Photosynthetica 2019, 57(4):1119-1129 | DOI: 10.32615/ps.2019.117

Response of the photosynthetic apparatus in the tropical fern Platycerium bifurcatum to increased ozone concentration

J. OLIWA1, I. STAWOSKA1, A. JANECZKO2, J. OKLEŠŤKOVÁ3, A. SKOCZOWSKI1
1 Institute of Biology, Pedagogical University of Krakow, Podchorążych 2, 30-084 Kraków, Poland
2 Polish Academy of Sciences, The Franciszek Górski Institute of Plant Physiology, Niezapominajek 21, 30-239 Kraków, Poland
3 Laboratory of Growth Regulators, Czech Academy of Sciences, Institute of Experimental Botany & Palacký University, Faculty of Science, Šlechtitelů 27, 78371 Olomouc, Czech Republic

A rapid increase of ozone concentration up to the phytotoxic level is currently observed in the tropical forests. However, the effect of elevated concentration of O3 on tropical ferns and epiphytes has not yet been described and mechanisms of tolerance remain unknown. The aim of this study was to determine the physiological response of the epiphytic fern Platycerium bifurcatum to a high concentration of ozone (150 ppb). In particular, changes in the course of photosynthesis and the pigment composition of sporotrophophyll leaves were taken into account. P. bifurcatum showed high resistance to the 4-week ozone stress. The effect of ozone was an initial decrease in net photosynthesis and reduction in transpiration. Ozone tolerance mechanisms are associated with the closure of stomata and the synthesis of carotenoids and flavonoids. We found that brassinosteroids play an important role in the resistance of P. bifurcatum to ozone. In response to ozone stress an increase in 28-homocastasterone content was observed.

Keywords: chlorophyll a fluorescence; gas exchange; leaf reflectance; SPAD; sporotrophophyll; tropical plants.

Received: March 19, 2019; Accepted: July 23, 2019; Prepublished online: October 14, 2019; Published: November 1, 2019Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
OLIWA, J., STAWOSKA, I., JANECZKO, A., OKLEŠŤKOVÁ, J., & SKOCZOWSKI, A. (2019). Response of the photosynthetic apparatus in the tropical fern Platycerium bifurcatum to increased ozone concentration. Photosynthetica, 57(4), 1119-1129. doi: 10.32615/ps.2019.117.
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. Anuradha S., Rao S.S.R.: Application of brassinosteroids to rice seeds (Oryza sativa L.) reduced the impact of salt stress on growth, prevented photosynthetic pigment loss and increased nitrate reductase activity. - Plant Growth Regul. 40: 29-32, 2003. Go to original source...
    2. Arnon D.I.: Copper enzymes in isolated chloroplasts. Polyphenol-oxidase in Beta vulgaris. - Plant Physiol. 24: 1-15, 1949.
    3. Bąba W., Kalaji H.M., Kompała-Bąba A., Goltsev V.: Acclimati-zation of photosynthetic apparatus of tor grass (Brachypodium pinnatum) during expansion. - PLoS ONE 11: e0156201, 2016. Go to original source...
    4. Bajguz A., Hayat S.: Effects of brassinosteroids on the plant responses to environmental stresses. - Plant Physiol. Bioch. 47: 1-8, 2009. Go to original source...
    5. Bartoli G., Forino L.M.C., Tagliasacchi A.M., Durante M.: Cell death induced by ozone stress in the leaves of Populus deltoides × maximowiczii. - Biol. Plantarum 57: 514-524, 2013.
    6. Benzing D.H., Arditti J., Nyman L.P., Temple P.J.: Effects of ozone and sulfur dioxide on four epiphytic bromeliads. - Environ. Exp. Bot. 32: 25-32, 1992.
    7. Bergmann E., Bender J., Weigel H.J.: Impact of tropospheric ozone on terrestrial biodiversity: A literature analysis to identify ozone sensitive taxa. - J. Appl. Bot. Food Qual. 90: 83-105, 2017.
    8. Bergweiler C.J., Manning W.J.: Inhibition of flowering and reproductive success in spreading dogbane (Apocynum androaemifolium) by exposure to ambient ozone. - Environ. Pollut. 105: 333-339, 1999.
    9. Bičárová S., Sitková Z., Pavlendová H. et al.: The role of environmental factors in ozone uptake of Pinus mugo Turra. - Atmos. Pollut. Res. 10: 283-293, 2019.
