Elsevier

Environmental Pollution

Volume 196, January 2015, Pages 527-533
Environmental Pollution

Review
Ozone induces stomatal narrowing in European and Siebold's beeches: A comparison between two experiments of free-air ozone exposure

https://doi.org/10.1016/j.envpol.2014.07.034Get rights and content

Highlights

  • We review stomatal response under recently conducted free-air O3 exposure experiments on beech.

  • O3 reduced stomatal conductance by 10–20% throughout the summer in European and Siebold's beech.

  • Stomatal closure occurred without reduced carboxylation capacity of Rubisco in early summer.

  • Observed stomatal closure was, however, diminished in autumn in both beeches.

  • Stomatal closure is a primary response in beech trees to chronic O3 impact.

Abstract

Stomata tend to narrow under ozone (O3) impact, leading to limitation of stomatal O3 influx. Here, we review stomatal response under recently conducted free-air O3 exposure experiments on two species of the same tree genus: Fagus sylvatica at Kranzberg Forest (Germany) and F. crenata at Sapporo Experimental Forest (Japan). Both beeches exhibited reduction in stomatal conductance (gs) by 10–20% under experimentally enhanced O3 regimes throughout the summer relative to ambient-air controls. Stomatal narrowing occurred, in early summer, in the absence of reduced carboxylation capacity of Rubisco, although photosynthetic net CO2 uptake rate temporarily reflected restriction to some minor extent. Observed stomatal narrowing was, however, diminished in autumn, suggesting gradual loss of stomatal regulation by O3. Monotonic decline in gs with cumulative O3 exposure or flux in current modeling concepts appear to be unrealistic in beech.

Introduction

Ground level ozone (O3) concentration has doubled to date in the northern hemisphere since pre-industrial times, while as depending on region continued enhancement or further increase are prognosticated globally throughout the upcoming decades (Akimoto, 2003, Vingarzan, 2004, Sitch et al., 2007). Ozone is recognized as a significant phytotoxic air pollutant to cause adverse effects on forest ecosystems (Karnosky et al., 2003, Matyssek and Sandermann, 2003, Ashmore, 2005, Bytnerowicz et al., 2007, Serengil et al., 2011, Matyssek et al., 2010a, Matyssek et al., 2014b).

Fagus (beech) is a widespread genus of ecologically and economically important deciduous tree species across Europe, Asia and North America. European beech (Fagus sylvatica) and Siebold's beech (Fagus crenata), being dominant beeches in Europe and Japan, respectively. Both species are distributed in temperate climate regions. European beech is found even in dry climate (southern Italy, ∼37.7 °N) whereas Siebold's beech is confined to humid climate (Fang and Lechowicz, 2006). These two species have been experimentally investigated in view of their O3 sensitivities previously under chamber conditions (Grams et al., 1999, Kozovits et al., 2005a, Kozovits et al., 2005b, Karlsson et al., 2007, Pritsch et al., 2005, Grams and Matyssek, 2010, Luedemann et al., 2005, Luedemann et al., 2009, Yamaguchi et al., 2011). As a result, both species have been classified as O3 sensitive (Kohno et al., 2005, Karlsson et al., 2007, Mills et al., 2010).

O3 impact is mediated through stomatal O3 flux (Omasa et al., 2002, Karlsson et al., 2007, Matyssek et al., 2007a, Matyssek et al., 2008, Mills et al., 2010), because stomata are the principal interface for entry of O3 into plants (cf. Wittmann et al., 2007). A meta-analytic review showed that stomatal narrowing was generally caused by O3 impact, hence, leading to reduce stomatal O3 influx (Wittig et al., 2007). Modeling studies for assessment of O3 impacts in forest trees strive for integrating empirical knowledge through considering O3-induced stomatal narrowing, assuming that stomatal conductance decreases monotonically with cumulative O3 exposure or flux (e.g., Felzer et al., 2004, Sitch et al., 2007, Collins et al., 2010, Mills et al., 2010).

Most of the information regarding O3 effects on trees, however, has been derived from chamber experiments (Pearson and Mansfield, 1993, Le Thiec et al., 1994, Grams et al., 1999, Bortier et al., 2000, Matyssek and Innes, 1999; Watanabe et al., 2005, Gerosa et al., 2008, Matyssek et al., 2010a, Watanabe et al., 2010). Particular meteorological conditions in chambers (e.g., enhanced air temperature, high air turbulence) can change plant response to O3 relative to actual field conditions (Nussbaum and Fuhrer, 2000). Hence, available knowledge and hypotheses have to be evaluated under ecologically relevant forest site conditions, e.g. through technologies such as the recently developed experimental free-air canopy O3 exposure approach (Matyssek et al., 2010a), being focused on forest trees in comparison with a limited number of similar experiments conducted around the world (Karnosky et al., 2007, Matyssek et al., 2010b, Watanabe et al., 2013).

