Gas exchange and JIP-test parameters of two Mediterranean maquis species are affected by sea spray and ozone interaction.

Mediterranean maquis coastal ecosystems are subject to multiple oxidative stresses of both natural and anthropic origin, as sea spray, drought, high irradiance and ozone. In this article it is hypothesized that the interaction of ozone and sea spray is additive as a consequence of a higher reactive oxigen species accumulation. To test the hypothesis, an experiment was conducted in an Open Top Chambers facility where plants of Quercus ilex L. and Arbutus unedo L. were exposed to two levels of ozone and two levels of sea spray. The response of the species was evaluated by measurements of structural parameters (shoot growth and leaf biomass) and physiological parameters (leaf level gas exchange and chlorophyll a fluorescence). The results contradict the hypothesis as the interaction of the two stresses is antagonistic on both species. The structure of both species was negatively affected by sea spray, however the two stresses combined allowed a higher growth and leaf area in A. unedo. The leaf level physiology of A. unedo was only moderately affected by the two stresses alone and in combined, while that of Q. ilex was altered to a further extent by sea spray and by its combination with ozone: photosynthesis and efficiency of the PSII was reduced by sea spray while the ratio of PSII to PSI was increased; the two stresses combined, instead, decreased the PSII to PSI ratio allowing for a higher photosynthesis. It is concluded that A. unedo is more resistant than Q. ilex to the two stresses alone and in combination, that ozone and sea spray interact antagonistically, and that the activity of PSI has a key role in the stress response.

[1]  R. Mittler,et al.  Abiotic stress, the field environment and stress combination. , 2006, Trends in plant science.

[2]  S. Wilkinson,et al.  Ozone suppresses soil drying- and abscisic acid (ABA)-induced stomatal closure via an ethylene-dependent mechanism. , 2009, Plant, cell & environment.

[3]  A. Noormets,et al.  Photosynthetic parameters and stomatal conductance of aspen under elevated CO2 and O3 as affected by leaf hydraulic properties. Proc. Air Pollution, Global Change and Forests in the New Millennium , 2000 .

[4]  B. Gimeno,et al.  Contrasting effects of ozone under different water supplies in two Mediterranean tree species , 2005 .

[5]  N. Katerji,et al.  Analysis of the ozone effect on soybean in the Mediterranean region: II. The consequences on growth, yield and water use efficiency , 2008 .

[6]  A. Ranieri,et al.  Detoxification and repair process of ozone injury: from O3 uptake to gene expression adjustment. , 2009, Environmental pollution.

[7]  D. Inzé,et al.  Dual action of the active oxygen species during plant stress responses , 2000, Cellular and Molecular Life Sciences CMLS.

[8]  Dirk Inzé,et al.  SUPEROXIDE DISMUTASE AND STRESS TOLERANCE , 1992 .

[9]  Walter W. Heck,et al.  An Open‐Top Field Chamber to Assess the Impact of Air Pollution on Plants , 1973 .

[10]  T. Sharkey,et al.  Fitting photosynthetic carbon dioxide response curves for C(3) leaves. , 2007, Plant, cell & environment.

[11]  M. Fagnano,et al.  Responses to ozone pollution of alfalfa exposed to increasing salinity levels. , 2009, Environmental pollution.

[12]  F. Loreto,et al.  Photosynthetic limitations in olive cultivars with different sensitivity to salt stress , 2003 .

[13]  F. Loreto,et al.  Physiological responses of forest trees to heat and drought. , 2006, Plant biology.

[14]  T. Sharkey,et al.  Diffusive and metabolic limitations to photosynthesis under drought and salinity in C(3) plants. , 2004, Plant biology.

[15]  Nobuhiro Suzuki,et al.  Reactive oxygen species homeostasis and signalling during drought and salinity stresses. , 2010, Plant, cell & environment.

[16]  R. Strasser,et al.  Foliar responses to ozone of Fagus sylvatica L. seedlings grown in shaded and in full sunlight conditions , 2010 .

[17]  E. Biondi,et al.  Carta delle Serie di Vegetazione della regione Sardegna. In Blasi C. (ed.). La Vegetazione d’Italia, Carta delle Serie di Vegetazione, scala 1:500.000. Palombi & Partner S.r.l. Roma , 2010 .

