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The Use of OJIP Fluorescence Transients to Monitor the Effect of Elevated Ozone on Biomass of Canola Plants

  • Bheki G. MalibaEmail author
  • Prabhu M. Inbaraj
  • Jacques M. Berner
Article
  • 92 Downloads

Abstract

The effects of elevated ozone (O3) levels (80 ppb and 120 ppb) on photosynthetic efficiency and growth of canola plants were studied in open-top chambers. The chlorophyll a polyphasic fluorescence rise kinetics OJIP, stomatal conductance and Chlorophyll Content Index (CCI) were measured after 15 and 30 days of O3 fumigation, as well as in control plants; biomass measurements were done only after 30 days with and without fumigation. Analysis of the OJIP kinetics by the JIP-test led to the calculation of several photosynthetic parameters and the total Performance Index (PItotal). The decline of PItotal under the 80 ppb O3 treatment was due to a lower density of reaction centres (RC/ABS), while the notable decline under the 120 ppb treatment was found to be due both to a further decline of RC/ABS and to a pronounced lowering of the efficiency with which an electron can move from the reduced intersystem electron acceptors to the PSI end acceptors (δRo). Stomatal conductance was affected by both treatments. Biomass was found to be affected by O3 fumigation (for 30 days), decreasing by 40% at 80 ppb and by more than 70% under 120 ppb. Our findings indicate that biomass decline is due both to the lowering of CCI and the lowering of photosynthetic efficiency parameters. They thus suggest that two simple, non-invasive and rapid methods, namely, the analysis of OJIP fluorescence transients and the measurement of CCI, can be used to screen the effect of elevated O3 on biomass of canola plants.

Keywords

Biomass Canola Chlorophyll a fluorescence JIP-test Open-top chamber Ozone 

Abbreviations

ABS

Absorption (proportional to chlorophyll)

Chl

Chlorophyll

CCI

Chlorophyll Content Index

OTC

Open-top chamber

RCs

Reaction centres

PItotal

Total Performance Index

PSII

Photosystem II

PSI

Photosystem I

Notes

Acknowledgments

Acknowledgements are due to Dr. Merope Tsimilli-Michael (Cyprus) for her helpful of explanations concerning the concepts, application and interpretation of the JIP test and Prof. Suria Ellis (North-West University) for her kind assistance with regard to statistical analysis.

Funding Information

This study was supported by the Cuomo foundation through the partnership with the Intergovernmental Panel on Climate Change (IPCC) scholarship programme and by the Applied Centre for Climate and Earth Systems Science (ACCESS).

Compliance with Ethical Standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Disclaimer

The contents of this paper are solely the liability of the authors and under no circumstances may be considered as a reflection of the Cuomo Foundation, IPCC and/or ACCESS.

