Download PDF
Plant Biol (Stuttg) 2007; 9(4): 478-488
DOI: 10.1055/s-2007-964942
Research Paper

Georg Thieme Verlag Stuttgart KG · New York

The Impact of Ozone on Juvenile Maize (Zea mays L.) Plant Photosynthesis: Effects on Vegetative Biomass, Pigmentation, and Carboxylases (PEPc and Rubisco)

L. Leitao1 , O. Bethenod2 , J.-P. Biolley1
  • 1Laboratoire d'Ecologie Moléculaire - IBEAS - EA3525, Université de Pau et des Pays de l'Adour, Avenue de l'Université, BP 1155, 64013 Pau Cedex, France
  • 2UMR1091 Environnement et Grandes Cultures, INRA, 78850 Thiverval-Grignon, France
Further Information

Publication History

Received: August 6, 2006

Accepted: December 8, 2006

Publication Date:
02 April 2007 (online)

   Permissions and Reprints

Abstract

The impact of ozone on crops was more studied in C3 than in C4 species. In C3 plants, ozone is known to induce a photosynthesis impairment that can result in significant depressions in biomass and crop yields. To investigate the impact of O3 on C4 plant species, maize seedlings (Zea mays L. cv. Chambord) were exposed to 5 atmospheres in open-top chambers: non-filtered air (NF, 48 nL L-1 O3) and NF supplied with 20 (+ 20), 40 (+ 40), 60 (+ 60), and 80 (+ 80) nL L-1 ozone. An unchambered plot was also available. Leaf area, vegetative biomass, and leaf dry mass per unit leaf area (LMA) were evaluated 33 days after seedling emergence in OTCs. At the same time, photosynthetic pigments as well as carboxylase (PEPc and Rubisco) activities and amounts were also examined in the 5th leaf. Ozone enhanced visible symptoms characterizing foliar senescence. Across NF, + 20, + 40, and + 60 atmospheres, both chlorophylls and carotenoids were found to be linearly decreased against increasing AOT40 (ca. - 50 % in + 60). No supplementary decrease was observed between + 60 and + 80. Total above-ground biomass was reduced by 26 % in + 80 atmosphere; leaf dry matter being more depressed by ozone than leaf area. In some cases, LMA index was consistent to reflect low negative effects caused by a moderate increase in ozone concentration. PEPc and Rubisco were less sensitive to ozone than pigments: only the two highest external ozone doses reduced their activities by about 20 - 30 %. These changes might be connected to losses in PEPc and Rubisco proteins that were decreased by about one-third. The underlying mechanisms for these results were discussed with special reference to C3 species. To conclude, we showed that both light and dark reactions of C4 photosynthesis can be impaired by realistic ozone doses.

Key words

Pigment - leaf mass per area (LMA) - maize - ozone - phosphoenolpyruvate carboxylase (PEPc) - ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco)