[18]  F. Bussotti,et al.  Ultrastructural response of a Mediterranean shrub species to O3 , 2003 .

[19]  A. Herrera,et al.  Photosynthetic responses of the tropical spiny shrub Lycium nodosum (Solanaceae) to drought, soil salinity and saline spray. , 2003, Annals of botany.

[20]  A. Das,et al.  Salt tolerance and salinity effects on plants: a review. , 2005, Ecotoxicology and environmental safety.

[21]  L. Guidi,et al.  Ozone effects on high light-induced photoinhibition in Phaseolus vulgaris , 2008 .

[22]  J. Flexas,et al.  Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. , 2009, Annals of botany.

[23]  G. P. Cheplick,et al.  Impact of saltwater spray andsand deposition on the coastal annualTriplasis purpurea (Poaceae). , 1999, American journal of botany.

[24]  K. Siebke,et al.  Relationship between the inhibition of leaf respiration by light and enhancement of leaf dark respiration following light treatment , 1998 .

[25]  E. Olmos,et al.  Effects of sodium chloride on water potential components, hydraulic conductivity, gas exchange and leaf ultrastructure of Arbutus unedo plants , 2007 .

[26]  F. Loreto,et al.  Physiological responses of Quercus ilex Leaves to Water Stress and Acute Ozone Exposure Under Controlled Conditions , 2008 .

[27]  Christian Wilhelm,et al.  Energy dissipation is an essential mechanism to sustain the viability of plants: The physiological limits of improved photosynthesis. , 2011, Journal of plant physiology.

[28]  F. Loreto,et al.  The use of low [CO2] to estimate diffusional and non‐diffusional limitations of photosynthetic capacity of salt‐stressed olive saplings , 2003 .

[29]  S. Wilkinson,et al.  Drought, ozone, ABA and ethylene: new insights from cell to plant to community. , 2010, Plant, cell & environment.

[30]  M. G. Barreiro,et al.  BULGARIAN JOURNAL OF PLANT PHYSIOLOGY , 2003 .

[31]  M. H. D. Carvalho Drought stress and reactive oxygen species , 2008 .

[32]  K. Asada,et al.  THE WATER-WATER CYCLE IN CHLOROPLASTS: Scavenging of Active Oxygens and Dissipation of Excess Photons. , 1999, Annual review of plant physiology and plant molecular biology.

[33]  M. Sanz,et al.  Contrasting ozone sensitivity in related evergreen and deciduous shrubs. , 2010, Environmental pollution.

[34]  F. Bussotti,et al.  Cytological and structural changes in Pinus pinea L. needles following the application of an anionic surfactant , 1997 .

[35]  Water sources and water-use efficiency in mediterranean coastal dune vegetation. , 2004, Plant biology.

[36]  J. Kangasjärvi,et al.  Signalling and cell death in ozone‐exposed plants , 2005 .

[37]  R. Mittler Oxidative stress, antioxidants and stress tolerance. , 2002, Trends in plant science.

[38]  Jon E. Keeley,et al.  Ecology, Biogeography and Management of Pinus halepensis and P. brutia Forest Ecosystems in the Mediterranean Basin , 2001 .

[39]  A. Hanson,et al.  Metabolic engineering of osmoprotectant accumulation in plants. , 2002, Metabolic engineering.

[40]  H. Hirt,et al.  Reactive oxygen species: metabolism, oxidative stress, and signal transduction. , 2004, Annual review of plant biology.

[41]  Bart Muys,et al.  An integrated approach shows different use of water resources from Mediterranean maquis species in a coastal dune ecosystem. , 2009 .

[42]  R. Strasser,et al.  Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. , 2005, Biochimica et biophysica acta.

[43]  R. Strasser,et al.  Photosynthesis responses to ozone in young trees of three species with different sensitivities, in a 2-year open-top chamber experiment (Curno, Italy) , 2007 .

[44]  S. Allakhverdiev,et al.  Photoinhibition of photosystem II under environmental stress. , 2007, Biochimica et biophysica acta.

[45]  Filippo Bussotti,et al.  Ozone stress in woody plants assessed with chlorophyll a fluorescence. A critical reassessment of existing data , 2011 .

