Skip to main content
Log in

Effects of the interaction between ozone and carbon dioxide on gas exchange, photosystem II and antioxidants in rice leaves

  • Original Papers
  • Published:
Photosynthetica

Abstract

To understand the interactive effects of O3 and CO2 on rice leaves; gas exchange, chlorophyll (Chl) fluorescence, ascorbic acid and glutathione were examined under acute (5 h), combined exposures of O3 (0, 0.1, or 0.3 cm3 m−3, expressed as O0, O0.1, or O0.3, respectively), and CO2 (400 or 800 cm3 m−3, expressed as C400 or C800, respectively) in natural-light gas-exposure chambers. The net photosynthetic rate (P N), maximum (Fv/Fm) and operating (Fq′/Fm′) quantum efficiencies of photosystem II (PSII) in young (8th) leaves decreased during O3 exposure. However, these were ameliorated by C800 and fully recovered within 3 d in clean air (O0 + C400) except for the O0.3 + C400 plants. The maximum PSII efficiency at 1,500 μmol m−2 s−1 PPFD (Fv′/Fm′) for the O0.3 + C400 plants decreased for all measurement times, likely because leaves with severely inhibited P N also had a severely damaged PSII. The P N of the flag (16th) leaves at heading decreased under O3 exposure, but the decline was smaller and the recovery was faster than that of the 8th leaves. The Fq′/Fm′ of the flag leaves in the O0.3 + C400 and O0.3 + C800 plants decreased just after gas exposure, but the Fv/Fm was not affected. These effects indicate that elevated CO2 interactively ameliorated the inhibition of photosynthesis induced by O3 exposure. However, changes in antioxidant levels did not explain the above interaction.

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

AA:

ascorbic acid

C i :

intercellular CO2 concentration

Chl:

chlorophyll

DHA:

dehydroascorbic acid

g s :

stomatal conductance

F′:

steady fluorescence

F0 :

minimum flouorescence of dark-adapted state

F0′:

minimum fluorescence in the steady state

Fm :

maximum fluorescence of dark-adapted state

Fm′:

maximum fluorescence in the steady state

Fq′:

difference between Fm′ and F′

Fv :

variable fluorescence

Fv′:

variable fluorescence in the steady state

GSH:

glutathione

GSSG:

oxidized glutathione

P N :

net photosynthetic rate

PPFD:

photosynthetic photon flux density

PSII:

photosystem II

qN :

nonphotochemical quenching coefficient

qP :

photochemical quenching coefficient

R D :

respiration rate

RDS:

redox state

ROS:

reactive oxygen species

References

  • Baier, M., Kandlbinder, A., Golldack, D., Dietz, K.-J.: Oxidative stress and ozone: perception, signaling and response. — Plant Cell Environ. 28: 1012–1020, 2005.

    Article  CAS  Google Scholar 

  • Baker, N.R.: Chlorophyll fluorescence: A probe of photosynthesis in vivo. — Annu. Rev. Plant Biol. 59: 89–113, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Booker, F.L., Fiscus, E.L.: The role of ozone flux and antioxidants in the suppression of ozone injury by elevated CO2 in soybean. — J. Exp. Bot. 56: 2139–2151, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Cabrera, H., Dawson, S.V., Stromberg, C.: A California air standard to protect vegetation from ozone. — Environ. Pollut. 53: 397–408, 1988.

    Article  PubMed  CAS  Google Scholar 

  • Donnelly, A., Jones, M.B., Burke, J.I., Schnieders, B.: Elevated CO2 provides protection from O3 induced photosynthetic damage and chlorophyll loss in flag leaves of spring wheat (Triticum aestivum L., cv. ‘Minaret’). — Agric. Ecosyst. Environ. 80: 159–168, 2000.

    Article  CAS  Google Scholar 

  • Environ. Improve. Div., Tokyo Metropolitan Government Bureau Environ.: [Review report on the photochemical oxidant measures.] — J. Jap. Soc. Atmos. Environ. 40: A65–A77, 2005. [In Jap.]

    Google Scholar 

  • Haun, J.R.: Visual quantification of wheat development. — Agron. J. 65: 116–119, 1973.

    Article  Google Scholar 

  • Heath, R.L.: Possible mechanisms for the inhibition of photosynthesis by ozone. — Photosynth. Res. 39: 439–451, 1994.