References

  1. Ainsworth, E. A., Yendrek, C. R., Sitch, S., Collins, W. J., & Emberson, L. D. (2012). The effects of tropospheric ozone on net primary productivity and implications for climate change. Annual Review of Plant Biology, 63, 637–661.CrossRefGoogle Scholar
  2. Avnery, S., Mauzerall, D. L., Liu, J., & Horowitz, L. W. (2011). Global crop yield reductions due to surface ozone exposure: 2. Year 2030 potential crop production losses and economic damage under two scenarios of O3 pollution. Atmospheric Environment, 45(13), 2297–2309.CrossRefGoogle Scholar
  3. Bagard, M., Jolivet, Y., Hasenfratz-Sauder, M. P., Gérard, J., Dizengremel, P., & Le Thiec, D. (2015). Ozone exposure and flux-based response functions for photosynthetic traits in wheat, maize and poplar. Environmental Pollution, 206, 411–420.CrossRefGoogle Scholar
  4. Bindi, M., Hacour, A., Vandermeiren, K., Craigon, J., Ojanperä, K., Selldén, G., Högy, P., Finnan, J., & Fibbi, L. (2002). Chlorophyll concentration of potatoes grown under elevated carbon dioxide and/or ozone concentrations. European Journal of Agronomy, 17(4), 319–335.CrossRefGoogle Scholar
  5. Black, V. J., Black, C. R., Roberts, J. A., & Stewart, C. A. (2000). Impact of ozone on the reproductive development of plants. The New Phytologist, 147(3), 421–447.CrossRefGoogle Scholar
  6. Booker, F., Muntifering, R., Mcgrath, M., Burkey, K., Decoteau, D., Fiscus, E., Manning, W., Krupa, S., Chappelka, A., & Grantz, D. (2009). The ozone component of global change: potential effects on agricultural and horticultural plant yield, product quality and interactions with invasive species. Journal of Integrative Plant Biology, 51(4), 337–351.CrossRefGoogle Scholar
  7. Bussotti, F., Strasser, R. J., & Schaub, M. (2007). Photosynthetic behavior of woody species under high ozone exposure probed with the JIP-test: a review. Environmental Pollution, 147(3), 430–437.CrossRefGoogle Scholar
  8. Bussotti, F., Desotgiu, R., Cascio, C., Pollastrini, M., Gravano, E., Gerosa, G., Marzuoli, R., Nali, C., Lorenzini, G., Salvatori, E., & Manes, F. (2011). Ozone stress in woody plants assessed with chlorophyll a fluorescence. A critical reassessment of existing data. Environmental and Experimental Botany, 73, 19–30.CrossRefGoogle Scholar
  9. Calatayud, V., Cerveró, J., & Sanz, M. J. (2007). Foliar, physiologial and growth responses of four maple species exposed to ozone. Water, Air and Soil Pollution, 185(1–4), 239–254.CrossRefGoogle Scholar
  10. Cho, K., Tiwari, S., Agrawal, S. B., Torres, N. L., Agrawal, M., Sarkar, A., Shibato, J., Agrawal, G. K., Kubo, A., & Rakwal, R. (2011). Tropospheric ozone and plants: absorption, responses, and consequences. Reviews of Environmental Contamination and Toxicology Volume, 212, 61–111.Google Scholar
  11. Clark, A. J., Landolt, W., Bucher, J. B., & Strasser, R. J. (2000). Beech (Fagus sylvatica) response to ozone exposure assessed with a chlorophyll a fluorescence performance index. Environmental Pollution, 109(3), 501–507.CrossRefGoogle Scholar
  12. Clausen, S. K., Frenck, G., Linden, L. G., Mikkelsen, T. N., Lunde, C., & Jørgensen, R. B. (2011). Effects of single and multifactor treatments with elevated temperature, CO2 and ozone on oilseed rape and barley. Journal of Agronomy and Crop Science, 197(6), 442–453.CrossRefGoogle Scholar
  13. Desotgiu, R., Bussotti, F., Faoro, F., Iriti, M., Agati, G., Marzuoli, R. I., Gerosa, G., & Tani, C. (2010). Early events in Populus hybrid and Fagus sylvatica leaves exposed to ozone. The Scientific World Journal, 10, 512–527.CrossRefGoogle Scholar
  14. Desotgiu, R., Pollastrini, M., Cascio, C., Gerosa, G., Marzuoli, R., & Bussotti, F. (2012). Chlorophyll a fluorescence analysis along a vertical gradient of the crown in a poplar (Oxford clone) subjected to ozone and water stress. Tree Physiology, 32(8), 976–986.CrossRefGoogle Scholar
  15. Desotgiu, R., Pollastrini, M., Cascio, C., Gerosa, G., Marzuoli, R. I., & Bussotti, F. (2013). Responses to ozone on Populus “Oxford” clone in an open top chamber experiment assessed before sunrise and in full sunlight. Photosynthetica, 51(2), 267–280.CrossRefGoogle Scholar
