Elsevier

Science of The Total Environment

Volume 651, Part 1, 15 February 2019, Pages 1310-1320
Science of The Total Environment

Different belowground responses to elevated ozone and soil water deficit in three European oak species (Quercus ilex, Q. pubescens and Q. robur)

https://doi.org/10.1016/j.scitotenv.2018.09.246Get rights and content

Highlights

  • Combined effects of ozone and water deficit on roots and ectomycorrhizae are not known.

  • Greater effects of ozone were observed in well-watered oak plants.

  • Effects were complex, species-specific and root-trait specific.

  • Belowground responses may change water, nutrient and carbon cycling in plants.

Abstract

Effects on roots due to ozone and/or soil water deficit often occur through diminished belowground allocation of carbon. Responses of root biomass, morphology, anatomy and ectomycorrhizal communities were investigated in seedlings of three oak species: Quercus ilex L., Q. pubescens Willd. and Q. robur L., exposed to combined effects of elevated ozone (ambient air and 1.4 × ambient air) and water deficit (100% and 10% irrigation relative to field capacity) for one growing season at a free-air ozone exposure facility. Effects on root biomass were observed as general reduction in coarse root biomass by −26.8% and in fine root biomass by −13.1% due to water deficit. Effect on coarse root biomass was the most prominent in Q. robur (−36.3%). Root morphological changes manifested as changes in proportions of fine root (<2 mm) diameter classes due to ozone and water deficit in Q. pubescens and due to water deficit in Q. robur. In addition, reduced fine root diameter (−8.49%) in Q. robur was observed under water deficit. Changes in root anatomy were observed as increased vessel density (+18.5%) due to ozone in all three species, as reduced vessel tangential diameter (−46.7%) in Q. ilex due to interaction of ozone and water, and as generally increased bark to secondary xylem ratio (+47.0%) due to interaction of ozone and water. Water deficit influenced occurrence of distinct growth ring boundaries in roots of Q. ilex and Q. robur. It shifted the ectomycorrhizal community towards dominance of stress-resistant species, with reduced relative abundance of Tomentella sp. 2 and increased relative abundances of Sphaerosporella brunnea and Thelephora sp. Our results provide evidence that expression of stress effects varies between root traits; therefore the combined analysis of root traits is necessary to obtain a complete picture of belowground responses.

Introduction

Tropospheric ozone (O3) is a phytotoxic air pollutant that is produced by photochemical oxidation of carbon monoxide and hydrocarbons in the presence of nitric oxides. Ozone is transported with air masses from polluted areas with high concentrations of its precursors, consequently affecting air quality on regional, intercontinental and hemispheric scales (Monks et al., 2015). Globally, tropospheric ozone concentrations have increased by 30% since the pre-industrial era (Young et al., 2013), while the predictions of future trends deal with several challenges and uncertainties (Monks et al., 2015; Ridley et al., 2017). In some parts of the world, emissions of ozone precursors are still rising, thereby affecting ozone concentrations on a global scale (Verstraeten et al., 2015). Ozone affects plant metabolism through the generation of free radicals and has the potential to modulate plant response to water deficit through interference with stomatal control mechanisms (Hayes et al., 2012; Hoshika et al., 2015; Monks et al., 2015). Plants often face a water deficit, even outside arid or semi-arid areas (Chaves et al., 2002). Global warming has already increased drying over many land areas in the last 30 years and is expected to further increase soil moisture deficit in space and time over the 21st century (Dai, 2011).

Different studies on the interactive effects of ozone exposure and water deficit in trees have resulted in contradictory findings. Either a protective role of water deficit against ozone stress - by means of decreasing ozone uptake due to stomatal closure (Temple et al., 1992; Paoletti and Grulke, 2005; Hoshika et al., 2015; Gao et al., 2017; Hoshika et al., 2018) - or no interactive effect of ozone and water deficiency (Le Thiec et al., 1994; Karlsson et al., 2002; Matyssek et al., 2006; Alonso et al., 2014) have been suggested. Although the primary site of ozone effects is leaves, responses in roots occur through diminished allocation of carbohydrates belowground (Matyssek et al., 2010). In some cases, root responses develop even before shoot effects are observed (Andersen, 2003). Ozone has an effect on cytokinin levels in leaves depending on the age of the tree, resulting in contrasting responses of roots and associated mycorrhizal fungi in adult trees and seedlings (Kraigher et al., 2008). Although water deficit has a similar negative effect on belowground allocation of carbon (Hagedorn et al., 2016) as ozone, studies of the interactive effects of ozone and water deficit on belowground parts of trees are limited to investigations of total root biomass as a part of total biomass measurements or carbon allocation patterns (reviewed by Agathokleous et al., 2015).

