A unifying explanation for variation in ozone sensitivity among woody plants

Tropospheric ozone is considered the most detrimental air pollutant for vegetation at the global scale, with negative consequences for both provisioning and climate regulating ecosystem services. In spite of recent developments in ozone exposure metrics, from a concentration-based to a more physiologically relevant stomatal flux-based index, large-scale ozone risk assessment is still complicated by a large and unexplained variation in ozone sensitivity among tree species. Here, we explored whether the variation in ozone sensitivity among woody species can be linked to interspecific variation in leaf morphology. We found that ozone tolerance at the leaf level was closely linked to leaf dry mass per unit leaf area (LMA) and that whole-tree biomass reductions were more strongly related to stomatal flux per unit leaf mass (r2  = 0.56) than to stomatal flux per unit leaf area (r2  = 0.42). Furthermore, the interspecific variation in slopes of ozone flux-response relationships was considerably lower when expressed on a leaf mass basis (coefficient of variation, CV = 36%) than when expressed on a leaf area basis (CV = 66%), and relationships for broadleaf and needle-leaf species converged when using the mass-based index. These results show that much of the variation in ozone sensitivity among woody plants can be explained by interspecific variation in LMA and that large-scale ozone impact assessment could be greatly improved by considering this well-known and easily measured leaf trait.

[1]  V. Gutschick Biotic and abiotic consequences of differences in leaf structure , 1999 .

[2]  D. G. Adams,et al.  Tansley Review No. 107. Heterocyst and akinete differentiation in cyanobacteria , 1999 .

[3]  J. McGrath,et al.  Effects of chronic elevated ozone concentration on antioxidant capacity, photosynthesis and seed yield of 10 soybean cultivars. , 2010, Plant, cell & environment.

[4]  M. Sanz,et al.  Promoting the O3 flux concept for European forest trees. , 2007, Environmental pollution.

[5]  S. Long,et al.  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. , 2007, Plant, cell & environment.

[6]  F. Loreto,et al.  Role of Biogenic Volatile Organic Compounds (BVOC) emitted by urban trees on ozone concentration in cities: a review. , 2013, Environmental pollution.

[7]  B. Gimeno,et al.  New critical levels for ozone effects on young trees based on AOT40 and simulated cumulative leaf uptake of ozone , 2004 .

[8]  E. Ainsworth,et al.  Elevated Ozone Concentration Reduces Photosynthetic Carbon Gain but Does Not Alter Leaf Structural Traits, Nutrient Composition or Biomass in Switchgrass , 2019, Plants.

[9]  Mohammad Pessarakli,et al.  Reactive Oxygen Species, Oxidative Damage, and Antioxidative Defense Mechanism in Plants under Stressful Conditions , 2012 .

[10]  D. Falster,et al.  Leaf mass per area, not total leaf area, drives differences in above-ground biomass distribution among woody plant functional types. , 2016, The New phytologist.

[11]  Ülo Niinemets,et al.  Research review. Components of leaf dry mass per area – thickness and density – alter leaf photosynthetic capacity in reverse directions in woody plants , 1999 .

[12]  F. Bussotti Functional leaf traits, plant communities and acclimation processes in relation to oxidative stress in trees: a critical overview , 2008 .

[13]  N. Unger,et al.  Fire air pollution reduces global terrestrial productivity , 2018, Nature Communications.

[14]  F. Loreto,et al.  Abiotic stresses and induced BVOCs. , 2010, Trends in plant science.

[15]  E. Ainsworth,et al.  Understanding and improving global crop response to ozone pollution. , 2017, The Plant journal : for cell and molecular biology.

[16]  G. Mills,et al.  New flux based dose-response relationships for ozone for European forest tree species. , 2015, Environmental Pollution.

[17]  G. Wieser,et al.  Modelling of stomatal conductance and ozone flux of Norway spruce: comparison with field data. , 2000, Environmental pollution.

[18]  B. Gimeno,et al.  Risk assessments for forest trees: the performance of the ozone flux versus the AOT concepts. , 2007, Environmental pollution.

[19]  C. Huntingford,et al.  Indirect radiative forcing of climate change through ozone effects on the land-carbon sink , 2007, Nature.

[20]  L. Poorter,et al.  Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. , 2009, The New phytologist.

[21]  Michael H. Depledge,et al.  Ground-level ozone in the 21st century: future trends, impacts and policy implications , 2008 .

[22]  G. Mills,et al.  Updated stomatal flux and flux-effect models for wheat for quantifying effects of ozone on grain yield, grain mass and protein yield. , 2012, Environmental pollution.

[23]  S. Long,et al.  Quantifying the impact of current and future tropospheric ozone on tree biomass, growth, physiology and biochemistry: a quantitative meta‐analysis , 2009 .

[24]  Xiaoke Wang,et al.  Responses of native broadleaved woody species to elevated ozone in subtropical China. , 2012, Environmental pollution.

[25]  A. Tuzet,et al.  Integrative leaf-level phytotoxic ozone dose assessment for forest risk modelling , 2013 .

[26]  V. Calatayud,et al.  Differences in ozone sensitivity among woody species are related to leaf morphology and antioxidant levels. , 2016, Tree physiology.

[27]  M. Lerdau A Positive Feedback with Negative Consequences , 2007, Science.

[28]  Keith E. MasJeus,et al.  Quantifying the Impact of , 2000 .

[29]  Stephen Sitch,et al.  The effects of tropospheric ozone on net primary productivity and implications for climate change. , 2012, Annual review of plant biology.

[30]  Jianguo Zhu,et al.  Apoplastic ascorbate contributes to the differential ozone sensitivity in two varieties of winter wheat under fully open-air field conditions. , 2010, Environmental pollution.

[31]  P. Reich,et al.  Quantifying plant response to ozone: a unifying theory. , 1987, Tree physiology.

[32]  L. Horowitz,et al.  Global crop yield reductions due to surface ozone exposure: 1. Year 2000 crop production losses and economic damage , 2011 .

[33]  D. Royer,et al.  Roles of climate and functional traits in controlling toothed vs. untoothed leaf margins. , 2012, American journal of botany.

[34]  H. Pleijel,et al.  Differential effects of ozone on photosynthesis of winter wheat among cultivars depend on antioxidative enzymes rather than stomatal conductance. , 2016, The Science of the total environment.

[35]  Ü. Niinemets,et al.  Glandular trichomes as a barrier against atmospheric oxidative stress: Relationships with ozone uptake, leaf damage, and emission of LOX products across a diverse set of species. , 2018, Plant, cell & environment.