Photosynthetica 2014, 52(4):604-613 | DOI: 10.1007/s11099-014-0070-5

Photosynthesis of ozone-sensitive and -resistant Phaseolus vulgaris genotypes under ambient ozone and moderate heat stress

V. Villányi1, Z. Ürmös1, B. Turk2, F. Batič2, Z. Csintalan1,*
1 Institute of Botany and Ecophysiology, Szent István University, Gödöllő, Hungary
2 Department of Agronomy, University of Ljubljana, Ljubljana, Slovenia

Physiological responses from sensitive (S156) and resistant (R123) genotypes of ozone bioindicator, snap bean, were investigated after exposing the plants to cumulative, phytotoxic ozone amounts. Daily course of gas-exchange parameters showed delayed stomatal response in S156 leaves to environmental changes comparing to the response of R123 leaves. Potential photosynthetic quantum conversion, Stern-Volmer nonphotochemical quenching (NPQ), and maximum photochemical efficiency of PSII (Fv/Fm) values changed differently in the two genotypes between the first and last measuring days. We concluded that the higher ozone sensitivity originated at least partly from inferior regenerating and/or antioxidant capacity. Experimental protocol proved to be determinant on chlorophyll fluorescence parameters: Fv/Fm and NPQ declined at midday, and only the sensitive leaves showed a slight increase in NPQ between 12 h and 16 h. We explained these results by moderately high temperatures and shade-adapted state of our experimental plants under substantial ozone stress. On the base of temperature dependence of minimal fluorescence yield (F0), critical temperature proved to be higher than 32.7°C for Phaseolus vulgaris under these conditions. We found a strong linear correlation between NPQ and nonphotochemical quenching of F0, indicating that NPQ was determined mostly by energy-dependent quenching (qE). The qE is the light-harvesting complex located component of NPQ and depends on the amount of zeaxanthin molecules bound in PSII proteins. Thus, difference between daily courses of NPQ in the two genotypes was probably due to different ways of utilization of the zeaxanthin pool under the interactive effect of ozone and moderate heat stress.

Keywords: AOT40; chlorophyll fluorescence; gas exchange; midday depression; nonphotochemical quenching; ozone sensitivity; snap bean; shaded conditions

Received: July 16, 2013; Accepted: April 18, 2014; Published: December 1, 2014Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Villányi, V., Ürmös, Z., Turk, B., Batič, F., & Csintalan, Z. (2014). Photosynthesis of ozone-sensitive and -resistant Phaseolus vulgaris genotypes under ambient ozone and moderate heat stress. Photosynthetica, 52(4), 604-613. doi: 10.1007/s11099-014-0070-5.
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)