    Article  CAS  Google Scholar 

  • Hoshikawa: The Growing Rice Plant. — Nobunkyo, Tokyo 1989. [In Jap.]

  • Imai, K., Kobori, K.: Effects of the interaction between ozone and carbon dioxide on gas exchange, ascorbic acid content, and visible leaf symptoms in rice leaves. — Photosynthetica 46: 387–394, 2008.

    Article  CAS  Google Scholar 

  • Inada, H., Yamaguchi, M., Satoh, R., Hoshino, D., Nagasawa, A., Negishi, Y., Nouchi, I., Kobayashi, K., Izuta, T.: Effects of ozone on photosynthetic components and radical scavenging system in leaves of rice (Oryza sativa L.). — J. Agric. Meteorol. 64: 243–255, 2008.

    Article  Google Scholar 

  • Ishioh, T., Imai, K.: [Effects of atmospheric ozone and carbon dioxide concentrations on gas exchanges, contents of Rubisco and chlorophyll in leaves of lowland rice.] — Proc. Kanto Branch,Crop Sci. Soc. Jap. 20: 54–55, 2005. [In Jap.]

    Google Scholar 

  • Ishioh, T., Kobori, K., Imai, K.: The detrimental effect of tropospheric O3 on lowland rice is meliorated by elevated CO2. — In: Toriyama, K., Heong, K. L., Hardy, B.,(ed.): Rice is Life: Scientific Perspectives for the 21st Century. Pp 557–560. IRRI, Los Baños 2005.

    Google Scholar 

  • Ito, A., Udagawa, T., Uchijima, Z.: [Phytometrical studies of crop canopies. II. Canopy structure of rice crops in relation to varieties and growing stage.] — Jap. J. Crop. Sci. 42: 334–342, 1973. [In Jap.]

    Google Scholar 

  • Kobayashi, K.: [Assessing the impacts of tropospheric ozone on agricultural production.] — J. Jap. Soc. Atmos. Environ. 34: 162–175, 1999. [In Jap.]

    CAS  Google Scholar 

  • Mano, J., Khorobrykh, S., Amako, K.: [Reactive oxygen species and antioxidants associated with photosynthesis.] — Low Temp. Sci. 67: 179–195, 2009. [In Jap.]

    Google Scholar 

  • McKee, I.F., Eiblmeier, M., Polle, A.: Enhanced ozonetolerance in wheat grown at an elevated CO2 concentration: ozone exclusion and detoxification. — New Phytol. 137: 275–284, 1997.

    Article  CAS  Google Scholar 

  • Morita, S., Tanaka, K.: Detoxification of active oxygen species and tolerance in plants exposed to air pollutants and CO2. — In: Omasa, K., Saji, H., Youssefian, S., Kondo, N. (ed.): Air Pollution and Plant Biotechnology. Prospects for Phytomonitoring and Phytoremediation. Pp. 253–267. Springer-Verlag, Tokyo 2002.

    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 

  • Nakanishi, J., Shinozaki, H., Inoue, K.: [Ozone — Photochemical Oxidant.] — Maruzen Co., Tokyo 2009. [In Jap.]

    Google Scholar 

  • Nouchi, I.: Changes in antioxidant levels and activities of related enzymes in rice leaves exposed to ozone. — Soil. Sci. Plant Nutr. 39: 309–320, 1993.

    CAS  Google Scholar 

  • Nouchi, I., Ito, O., Harazono, Y., Kouchi, H.: Acceleration of 13C-labelled photosynthate partitioning from leaves to panicles in rice plants exposed to chronic ozone at the reproductive stage. — Environ. Pollut. 88: 253–260, 1995.

    Article  PubMed  CAS  Google Scholar 

  • Olszyk, D.M., Wise, C.: Interactive effects of elevated CO2 and O3 on rice and flacca tomato. — Agr. Ecosyst. Environ. 66: 1–10, 1997.

    Article  CAS  Google Scholar 

  • Overmyer, K., Tuominen, H., Kettunen, R., Betz, C., Langebartels, C., Sandermann, H., Jr, Kangasjärvi, J.: Ozonesensitive Arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death. — Plant Cell 12: 1849–1862, 2000.

    Article  PubMed  CAS  Google Scholar 

  • Pang, J., Kobayashi, K., Zhu, J.G.: Yield and photosynthetic characteristics of flag leaves in Chinese rice (Oryza sativa L.) varieties subjected to free-air release of ozone. — Agr. Ecosyst. Environ. 132: 203–211, 2009.