    10. Booker F., Muntifering R., McGrath M. et al.: 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.
    11. Bortier K., Ceulemans R., de Temmerman L.: Effects of ozone exposure on growth and photosynthesis of beech seedlings (Fagus sylvatica). - New Phytol. 146: 271-280, 2000.
    12. Bosley A., Petersen R., Rebbeck J.: The resistance of the moss Polytrichum commune to acute exposure of simulated acid rain or ozone compared to two fern species: Spore germination. -Bryologist 101: 512-518, 1999.
    13. Brunetti C., Guidi L., Sebastiani F., Tattini M.: Isoprenoids and phenylpropanoids are key components of the antioxidant defense system of plants facing severe excess light stress. - Environ. Exp. Bot. 119: 54-62, 2015.
    14. Bussotti F., Desotgiu R., Cascio 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. Go to original source...
    15. Bussotti F., Strasser R.J., Novak K. et al.: Photosynthetic efficiency in Populus nigra and Viburnum lantana grown in open-top chambers. - Acta Physiol. Plant. 26: 243, 2004.
    16. Bussotti F., Strasser R.J., Schaub M.: Photosynthetic behavior of woody species under high ozone exposure probed with the JIP-test - A review. - Environ. Pollut. 147: 430-437, 2007.
    17. Carter G.A.: Responses of leaf spectral reflectance to plant stress. -Am. J. Bot. 80: 239-243, 1993. Go to original source...
    18. Carter G.A., Knapp A.K.: Leaf optical properties in higher plants: linking spectral characteristics to stress and chlorophyll concentration. - Am. J. Bot. 88: 677-684, 2001. Go to original source...
    19. Carter G.A., Mitchell R.J., Chappelka A.H., Brewer C.H.: Response of leaf reflectance in loblolly pine to increased atmospheric ozone and precipitation acidity. - J. Exp. Bot. 43: 577-584, 1992.
    20. Clark A.J., Landolt W., Bucher J.B., Strasser R.J.: Beech (Fagus sylvatica) response to ozone exposure assessed with a chlorophyll a fluorescence performance index. - Environ. Pollut. 109: 501-507, 2000.
    21. Dai L., Li P., Shang B. et al.: Differential responses of peach (Prunus persica) seedlings to elevated ozone are related with leaf mass per area, antioxidant enzymes activity rather than stomatal conductance. - Environ. Pollut. 227: 380-388, 2017.
    22. Degl'Innocenti E., Guidi L., Soldatini G.F.: Characterisation of the photosynthetic response of tobacco leaves to ozone: CO2 assimilation and chlorophyll fluorescence. - J. Plant Physiol. 159: 845-853, 2002.
    23. Demming-Adams B., Adams III W.W.: The role of xanthophyll cycle carotenoids in the protection of photosynthesis. - Trends Plant Sci. 1: 21-26, 1996.
    24. Fernandes F.F., Esposito M.P., Gonçalves da Silva Engela M.R. et al.: The passion fruit liana (Passiflora edulis Sims, Passifloraceae) is tolerant to ozone. - Sci. Total Environ. 656: 1091-1101, 2019.
    25. Filek M., Rudolphi-Skórska E., Sieprawska A. et al.: Regulation on the membrane structure by brassinosteroids and progesterone in winter wheat seedlings exposed to low temperature. - Steroids 128: 37-45, 2017.
    26. Gamon J.A., Peñuelas J., Field C.B.: A narrow-waveband spectral index that tracks diurnal changes in photosynthetic efficiency. - Remote. Sens. Environ. 41: 35-44, 1992.
    27. Gamon J.A., Serrano L., Surfus J.S.: The photochemical reflectance index: An optical indicator of photosynthetic radiation use efficiency across species, functional types, and nutrient levels. - Oecologia 112: 492-501, 1997.
    28. Gill S.S., Tuteja N.: Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. - Plant Physiol. Bioch. 48: 909-930, 2010.
    29. Gitelson A.A., Merzylak M.N., Chivkunova O.B.: Optical properties and nondestructive estimation of anthocyanin content in plant leaves. - Photochem. Photobiol. 71: 38-45, 2001.
    30. Gómez-Garay A., Gabriel y Galán J.M., Cabezuelo A. et al.: Ecological significance of brassinosteroids in three temperate ferns. - In: Fernández H. (ed.): Current Advances in Fern Research. Pp. 453-466. Springer, Cham 2018.
    31. Gottardini E., Cristofori A., Cristofolini F. et al.: Chlorophyll-related indicators are linked to visible ozone symptoms: Evidence from a field study on native Viburnum lantana L. plants in northern Italy. - Ecol. Indic. 39: 65-74, 2014.
