Skip to main content
SpringerLink
Log in

15N-labeled ammonium nitrogen uptake and physiological responses of poplar exposed to PM2.5 particles

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Air pollution caused by particulate matter with aerodynamic diameters less than 2.5 μm (PM2.5) is a serious environmental problem. Plants can improve air quality by removing PM2.5 from the atmosphere. However, direct evidence of PM2.5 absorption and assimilation into plants has not yet been found. In this study, we demonstrate that 15NH4 + in PM2.5 was absorbed by poplar leaves in low and high PM2.5 treatment groups (namely, LPT and HPT). Then, 15N was subsequently transferred to other parts of the treated seedlings as shown by 15N tracing and simulated PM2.5 generation. 15N and total N contents were the highest in high pollution treatment (HPT), followed by that in low pollution treatment (LPT) and the control. Glutamate dehydrogenase (GDH) contributed more to NH4 + assimilation than glutamine synthetase and glutamate synthase in the leaves of treated seedlings. GDH aminating activity was induced upon NH4 + exposure whereas GDH deaminating activity was repressed in both LPT and HPT, suggesting that poplar seedlings can alleviate NH4 + toxicity by enhancing NH4 + assimilation. At the end of PM2.5 treatment period, the decreased amino acid content in the treated seedlings was attributed to the probably altered balance of amino acid metabolism. The decline in the net photosynthetic rate (Pn) was accompanied by the decrease in the stomatal conductance in poplar leaves with the extension of PM2.5 treatment time, indicating that stomatal limitation is a major reason for Pn reduction. This study may provide novel insights into the relationship between PM2.5 pollution and plants.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Bressi M, Sciare J, Ghersi V, Bonnaire N, Nicolas JB, Petit JE, Moukhtar S, Rosso A (2013) A one-year comprehensive chemical characterization of fine aerosol (PM2.5) at urban, suburban and rural background sites in the region of Paris (France). Atmos Chem Phys 13:7825–7844. doi:10.5194/acp-13-7825-2013

    Article  Google Scholar 

  • Brook RD, Rajagopalan S, Pope CA III, Brook JR, Bhatnagar A, Diez-Roux AV, Holguin F, Hong YL, Luepker RV, Mittleman MA, Peters A, Siscovick D, Smith SC, Whitsel L, Kaufman JD (2010) Particulate matter air pollution and cardiovascular disease: an update to the scientific statement from the American Heart Association. Circulation 121:2331–2378. doi:10.1161/CIR.0b013e3181dbece1

    Article  CAS  Google Scholar 

  • Chan CK, Yao XH (2008) Air pollution in mega cities in China. Atmos Environ 42:1–42. doi:10.1016/j.atmosenv.2007.09.003

    Article  CAS  Google Scholar 

  • Dawar K, Zaman M, Rowarth JS, Turnbull MH (2012) Applying urea with urease inhibitor (N-(n-butyl) thiophosphoric triamide) in fine particle application improves nitrogen uptake in ryegrass (Lolium perenne L.). Soil Sci Plant Nutr 58:309–318. doi:10.1080/00380768.2012.680050

    Article  CAS  Google Scholar 

  • Dumont J, Keski-Saari S, Keinänen M, Cohen D, Ningre N, Kontunen-Soppela S, Baldet P, Gibon Y, Dizengremel P, Vaultier MN, Jolivet Y, Oksanen E, Thiec DL (2014) Ozone affects ascorbate and glutathione biosynthesis as well as amino acid contents in three Euramerican poplar genotypes. Tree Physiol 34:253–266. doi:10.1093/treephys/tpu004

    Article  CAS  Google Scholar 

  • Escobar MA, Geisler DA, Rasmusson AG (2006) Reorganization of the alternative pathways of the Arabidopsis respiratory chain by nitrogen supply: opposing effects of ammonium and nitrate. Plant J 45:775–788. doi:10.1111/j.1365-313X.2005.02640.x