  16. Digrado, A., Bachy, A., Mozaffar, A., Schoon, N., Bussotti, F., Amelynck, C., Dalcq, A. C., Fauconnier, M. L., Aubinet, M., Heinesch, B., & du Jardin, P. (2017). Long-term measurements of chlorophyll a fluorescence using the JIP-test show that combined abiotic stresses influence the photosynthetic performance of the perennial ryegrass (Lolium perenne) in a managed temperate grassland. Physiologia Plantarum, 161(3), 355–371.CrossRefGoogle Scholar
  17. Felzer, B. S., Cronin, T., Reilly, J. M., Melillo, J. M., & Wang, X. (2007). Impacts of ozone on trees and crops. Comptes Rendus Geoscience, 339(11–12), 784–798.CrossRefGoogle Scholar
  18. Feng, Z., Kobayashi, K., & Ainsworth, E. A. (2008). Impact of elevated ozone concentration on growth, physiology, and yield of wheat (Triticum aestivum L.): a meta-analysis. Global Change Biology, 14(11), 2696–2708.Google Scholar
  19. Fiscus, E. L., Booker, F. L., & Burkey, K. O. (2005). Crop responses to ozone: uptake, modes of action, carbon assimilation and partitioning. Plant, Cell and Environment, 28(8), 997–1011.CrossRefGoogle Scholar
  20. Frenck, G., van der Linden, L., Mikkelsen, T. N., Brix, H., & Jørgensen, R. B. (2011). Increased [CO2] does not compensate for negative effects on yield caused by higher temperature and [O3] in Brassica napus L. European Journal of Agronomy, 35(3), 127–134.CrossRefGoogle Scholar
  21. Fuhrer, J., & Bungener, P. (1999). Effects of air pollutants on plants. Analusis, 27(4), 355–362.CrossRefGoogle Scholar
  22. Fuhrer, J., Skärby, L., & Ashmore, M. R. (1997). Critical levels for ozone effects on vegetation in Europe. Environmental Pollution, 97(1–2), 91–106.CrossRefGoogle Scholar
  23. Heyneke, E., Smit, P. R., Van Rensburg, L., & Krüger, G. H. J. (2012). Open-top chambers to study air pollution impacts in South Africa. Part I: microclimate in open-top chambers. South African Journal of Plant and Soil, 29(1), 1–7.CrossRefGoogle Scholar
  24. Huang, M., Ai, H., Xu, X., Chen, K., Niu, H., Zhu, H., Sun, J., Du, D., & Chen, L. (2018). Nitric oxide alleviates toxicity of hexavalent chromium on tall fescue and improves performance of photosystem II. Ecotoxicology and Environmental Safety, 164, 32–40.CrossRefGoogle Scholar
  25. Kalaji, H.M., Jajoo, A., Oukarroum, A., Brestic, M., Zivcak, M., Samborska, I.A., Cetner, M.D., Łukasik, I., Goltsev, V., Ladle, R.J., & Dąbrowski, P. (2014). The use of chlorophyll fluorescence kinetics analysis to study the performance of photosynthetic machinery in plants. In: P. Ahmad (Ed.), Emerging technologies and management of crop stress tolerance (pp. 347–384). Elsevier Academic Press.Google Scholar
  26. Kalaji, H. M., Jajoo, A., Oukarroum, A., Brestic, M., Zivcak, M., Samborska, I. A., Cetner, M. D., Łukasik, I., Goltsev, V., & Ladle, R. J. (2016). Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiologiae Plantarum, 38(4), 102.CrossRefGoogle Scholar
  27. Kalaji, H. M., Rastogi, A., Živčák, M., Brestic, M., Daszkowska-Golec, A., Sitko, K., Alsharafa, K. Y., Lotfi, R., Stypiński, P., Samborska, I. A., & Cetner, M. D. (2018). Prompt chlorophyll fluorescence as a tool for crop phenotyping: an example of barley landraces exposed to various abiotic stress factors. Photosynthetica, 56(3), 953–961.CrossRefGoogle Scholar
  28. Kleier, C., Farnsworth, B., & Winner, W. (1998). Biomass, reproductive output, and physiological responses of rapid-cycling Brassica (Brassica rapa) to ozone and modified root temperature. The New Phytologist, 139(4), 657–664.CrossRefGoogle Scholar
  29. Laakso, L., Beukes, J. P., Van Zyl, P. G., Pienaar, J. J., Josipovic, M., Venter, A., Jaars, K., Vakkari, V., Labuschagne, C., Chiloane, K., & Tuovinen, J. P. (2013). Ozone concentrations and their potential impacts on vegetation in Southern Africa. Developments in Environmental Science, 13, 429–450.CrossRefGoogle Scholar
  30. Mills, G., & Harmens, H. 2011. Ozone pollution: a hidden threat to food security. Programme Coordination Centre for the ICP Vegetation, Centre for Ecology and Hydrology, Bangor.Google Scholar