    • Open full article

    References

    1. Apel, K., Hirt, H.: Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. - Annu. Rev. Plant Biol. 55: 373-399, 2004. Go to original source...
    2. Armond, P.A., Bjorkman, O., Staehelin, L.A.: Dissociation of supramolecular complexes in chloroplast membranes - a manifestation of heat damage to the photosynthetic apparatus. - Biochim. Biophys. Acta 601: 433-442, 1980. Go to original source...
    3. Balaguer, L., Pugnaire, F.I., Martinez-Ferri, E. et al.: Ecophysiological significance of chlorophyll loss and reduced photochemical efficiency under extreme aridity in Stipa tenacissima L. - Plant Soil 240: 343-352, 2002. Go to original source...
    4. Bilger, H.W., Schreiber, U., Lange, O.L.: Determination of leaf heat-resistance - comparative investigation of chlorophyll fluorescence changes and tissue necrosis methods. - Oecologia 63: 256-262, 1984. Go to original source...
    5. Burkey, K.O., Booker, F.L., Ainsworth, E.A., Nelson, R.L.: Field assessment of a snap bean ozone bioindicator system under elevated ozone and carbon dioxide in a free air system. - Environ. Pollut. 166: 167-171, 2012. Go to original source...
    6. Burkey, K.O., Miller, J.E., Fiscus, E.L.: Assessment of ambient ozone effects on vegetation using snap bean as a bioindicator species. - J. Environ. Qual. 34: 1081-1086, 2005. Go to original source...
    7. Calatayud, A., Alvarado, J.W., Barreno, E.: Differences in ozone sensitivity in three varieties of cabbage (Brassica oleracea L.) in the rural Mediterranean area. - J. Plant Physiol. 159: 863-868, 2002a. Go to original source...
    8. Calatayud, A., Alvarado, J.W., Barreno, E.: Similar effects of ozone on four cultivars of lettuce in open top chambers during winter. - Photosynthetica 40: 195-200, 2002b. Go to original source...
    9. Calatayud, A., Barreno, E.: Chlorophyll a fluorescence, antioxidant enzymes and lipid peroxidation in tomato in response to ozone and benomyl. - Environ. Pollut. 115: 283-289, 2001. Go to original source...
    10. Calatayud, A., Barreno, E.: Response to ozone in two lettuce varieties on chlorophyll a fluorescence, photosynthetic pigments and lipid peroxidation. - Plant Physiol. Bioch. 42: 549-555, 2004. Go to original source...
    11. Calatayud, V., Cervero, J., Sanz, M.J.: Foliar, physiologial and growth responses of four maple species exposed to ozone. - Water Air Soil Poll. 185: 239-254, 2007. Go to original source...
    12. Castagna, A., Nali, C., Ciompi, S. et al.: Ozone exposure affects photosynthesis of pumpkin (Cucurbita pepo) plants. - New Phytol. 152: 223-229, 2001. Go to original source...
    13. Degl'Innocenti, E., Guidi, L., Soldatini, G.F.: Effects of elevated ozone on chlorophyll a fluorescence in symptomatic and asymptomatic leaves of two tomato genotypes. - Biol. Plantarum 51: 313-321, 2007.
    14. Demmig-Adams, B., Adams, W.W., Logan, B.A., Verhoeven, A.S.: Xanthophyll cycle-dependent energy-dissipation and flexible photosystem II efficiency in plants acclimated to light stress. - Aust. J. Plant Physiol. 22: 249-260, 1995. Go to original source...
    15. Faoro, F., Iriti, M.: Cell death behind invisible symptoms: early diagnosis of ozone injury. - Biol. Plantarum 49: 585-592, 2005. Go to original source...
    16. Fiscus, E.L., Booker, F.L., Burkey, K.O.: Crop responses to ozone: uptake, modes of action, carbon assimilation and partitioning. - Plant Cell Environ. 28: 997-1011, 2005. Go to original source...
    17. Flowers, M.D., Fiscus, E.L., Burkey, K.O., Booker, F.L., Dubois, J.-J.B.: Photosynthesis, chlorophyll fluorescence, and yield of snap bean (Phaseolus vulgaris L.) genotypes differing in sensitivity to ozone. - Environ. Exp. Bot. 61: 190-198, 2007. Go to original source...
    18. Fredericksen, T.S., Skelly, J.M., Steiner, K.C. et al.: Sizemediated foliar response to ozone in black cherry trees. - Environ. Pollut. 91: 53-63, 1996. Go to original source...
    19. Gerosa, G., Marzuoli, R., Rossini, M. et al.: A flux-based assessment of the effects of ozone on foliar injury, photosynthesis, and yield of bean (Phaseolus vulgaris L. cv. Borlotto Nano Lingua di Fuoco) in open-top chambers. - Environ. Pollut. 157: 1727-1736, 2009. Go to original source...
    20. Grams, T.E.E., Anegg, S., Haberle, K.H. et al.: Interactions of chronic exposure to elevated CO2 and O3 levels in the photosynthetic light and dark reactions of European beech (Fagus sylvatica). - New Phytol. 144: 95-107, 1999. Go to original source...