    Article  CAS  Google Scholar 

  • 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. doi:10.1007/BF02374940

    Article  CAS  Google Scholar 

  • Guo HJ, Sun YC, LI YF, Tong B, Harris M, Zhu-Salzman K, Ge F (2013) Pea aphid promotes amino acid metabolism both in Medicago truncatula and bacteriocytes to favor aphid population growth under elevated CO2. Glob Chang Biol 19:3210–3223. doi:10.1111/gcb.12260

  • Harper CJ, Hayward D, Kidd M, Wiid I, Helden PV (2010) Glutamate dehydrogenase and glutamine synthetase are regulated in response to nitrogen availability in Myocbacterium smegmatis. BMC Microbiol 10:138–149. doi:10.1186/1471-2180-10-138

    Article  Google Scholar 

  • Herzog H, Götz K-P (2004) Influence of water deficit on uptake and distribution of nitrogen in soybeans monitored by soil injected 15N. J Agron Crop Sci 190:161–167. doi:10.1111/j.1439-037X.2004.00085.x

    Article  CAS  Google Scholar 

  • Iriti M, Maro AD, Bernasconi S, Burlini N, Simonetti P, Picchi V, Panigada C, Gerosa G, Parente A, Faoro F (2009) Nutritional traits of bean (Phaseolus vulgaris) seeds from plants chronically exposed to ozone pollution. J Agric Food Chem 57:201–208. doi:10.1021/jf802819m

    Article  CAS  Google Scholar 

  • Kampa M, Castanas E (2008) Human health effects of air pollution. Environ Pollut 151:362–367. doi:10.1016/j.envpol.2007.06.012

    Article  CAS  Google Scholar 

  • Lai SC, Zou SC, Cao JJ, Lee SC, Ho KF (2007) Characterizing ionic species in PM2.5 and PM10 in four Pearl River Delta cities, South China. J Environ Sci 19:939–947. doi:10.1016/S1001-0742(07)60155-7

    Article  CAS  Google Scholar 

  • Larsen T, Taylor DL, Leigh MB, O’Brien DM (2009) Stable isotope fingerprinting: a novel method for identifying plant, fungal, or bacterial origins of amino acids. Ecology 90:3526–3535. doi:10.1890/08-1695.1

    Article  Google Scholar 

  • Lea PJ, Miflin BJ (2011) Nitrogen assimilation and its relevance to crop improvement. In: Foyer CH, Zhang H (eds) Nitrogen metabolism in plants in the post-genomic era. Wiley-Blackwell, Chichester, pp. 1–40

    Google Scholar 

  • Mai HJ, Jiang JK, He ZX, Hao JM (2013) Design and evaluation of an aerosol nanoparticle generation system. Environ Sci 34:26–30. doi:10.13227/j.hjkx.2013.08.019

    Google Scholar 

  • Malm WC, Hand JL (2007) An examination of the physical and optical properties of aerosols collected in the IMPROVE program. Atmos Environ 41:3407–3427. doi:10.1016/j.atmosenv.2006.12.012

    Article  CAS  Google Scholar 

  • McDonald A, Bealey W, Fowler D, Dragosits U, Skiba U, Smith R, Donovan R, Brett H, Hewitt C, Nemitz E (2007) Quantifying the effect of urban tree planting on concentrations and depositions of PM10 in two UK conurbations. Atmos Environ 41:8455–8467. doi:10.1016/j.atmosenv.2007.07.025

    Article  CAS  Google Scholar 

  • Mishra AK, Rai R, Agrawal SB (2013) Differential response of dwarf and tall tropical wheat cultivars to elevated ozone with and without carbon dioxide enrichment: growth, yield and grain quality. Field Crop Res 145:21–32. doi:10.1016/j.fcr.2013.02.007

    Article  Google Scholar 

  • Nawahda A, Yamashita K, Ohara T, Kurokawa J, Yamaji K (2012) Evaluation of premature mortality caused by exposure to PM2.5 and ozone in East Asia: 2000, 2005, 2020. Water Air Soil Pollut 223:3445–3459. doi:10.1007/s11270-012-1123-7

