, Volume 50, Issue 1, pp 67–76 | Cite as

Growth and photosynthetic responses of four landscape shrub species to elevated ozone

  • L. Zhang
  • B. Y. Su
  • H. Xu
  • Y. G. Li


Attention should be paid to ozone (O3) sensitivity of greening plant since ground-level O3 concentrations are increasing especially in urban and suburban area. We studied the ecophysiological responses to elevated O3 of four shrub species [Euonymus bungeanus Maxim. (EB), Photinia × fraseri (PF), Chionanthus retusus Lindl. & Paxt. (CR) and Cornus alba L. (CA)], which are often used for garden greening in China. Saplings of those species were exposed to high O3 concentration (70 nmol mol−1, 7 h d−1 for 65 d) in open-top growth chambers. Responses to O3 were assessed by gas exchanges, chlorophyll (Chl) fluorescence and dry mass. We found that elevated O3 significantly decreased lightsaturated net photosynthetic rate (P Nsat), transpiration rate (E) and stomatal conductance (g s). The ratio of intercellular CO2 to ambient CO2 concentration (C i/C a) did not reduce under O3 fumigation which suggested that the O3-induced depressions of P Nsat under O3 fumigation were probably due to limitation of mesophyll processes rather than stomatal limitation. High O3 exposure also significantly depressed the maximum efficiency of photosystem II (PSII) photochemistry in the dark-adapted state (Fv/Fm) which meant the O3-induced photoinhibition. Both root dry mass and root/shoot ratios were significantly decreased under ozone fumigation, but the total mass was unchanged. The responses of gas exchange such as P Nsat in these four shrubs to O3 exposure were species-specific. Highest loss of P Nsat was observed in EB (−49.6%), while the CR had the lowest loss (−36.5%). Moreover, the O3-exposed CR showed similar g s as CF, reflecting that its O3 flux might be unchanged under elevated O3 environment. Ozone drastically decreased actual quantum yield of PSII (ΦPSII) and electron transport rate (ETR) in EB while increased ΦPSII and ETR in CR. Furthermore, the relative losses in P Nsat positively correlated with the relative decreases in ΦPSII and ETR which indicated that the impairment of photosynthesis was probably affected by the light reaction process. The light reaction of EB was impaired most seriously but that of CR was not damaged. All results indicated that EB was probably the most sensitive shrub species to O3 while CR the most tolerant one. Therefore, CR might be an ideal choice for greening in ozone-polluted areas.

Additional key words

biomass Chionanthus retusus Lindl. & Paxt. chlorophyll a fluorescence Cornus alba Euonymus bungeanus gas exchange ozone Photinia × fraseri 



the cumulative O3 exposure over a threshold of the 1-h average [O3] of 40 nmol mol−1 during daytime


Cornus alba L.


charcoal-filtered air


Chionanthus retusus Lindl. & Paxt.


ambient CO2 concentration


intercellular CO2 concentration




transpiration rate


Euonymus bungeanus Maxim.


electron transport rate


minimal fluorescence of the dark-adapted state


maximal fluorescence of the dark-adapted state


the maximum efficiency of photosystem II photochemistry in the dark-adapted state