    21. Guidi, L., Degl'Innocenti, E., Soldatini, G.F.: Assimilation of CO2, enzyme activation and photosynthetic electron transport in bean leaves, as affected by high light and ozone. - New Phytol. 156: 377-388, 2002. Go to original source...
    22. 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. Go to original source...
    23. Guidi, L., Nali, C., Ciompi, S. et al.: The use of chlorophyll fluorescence and leaf gas exchange as methods for studying the different responses to ozone of two bean cultivars. - J. Exp. Bot. 48: 173-179, 1997. Go to original source...
    24. Guidi, L., Nali, C., Lorenzini, G. et al.: Effect of chronic ozone fumigation on the photosynthetic process of poplar clones showing different sensitivity. - Environ. Pollut. 113: 245-254, 2001. Go to original source...
    25. Harmens, H., Mills, G., Hayes, F. et al.: Air Pollution and Vegetation: ICP Vegetation Annual Report 2005/2006. Pp. 46. Centre for Ecology and Hydrology, Bangor 2006.
    26. Havaux, M.: Carotenoids as membrane stabilizers in chloroplasts. - Trends Plant Sci. 3: 147-151, 1998. Go to original source...
    27. Havaux, M., Dall'Osto, L., Bassi, R.: Zeaxanthin has enhanced antioxidant capacity with respect to all other xanthophylls in Arabidopsis leaves and functions independent of binding to PSII antennae (1[C][W]). - Plant Physiol. 145: 1506-1520, 2007. Go to original source...
    28. Havaux, M., Gruszecki, W.I., Dupont, I., Leblanc, R.M.: Increased heat emission and its relationship to the xanthophyll cycle in pea leaves exposed to strong light stress. - J. Photoch. Photobio. B 8: 361-370, 1991. Go to original source...
    29. Havaux, M., Niyogi, K.K.: The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. - P. Natl. Acad. Sci. USA 96: 8762-8767, 1999. Go to original source...
    30. Havaux, M., Tardy, F., Ravenel, J. et al.: Thylakoid membrane stability to heat stress studied by flash spectroscopic measurements of the electrochromic shift in intact potato leaves: Influence of the xanthophyll content. - Plant Cell Environ. 19: 1359-1368, 1996. Go to original source...
    31. He, X.Y., Fu, S.L., Chen, W. et al.: Changes in effects of ozone exposure on growth, photosynthesis, and respiration of Ginkgo biloba in Shenyang urban area. - Photosynthetica 45: 555-561, 2007. Go to original source...
    32. Hieber, A.D., Kawabata, O., Yamamoto, H.Y.: Significance of the lipid phase in the dynamics and functions of the xanthophyll cycle as revealed by PsbS overexpression in tobacco and invitro de-epoxidation in monogalactosyldiacylglycerol micelles. - Plant Cell Physiol. 45: 92-102, 2004. Go to original source...
    33. ICP Vegetation: Yield response and ozone injury on Phaseolus vulgaris, ICP Vegetation Pilot study, 2008 season. CEH, Bangor 2008.
    34. Leipner, J., Oxborough, K., Baker, N.R.: Primary sites of ozoneinduced perturbations of photosynthesis in leaves: identification and characterization in Phaseolus vulgaris using high resolution chlorophyll fluorescence imaging. - J. Exp. Bot. 52: 1689-1696, 2001.
    35. Lichtenthaler, H.K., Buschmann, C.: Chlorophyll fluorescencespectra of green bean-leaves. - J. Plant Physiol. 129: 137-147, 1987. Go to original source...
    36. Lichtenthaler, H.K., Rinderle, U.: The role of chlorophyll fluorescence in the detection of stress conditions in plants. - CRC Cr. Rev. Anal. Chem. 19: S29-S85, 1988.
    37. Lim, B.P., Nagao, A., Terao, J. et al.: Antioxidant activity of xanthophylls on peroxyl radical-mediated phospholipid peroxidation. - Biochim. Biophys. Acta 1126: 178-184, 1992.
    38. Lorenzini, G., Guidi, L., Nali, C., Soldatini, G.F.: Quenching analysis in poplar clones exposed to ozone. - Tree Physiol. 19: 607-612, 1999. Go to original source...
    39. Miller, J.E.: Effects on photosynthesis, carbon allocation, and plant growth associated with air pollutant stress. - In: Heck, W.W., Taylor, O.C., Tingey, D.T. (ed.): Assessment of Crop Loss from Air Pollutants. Pp. 287-314. Elsevier Applied Science, London 1987. Go to original source...
    40. Morgan, P.B., Ainsworth, E.A., Long, S.P.: How does elevated ozone impact soybean? A meta-analysis of photosynthesis, growth and yield. - Plant Cell Environ. 26: 1317-1328, 2003. Go to original source...