    Article  CAS  Google Scholar 

  • Nelson DL, Cox MM (2004) Biosynthesis of amino acids, nucleotides, and related molecules. In: Nelson DL, Cox MM (eds) Lehninger principles of biochemistry, 4th edn. W.H. Freeman & Company, New York, pp. 833–880

    Google Scholar 

  • Nguyen T, Yu XX, Zhang ZM, Liu MM, Liu XH (2015) Relationship between types of urban forest and PM2.5 capture at three growth stages of leaves. J Environ Sci 27:33–41. doi:10.1016/j.jes.2014.04.019

    Article  Google Scholar 

  • Niu JF, Feng ZZ, Zhang WW, Zhao P, Wang XK (2014) Non-stomatal limitation to photosynthesis in Cinnamomum camphora seedings exposed to elevated O3. PLoS One 9:1–7. doi:10.1371/journal.pone.0098572

    Google Scholar 

  • Noctor G (2006) Metabolic signaling in defence and stress: the central roles of soluble redox couples. Plant Cell Environ 29:409–425. doi:10.1111/j.1365-3040.2005.01476.x

  • Nowak DJ, Hirabayashi S, Bodine A, Hoehn R (2013) Modeled PM2.5 removal by trees in ten U.S. cities and associated health effects. Environ Pollut 178:395–402. doi:10.1016/j.envpol.2013.03.050

    Article  CAS  Google Scholar 

  • Ocskay R, Salma I, Wang W, Maenhaut W (2006) Characterization and diurnal variation of size-resolved inorganic water-soluble ions at a rural background site. J Environ Monit 8:300–306. doi:10.1039/B513915E

    Article  CAS  Google Scholar 

  • Pathak RK, Wu WS, Wang T (2009) Summertime PM2.5 ionic species in four major cities of China: nitrate formation in an ammonia-deficient atmosphere. Atmos Chem Phys 9:1711–1722. doi:10.5194/acp-9-1711-2009

    Article  CAS  Google Scholar 

  • PRC MEP (2012) Ministry of Environmental Protection of the People’s Republic of China (PRC MEP). Ambient Air Quality Standard:GB3095–GB2012

  • Rubio-Wilhelmi MDM, Sanchez-Rodrigueza E, Rosalesa MA, Blascoa B, Riosa JJ, Romeroa L, Blumwaldb E, Ruiza JM (2012) Ammonium formation and assimilation in PSARK∷IPT tobacco transgenic plants under low N. J Plant Physiol 169:157–162. doi:10.1016/j.jplph.2011.09.011

    Article  CAS  Google Scholar 

  • Sæbø A, Popek R, Nawrot B, Hanslin HM, Gawronska H, Gawronski SW (2012) Plant species differences in particulate matter accumulation on leaf surfaces. Sci Total Environ 427–428:347–354. doi:10.1016/j.scitotenv.2012.03.084

    Article  Google Scholar 

  • Sarasketa A, González-Moro MB, González-Murua C, Marino D (2014) Exploring ammonium tolerance in a large panel of Arabidopsis thaliana natural accessions. J Exp Bot 65:6023–6033. doi:10.1093/jxb/eru342

    Article  CAS  Google Scholar 

  • Song YS, Maher BA, Li F, Wang XK, Sun X, Zhang HX (2015) Particulate matter deposited on leaf of five evergreen species in Beijing, China: source identification and size distribution. Atmos Environ 105:53–60. doi:10.1016/j.atmosenv.2015.01.032

    Article  CAS  Google Scholar 

  • Su SQ, Zhou YM, Qin JG, Wang W, Yao WZ, Song L (2012) Physiological responses of Egeria densa to high ammonium concentration and nitrogen deficiency. Chemosphere 86:538–545. doi:10.1016/j.chemosphere.2011.10.036