stomatal conductance


leaf dry mass


nonphotochemical quenching


open top chambers


photosynthetically active radiation


Photinia × fraseri


light-saturated net photosynthetic rate


photosynthetic photon flux density


photosystem II


root dry mass


stem dry mass


volatile organic compounds


the actual quantum yield of PSII


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ashmore, M.R., Dalpra, C., Tickle, A.K.: Effects of ozone and calcium nutrition on native plant species. — In: Mathy, P. (ed.): Air Pollution and Ecosystems. Pp. 647–652. Reidel, Dordrecht 1987.Google Scholar
  2. Bergmann, E., Bender, J., Weigel, H.J.: Growth responses and foliar sensitivities of native herbaceous species to ozone exposures. — Water Air Soil Pollut. 85: 1437–1442, 1995.CrossRefGoogle Scholar
  3. Bilger, W., Björkman, O.: Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis. — Photosynth. Res. 25: 173–185, 1990.CrossRefGoogle Scholar
  4. Biswas, D.K., Xu, H., Li, Y.G., Liu, M.Z., Chen, Y.H., Sun, J.Z., Jiang, G.M.: Assessing the genetic relatedness of higher ozone sensitivity of modern wheat to its wild and cultivated progenitors/relatives. — J. Exp. Bot. 59: 951–963, 2008.PubMedCrossRefGoogle Scholar
  5. Booker, F., Muntifering, R., McGrath, M., Burkey, K., Decoteau, D., Fiscus, E., Manning, W., Krupa, S., Chappelka, A., Grantz, D.: The ozone component of global change: potential effects on agricultural and horticultural plant yield, product quality and interactions with invasive species. — J. Integr. Plant Biol. 51: 337–351, 2009.PubMedCrossRefGoogle Scholar
  6. Bussotti, F., Schaub, M., Cozzi, A., Kräuchi, N., Ferretti, M., Novak, K., Skelly, J.: Assessment of ozone visible symptoms in the field: perspectives of quality control. — Environ. Pollut. 125: 81–89, 2003.PubMedCrossRefGoogle Scholar
  7. Bussotti, F., Desotgiua, R., Cascioa, C., et al.: Ozone stress in woody plants assessed with chlorophyll a fluorescence. A critical reassessment of existing data. — Environ. Exp. Bot. 73: 19–30, 2011.CrossRefGoogle Scholar
  8. Calatayud, A., Barreno, E.: Response to ozone in two lettuce varieties on chlorophyll a fluorescence, photosynthetic pigments and lipid peroxidation. — Plant Physiol. Biochem. 42: 549–555, 2004.PubMedCrossRefGoogle Scholar
  9. Calatayud, A., Iglesias, D.J., Talón, M., Barreno, E.: Effects of long-term ozone exposure on citrus: Chlorophyll a fluorescence and gas exchange. — Photosynthetica 44: 548–554, 2006.CrossRefGoogle Scholar
  10. Chien, C.T., Kuo-Huang, L.L., Shen, Y.C., Zhang, R.C., Chen, S.Y., Yang, J.C., Pharis, R.P.: Storage behavior of Chionanthus retusus seed and asynchronous development of the radicle and shoot apex during germination in relation to germination inhibitors, including abscisic acid and four phenolic glucosides. — Plant Cell Environ. 45: 1158–1167, 2004.Google Scholar
  11. Contran, N., Paoletti, E., Manning, W.J., Tagliaferro, F.: Ozone sensitivity and ethylenediurea protection in ash trees assessed by JIP chlorophyll a fluorescence transient analysis. — Photosynthetica 47: 68–78, 2009.CrossRefGoogle Scholar
  12. Cooley, D.R., Manning, W.J.: The impact of ozone on assimilate partitioning in plants: A review. — Environ. Pollut. 47: 95–113, 1987.PubMedCrossRefGoogle Scholar
  13. Dirr, M.A.: Effects of PTB and IBA on the rooting response of 19 landscape taxa. — J. Environ. Hort. 8: 83–85, 1990.Google Scholar
  14. Feng, Z.Z., Zheng, H.Q., Wang, X.K., Zheng, Q.W., Feng, Z.W.: Sensitivity of Metasequoia glyptostroboides to ozone stress. — Photosynthetica 46: 463–465, 2008.CrossRefGoogle Scholar