    32. Gravano E., Bussotti F., Strasser J.R. et al.: Ozone symptoms in leaves of woody plants in open top chambers: Ultrastructural and physiological characteristics. - Physiol. Plantarum 121: 620-633, 2004. Go to original source...
    33. Ismail I.M., Basahi J.M., Hassan I.A.: Gas exchange and chlorophyll fluorescence of pea (Pisum sativum L.) plants in response to ambient ozone at a rural site in Egypt. - Sci. Total Environ. 497-498: 585-593, 2014.
    34. Jaeger N., Besaury L., Röhling A.N. et al.: Chloromethane formation and degradation in the fern phyllosphere. - Sci. Total Environ. 634: 1278-1287, 2018. Go to original source...
    35. Jahns P., Latowski D., Strzałka K.: Mechanism and regulation of the violaxanthin cycle: The role of antenna proteins and membrane lipids. - BBA-Bioenergetics 1787: 3-14, 2009.
    36. Kalaji H.M., Bąba W., Gediga K.: Chlorophyll fluorescence as a tool for nutrient status identification in rapeseed plants. - Photosynth. Res. 136: 329-343, 2018.
    37. Kalaji M.H., Jajoo A., Oukarroum A. et al.: The use of chlorophyll fluorescence kinetics analysis to study the performance of photosynthetic machinery in plants. - In: Ahmad P., Rasool S. (ed.): Emerging Technologies and Management of Crop Stress Tolerance. Vol. 2. Pp. 347-384. Academic Press, San Diego 2014.
    38. Kalaji H.M., Jajoo A., Oukarroum A. et al.: Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. - Acta Physiol. Plant. 38: 102, 2016.
    39. Kitao M., Löw M., Heerdt C. et al.: Effects of chronic elevated ozone exposure on gas exchange responses of adult beech trees (Fagus sylvatica) as related to the within-canopy light gradient. - Environ. Pollut. 157: 537-544, 2009.
    40. Krishna P.: Brassinosteroid-mediated stress responses. - J. Plant Growth Regul. 22: 289-297, 2003.
    41. Mazorra L.M., Núñez M., Hechavarria M. et al.: Influence of brassinosteroids on antioxidant enzymes activity in tomato under different temperatures. - Biol. Plantarum 45: 593-596, 2002.
    42. Meroni M., Panigada C., Rossini M. et al.: Using optical remote sensing techniques to track the development of ozone-induced stress. - Environ. Pollut. 157: 1413-1420, 2009.
    43. Merzlyak M.N., Solovchenko A.E., Smagin A.I., Gitelson A.A.: Apple flavonols during fruit adaptation to solar radiation: spectral features and technique for non-destructive assess-ment. - J. Plant. Physiol. 162: 151-160, 2005. Go to original source...
    44. Mills G., Hayes F., Simpson D. et al.: Evidence of widespread effects of ozone on crops and (semi-)natural vegetation in Europe (1990-2006) in relation to AOT40- and flux-based risk maps. - Glob. Change Biol. 17: 592-613, 2011. Go to original source...
    45. Minnocci A., Panicucci A., Sebastiani L. et al.: Physiological and morphological responses of olive plants to ozone exposure during a growing season. - Tree Physiol. 19: 391-397, 1999. Go to original source...
    46. Moraes R.M., Bulbovas P., Furlan C.M. et al.: Physiological responses of saplings of Caesalpinia echinata Lam., a Brazilian tree species, under ozone fumigation. - Ecotox. Environ. Safe. 63: 306-312, 2006. Go to original source...
    47. Moura B.B., Alves E.S., Marabesi M.A. et al.: Ozone affects leaf physiology and causes injury to foliage of native tree species from the tropical Atlantic Forest of southern Brazil. - Sci. Total Environ. 610-611: 912-925, 2018. Go to original source...
    48. Nali C., Paoletti E., Marabottini R. et al.: Ecophysiological and biochemical strategies of response to ozone in Mediterranean evergreen broadleaf species. - Atmos. Environ. 38: 2247-2257, 2004. Go to original source...
    49. Neill S.O., Gould K.S.: Anthocyanins in leaves: light attenuators or antioxidants? - Funct. Plant Biol. 30: 865-873, 2003.
    50. Niu J., Zhang W., Li L. et al.: Effects of elevated ozone on foliar chlorophyll content and antioxidant capacity in leaves of Cinnamomum camphora under enhanced nitrogen loads. - Acta Ecol. Sin. 32: 5062-5070, 2012.