    41. Neufeld, H.S., Peoples, S.J., Davison, A.W. et al.: Ambient ozone effects on gas exchange and total non-structural carbohydrate levels in cutleaf coneflower (Rudbeckia laciniata L.) growing in Great Smoky Mountains National Park. - Environ. Pollut. 160: 74-81, 2012. Go to original source...
    42. Paoletti, E., Nali, C., Lorenzini, G.: Early responses to acute ozone exposure in two Fagus sylvatica clones differing in xeromorphic adaptations: Photosynthetic and stomatal processes, membrane and epicuticular characteristics. - Environ. Monit. Assess. 128: 93-108, 2007. Go to original source...
    43. Peguero-Pina, J.J., Gil-Pelegrin, E., Morales, F.: Three pools of zeaxanthin in Quercus coccifera leaves during light transitions with different roles in rapidly reversible photoprotective energy dissipation and photoprotection. - J. Exp. Bot. 64: 1649-1661, 2013. Go to original source...
    44. Pell, E.J., Schlagnhaufer, C.D., Arteca, R.N.: Ozone-induced oxidative stress: Mechanisms of action and reaction. - Physiol. Plantarum 100: 264-273, 1997. Go to original source...
    45. Pollet, B., Steppe, K., van Labeke, M.C., Lemeur, R.: Diurnal cycle of chlorophyll fluorescence in Phalaenopsis. - Photosynthetica 47: 309-312, 2009. Go to original source...
    46. Pospíšil, P., Skotnica, J., Nauš, J.: Low and high temperature dependence of minimum F-O and maximum F-M chlorophyll fluorescence in vivo. - BBA-Bioenergetics 1363: 95-99, 1998.
    47. Pye, J.M.: Impact of ozone on the growth and yield of trees - a review. - J. Environ. Qual. 17: 347-360, 1988. Go to original source...
    48. Reiling, K., Davison, A.W.: The response of native, herbaceous species to ozone - growth and fluorescence screening. - New Phytol. 120: 29-37, 1992. Go to original source...
    49. Ruth, B., Weisel, B.: Investigations on the photosynthetic system of spruce affected by forest decline and ozone fumigation in closed chambers. - Environ. Pollut. 79: 31-35, 1993. Go to original source...
    50. Salvatori, E., Fusaro, L., Mereu, S. et al.: Different O3 response of sensitive and resistant snap bean genotypes (Phaseolus vulgaris L.): The key role of growth stage, stomatal conductance, and PSI activity. - Environ. Exp. Bot. 87: 79-91, 2013. Go to original source...
    51. Sarry, J.E., Montillet, J.L., Sauvaire, Y., Havaux, M.: The protective function of the xanthophyll cycle in photosynthesis. - FEBS Lett. 353: 147-150, 1994. Go to original source...
    52. Schreiber, U., Vidaver, W., Runeckles, V.C., Rosen, P.: Chlorophyll fluorescence assay for ozone injury in intact plants. - Plant Physiol. 61: 80-84, 1978. Go to original source...
    53. Shirke, P.A., Pathre, U.V.: Diurnal and seasonal changes in photosynthesis and photosystem 2 photochemical efficiency in Prosopis juliflora leaves subjected to natural environmental stress. - Photosynthetica 41: 83-89, 2003. Go to original source...
    54. Sielewiesiuk, J., Matula, M., Gruszecki, W.I.: Photo-oxidation of chlorophyll a in digalactosyldiacylglycerol liposomes containing xanthophyll pigments: indication of a special photoprotective ability of zeaxanthin. - Cell. Mol. Biol. Lett. 2: 59-68, 1997.
    55. Subczynski, W.K., Markowska, E., Gruszecki, W.I., Sielewiesiuk, J.: Effects of polar carotenoids on dimyristoylphosphatidylcholine membranes - a spin-label study. - Biochim. Biophys. Acta 1105: 97-108, 1992. Go to original source...
    56. Sun, G.C., Zeng, X.P., Liu, X.J., Zhao, P.: Effects of moderate high-temperature stress on photosynthesis in three species of saplings of the constructive tree species from subtropical forest. - Acta Ecol. Sin. 27: 1283-1291, 2007.
    57. Thayer, S.S., Björkman, O.: Leaf xanthophyll content and composition in sun and shade determined by HPLC. - Photosynth. Res. 23: 331-343, 1990. Go to original source...
    58. Weng, J.H., Lai, M.F.: Estimating heat tolerance among plant species by two chlorophyll fluorescence parameters. - Photosynthetica 43: 439-444, 2005. Go to original source...
    59. Zhang, R., Cruz, J.A., Kramer, D.M., Magallanes-Lundback, M.E., Dellapenna, D., Sharkey, T.D.: Moderate heat stress reduces the pH component of the transthylakoid proton motive force in light-adapted, intact tobacco leaves. - Plant Cell Environ. 32: 1538-1547, 2009. Go to original source...
    60. Zhang, X., Zhang, L., Dong, F.C. et al.: Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. - Plant Physiol. 126: 1438-1448, 2001. Go to original source...

    Return to the content