References

  • 1 Aly M. M., El-Sabbagh S. M., El-Shouny W. A., Ebrahim M. K. H.. Physiological response of Zea mays to NaCl stress with respect to Azotobacter chroococcum and Streptomyces niveus.  Pakistan Journal of Biological Science. (2003);  6 2073-2080
    PubMedGoogle Scholar
  • 2 Birch C. J., Vos J., Van der Putten P. E. L.. Plant development and leaf area production in contrasting cultivars of maize grown in a cool temperature environment in the field.  European Journal of Agronomy. (2003);  19 173-188
    CrossrefPubMedGoogle Scholar
  • 3 Bradford M. M.. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.  Analytical Biochemistry. (1976);  72 248-254
    PubMedGoogle Scholar
  • 4 Calatayud A., Barreno E.. Response to ozone in two lettuce varieties on chlorophyll a fluorescence, photosynthetic pigments and lipid peroxidation.  Plant Physiology and Biochemistry. (2004);  42 549-555
    CrossrefPubMedGoogle Scholar
  • 5 Calatayud A., Iglesias D. J., Talon M., Barreno E.. Effects of 2-month ozone exposure in spinach leaves on photosynthesis, antioxidant systems and lipid peroxidation.  Plant Physiology and Biochemistry. (2003);  41 839-845
    CrossrefPubMedGoogle Scholar
  • 6 Dizengremel P.. Effects of ozone on the carbon metabolism of forest trees.  Plant Physiology and Biochemistry. (2001);  39 729-742
    CrossrefPubMedGoogle Scholar
  • 7 Drouet J.-L., Pages L., Serra V.. Dynamics of leaf mass per unit leaf area and root mass per unit root volume of young maize plants: implications for growth models.  European Journal of Agronomy. (2005);  22 185-193
    CrossrefPubMedGoogle Scholar
  • 8 Eckardt N. A., Pell E. J.. Oxidative modification of rubisco from potato foliage in response to ozone.  Plant Physiology and Biochemistry. (1995);  33 273-282
    PubMedGoogle Scholar
  • 9 El-Khatib A. A.. The response of some common Egyptian plants to ozone and their use as biomonitors.  Environmental Pollution. (2003);  124 419-428
    CrossrefPubMedGoogle Scholar
  • 10 Enyedi A., Eckardt N. A., Pell E. J.. Activity of ribulose bisphosphate carboxylase/oxygenase from potato cultivars with differential response to ozone stress.  New Phytologist. (1992);  122 493-500
    CrossrefPubMedGoogle Scholar
  • 11 Fontaine V., Pelloux J., Podor M., Afif D., Gérant D., Grieu P., Dizengremel P.. Carbon fixation in Pinus halepensis submitted to ozone. Opposite reponse of ribulose-1,5-bisphosphate carboxylase/oxygenase and phosphoenolpyruvate carboxylase.  Physiologia Plantarum. (1999);  1054 187-192
    PubMedGoogle Scholar
  • 12 Fournier C., Andrieu B.. Dynamics of the elongation of internodes in maize (Zea mays L.): analysis of phases of elongation and their relationships to phytomer development.  Annals of Botany. (2000);  86 551-563
    CrossrefPubMedGoogle Scholar
  • 13 Fukayama H., Hatch M. D., Tamai T., Tsuchida H., Sudoh S., Furbank R. T., Miyao M.. Activity regulation and physiological impacts of maize C4-specific phosphoenolpyruvate carboxylase overproduced in transgenic rice plants.  Photosynthesis Research. (2003);  77 227-239
    CrossrefPubMedGoogle Scholar
  • 14 Grünhage L., Jäger H. J., Haenel H. D., Löpmeier F. J., Hanewald K.. The European critical levels for ozone: improving their usage.  Environmental Pollution. (1999);  105 163-173
    CrossrefPubMedGoogle Scholar
  • 15 Heagle A. S.. Ozone and crop yield.  Annual Review of Phytopathology. (1989);  27 397-423
    PubMedGoogle Scholar
  • 16 Heath R. L., Taylor T. G. E.. Physiological and plant responses to ozone exposure. Sandermann, H., Wellburn, A. R., and Heath, R. L., eds. Forest Decline and Ozone. Berlin; Springer-Verlag (1997): 317-398
    Google Scholar
  • 17 Hegedüs A., Erdei S., Horváth G.. Comparative studies of H2O2 detoxifying enzymes in green and greening barley seedlings under cadmium stress.  Plant Science. (2001);  160 1085-1093
    CrossrefPubMedGoogle Scholar
  • 18 Hegedüs A., Erdei S., Janda T., Tóth E., Horváth G., Dudits D.. Transgenic tobacco plants overproducing alfalfa aldose/aldehyde reductase show higher tolerance to low temperature and cadmium stress.  Plant Science. (2004);  166 1329-1333
    CrossrefPubMedGoogle Scholar
  • 19 Herbinger K., Tausz M., Wonisch A., Soja G., Sorger A., Grill D.. Complex interactive effects of drought and ozone stress on the antioxidant defence systems of two wheat cultivars.  Plant Physiology and Biochemistry. (2002);  40 691-696
    CrossrefPubMedGoogle Scholar