    51. Novak K., Schaub M., Fuhrer J. et al.: Seasonal trends in reduced leaf gas exchange and ozone-induced foliar injury in three ozone sensitive woody plants species. - Environ. Pollut. 136: 33-45, 2005.
    52. Oklešťková J., Tarkowská D., Eyer L. et al.: Immunoaffinity chromatography combined with tandem mass spectrometry: A new tool for the selective capture and analysis of brassinosteroid plant hormones. - Talanta 170: 432-440, 2017.
    53. Oksanen E.: Trichomes form an important first line of defence against adverse environment - New evidence for ozone stress mitigation. - Plant Cell Environ. 41: 1497-1499, 2018.
    54. Oksanen E., Pandey V., Pandey A.K. et al.: Impacts of increasing ozone on Indian plants. - Environ. Pollut. 177: 189-200, 2013.
    55. Oliwa J., Kornas A., Skoczowski A.: Morphogenesis of sporo-trophophyll leaves in Platycerium bifurcatum depends on the red/far-red ratio in the light spectrum. - Acta Physiol. Plant. 38: 247, 2016.
    56. Oliwa J., Kornas A., Skoczowski A.: A low ratio of red/far-red in the light spectrum accelerates senescence in nest leaves of Platycerium bifurcatum. - Acta Biol. Cracov. Bot. 59: 17-30, 2017. Go to original source...
    57. Oliwa J., Skoczowski A.: Different response of photosynthetic apparatus to high-light stress in sporotrophophyll and nest leaves of Platycerium bifurcatum. - Photosynthetica 57: 147-159, 2019.
    58. Orendovici T., Skelly J.M., Ferdinand J.A. et al.: Response of native plants of northeastern United States and southern Spain to ozone exposure; determining exposure/response relationships. - Environ. Pollut. 125: 31-40, 2003. Go to original source...
    59. Oukarroum A., El Madidi S., Schansker G., Strasser R.J.: Probing the responses of barley cultivars (Hordeum vulgare L.) by chlorophyll a fluorescence OLKJIP under drought stress and re-watering. - Environ. Exp. Bot. 60: 438-446, 2007. Go to original source...
    60. Pellegrini E., Hoshika Y., Dusart N. et al.: Antioxidative responses of three oak species under ozone and water stress conditions. - Sci. Total Environ. 647: 390-399, 2019. Go to original source...
    61. Peñuelas J., Filella I., Baret F.: Semiempirical indices to assess carotenoids/chlorophyll a ratio from leaf spectra reflectance. -Photosynthetica 31: 221-230, 1995.
    62. Peñuelas J., Filella I., Biel C. et al.: The reflectance at the 950-970 nm region as an indicator of plant water status. - Int. J. Remote Sens. 14: 1887-1905, 1993.
    63. Peñuelas J., Garbulsky M.F., Filella I.: Photochemical reflectance index (PRI) and remote sensing of plant CO2 uptake. - New Phytol. 191: 596-598, 2011.
    64. Rai R., Agrawal M., Agrawal S.B.: Assessment of yield losses in tropical wheat using open top chambers. - Atmos. Environ. 41: 9543-9554, 2007.
    65. Retuerto R., Fernandez-Lema B., Roiloa R., Obeso J.R.: Increased photosynthetic performance in holly trees infested by scale insects. - Funct. Ecol. 18: 664-669, 2004.
    66. Rozpądek P., Ślesak I., Cebula S. et al.: Ozone fumigation results in accelerated growth and persistent changes in the antioxidant system of Brassica oleracea L. var. capitata f. alba. - J. Plant. Physiol. 170: 1259-1266, 2013.
    67. Rut G., Krupa J., Rzepka A.: The influence of simulated osmotic drought on functioning of the photosynthetic apparatus in gametophytes of the epiphytic fern Platycerium bifurcatum. -Pol. J. Nat. Sci. Suppl. 1: 114-115, 2003.
    68. Sadura I., Janeczko A.: Physiological and molecular mechanisms of brassinosteroid-induced tolerance to high and low temperature in plants. - Biol. Plantarum 62: 601-616, 2018.
    69. Sandermann H., Wellburn A.R., Heath R.L.: Forest decline and ozone: Synopsis. - In: Sandermann H., Wellburn A.R., Heath R.L. (ed.): Forest Decline and Ozone: A Comparison of Controlled Chamber and Field Experiments. Pp. 369-377. Springer, Berlin-Heidelberg 1997.
    70. Sarkar A., Agrawal S.B.: Elevated ozone and two modern wheat cultivars: An assessment of dose dependent sensitivity with respect to growth, reproductive and yield parameters. - Environ. Exp. Bot. 69: 328-337, 2010. Go to original source...
