Main conclusion
Atmospheric p CO 2 impacts Quercus petraea biomass production and cell wall composition of the leaves in favor of cellulose at the expense of lignin, and enhances foliar non-structural carbohydrate levels and sucrose contents in a pCO 2 concentration-dependent manner.
Sessile oak (Quercus petraea Liebl.) was grown for ca. half a year from seeds at ambient control (525 ppm), 750, 900, and 1000 ppm atmospheric pCO2 under controlled conditions. Increasing pCO2 enhanced biomass production, modified the cell wall composition of the leaves in favor of cellulose at the expense of lignin, and enhanced the foliar non-structural carbohydrate level, in particular the sucrose content; as well as total N content of leaves by increased levels of all major N fractions, i.e., soluble proteins, total amino acids, and structural N. The enhanced total amino acid level was largely due to 2-ketoglutarate and oxalo acetate-derived compounds. Increasing pCO2 alleviated oxidative stress in the leaves as indicated by reduced H2O2 contents. High in vitro glutathione reductase activity at reduced H2O2 contents suggests enhanced ROS scavenging, but increased lipid peroxidation may also have contributed, as indicated by a negative correlation between malone dialdehyde and H2O2 contents. Almost all these effects were at least partially reversed, when pCO2 exceeded 750 or 900 ppm. Apparently, the interaction of atmospheric pCO2 with leaf structural and physiological traits of Q. petraea seedlings is characterized by a dynamic response depending on the pCO2 level.
Similar content being viewed by others
Abbreviations
- CO2 :
-
Carbon dioxide
- DW:
-
Dry weight
- FW:
-
Fresh weight
- SBM:
-
Structural biomass
- MDA:
-
Malone dialdehyde
- GR:
-
Glutathione reductase
- ROS:
-
Reactive oxygen species
References
Abrams MD (1990) Adaptations and responses to drought in Quercus species of North America. Tree Physiol 7:227–238
Ainsworth EA, Long S (2005) What have we learned from 15 years of free-air CO2 enrichment (FACE)? A meta-analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytol 165:351–372
Ainsworth EA, Davey PA, Bernacchi CJ, Dermody OC, Heaton EA, Moore DJ, Morgan PB, Naidu SL, Yoo Ra HS, Zhu XG, Curtis PS (2002) A meta-analysis of elevated [CO2] effects on soybean (glycine max) physiology, growth and yield. Glob Chang Biol 8:695–709
Ainsworth EA, Rogers A, Leakey AD, Heady LE, Gibon Y, Stitt M, Schurr U (2007) Does elevated atmospheric [CO2] alter diurnal C uptake and the balance of C and N metabolites in growing and fully expanded soybean leaves? J Exp Bot 58:579–591
Albert KR, Ro-Poulsen H, Mikkelsen TN, Michelsen A, Van der Linden L, Beier C (2011) Interactive effects of elevated CO2, warming, and drought on photosynthesis of Deschampsia flexuosa in a temperate heath ecosystem. J Exp Bot 62:4253–4266
Al-Saidi A, Fukuzawa Y, Furukawa N, Ueno M, Baba S, Kawamitsu Y (2009) A system for the measurement of vertical gradients of CO2, H2O and air temperature within and above the canopy of plant. Plant Prod Sci 12:139–149
Annighöfer P, Beckschäfer P, Vor T, Ammer C (2015) Regeneration patterns of European oak species [Quercus petraea (Matt.) Liebl., Quercus robur L.] in dependence of environment and neighborhood. PLoS One 10:e0134935
Aranjuelo I, Cabrera-Bosquet L, Morcuende R, Avice JC, Nogués S, Araus JL, Martínez-Carrasco R, Pérez P (2011) Does ear C sink strength contribute to overcoming photosynthetic acclimation of wheat plants exposed to elevated CO2? J Exp Bot 62:3957–3969
Bazzaz FA, Williams WE (1991) Atmospheric CO2 concentrations within a mixed forest: implications for seedling growth. Ecology 72:12–16
Billings SA, Zitzer SF, Weatherly H, Schaeffer SM, Charlet T, Arnone JA, Evans RD (2003) Effects of elevated carbon dioxide on green leaf tissue and leaf litter quality in an intact Mojave Desert ecosystem. Global Change Biol 9:729–735
Blaschke L, Schulte M, Raschi A, Slee N, Rennenberg H, Polle A (2001) Photosynthesis, soluble and structural carbon compounds in two Mediterranean oak species (Quercus pubescens and Q. ilex) after lifetime growth at naturally elevated CO2 concentrations. Plant Biol 3:288–298
Blaschke L, Forstreuter M, Sheppard LJ, Leith IK, Murray MB, Polle A (2002) Lignification in beech (Fagus sylvatica) grown at elevated CO2 concentrations: interaction with nutrient availability and leaf maturation. Tree Physiol 22:469–477
