Scholar 

  • Liu ZP, Shao MA, Wang YQ (2013b) Spatial patterns of soil total nitrogen and soil total phosphorus across the entire loess plateau region of China. Geoderma 197–198:67–78

    Article  Google Scholar 

  • Liu JX, Fang X, Deng Q, Han TF, Huang WJ, Li YY (2015) CO2 enrichment and N addition increase nutrient loss from decomposing leaf litter in subtropical model forest ecosystems. Sci Rep 5:7952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu J, Wu NN, Wang H, Sun JF, Peng B, Jiang P, Bai E (2016) Nitrogen addition affects chemical compositions of plant tissues, litter and soil organic matter. Ecology 97:1796–1806

    Article  PubMed  Google Scholar 

  • Loladze I (2002) Rising atmospheric CO2 and human nutrition: toward globally imbalanced plant stoichiometry? Trends Ecol Evol 17:457–461

    Article  Google Scholar 

  • Luo YQ, Su B, Currie WS, Dukes JS, Finzi A, Hartwig U, Hungate B, McMurtrie RE, Oren R, Parton WJ, Pataki DE, Shaw RM, Zak DR, Field CB (2004) Progressive nitrogen limitation of ecosystem responses to rising atmospheric carbon dioxide. Bioscience 54:731–739

    Article  Google Scholar 

  • Marklein AR, Houlton BZ (2012) Nitrogen inputs accelerate phosphorus cycling rates across a wide variety of terrestrial ecosystems. New Phytol 193:696–704

    Article  CAS  PubMed  Google Scholar 

  • Newingham BA, Vanier CH, Charlet TN, Ogle K, Smith SD, Nowak RS (2013) No cumulative effect of 10 years of elevated CO2 on perennial plant biomass components in the Mojave Desert. Glob Change Biol 19:2168–2181

    Article  Google Scholar 

  • NOAA (2013) http://www.esrl.noaa.gov/gmd/ccgg/trends/

  • Novotny AM, Schade JD, Hobbie SE, Kay AD, Kyle AD, Reich PB, Elser JJ (2007) Stoichiometric response of nitrogen-fixing and non-fixing dicots to manipulations of CO2, nitrogen, and diversity. Oecologia 151:687–696

    Article  PubMed  Google Scholar 

  • Novriyanti E, Watanabe M, Kitao M, Utsugi H, Uemura A, Koike T (2012) High nitrogen and elevated CO2 effects on the growth, defense and photosynthetic performance of two eucalypt species. Environ Pollut 170:124–130

    Article  CAS  PubMed  Google Scholar 

  • Pelletier S, Tremblay GF, Lafreniere C, Bertrand A, Belanger G, Castonguay Y, Rowsell J (2009) Nonstructural carbohydrate concentrations in timothy as affected by N fertilization, stage of development, and time of cutting. Agron J 101:1372–1380

    Article  CAS  Google Scholar 

  • Phoenix GK, Booth RE, Leake JR, Read DJ, Grime JP, Lee JA (2004) Simulated pollutant nitrogen deposition increases P demand and enhances root-surface phosphatase activities of three plant functional types in a calcareous grassland. New Phytol 161:279–289

    Article  CAS  Google Scholar 

  • Quentin AG, Pinkard EA, Ryan MG, Tissue DT, Baggett LS, Adams HD, Maillard P, Marchand J, Landhäusser SM, Lacointe A, Gibon Y, Anderegg WR, Asao S, Atkin OK, Bonhomme M, Claye C, Chow PS, Clément-Vidal A, Davies NW, Dickman LT, Dumbur R, Ellsworth DS, Falk K, Galiano L, Grünzweig JM, Hartmann H, Hoch G, Hood S, Jones JE, Koike T, Kuhlmann I, Lloret F, Maestro M, Mansfield SD, Martínez-Vilalta J, Maucourt M, McDowell NG, Moing A, Muller B, Nebauer SG, Niinemets Ü, Palacio S, Piper F, Raveh E, Richter A, Rolland G, Rosas T, Saint Joanis B, Sala A, Smith RA, Sterck F, Stinziano JR, Tobias M, Unda F, Watanabe M, Way DA, Weerasinghe LK, Wild B, Wiley E, Woodruff DR (2015) Non-structural carbohydrates in woody plants compared among laboratories. Tree Physiol 35:1146–1165

    CAS  PubMed  Google Scholar 

  • Reich PB, Hobbie SE, Lee T, Ellsworth DS, West JB, Tilman D, Knops JM, Naeem S, Trost J (2006) Nitrogen limitation constrains sustainability of ecosystem response to CO2. Nature 440:922–925

