Skip to main content
Log in

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

  • Published:
Photosynthetica

Abstract

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.

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.

Similar content being viewed by others

Abbreviations

AOT40:

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

CA:

Cornus alba L.

CF:

charcoal-filtered air

CR:

Chionanthus retusus Lindl. & Paxt.

C a :

ambient CO2 concentration

C i :

intercellular CO2 concentration

Chl:

chlorophyll

E :

transpiration rate

EB:

Euonymus bungeanus Maxim.

ETR:

electron transport rate

Fo :

minimal fluorescence of the dark-adapted state

Fm :

maximal fluorescence of the dark-adapted state

Fv/Fm :

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

g s :

stomatal conductance

LDM:

leaf dry mass

NPQ:

nonphotochemical quenching

OTCs:

open top chambers

PAR:

photosynthetically active radiation

PF:

Photinia × fraseri

P Nsat :

light-saturated net photosynthetic rate

PPFD:

photosynthetic photon flux density

PSII:

photosystem II

RDM:

root dry mass

SDM:

stem dry mass

VOCs:

volatile organic compounds

ΦPSII :

the actual quantum yield of PSII

References

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Cooley, D.R., Manning, W.J.: The impact of ozone on assimilate partitioning in plants: A review. — Environ. Pollut. 47: 95–113, 1987.

    Article  PubMed  CAS  Google Scholar 

  • Dirr, M.A.: Effects of PTB and IBA on the rooting response of 19 landscape taxa. — J. Environ. Hort. 8: 83–85, 1990.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Heath, R.L.: Initial events in injury to plants by air pollutants. — Annu. Rev. Plant Physiol. 31: 395–431, 1980.

    Article  CAS  Google Scholar 

  • Heath, R.L.: The biochemistry of ozone attack on plasma membrane of plant cells. — Rec. Adv. Phytochem. 21: 29–54, 1987.

    CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Lumis, G.P., Ormrod, D.P.: Effects of ozone on growth of four woody ornamental plants. — Can. J. Plant Sci. 58: 769–773, 1978.

    Article  CAS  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • Overmyer, K., Broshe, M., Kangasjärvi, J.: Reactive oxygen species and hormonal control of cell death. — Trends Plant Sci. 8: 335–342, 2003.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Chapter  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Pleijel, H., Danielsson, H.: Growth of 27 herbs and grasses in relation to ozone exposure and plant strategy. — New Phytol. 135: 361–367, 1997.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Reich, P.B.: Quantifying plant response to ozone: a unifying theory. — Tree Physiol. 3: 63–91, 1987.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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 

  • Seinfeld, J.H.: Urban air pollution: State of the science. — Science. 243: 745–752, 1989.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Shao, M., Tang, X., Zhang, Y., Li, W.: City clusters in China: air and surface water pollution. — Front. Ecol. Environ. 4: 353–361, 2006.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Spivey, A.C., Weston, M., Woodhead, S.: Celastraceae sesquiterpenoids: biological activity and synthesis. — Chem. Soc. Rev. 31: 43–59, 2002.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Tu, Y.G., Wu, D.G., Zhou, J., Chen, Y.Z.: Sesquiterpenoids from two species of celastraceae. — Phytochemistry 31: 1281–1283, 1992.

    Article  CAS  Google Scholar 

  • von Caemmerer, S., Farquhar, G.: Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. — Planta 153: 376–387, 1981.

    Article  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Y. G. Li.

Additional information

Acknowledgment: This investigation was funded by National Natural Science Foundation of China (No. 30900200 & No. 30871735).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, L., Su, B.Y., Xu, H. et al. Growth and photosynthetic responses of four landscape shrub species to elevated ozone. Photosynthetica 50, 67–76 (2012). https://doi.org/10.1007/s11099-012-0004-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11099-012-0004-z

Additional key words

Navigation