  31. Monga, R., Marzuoli, R., Alonso, R., Bermejo, V., González-Fernández, I., Faoro, F., & Gerosa, G. (2015). Varietal screening of ozone sensitivity in Mediterranean durum wheat (Triticum durum, Desf.). Atmospheric Environment, 110, 18–26.CrossRefGoogle Scholar
  32. Morgan, P. B., Ainsworth, E. A., & Long, S. P. (2003). How does elevated ozone impact soybean? A meta-analysis of photosynthesis, growth and yield. Plant, Cell and Environment, 26(8), 1317–1328.CrossRefGoogle Scholar
  33. Morgan, P. B., Mies, T. A., Bollero, G. A., Nelson, R. L., & Long, S. P. (2006). Season-long elevation of ozone concentration to projected 2050 levels under fully open-air conditions substantially decreases the growth and production of soybean. New Phytologist, 170(2), 333–343.CrossRefGoogle Scholar
  34. Ollerenshaw, J. H., Lyons, T., & Barnes, J. D. (1999). Impacts of ozone on the growth and yield of field-grown winter oilseed rape. Environmental Pollution, 104(1), 53–59.CrossRefGoogle Scholar
  35. Oukarroum, A., El Madidi, S., Schansker, G., & Strasser, R. J. (2007). Probing the responses of barley cultivars (Hordeum vulgare L.) by chlorophyll a fluorescence OLKJIP under drought stress and re-watering. Environmental and Experimental Botany, 60(3), 438–446.CrossRefGoogle Scholar
  36. Perboni, A., Cassol, D., Silva, F., Silva, D., & Bacarin, M. (2012). Chlorophyll a fluorescence study revealing effects of flooding in canola hybrids. Biologia, 67(2), 338–346.CrossRefGoogle Scholar
  37. Pollastrini, M., Desotgiu, R., Cascio, C., Bussotti, F., Cherubini, P., Saurer, M., Gerosa, G., & Marzuoli, R. (2010). Growth and physiological responses to ozone and mild drought stress of tree species with different ecological requirements. Trees, 24(4), 695–704.CrossRefGoogle Scholar
  38. Porter, J. R., Xie, L., Challinor, A. J., Cochrane, K., Howden, S. M., Iqbal, M. M., Lobell, D. B., & Travasso, M. I. (2014). Food security and food production systems. In C. B. Field, V. R. Barros, D. J. Dokken, K. J. Mach, M. D. Mastrandrea, T. E. Bilir, M. Chatterjee, K. L. Ebi, Y. O. Estrada, R. C. Genova, B. Girma, E. S. Kissel, A. N. Levy, S. MacCracken, P. R. Mastrandrea, & L. L. White (Eds.), Climate change 2014: impacts, adaptation, and vulnerability. Part A: global and sectoral aspects. Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change (pp. 485–533). United Kingdom: Cambridge University Press.Google Scholar
  39. Pšidová, E., Živčák, M., Stojnić, S., Orlović, S., Gömöry, D., Kučerová, J., Ditmarová, Ľ., Střelcová, K., Brestič, M., & Kalaji, H. M. (2018). Altitude of origin influences the responses of PSII photochemistry to heat waves in European beech (Fagus sylvatica L.). Environmental and Experimental Botany, 152, 97–106.CrossRefGoogle Scholar
  40. Rastogi, A., ZIVCAK, M., Tripathi, D.K., Yadav, S., Kalaji, H.M., & Brestic, M. (2019). Phytotoxic effect of silver nanoparticles in Triticum aestivum: improper regulation of photosystem I activity as the reason for oxidative damage in the chloroplast. Photosynthetica, 57. In press.Google Scholar
  41. Salvatori, E., Fusaro, L., Mereu, S., Bernardini, A., Puppi, G., & Manes, F. (2013). Different O3 response of sensitive and resistant snap bean genotypes (Phaseolus vulgaris L.): the key role of growth stage, stomatal conductance, and PSI activity. Environmental and Experimental Botany, 87, 79–91.CrossRefGoogle Scholar
  42. Schansker, G., Tóth, S. Z., & Strasser, R. J. (2005). Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1706(3), 250–261.CrossRefGoogle Scholar
  43. Scholes, R. J., & Scholes, M. C. (1998). Natural and human-related sources of ozone-forming trace gases in southern Africa. South African Journal of Science, 94, 422–425.Google Scholar
  44. Strasser, R. J., Tsimilli-Michael, M., & Srivastava, A. (2004). Analysis of the chlorophyll a fluorescence transient. In G. C. Papageorgiou & Govindjee (Eds.), Chlorophyll fluorescence: a signature of photosynthesis (pp. 321–362). The Netherlands: Kluwer Academic Publishers.CrossRefGoogle Scholar
  45. Strasser, R. J., Tsimilli-Michael, M., Dangre, D., & Rai, M. (2007). Biophysical phenomics reveals functional building blocks of plants systems biology: a case study for the evaluation of the impact of mycorrhization with Piriformospora indica. In A. Varma & R. Oelmüller (Eds.), Advanced techniques in soil microbiology (pp. 319–342). Berlin: Springer.CrossRefGoogle Scholar