The role of roots with associated mycorrhizal symbionts in water and nutrient acquisition from soil and transport to aboveground parts is crucial for tree survival and growth. Moreover, they play a key role in ecosystem processes (Bardgett et al., 2014; Ellison et al., 2017; van der Linde et al., 2018). Given the enormous plasticity of roots in relation to their environment (Bardgett et al., 2014), their responses to a combination of ozone and water deficit could be substantial. In aboveground parts of three oak species (Quercus ilex, Q. pubescens and Q. cerris), biometric plasticity accounted for 40–50% of phenotypic plasticity in response to ozone and water deficit (Cotrozzi et al., 2016).

Mediterranean Europe is a hotspot of high tropospheric ozone in summer due to intense solar radiation, high temperatures and very dry conditions (Millán et al., 1997). For this area, further decrease in soil moisture in summer is expected to occur in 2021–2050 due to global changes (Kovats et al., 2014). The main objective of our study was to investigate the effects of elevated ozone and water deficit on tree root biomass, morphology, anatomy and ectomycorrhizal communities. Seedlings of three common European oak species with different levels of adaptation to water deficit were used. Holm oak (Quercus ilex L.) is an evergreen sclerophyllous drought-tolerant Mediterranean species, distributed in the central-western part of the Mediterranean basin (de Rigo and Caudullo, 2016); pubescent oak (Q. pubescens Willd.) is a deciduous or semi-deciduous tree of south-eastern Europe with the ability to withstand moderate summer drought (Pasta et al., 2016), while pedunculate oak (Q. robur L.) is a deciduous species widespread in Europe with preference for moist soils (Eaton et al., 2016). These species are all ectomycorrhizal. As a typical representative of sclerophyllous vegetation with low gas exchange rates and high constitutive levels of antioxidants (Paoletti, 2006; Alonso et al., 2014), Q. ilex was hypothesized to suffer less ozone damage to belowground parts in full water supply conditions compared to Q. pubescens and Q. robur. In water deficient conditions, Q. ilex was expected to suffer from combined effects of water deficit and ozone due to its keeping stomata open (i.e. anisohydric behaviour), which leads to ozone uptake into plants even under water deficit, whereas in Q. robur only effects of water deficit were postulated due to its isohydric strategy, which results in the limitation of ozone uptake due to stomatal closure under water deficit. Finally, Q. pubescens was expected to show an intermediate behaviour.

In detail, we hypothesized that ozone and water deficiency as single factors would: (a) decrease root biomass and change root morphological properties, b) induce root anatomical changes, such as vessel size, vessel density and tissue ratios and c) reduce mycorrhization and shift ectomycorrhizal communities towards stress-resistant types. For the combined factors, we hypothesized that: d) greater negative effects of ozone on roots and ectomycorrhizal communities occur for well-watered plants, and e) species-specific effects occur due to the different strategies of these plant species to cope with water deficit.

Section snippets

Origin of seedlings

Two-year-old Q. ilex seedlings of provenance LRBS 45 (Pineta di Classe, Ravenna, Italy) were obtained from the tree nursery Vivaio di Pieve S. Stefano (Arezzo, Italy). Seedlings were raised from seeds in pots (10 × 10 × 30 cm), using a substrate mixture composed of 1/3 local soil (calcareous geological bedrock), 1/3 white Lithuanian peat and 1/3 calcareous local river sand. To this mixture, pumice from Viterbo (Italy) was added. Two-year-old seedlings of Q. pubescens of provenance SR. n.

Results

Figures and tables in the main text refer to statistically significant results, while the SM shows all the data.

Discussion

Root traits are increasingly recognized as drivers of many ecosystem processes, such as carbon, water and nutrient cycling, soil formation and structural stability (Bardgett et al., 2014; Ellison et al., 2017; Fort et al., 2017). To be able to predict responses of terrestrial ecosystems to expected future abiotic changes with higher accuracy, the response of root traits needs to be better investigated (Bardgett et al., 2014). In the experiment described here, the combined effects of elevated

Conclusions

The effects of elevated ozone and water deficit on three oak species were species-specific and complex, suggesting that belowground responses to these stress factors should be studied holistically, as investigation of only one root trait or plant species can be misleading. The hypothesized decrease in root biomass for both stress factors was confirmed only for water deficit. Root morphological parameters were changed due to either ozone or water deficit in Q. pubescens and just due to water

Acknowledgements

The authors would like to thank Alessandro Materassi and Gianni Fasano from IBIMET-CNR for the management of the O3 FACE, Moreno Lazzara from IPSP-CNR for support during the field work, and employees and students of the Department of Tree Physiology and Genetics of Slovenian Forestry Institute for cleaning of roots, separation of ectomycorrhizal morphotypes and scanning. The study was financially supported by: Fondazione Cassa di Risparmio di Firenze (2013/7956), LIFE15 ENV/IT/000183 project

References (82)

  • X. Wang et al.