In addition to the different site conditions, tree ages differ between free-air O3 exposure experiments. Difference in the response to O3 between different aged trees has been discussed in several studies (Kolb et al., 1997, Kolb and Matyssek, 2001, Matyssek and Sandermann, 2003). Matyssek et al. (2010a) concluded that adult and juvenile trees of pioneer and climax tree species show similar sensitivity of tree growth to chronic O3 stress, and, however, suggested that the response mechanisms may differ. In general, some leaf physiological parameters are known to change with tree size and age (e.g., Steppe et al., 2011). For instance, stomatal conductance declines with advancing tree dimension and age due to hydraulic constraints (Schäfer et al., 2000, Ryan et al., 2006, Nabeshima and Hiura, 2008), although adverse effects stayed absent on photosynthetic capacity in aging Siebold's beech (Koike, 1988) and adult European beech (Herbinger et al., 2005, Häberle et al., 2012). Experimental examination is advocated, therefore about the ways O3 may affect stomatal regulation in aging forest trees for consolidating ecologically meaningful knowledge about O3 impacts throughout tree ontogeny. Evidential consistency may infer genericness in tree response to chronic O3 stress. Absence of consistency would imply species-driven O3 response, notwithstanding potential effects e.g. by ontogenetic stage, tree dimension or site conditions.

Here, we exemplify a comparison within Fagus between the two above-mentioned species as growing either in Germany (European beech, Kranzberg Forest) or in Japan (Siebold's beech, Sapporo Experimental Forest). At both locations, free-air canopy O3 exposure experiments were operated, consistently employing the methodology as described by Nunn et al., 2002, Werner and Fabian, 2002 and Karnosky et al. (2007). In both cases, O3 effects on stomatal conductance were of interest (Matyssek et al., 2010b, Watanabe et al., 2013). Humid years were selected for the comparison, excluding drought effects on stomata from the analysis. Assessment of stomatal conductance was performed during 09:00 through 15:00 h at both sites, when photosynthetic activity was stable (no midday depression). A differential evaluation will be presented, concluding about regulatory mechanisms that may underlie stomatal responsiveness in either case. The envisaged clarification is intended to consolidate risk assessment and providing grounds for cause-effect based modeling of O3 impacts on forest trees.

Section snippets

Kranzberg Forest

The mixed Fagus sylvatica L./Picea abies [L.] Karst. stand was part of Kranzberg Forest, located near Freising, southern Germany, in the vicinity of Munich (48°25′08″ N, 11°39′41″ E, 485 m a.s.l., annual mean temperature and precipitation: 8.8 °C and 698 mm, respectively, in 2006; see Table 1). Ambient CO2 concentration was around 385 μmol mol−1 (Grams et al., 2011). The soil at the site was a luvisol derived from loess over Tertiary sediments. The European beech trees were about 80 years old

Reduced stomatal conductance under enhanced O3 stress

Leaf mass per area (LMA) was used as an index of light environment for each assessed leaf regardless of O3 treatments, yielding no difference in LMA between ambient and elevated O3 regimes both in European and Siebold's beech (Kitao et al., 2009, Watanabe et al., 2013, Watanabe et al., 2014). Leaf gas exchange along the within-canopy light gradient revealed reduced stomatal aperture under enhanced O3 stress in trees of European and Siebold's beech (Kitao et al., 2009, Watanabe et al., 2014,

Conclusion

Our findings provide evidence that O3-induced stomatal narrowing occurred in trees of European and Siebold's beech that expand in dimension. Reduction of stomatal conductance coincided with unchanged carboxylation capacity and mesophyll conductance during early summer, which did not rule out, however, temporary restriction of the photosynthetic net CO2 uptake rate to some extent. Observed O3-induced stomatal narrowing was, however, diminished in autumn in both sites. This emphasizes interaction

Acknowledgments

We thank Dr. Manuela Baumgarten for providing ozone data at Kranzberg Forest. We are grateful for financial support by the Environment Research & Technology Development Fund of Japan (B-1105) and for a Grant-in-aid from the Japanese Society for Promotion of Science (Type B 23380078, 26292075, Young Scientists B 24710027 and ditto B 24780239, and Young Scientists for research abroad). Outcome from Kranzberg Forest/Germany was based on the CASIROZ project (“The carbon sink strength of beech in a

References (99)

  • R. Matyssek et al.

    Promoting the O3 flux concept for European forest trees

    Environ. Pollut.

    (2007)
  • R. Matyssek et al.