[46]  A. Srivastava,et al.  POLYPHASIC CHLOROPHYLL a FLUORESCENCE TRANSIENT IN PLANTS AND CYANOBACTERIA * , 1995 .

[47]  Michele Meroni,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. , 2009, Environmental pollution.

[48]  R. Strasser,et al.  Ozone symptoms in leaves of woody plants in open‐top chambers: ultrastructural and physiological characteristics , 2004 .

[49]  B. Halliwell,et al.  Free radicals in biology and medicine , 1985 .

[50]  J. Lloyd,et al.  Climate‐dependent variations in leaf respiration in a dry‐land, low productivity Mediterranean forest: the importance of acclimation in both high‐light and shaded habitats , 2007 .

[51]  G. Agati,et al.  Antioxidant defences and oxidative damage in salt-treated olive plants under contrasting sunlight irradiance. , 2009, Tree physiology.

[52]  R. Strasser,et al.  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. , 2010, Biochimica et biophysica acta.

[53]  J. Peñuelas,et al.  Sap flow of three co-occurring Mediterranean woody species under varying atmospheric and soil water conditions. , 2003, Tree physiology.

[54]  M. Vitale,et al.  Physiological response of Pinus halepensis needles under ozone and water stress conditions. , 2001, Physiologia plantarum.

[55]  S. Long,et al.  Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. , 2003, Journal of experimental botany.

[56]  P. Horton,et al.  REGULATION OF LIGHT HARVESTING IN GREEN PLANTS. , 1996, Annual review of plant physiology and plant molecular biology.

[57]  E. Olmos,et al.  Differences in the effects of simulated sea aerosol on water relations, salt content, and leaf ultrastructure of rock-rose plants. , 2004, Journal of environmental quality.

[58]  P. Sutton,et al.  The coasts of our world: Ecological, economic and social importance , 2007 .

[59]  R. Strasser,et al.  Drought stress effects on photosystem I content and photosystem II thermotolerance analyzed using Chl a fluorescence kinetics in barley varieties differing in their drought tolerance. , 2009, Physiologia plantarum.

[60]  G. Agati,et al.  Morpho-anatomical, physiological and biochemical adjustments in response to root zone salinity stress and high solar radiation in two Mediterranean evergreen shrubs, Myrtus communis and Pistacia lentiscus. , 2006, The New phytologist.

[61]  R. Matyssek,et al.  Interactions between drought and O3 stress in forest trees. , 2006, Plant biology.

[62]  S. Ivanov,et al.  INTERACTION BETWEEN STRESSES , 2003 .

[63]  P. Haldimann,et al.  Photosynthetic performance and water relations in young pubescent oak (Quercus pubescens) trees during drought stress and recovery. , 2007, The New phytologist.

[64]  Ülo Niinemets,et al.  Responses of forest trees to single and multiple environmental stresses from seedlings to mature plants: Past stress history, stress interactions, tolerance and acclimation , 2010 .

[65]  A. Varma Mycorrhiza : state of the art, genetics and molecular biology, eco-function, biotechnology, eco-physiology, structure and systematics , 2008 .

[66]  L. Sternberg,et al.  Linking marine resources to ecotonal shifts of water uptake by terrestrial dune vegetation. , 2006, Ecology.

[67]  R. Strasser,et al.  Photosynthetic behavior of woody species under high ozone exposure probed with the JIP-test: a review. , 2007, Environmental pollution.

[68]  J. Peñuelas,et al.  Drought-induced oxidative stress in strawberry tree (Arbutus unedo L.) growing in Mediterranean field conditions , 2004 .

[69]  E. Paoletti,et al.  Ecophysiological and biochemical strategies of response to ozone in Mediterranean evergreen broadleaf species , 2004 .

[70]  G. Johnson,et al.  Down-regulation of linear and activation of cyclic electron transport during drought , 2003, Planta.

[71]  G. Johnson,et al.  Contrasting Responses of Photosynthesis to Salt Stress in the Glycophyte Arabidopsis and the Halophyte Thellungiella: Role of the Plastid Terminal Oxidase as an Alternative Electron Sink1[C][OA] , 2008, Plant Physiology.

[72]  P. D. Heerden,et al.  Modulation of photosynthesis by drought in two desert scrub species exhibiting C3-mode CO2 assimilation , 2007 .