    Article  CAS  Google Scholar 

  • Papageorgiou, G.C., Govindjee. (ed.): Chlorophyll a Fluorescence. A Signature of Photosynthesis. Advances in Photosynthesis and Respiration. Vol. 19. — Springer, Dordrecht 2004.

    Google Scholar 

  • Rai, R., Agrawal, M.: Evaluation of physiological and biochemical responses of two rice (Oryza sativa L.) cultivars to ambient air pollution using open top chambers at a rural site in India. — Sci. Total Environ. 407: 679–691, 2008.

    Article  PubMed  CAS  Google Scholar 

  • Rai, R., Agrawal, M., Agrawal, S.B.: Threat to food security under current levels of ground level ozone: A case study for Indian cultivars of rice. — Atmos. Environ. 44: 4272–4282, 2010.

    Article  CAS  Google Scholar 

  • Rao, M.V., Hale, B.A., Ormrod, D.P.: Amelioration of ozoneinduced oxidative damage in wheat plants grown under high carbon dioxide (Role of antioxidant enzymes). — Plant Physiol. 109: 421–432, 1995.

    PubMed  CAS  Google Scholar 

  • Reid, C.D., Fiscus, E.L.: Ozone and density affect the response of biomass and seed yield to elevated CO2 in rice. — Global Change Biol. 14: 60–76, 2008.

    Google Scholar 

  • Roe, J.H., Oesterling, M.J.: The determination of dehydroascorbic acid and ascorbic acid in plant tissues by the 2,4-dinitrophenylhydrazine method. — J. Biol. Chem. 152: 511–517, 1944.

    CAS  Google Scholar 

  • Sasaki-Sekimoto, Y., Taki, N., Obayashi, T., Aono, M., Matsumoto, F., Sakurai, N., Suzuki, H., Hirai, M. Y., Noji, M., Saito, K., Masuda, T., Takamiya, K.-I., Shibata, D., Ohta, H.: Coordinated activation of metabolic pathways for antioxidants and defence compounds by jasmonates and their roles in stress tolerance in Arabidopsis. — Plant J. 44: 653–668, 2005.

    Article  PubMed  CAS  Google Scholar 

  • Sonoike, K.: [Basics of the measurements of photosynthesis by pulse amplitude modulation.] — Low Temp. Sci. 67: 507–524, 2009. [In Jap.]

    Google Scholar 

  • Torsethaugen, G., Pell, E.J., Assman, S.M.: Ozone inhibits guard cell K+ channels implicated in stomatal opening. — Proc. nat. Acad. Sci. USA 96: 13577–13582, 1999.

    Article  PubMed  CAS  Google Scholar 

  • Toyama, S., Yoshida, M., Niki, T., Ohashi, T., Koyama, I.: Studies on ultrastructure and function of photosynthetic apparatus in rice cells. IV. Effects of low dose and intermittent fumigation of ozone on the ultrastructure of chloroplasts in rice leaf cells. — Jap. J. Crop Sci. 58: 664–672, 1989.

    Google Scholar 

  • WMO WDCGG: Data Summary No. 34. Pp. 1–13. JMA (Japan), Tokyo 2010.

  • Yamaguchi, M., Inada, H., Satoh, R., Hoshino, D., Nagasawa, A., Negishi, Y., Sasaki, H., Nouchi, I., Kobayashi, K., Izuta, T.: Effects of ozone on the growth, yield and leaf gas exchange rates of two Japanese cultivars of rice (Oryza sativa L.) — J. Agr. Meteorol. 64: 131–141, 2008.

    Article  Google Scholar 

Download references

Acknowledgment

This work was supported in part by a grant for the Private University Strategic Infrastructure Formation Support Project from the Ministry of Education, Culture, Sports, Science and Technology, Japan (No. S0901028). The authors are grateful to editors and anonymous reviewers for their valuable suggestions.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to K. Imai.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kobayakawa, H., Imai, K. Effects of the interaction between ozone and carbon dioxide on gas exchange, photosystem II and antioxidants in rice leaves. Photosynthetica 49, 227–238 (2011). https://doi.org/10.1007/s11099-011-0024-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11099-011-0024-0

Additional key words

Navigation