    The challenge of making ozone risk assessment for forest trees more mechanistic

    Environ. Pollut.

    (2008)
  • R. Matyssek et al.

    Advances in understanding ozone impact on forest trees: messages from novel phytotron and free-air fumigation studies

    Environ. Pollut.

    (2010)
  • R. Matyssek et al.

    Enhanced ozone strongly reduces carbon sink strength of adult beech (Fagus sylvatica) – resume from the free-air fumigation study at Kranzberg forest

    Environ. Pollut.

    (2010)
  • A.J. Nunn et al.

    Comparison of ozone uptake and sensitivity between a phytotron study with young beech and a field experiment with adult beech

    Environ. Pollut.

    (2005)
  • S. Nussbaum et al.

    Difference in ozone uptake in grassland species between open-top chambers and ambient air

    Environ. Pollut.

    (2000)
  • E. Pääkkönen et al.

    Variation of ozone sensitivity among clones of Betula pendula and Betula pubescens

    Environ. Pollut.

    (1997)
  • E. Paoletti

    Ozone slows stomatal response to light and leaf wounding in a Mediterranean evergreen broadleaf, Arbutus unedo

    Environ. Pollut.

    (2005)
  • E. Paoletti et al.

    Does living in elevated CO2 ameliorate tree response to ozone? A review on stomatal responses

    Environ. Pollut.

    (2005)
  • E. Paoletti et al.

    Structural and physiological responses to ozone in Manna ash (Fraxinus ornus L.) leaves of seedlings and mature trees under controlled and ambient conditions

    Sci. Total Environ.

    (2009)
  • R. Vingarzan

    A review of surface ozone background levels and trends

    Atmos. Environ.

    (2004)
  • C.R. Warren et al.

    Internal conductance to CO2 transfer of adult Fagus sylvatica: variation between sun and shade leaves and due to free-air ozone fumigation

    Environ. Exp. Botany.

    (2007)
  • M. Watanabe et al.

    Photosynthetic traits of Siebold's beech and oak saplings grown under free air ozone exposure

    Environ. Pollut.

    (2013)
  • M. Watanabe et al.

    Canopy carbon budget of Siebold's beech (Fagus crenata) sapling under free air ozone exposure

    Environ. Pollut.

    (2014)
  • C. Wittmann et al.

    Effects of ozone impact on the gas exchange and chlorophyll fluorescence of juvenile birch stems (Betula pendula Roth

    Environ. Pollut.

    (2007)
  • R. Ahlfors et al.

    Arabidopsis Radical-induced cell death1 belongs to WWE protein-protein interaction domain protein family and modulates abscisic acid, ethylene, and methyl jasmonate responses

    Plant Cell.

    (2004)
  • H. Akimoto

    Global air quality and pollution

    Science

    (2003)
  • M.R. Ashmore

    Assesing the future global impacts of ozone on vegetation

    Plant Cell. Environ.

    (2005)
  • K. Bortier et al.

    Effects of ozone exposure on growth and photosynthesis of beech seedlings (Fagus sylvatica)

    New Phytol.

    (2000)
  • W.J. Collins et al.

    How vegetation impacts affect climate metrics for ozone precursors

    J. Geophys. Res.

    (2010)
  • J. Dumont et al.

    Distinct responses to ozone of abaxial and adaxial stomata in three Euramerican poplar genotypes

    Plant Cell. Environ.

    (2014)
  • J. Fang et al.

    Climatic limits for the present distribution of beech (Fagus L.) species in the world

    J. Biogeogr.

    (2006)
  • P.K. Farage et al.

    An in vivo analysis of photosynthesis during short-term O3 exposure in three contrasting species

    Photosynth. Res.

    (1995)
  • G.D. Farquhar et al.

    On the relationship between carbon isotope discrimination and the intercellular carbon dioxide concentration in leaves

    Aust. J. Plant Physiol.

    (1982)
  • B. Felzer et al.

    Effects of ozone on net primary production and carbon sequestration in the conterminous United States using a biogeochemistry model

    Tellus B

    (2004)
  • A. Furukawa et al.

    Hybrid poplar stomata unresponsive to changes in environmental conditions

    Trees

    (1990)
  • A. Gessler et al.

    Within-canopy and ozone fumigation effects on δ13C and Δ18O in adult beech (Fagus sylvatica) trees: relation to meteorological and gas exchange parameters

    Tree Physiol.

    (2009)
  • T.E.E. Grams 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.

    (1999)
  • T.E.E. Grams et al.

    Combining δ13C andδ18O analysis to unravel competition, CO2 and O3 effects on the physiological performance of different-aged trees

    Plant, Cell. Environ.

    (2007)
  • T.E.E. Grams et al.