    Article  Google Scholar 

  • Turano FJ, Dashner R, Upadhyaya A, Caldwell CR (1996) Purification of mitochondrial glutamate dehydrogenase from dark-grown soybean seedlings. Plant Physiol 112:1357–1364

    Article  CAS  Google Scholar 

  • Varone L, Ribas-Carbo M, Cardona C, Gallé A, Medrano H, Gratani L, Flexasb J (2012) Stomatal and non-stomatal limitations to photosynthesis in seedlings and saplings of Mediterranean species pre-conditioned and aged in nurseries: different response to water stress. Environ Exp Bot 75:235–247. doi:10.1016/j.envexpbot.2011.07.007

    Article  CAS  Google Scholar 

  • Voutsa D, Samara C, Manoli E, Lazarou D, Tzoumaka P (2014) Ionic composition of PM2.5 at urban sites of northern Greece: secondary inorganic aerosol formation. Environ Sci Pollut Res 21:4995–5006. doi:10.1007/s11356-013-2445-8

    Article  CAS  Google Scholar 

  • Woo SY, Lee DK, Lee YK (2007) Net photosynthetic rate, ascorbate peroxidase and glutathione reductase activities of Erythrina orientalis in polluted and non-polluted areas. Photosynthetica 45:293–295. doi:10.1007/s11099-007-0047-8

  • Yang J, Chang YM, Yan PB (2015) Ranking the suitability of common urban tree species for controlling PM2.5 pollution. Atmos Pollut Res 6:267–277. doi:10.5094/APR.2015.031

    Article  CAS  Google Scholar 

  • Yin LQ, Niu ZC, Chen XQ, Chen JS, Zhang FW, Xu LL (2014) Characteristics of water-soluble inorganic ions in PM2.5 and PM2.5–10 in the coastal urban agglomeration along the Western Taiwan Strait Region, China. Environ Sci Pollut Res 21:5141–5156. doi:10.1007/s11356-013-2134-7

    Article  CAS  Google Scholar 

  • Yoneyama T, Ito O, Engelaar WMHG (2003) Uptake, metabolism and distribution of nitrogen in crop plants traced by enriched and natural 15N: progress over the last 30 years. Phytochem Rev 2:121–132. doi:10.1023/B:PHYT.0000004198.95836.ad

    Article  CAS  Google Scholar 

  • Zhang LL, Wang HE, Li J, Kuang YW, Wen DZ (2013) Physiological responses and accumulation of pollutants in woody species under in situ polluted condition in southern China. J Plant Res 126:95–103. doi:10.1007/s10265-012-0508-4

    Article  Google Scholar 

  • Zhang LX, Zheng P, Ruan Z, Tian L, Ashraf M (2015) Nitric oxide accumulation and glycinebetaine metabolism in two osmotically stressed maize cultivars supplied with different nitrogen forms. Biol Plant 59:183–186. doi:10.1007/s10535-014-0458-x

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Forestry Public Welfare Project of China (No. 201304301).

Author information

Authors and Affiliations

  1. College of Biological Science and Biotechnology, Beijing Forestry University, No. 35, Tsing Hua East Road, Haidian District, Beijing, 100083, China

    Huihong Guo, Hui Wang, Qingqian Liu, Hailong An, Chao Liu, Xinli Xia & Weilun Yin

Authors
  1. Huihong Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hui Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Qingqian Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Hailong An
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chao Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xinli Xia
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Weilun Yin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Xinli Xia or Weilun Yin.

Additional information

Responsible editor: Yi-ping Chen

Electronic supplementary material

ESM 1

(PDF 1878 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guo, H., Wang, H., Liu, Q. et al. 15N-labeled ammonium nitrogen uptake and physiological responses of poplar exposed to PM2.5 particles. Environ Sci Pollut Res 24, 500–508 (2017). https://doi.org/10.1007/s11356-016-7620-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-016-7620-2

Keywords

Search

Navigation