  • 20 Junqua M., Biolley J. P., Pié S., Kanoun M., Duran R., Goulas P.. In vivo occurrence of carbonyl residues in Phaseolus vulgaris proteins as a direct consequence of a chronic ozone stress.  Plant Physiology and Biochemistry. (2000);  38 853-861
    CrossrefPubMedGoogle Scholar
  • 21 Kanoun M., Goulas P., Bassères A., Biolley J. P.. Ozone-induced oxidation of Rubisco: from an ELISA quantification of carbonyls to putative pathways leading to oxidizing mechanisms.  Functional Plant Biology. (2002);  29 1357-1363
    CrossrefPubMedGoogle Scholar
  • 22 Karenlampi L., Skarby L.. Critical Levels for Ozone in Europe: Testing and Finalizing the Concepts. Kuopio; University of Kuopio, Department of Ecology and Environmental Science (1996)
    Google Scholar
  • 23 Kingston-Smith A. H., Foyer C. H.. Bundle sheath proteins are more sensitive to oxidative damage than those of the mesophyll in maize leaves exposed to paraquat or low temperatures.  Journal of Experimental Botany. (2000);  51 123-130
    CrossrefPubMedGoogle Scholar
  • 24 Kingston-Smith A. H., Harbinson J., Williams J., Foyer C. H.. Effect of chilling on carbon assimilation, enzyme activation, and photosynthetic electron transport in the absence of photoinhibition in maize leave.  Plant Physiology. (1997);  114 1039-1046
    PubMedGoogle Scholar
  • 25 Kiniry J.-L., Bonhomme R.. Predicting maize phenology. Hodges, T., ed. Predicting Crop Phenology. Boca Raton; CRC Press (1991): 115-132
    Google Scholar
  • 26 Krupa S. V., Manning W. J.. Atmospheric ozone: formation and effects on vegetation.  Environmental Pollution. (1988);  50 101-137
    CrossrefPubMedGoogle Scholar
  • 27 Lamb C. J., Dixon R. A.. The oxidative burst in plant disease resistance.  Molecular Biology. (1997);  48 251-275
    PubMedGoogle Scholar
  • 28 Le Thiec D., Manninen S.. Ozone and water deficit reduced growth of Aleppo pine seedlings.  Plant Physiology and Biochemistry. (2003);  41 55-63
    CrossrefPubMedGoogle Scholar
  • 29 Leegood R. C.. C4 photosynthesis: principles of CO2 concentration and prospects for its introduction into C3 plants.  Journal of Experimental Botany. (2002);  53 581-590
    CrossrefPubMedGoogle Scholar
  • 30 Leitao L., Goulas P., Biolley J.-P.. Time-course of Rubisco oxidation in beans (Phaseolus vulgaris L.) subjected to a long-term ozone stress.  Plant Science. (2003);  165 613-620
    CrossrefPubMedGoogle Scholar
  • 31 Lichtenthaler H. K.. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes.  Methods in Enzymology. (1987);  148 350-382
    PubMedGoogle Scholar
  • 32 Matile P., Hörtensteiner S., Thomas H.. Chlorophyll degradation.  Annual Review of Plant Physiology and Plant Molecular Biology. (1999);  50 67-95
    PubMedGoogle Scholar
  • 33 Miller J. E.. Effects on photosynthesis, carbon allocation and plant growth associated with air pollutant stress. Heck, W. W., Taylor, O. C., and Tingey, D. T., eds. Assessment of Crop Loss from Air Pollutants. London, New York; Elsevier Applied Science (1988): 287-314
    Google Scholar
  • 34 Morales A., Ortega-Delgado M. L., Molina-Galan J., Sanchez de Jiménez E.. Importance of Rubisco activase in maize productivity based on mass selection procedure.  Journal of Experimental Botany. (1999);  50 823-829
    CrossrefPubMedGoogle Scholar
  • 35 Munné-Bosch S., Alegre L.. Die and let live: leaf senescence contributes to plant survival under drought stress.  Functional Plant Biology. (2004);  31 203-216
    CrossrefPubMedGoogle Scholar
  • 36 Nyachiro J. M., Briggs K. G., Hoddinott J., Johnson-Flanagan A. M.. Chlorophyll content, chlorophyll fluorescence and water deficit in spring wheat.  Cereal Research Communications. (2001);  29 135-142
    PubMedGoogle Scholar
  • 37 Ojanperä K., Pätsikkä E., Yläranta T.. Effects of low ozone exposure of spring wheat on net CO2 uptake, Rubisco, leaf senescence and grain filling.  New Phytologist. (1997);  138 451-460
    PubMedGoogle Scholar
  • 38 Pauls K. P., Thompson J. E.. Effects of in vitro treatment with ozone on the physical and chemical properties of membranes.  Physiologia Plantarum. (1981);  53 255-262
    CrossrefPubMedGoogle Scholar
  • 39 Pell E. J., Eckardt N. A., Enyedi A. J.. Timing of ozone stress and resulting status of ribulose bisphosphate carboxylase/oxygenase and associated net photosynthesis.  New Phytologist. (1992);  120 397-405
    CrossrefPubMedGoogle Scholar
  • 40 Pell E. J., Schlagnhaufer C. D., Arteca R. N.. Ozone-induced oxidative stress: mechanisms of action and reaction.  Physiologia Plantarum. (1997);  100 264-273