    Ectomycorrhizal colonization and growth of the hybrid larch F1 under elevated O3 and CO2

    Environ. Pollut.

    (2015)
  • T.J. White et al.

    Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics

  • R.Z. Abramoff et al.

    Are above- and below-ground phenology in sync?

    New Phytol.

    (2015)
  • J. Abrantes et al.

    Environmental control of vessel traits in Quercus ilex under Mediterranean climate: relating xylem anatomy to function

    Trees

    (2013)
  • E. Agathokleous et al.

    A review study on past 40 years of research on effects of tropospheric O3 on belowground structure, functioning, and processes of trees: a linkage with potential ecological implications

    Water Air Soil Pollut.

    (2015)
  • R. Agerer et al.

    DEEMY – An Information System for Characterization and Determination of Ectomycorrhizae

    (2004–2017)
  • R. Aloni et al.

    Role of cytokinin and auxin in shaping root architecture: regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism

    Ann. Bot.

    (2006)
  • R. Alonso et al.

    Drought stress does not protect Quercus ilex L. from ozone effects: results from a comparative study of two subspecies differing in ozone sensitivity

    Plant Biol.

    (2014)
  • C.P. Andersen

    Source–sink balance and carbon allocation below ground in plants exposed to ozone

    New Phytol.

    (2003)
  • R.M. Atlas et al.

    Microbial Ecology: Fundamentals and Applications

    (1981)
  • G. Battipaglia et al.

    Structure and function of intra–annual density fluctuations: mind the gaps

    Front. Plant Sci.

    (2016)
  • I. Brunner et al.

    How tree roots respond to drought

    Front. Plant Sci.

    (2015)
  • P. Büker et al.

    DO3SE modelling of soil moisture to determine ozone flux to forest trees

    Atmos. Chem. Phys.

    (2012)
  • R. Burke et al.

    Laccases and other polyphenol oxidases in ecto- and ericoid mycorrhizal fungi

    Mycorrhiza

    (2002)
  • M.M. Chaves et al.

    How plants cope with water stress in the field? Photosynthesis and growth

    Ann. Bot.

    (2002)
  • J.V. Colpaert

    Thelephora

  • L. Cotrozzi et al.

    Variations in physiological and biochemical traits of oak seedlings grown under drought and ozone stress

    Physiol. Plant.

    (2016)
  • CRLTAP

    The UNECE Convention on Long-range Transboundary Air Pollution. Manual on Methodologies and Criteria for Modelling and Mapping Critical Loads and Levels and Air Pollution Effects, Risks and Trends: Chapter III Mapping Critical Levels for Vegetation

    (2017)
  • P. Cudlin et al.

    Fine roots and ectomycorrhizas as indicators of environmental change

    Plant Biosyst.

    (2007)
  • A. Dai

    Drought under global warming: a review

    Wiley Interdiscip. Rev. Clim. Chang.

    (2011)
  • R.M. Danielson

    Ectomycorrhiza formation by the operculate discomycete Sphaerosporella brunnea (Pezizales)

    Mycologia

    (1984)
  • D. de Rigo et al.

    Quercus ilex in Europe: distribution, habitat, usage and threats

  • N. Delpierre et al.

    Temperate and boreal forest tree phenology: from organ-scale processes to terrestrial ecosystem models

    Ann. For. Sci.

    (2016)
  • E. Eaton et al.

    Quercus robur and Quercus petraea in Europe: distribution, habitat, usage and threats

  • B. Eilmann et al.

    Drought-induced adaptation of the xylem in Scots pine and pubescent oak

    Tree Physiol.

    (2009)
  • D.M. Eissenstat

    Costs and benefits of constructing roots of small diameter

    J. Plant Nutr.

    (1992)
  • R.D. Finlay

    Ecological aspects of mycorrhizal symbiosis: with special emphasis on the functional diversity of interactions involving the extraradical mycelium

    J. Exp. Bot.

    (2008)
  • F. Fort et al.

    Root traits are related to plant water-use among rangeland Mediterranean species

    Funct. Ecol.

    (2017)
  • M.N. Fotelli et al.

    Water stress responses of seedlings of four Mediterranean oak species

    Tree Physiol.

    (2000)
  • M. Gardes et al.

    ITS primers with enhanced specificity for basidiomycetes–application to the identification of mycorrhizae and rusts

    Mol. Ecol.

    (1993)
  • C.A. Gehring et al.

    Convergence in mycorrhizal fungal communities due to drought, plant competition, parasitism, and susceptibility to herbivory: consequences for fungi and host plants

    Front. Microbiol.

    (2014)
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    Present address: Institute of Biometeorology, National Research Council of Italy (IBIMET-CNR), Via Gobetti 101, 40129 Bologna, Italy.

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