  46. Strasser, R. J., Tsimilli-Michael, M., Qiang, S., & Goltsev, V. (2010). Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1797(6–7), 1313–1326.CrossRefGoogle Scholar
  47. Strauss, A. J., Krüger, G. H. J., Strasser, R. J., & Van Heerden, P. D. R. (2006). Ranking of dark chilling tolerance in soybean genotypes probed by the chlorophyll a fluorescence transient OJIP. Environmental and Experimental Botany, 56(2), 147–157.CrossRefGoogle Scholar
  48. The Royal Society. (2008). Ground-level ozone in the 21st century: future trends, impacts and policy implications. Science Policy Report 15/08. London: The Royal Society.Google Scholar
  49. Tsimilli-Michael, M., & Strasser, R. J. (2001). Fingerprints for climate changes on the behaviour of the photosynthetic apparatus, monitored by the JIP-test. A case study on light and heat stress adaptation of the symbionts of temperate and coral reef foraminifers in hospite. In G.-R. Walther, C. A. Burga, & P. J. Edwards (Eds.), “Fingerprints” of climate changes–adapted behaviour and shifting species ranges (pp. 229–247). New York: Kluwer Academic Publishers.CrossRefGoogle Scholar
  50. Tsimilli-Michael, M., & Strasser, R. J. (2008). In vivo assessment of stress impact on plant’s vitality: applications in detecting and evaluating the beneficial role of mycorrhization on host plants. In mycorrhiza. In A. Varma (Ed.), Mycorrhiza: state of the art, genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics (pp. 679–670). Berlin: Springer.CrossRefGoogle Scholar
  51. Tsimilli-Michael, M., & Strasser, R. J. (2013). Biophysical phenomics: evaluation of the impact of mycorrhization with Piriformospora indica. In A. Varma, G. Kost, & R. Oelmüller (Eds.), Piriformospora indica. Soil biology 33 (pp. 173–189). Berlin: Springer.CrossRefGoogle Scholar
  52. Van Dingenen, R., Dentener, F. J., Raes, F., Krol, M. C., Emberson, L., & Cofala, J. (2009). The global impact of ozone on agricultural crop yields under current and future air quality legislation. Atmospheric Environment, 43(3), 604–618.CrossRefGoogle Scholar
  53. Van Tienhoven, A. M., Otter, L., Lenkopane, M., Venjonoka, K., & Zunckel, M. (2005). Assessment of ozone impacts on vegetation in southern Africa and directions for future research: commentary. South African Journal of Science, 101(3–4), 143–148.Google Scholar
  54. Wittig, V. E., Ainsworth, E. A., Naidu, S. L., Karnosky, D. F., & Long, S. P. (2009). Quantifying the impact of current and future tropospheric ozone on tree biomass, growth, physiology and biochemistry: a quantitative meta–analysis. Global Change Biology, 15(2), 396–424.CrossRefGoogle Scholar
  55. Yusuf, M. A., Kumar, D., Rajwanshi, R., Strasser, R. J., Tsimilli-Michael, M., & Sarin, N. B. (2010). Overexpression of γ-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: physiological and chlorophyll a fluorescence measurements. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1797(8), 1428–1438.CrossRefGoogle Scholar
  56. Zivcak, M., Brestic, M., Kunderlikova, K., Olsovska, K., & Allakhverdiev, S. I. (2015). Effect of photosystem I inactivation on chlorophyll a fluorescence induction in wheat leaves: does activity of photosystem I play any role in OJIP rise? Journal of Photochemistry and Photobiology B: Biology, 152, 318–324.CrossRefGoogle Scholar
  57. Zunckel, M., Venjonoka, K., Pienaar, J. J., Brunke, E. G., Pretorius, O., Koosialee, A., Raghunandan, A., & Van Tienhoven, A. M. (2004). Surface ozone over southern Africa: synthesis of monitoring results during the Cross border Air Pollution Impact Assessment project. Atmospheric Environment, 38(36), 6139–6147.CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Unit for Environmental Sciences and ManagementNorth-West UniversityPotchefstroomSouth Africa
  2. 2.Eskom Research, Testing and DevelopmentClevelandSouth Africa
  3. 3.Department of Chemistry, School of Basic SciencesManipal University JaipurJaipurIndia

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