    A free-air system for long-term stable carbon isotope labeling of adult forest trees

    Trees

    (2011)
  • K.-H. Häberle et al.

    Case study “Kranzberger Forst”: growth and defence in european beech (Fagus sylvatica l.) and Norway Spruce (Picea abies (L.) karst.)

  • P.J. Hanson et al.

    Seasonal patterns of light-saturated photosynthesis and leaf conductance for mature and seedling Quercus rubra L. foliage: differential sensitivity to ozone exposure

    Tree Physiol.

    (1994)
  • A.S. Heagle et al.

    Growth and yield responses of snap bean to mixtures of carbon dioxide and ozone

    J. Environ. Qual.

    (2002)
  • R.L. Heath et al.

    Physiological processes and plant responses to ozone exposure

  • Y. Hoshika et al.

    Modeling of stomatal ozone conductance for estimating ozone uptake of Fagus crenata under experimentally enhanced free-air ozone exposure

    Water Air Soil. Pollut.

    (2012)
  • Y. Hoshika et al.

    Model-based analysis of avoidance of ozone stress by stomatal closure in Siebold's beech (Fagus crenata)

    Ann. Bot.

    (2013)
  • S. Jehnes et al.

    Tree internal signaling and defence reactions under ozone exposure in sun and shade leaves of European beech (Fagus sylvatica L

    Trees Plant Biol.

    (2007)
  • J. Kangasjärvi et al.

    Signalling and cell death in ozone-exposed plants

    Plant Cell. Environ.

    (2005)
  • D. Karnosky et al.

    Air Pollution, Global Change and Forests in the New Millennium

    (2003)
  • Cited by (29)

    • Physiological and biochemical responses of two sugarcane genotypes growing under free-air ozone exposure

      2018, Environmental and Experimental Botany
      Citation Excerpt :

      On the other hand, O3 effects in C4 species may be related to decreases in phosphoenolpyruvate carboxylase (PEPCase) activity (Leitao et al., 2007, Grantz et al., 2012) as mesophyll cells are less protected from O3-induced damage by ROS as compared to the bundle-sheath cells (Leitao et al., 2007). Ozone stress is also known to induce stomatal impairment, with sluggish responses that affect water control (Paoletti and Grulke, 2010; Hoshika et al., 2015) and an overall closure that limits CO2 influx to leaf mesophyll and then reduces photosynthesis (Kitao et al., 2009, Matyssek et al., 2010, Hoshika et al., 2013, 2015). As an ultimate consequence of damage caused by O3, plants will present reduced biomass accumulation and yield production (Matyssek et al., 2010, Kitao et al., 2012).

    • Ozone affects leaf physiology and causes injury to foliage of native tree species from the tropical Atlantic Forest of southern Brazil

      2018, Science of the Total Environment
      Citation Excerpt :

      Whereas Pn and gwv decreased and RD increased in A. graveolens, gas exchange in C. floribundus showed little change except for an increase in RD. Lower Pn and gwv are classical stress reactions to elevated O3 levels, and they have been observed in many temperate (Fares et al., 2013; Novak et al., 2005, 2007; Reich and Amundson, 1985; Wittig et al., 2007) and tropical tree species (Moraes et al., 2006; Pina and Moraes, 2010). While the decrease in Pn was primarily related to injury caused to the photosynthetic machinery, the decrease in gwv could be related to the increased intercellular CO2 concentration (Ci – data not shown) as a consequence of O3-triggered reduction of carbon assimilation (Hoshika et al., 2015). Such a mechanism was also suggested by the well-retained cell structure of stomata (data not shown - Matyssek et al., 1991; Paoletti et al., 2010).

    • An epidemiological assessment of stomatal ozone flux-based critical levels for visible ozone injury in Southern European forests

      2016, Science of the Total Environment
      Citation Excerpt :

      Indeed, a standard for forest protection is biologically relevant when it translates into real-world forest impacts. Free-air ozone exposure sites assess the effects of increasing tropospheric O3 levels on the structure and function of adult trees (e.g. Karnosky et al., 2003; Matyssek et al., 2004; Karnosky et al., 2005, 2007a,b; Wittig et al., 2009; Matyssek et al., 2010; Hoshika et al., 2015). In Switzerland, Braun et al. (2014) carried out an epidemiological analysis of stem increment data from F. sylvatica and P. abies and confirmed the validity of the flux–response relationship to estimate the growth losses by O3 for adult F. sylvatica trees.

    • Ozone and plants

      2015, Environmental Pollution
    View all citing articles on Scopus
    1

    Present address: Institute of Sustainable Plant Protection, National Research Council of Italy, Via Madonna del Piano 10, I-50019 Sesto Fiorentino, Italy.

    View full text