    Article  CAS  PubMed  Google Scholar 

  • Sardans J, Rivas-Ubach A, Penuelas J (2012) The C:N:P stoichiometry of organisms and ecosystems in a changing word: a review and perspectives. Perspect Plant Ecol 14:33–47

    Article  Google Scholar 

  • Sillen WMA, Dieleman WIJ (2012) Effects of elevated CO2 and N fertilization on plant and soil carbon pools of managed grasslands: a meta-analysis. Biogeosciences 9:2247–2258

    Article  CAS  Google Scholar 

  • Song XZ, Peng CH, Zhou GM, Gu HH, Li Q, Zhang C (2016) Dynamic allocation and transfer of non-structural carbohydrates, a possible mechanism for the explosive growth of Moso bamboo (Phyllostachys heterocycla). Sci Rep 6:25908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stiling P, Cornelissen T (2007) How does elevated carbon dioxide (CO2) affect plant–herbivore interactions? A field experiment and meta-analysis of CO2-mediated changes on plant chemistry and herbivore performance. Glob Change Biol 13:1823–1842

    Article  Google Scholar 

  • Sullivan PF, Ellison SBZ, McNown RW, Brownlee AH, Sveinbjörnsson B (2015) Evidence of soil nutrient availability as the proximate constraint on growth of treeline tress in northwest Alaska. Ecology 96:716–727

    Article  PubMed  Google Scholar 

  • Wei Y, Tong YA, Qiao L, Liu XJ, Duan M, Li J (2010) Preliminary estimate of the atmospheric nitrogen deposition in different ecological regions of Shaanxi province. J Agro-Environ Sci 29:795–800

    CAS  Google Scholar 

  • Xiao L, Liu GB, Xue S (2016) Elevated CO2 concentration and drought stress exert opposite effects on plant biomass, nitrogen, and phosphorus allocation in Bothriochloa ischaemum. J Plant Growth Regul 35:1088–1097

    Article  CAS  Google Scholar 

  • Xu BC, Gao ZJ, Wang J, Xu WZ, Palta JA, Chen YL (2016) N:P ratio of the grass Bothriochloa ischaemum mixed with the legume Lespedeza davurica under varying water and fertilizer supplies. Plant Soil 1–2:67–79

    Article  Google Scholar 

  • Yang YH, Luo YQ, Lu M, Schädel C, Han WJ (2011) Terrestrial C:N stoichiometry in response to elevated CO2 and N addition: a synthesis of two meta-analyses. Plant Soil 343:393–400

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin JJ, Guo DL, He SY, Zhang L (2009) Non-structural carbohydrate, N, and P allocation patterns of two temperate tree species in a semi-arid region of Inner Mongolia. Acta Sci Nat Univ Pekin 45: 519–527

    CAS  Google Scholar 

  • Zhang YB, Duan BL, Qiao YZ, Wang KK, Korpelainen H, Li CY (2008) Leaf photosynthesis of Betula albosinensis seedlings as affected by elevated CO2 and planting density. For Ecol Manag 255:1937–1944

    Article  Google Scholar 

  • Zhang L, Yang YX, Zhan XY, Zhang CJ, Zhou SX, Wu DX (2010) Responses of a dominant temperate grassland plant (Leymus chinensis) to elevated carbon dioxide and nitrogen addition in China. J Environ Qual 39:251–259

    Article  PubMed  Google Scholar 

  • Zhang L, Wu DX, Shi HQ, Zhang CJ, Zhan XY, Zhou SX (2011) Effects of elevated CO2 and N addition on growth and N2 fixation of a legume subshrub (Caragana microphylla Lam.) in temperate grassland in China. PLoS ONE 6:e26842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang T, Cao Y, Chen YM, Liu GB (2015) Non-structural carbohydrate dynamics in Robinia pseudoacacia saplings under three levels of continuous drought stress. Trees 29:1837–1849

    Article  CAS  Google Scholar 

  • Zhu CW, Xu X, Wang D, Zhu JG, Liu G, Seneweera S (2016) Elevated atmospheric CO2 stimulates sugar accumulation and cellulose degradation rates of rice straw. GCB Bioenergy 8:579–587

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was funded by the Western Young Scholars of the Chinese Academy of Sciences (XAB2015A05), and the National Natural Science Foundation of China (41371510, 41371508, 41471438, and 41330858).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sha Xue.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xiao, L., Liu, G., Li, P. et al. Nitrogen addition has a stronger effect on stoichiometries of non-structural carbohydrates, nitrogen and phosphorus in Bothriochloa ischaemum than elevated CO2 . Plant Growth Regul 83, 325–334 (2017). https://doi.org/10.1007/s10725-017-0298-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-017-0298-8

Keywords

Navigation