  15. Genty, B., Briantais, J.M., Baker, N.R.: The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. — Biochem. Biophys. Acta 990: 87–92, 1989.CrossRefGoogle Scholar
  16. Gitelson, A.A., Chivkunova, O.B., Merzlyak, M.N.: Nondestructive estimation of anthocyanins and chlorophylls in anthocyanic leaves. — Amer. J. Bot. 96: 1861–1868, 2009.CrossRefGoogle Scholar
  17. Guidi, L., Di Cagno, R., Soldatini, G.F.: Screening of bean cultivars for their response to ozone as evaluated by visible symptoms and leaf chlorophyll fluorescence. — Environ. Pollut. 107: 349–355, 2000.PubMedCrossRefGoogle Scholar
  18. He, X.Y., Fu, S.L., Chen, W., Zhao, T.H., Xu, S., Tuba, Z.: Changes in effects of ozone exposure on growth, photosynthesis, and respiration of Ginkgo biloba in Shenyang urban area. — Photosynthetica 45: 555–561, 2007.CrossRefGoogle Scholar
  19. Heath, R.L.: Initial events in injury to plants by air pollutants. — Annu. Rev. Plant Physiol. 31: 395–431, 1980.CrossRefGoogle Scholar
  20. Heath, R.L.: The biochemistry of ozone attack on plasma membrane of plant cells. — Rec. Adv. Phytochem. 21: 29–54, 1987.Google Scholar
  21. IPCC (Intergovernmental Panel on Climate Change): Climate change 2007: the physical science basis. In Solomon, S., Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K.B., Tignor, M., Miller, H.L. (ed.): Contribution of Working Group I to the Fourth Annual Assessment Report of the Intergovernmental Panel on Climate Change. Pp. 996. — Cambridge Univ. Press, Cambridge 2007.Google Scholar
  22. Jim, C.Y., Chen, W.Y.: Assessing the ecosystem service of air pollutant removal by urban trees in Guangzhou (China). — J. Environ. Manage. 88: 665–676, 2008.PubMedCrossRefGoogle Scholar
  23. Kim, K.J., Kim, Y.J., Ma, Y.I., Kim, J.C., Sunwoo, Y.: A modeling study of the impact of natural and urban forest on ambient ozone. — Korean J. Chem. Eng. 25: 483–492, 2008.CrossRefGoogle Scholar
  24. Larraburu, E.E., Carletti, S.M., Rodríguez Cáceres, E.A., Llorente, B.E.: Micropropagation of photinia employing rhizobacteria to promote root development. — Plant Cell Rep. 26: 711–717, 2007.PubMedCrossRefGoogle Scholar
  25. Lumis, G.P., Ormrod, D.P.: Effects of ozone on growth of four woody ornamental plants. — Can. J. Plant Sci. 58: 769–773, 1978.CrossRefGoogle Scholar
  26. Ma, Y.L., Zhang, Y.H.: [The study on pollution of atmospheric photochemical oxidants in Beijing.] — Res. Environ. Sci. 13: 14–17, 2000. [In Chin.]Google Scholar
  27. Mulholland, B.J., Craigon, J., Black, C.R., Colls, J.J., Atherton, J., Landon, G.: Impact of elevated atmospheric CO2 and O3 on gas exchange and chlorophyll content in spring wheat (Triticum aestivum L.). — J. Exp. Bot. 48: 1853–1863, 1997.Google Scholar
  28. Nowak, D.J., Civerolo, J.C., Rao, S.T., Sistla, G., Luley, C.J., Crane, D.E.: A modeling study of the impact of urban trees on ozone. — Atmos. Environ. 34: 1601–1613, 2000.CrossRefGoogle Scholar
  29. Overmyer, K., Broshe, M., Kangasjärvi, J.: Reactive oxygen species and hormonal control of cell death. — Trends Plant Sci. 8: 335–342, 2003.PubMedCrossRefGoogle Scholar
  30. Owens, T.G.: In vivo chlorophyll fluorescence as a probe of photosynthetic physiology. — In: Alscher, R.G., Wellburn, A.R. (ed.): Plant Responses to the Gaseous Environment. Pp. 195–217. Chapman & Hall, London 1994.CrossRefGoogle Scholar
  31. Paoletti, E., Ferrara, A.M., Calatayud, V., Cervero, J., Giannetti, F., Sanz, M.J., Manning, W.J.: Deciduous shrubs for ozone bioindication: Hibiscus syriacus as an example. — Environ. Pollut. 157: 865–870, 2009.PubMedCrossRefGoogle Scholar