    71. Schaub M., Skelly J.M., Steiner K.C. et al.: Physiological and foliar injury responses of Prunus serotina, Fraxinus americana, and Acer rubrum seedlings to varying soil moisture and ozone. - Environ. Pollut. 124: 307-320, 2003. Go to original source...
    72. Ślesak I., Libik M., Karpińska B. et al.: The role of hydrogen peroxide in regulation of plant metabolism and cellular signalling in response to environmental stress. - Acta Biochim. Pol. 54: 39-50, 2007.
    73. Soja G., Pfeifer U., Soja A.M.: Photosynthetic parameters as early indicators of ozone injury in apple leaves. - Physiol. Plantarum 104: 639-645, 1998. Go to original source...
    74. Solovchenko A.: Quantification of screening pigments and their efficiency in situ. - In: Solovchenko A. (ed.): Photoprotection in Plants. Pp. 119-141. Springer-Verlag, Berlin-Heidelberg 2010. Go to original source...
    75. Staehelin J.: Ozone measurements and trends (Troposphere). - In: Meyers R.A. (ed.): Encyclopedia of Physical Science and Technology. Third Edition. Pp. 539-561. Academic Press, New York 2003.
    76. Steyn W.J., Wand S.J.E., Holcroft D.M., Jacobs G.: Anthocyanins in vegetative tissues: A proposed unified function in photo-protection. - New Phytol. 155: 349-361, 2002. Go to original source...
    77. Strasser R.J., Srivastava A., Tsimilli-Michael M.: The fluores- cence transient as a tool to characterize and screen photosyn-thetic samples. - In: Yunus M., Pathre U., Mohanty P. (ed.): Probing Photosynthesis: Mechanism, Regulation and Adaptation. Pp. 443-480. Taylor and Francis, London 2000.
    78. Strasser R.J., Tsimilli-Michael M., Qiang S., Goltsev V.: 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. - BBA-Bioenergetics 1797: 1313-1326, 2010.
    79. The Royal Society: Ground-level Ozone in the 21st Century: Future Trends, Impacts and Policy Implications. Pp. 134. The Royal Society, London 2008.
    80. Tsimilli-Michael M., Strasser R.J.: Biophysical phenomics: evaluation of the impact of mycorrhization with Piriformo-spora indica. - In: Varma A., Kost G., Oelmüller R. (ed.): Piriformospora indica. Pp. 173-190. Springer, Berlin 2013a. Go to original source...
    81. Tsimilli-Michael M., Strasser R.J.: The energy flux theory 35 years later: Formulations and applications. - Photosynth. Res. 117: 289-320, 2013b. Go to original source...
    82. Vingarzan R.: A review of surface ozone background levels and trends. - Atmos. Environ. 38: 3431-3442, 2004.
    83. Vollenweider P., Günthardt-Goerg M.S.: Diagnosis of abiotic and biotic stress factors using the visible symptoms in foliage. - Environ. Pollut. 140: 562-571, 2006. Go to original source...
    84. Williams J.H., Ashenden T.W.: Differences in the spectral characteristics of white clover exposed to gaseous pollutants and acid mist. - New Phytol. 120: 69-75, 1992.
    85. Wittig V.E., Ainsworth E.A., Long S.P.: To what extent do current and projected increases in surface ozone affect photosynthesis and stomatal conductance of trees? A meta-analytic review of the last 3 decades of experiments. - Plant Cell Environ. 30: 1150-1162, 2007.
    86. Wittig V.E., Ainsworth E.A., Naidu S.L. et al.: Quantifying the impact of current and future tropospheric ozone on tree biomass, growth, physiology and biochemistry: A quantitative meta-analysis. - Glob. Change Biol. 15: 396-424, 2009.
    87. Wohlgemuth H., Mittelstrass K., Kschieschan S.: Activation of an oxidative burst is a general feature of sensitive plants exposed to the air pollutant ozone. - Plant Cell Environ. 25: 717-726, 2002. Go to original source...
    88. Yang N., Wang X., Cotrozzi L. et al.: Ozone effects on photosynthesis of ornamental species suitable for urban green spaces of China. - Urban For. Urban Gree. 20: 437-447, 2016.
    89. Yokota T., Ohnishi T., Shibata K. et al.: Occurrence of brassinosteroids in non-flowering land plants, liverwort, moss, lycophyte and fern. - Phytochemistry 136: 46-55, 2017.

    Return to the content