    CrossrefPubMedGoogle Scholar
  • 41 Pell E. J., Sinn J. P., Brendley B. W., Samuelson L., Vinten-Johansen C., Tien M., Skillman J.. Differential reponse of four tree species to ozone-induced acceleration of foliar senescence.  Plant, Cell and Environment. (1999);  22 779-790
    CrossrefPubMedGoogle Scholar
  • 42 Pelloux J., Jolivet Y., Fontaine V., Banvoy J., Dizengremel P.. Changes in Rubisco and Rubisco activase gene expression and polypeptide content in Pinus halepensis Mill. subjected to ozone and drought.  Plant, Cell and Environment. (2001);  24 123-132
    CrossrefPubMedGoogle Scholar
  • 43 Pino M. E., Mudd J. B., Bailey-Serres J.. Ozone-induced alterations in the accumulation of newly synthesized proteins in leaves of maize.  Plant Physiology. (1995);  108 777-785
    PubMedGoogle Scholar
  • 44 Reid C. D., Tissue D. T., Fiscus E. L., Strain B. R.. Comparison of spectrophotometric and radioisotopic methods for the assay of Rubisco in ozone-treated plants.  Physiologia Plantarum. (1997);  101 398-404
    CrossrefPubMedGoogle Scholar
  • 45 Ribas A., Penuelas J., Elvira S., Gimeno B. S.. Ozone exposure induces the activation of leaf senescence-related processes and morphological and growth changes in seedlings of Mediterranean tree species.  Environmental Pollution. (2005);  134 291-300
    CrossrefPubMedGoogle Scholar
  • 46 Robinson D. C., Wellburn A. R.. Seasonal changes in the pigments of Norway spruce, Picea abies (L.) Karst. and the influence of summer ozone exposure.  New Phytologist. (1991);  119 251-259
    CrossrefPubMedGoogle Scholar
  • 47 Ruzsa S. M., Mylona P., Scandalios J. G.. Differential response of antioxidant genes in maize leaves exposed to ozone.  Redox Report. (1999);  4 95-103
    CrossrefPubMedGoogle Scholar
  • 48 Sandermann H.. Active oxygen species as mediators of plant immunity: three case studies.  Biological Chemistry. (2000);  381 649-653
    CrossrefPubMedGoogle Scholar
  • 49 Sanderson J. B., Daynard T. B., Tollenaar M.. A mathematical model of the shape of corn leaves.  Canadian Journal of Plant Science. (1981);  61 1009-1011
    PubMedGoogle Scholar
  • 50 Schraudner M., Moeder H., Wiese W., Van Camp W., Inzé D., Langebartels C., Sandermann H. J.. Ozone-induced oxidative burst in the ozone biomonitor plant, tobacco Bel W3.  The Plant Journal. (1998);  16 235-245
    CrossrefPubMedGoogle Scholar
  • 51 Sokal R. R., Rohlf F. J.. Biometry: The Principles and Practice of Statistics in Biological Research, 3rd ed. New York; W. H. Freeman and Company (2001): 887 p
    Google Scholar
  • 52 Stockwell W. R., Kirchner F., Kuhn M., Seefeld S.. A new mechanism for regional atmospheric chemistry modeling.  Journal of Geophysical Research-Atmospheres. (1997);  102 25847-25879
    PubMedGoogle Scholar
  • 53 Sugiyama T., Mizuno M., Hayashi M.. Partitioning of nitrogen among ribulose-1,5-bisphosphate carboxylase/oxygenase, phosphoenolpyruvate carboxylase, and pyruvate orthophosphate dikinase as related to biomass productivity in maize seedlings.  Plant Physiology. (1984);  75 665-669
    PubMedGoogle Scholar
  • 54 Tamaoki M., Nakajima N., Kubo A., Aono M., Matsuyama T., Saji H.. Transcriptome analysis of O3-exposed Arabidopsis reveals that multiple signal pathways act mutually antagonistically to induce gene expression.  Plant Molecular Biology. (2003);  53 443-456
    CrossrefPubMedGoogle Scholar
  • 55 Thomas H.. Chlorophyll: a symptom and a regulator of plastid development.  New Phytologist. (1997);  136 163-181
    CrossrefPubMedGoogle Scholar
  • 56 Ueno Y., Imanari E., Emura J., Yoshizawa-Kumagaye K., Nakajima K., Inami K., Shiba T., Sakakibara H., Sugiyama T., Izui K.. Immunological analysis of the phosphorylation state of maize C4-form phosphoenolpyruvate carboxylase with specific antibodies raised against a synthetic phosphorylated peptide.  The Plant Journal. (2000);  21 17-26
    CrossrefPubMedGoogle Scholar
  • 57 Von Caemmerer S., Furbank R. T.. The C4 pathway: an efficient CO2 pump.  Photosynthesis Research. (2003);  77 191-207
    CrossrefPubMedGoogle Scholar
  • 58 Voznesenskaya E. V., Franceschi V. R., Kiirats O., Freitag H., Edwards G. E.. Kranz anatomy is not essential for terrestrial C4 photosynthesis.  Nature. (2001);  414 543-546
    CrossrefPubMedGoogle Scholar

J.-P. Biolley

Laboratoire d'Ecologie Moléculaire - IBEAS - EA3525
Université de Pau et des Pays de l'Adour

Avenue de l'Université

BP 1155

64013 Pau Cedex

France

Email: jean-philippe.biolley@univ-pau.fr

Editor: J. T. M. Elzenga

      >