  32. Pleijel, H., Danielsson, H.: Growth of 27 herbs and grasses in relation to ozone exposure and plant strategy. — New Phytol. 135: 361–367, 1997.CrossRefGoogle Scholar
  33. Ramírez-Malagón, R, Borodanenko, A, Barrera-Guerra, J, Ochoa-Alejo, N.: Micropropagation for fraser photinia (Photinia×fraseri). — Plant Cell Tissue Organ Cult. 48: 219–222, 1997.CrossRefGoogle Scholar
  34. Reich, P.B.: Quantifying plant response to ozone: a unifying theory. — Tree Physiol. 3: 63–91, 1987.PubMedGoogle Scholar
  35. Ryang, S.Z., Woo, S.Y., Kwon, S.Y., Kim, S.H., Lee, S.H., Kim, K.N., Lee, D.K.: Changes of net photosynthesis, antioxidant enzyme activities, and antioxidant contents of Liriodendron tulipifera under elevated ozone. — Photosynthetica 47: 19–25, 2009.CrossRefGoogle Scholar
  36. Schreiber, U.: Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: an overview. — In: Papageorgiu, G.C., Govindjee (ed.): Chlorophyll a Fluorescence. A Signature of Photosynthesis. Pp. 279–319. Springer, Dordrecht 2004.Google Scholar
  37. Seinfeld, J.H.: Urban air pollution: State of the science. — Science. 243: 745–752, 1989.PubMedCrossRefGoogle Scholar
  38. Seppo, K., Wang, K.Y. Effects of elevated O3 and CO2 on chlorophyll fluorescence and gas exchange in Scots pine during the third growing season. — Environ. Pollut. 97: 17–27, 1997.CrossRefGoogle Scholar
  39. Shao, M., Tang, X., Zhang, Y., Li, W.: City clusters in China: air and surface water pollution. — Front. Ecol. Environ. 4: 353–361, 2006.CrossRefGoogle Scholar
  40. Skärby, L., Ro-Poulsen, H., Wellburn, F.A.M., Sheppard, L.J.: Impacts of ozone on forests: a European perspective. — New Phytol. 139: 109–122, 1998.CrossRefGoogle Scholar
  41. Soejima, A., Maki, M., Ueda, K.: Genetic variation in relic and isolated populations of Chionanthus retusus (Oleaceae) of Tsushima Island and the Tôno region, Japan. — Genes Genet. Syst. 73: 29–37, 1998.CrossRefGoogle Scholar
  42. Spivey, A.C., Weston, M., Woodhead, S.: Celastraceae sesquiterpenoids: biological activity and synthesis. — Chem. Soc. Rev. 31: 43–59, 2002.PubMedCrossRefGoogle Scholar
  43. Szantoi, Z., Chappelka, A.H., Muntifering, R.B., Somers, G.L.: Cutleaf coneflower (Rudbeckia laciniata L.) response to ozone and ethylenediurea (EDU). — Environ. Pollut. 157: 840–846, 2009.PubMedCrossRefGoogle Scholar
  44. Tu, Y.G., Wu, D.G., Zhou, J., Chen, Y.Z.: Sesquiterpenoids from two species of celastraceae. — Phytochemistry 31: 1281–1283, 1992.CrossRefGoogle Scholar
  45. von Caemmerer, S., Farquhar, G.: Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. — Planta 153: 376–387, 1981.CrossRefGoogle Scholar
  46. Weber, J.A., Clark, C.S., Hogsett, W.E.: Analysis of the relationships among O3 uptake, conductance, and photosynthesis in needles of Pinus ponderosa. — Tree Physiol. 13: 157–172, 1993.PubMedGoogle Scholar
  47. Xu, H., Chen, S.B., Biswas, D.K., Li, Y.G., Jiang, G.M.: Photosynthetic and yield responses of an old and a modern winter wheat cultivars to short-term ozone exposure. — Photosynthetica 47: 247–254, 2009.CrossRefGoogle Scholar
  48. Zhang, L., Xu, H., Yang, J.C., Li, W.D., Jiang, G.M., LI, Y.G.: Photosynthetic characteristics of diploid honeysuckle (Lonicera japonica Thumb.) and its autotetraploid cultivar subjected to elevated ozone exposure. — Photosynthetica 48: 87–95, 2010.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  1. 1.College of HorticultureNortheast Agricultural UniversityHarbinP.R.China
  2. 2.State Key Laboratory of Vegetation and Environmental Change, Institute of BotanyChinese Academy of SciencesBeijingP.R.China
  3. 3.College of AgronomySichuan Agricultural UniversityYa’an, SichuanP.R.China

Personalised recommendations