Brändli UB (1996) Die häufigsten Waldbäume der Schweiz. Ergebnisse aus dem Landesforstinventar 1983–85. Verbreitung, Standort und Häufigkeit von 30 Baumarten. Ber. Eidgenöss. Forsch WSL 342:107–120
Brinkmann K, Blaschke L, Polle A (2002) Comparison of different methods for lignin determination as a basis for calibration of near-infrared reflectance spectroscopy and implications of lingoproteins. J Chem Ecol 28:2483–2501
Cha S, Chae HM, Lee SH, Shim JK (2017) Effect of elevated atmospheric CO2 concentration on growth and leaf litter decomposition of Quercus acutissima and Fraxinus rhynchophylla. PLoS One 12:e0171197
Ciais P, Reichstein M, Viovy N, Granier A, Ogeé J, Allard V, Aubinet M, Buchmann N, Bernhofer C, Carrara A, Chevallier F, De Noblet N, Friend AD, Friedlingstein P, Grünwald T, Heinesch B, Keronen P, Knohl A, Krinner G, Loustau D, Manca G, Matteuci G, Migletta F, Ourcival JM, Papale D, Pilegaard K, Rambal S, Seufert G, Soussana JF, Sanz MJ, Schulze ED, Vesala T, Valentine R (2005) Europe-wide reduction in primary productivity caused by heat and drought in 2003. Nature 437:529–533
Contin DR, Soriani HH, Hernandez I, Furriel RPM, Munne-Bosch S, Martinez CA (2014) Antioxidant and photoprotective defenses in response to gradual water stress under low and high irradiance in two Malvaceae tree species used for tropical forest restoration. Trees 28:1705–1722
Cubasch U, Wuebbles D, Chen D, Facchini MC, Frame D, Mahowald N, Winther J-G (2013) Introduction. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate change 2013: the physical science basis. Contribution of Working Group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, pp 119–158
Dannenmann M, Simon J, Gasche R, Holst J, Naumann PS, Kögel-Knabner I, Knicker H, Mayer H, Schloter M, Pena R, Polle A, Rennenberg H, Papen H (2009) Tree girdling provides insight on the role of labile carbon in nitrogen partitioning between soil microorganisms and adult European beech. Soil Biol Biochem 41:1622–1631
Davidson EA, Richardson AD, Savage KE, Hollinger DY (2006) A distinct seasonal pattern of the ratio of soil respiration to total ecosystem respiration in a spruce-dominated forest. Glob Chang Biol 12:230–239
Endler C, Oehler K, Matzarakis A (2010) Vertical gradient of climate change and climate tourism conditions in the Black Forest. Int J Biometeorol 54:45–61
Foyer CH, Halliwell B (1976) The presence of glutathione and glutathione reductase in chloroplasts: a proposed role in ascorbic acid metabolism. Planta 133:21–25
Fürstenberg-Hägg J, Zagrobelny M, Bak S (2013) Plant defense against insect herbivores. Int J Mol Sci 14:10242–10297
Geßler A, Duarte HM, Franco AC, Luettge U, de Mattos EA, Nahm M, Scarano FR, Zaluar HLT, Rennenberg H (2005) Ecophysiology of selected tree species in different plant communities at the periphery of the Atlantic Forest of SE-Brazil II. Spatial and ontogenetic dynamics in Andira legalis, a deciduous legume tree. Trees 19:510–522
Goh CH, Ko SM, Koh S, Kim YJ, Bae HJ (2012) Photosynthesis and environments: photoinhibition and repair mechanisms in plants. J Plant Biol 55:93–101
Gomez L, Faurobert M (2002) Contribution of vegetative storage proteins to seasonal nitrogen variations in the young shoots of peach trees (Prunus persica L. Batsch). J Exp Bot 53:2431–2439
Hall MC, Stiling P, Moon DC, Drake BG, Hunter MD (2005) Effects of elevated CO2 on foliar quality and herbivore damage in a scrub oak ecosystem. J Chem Ecol 31:267–286
Hoffmann WA, Bazzaz FA, Chatterton NJ, Harrison PA, Jackson RB (2000) Elevated CO2 enhances resprouting of a tropical savanna tree. Oecologia 123:312–317
Holzinger R, Sandoval-Soto L, Rottenberger S, Crutzen PJ, Kesselmeier J (2000) Emissions of volatile organic compounds from Quercus ilex L. measured by proton transfer reaction mass spectrometry under different environmental conditions. J Geophys Res Atmos 105:20573–20579
Hu B, Simon J, Kuster TM, Arend M, Siegwolf R, Rennenberg H (2013a) Nitrogen partitioning in oak leaves depends on species, provenance, climate conditions and soil type. Plant Biol 15:198–209
Hu B, Simon J, Rennenberg H (2013b) Drought and air warming affect the levels of stress related metabolites in leaves of oak trees on acidic and calcareous soil. Tree Physiol 33:489–504
Huang JG, Bergeron Y, Denneler B, Berninger F, Tardif J (2007) Response of forest trees to increased atmospheric CO2. Crit Rev Plant Sci 26:265–283
IPCC (2013) Summary for policy makers. In: Stocker TF, Qin D, Plattner GK, Tignor M, Allen SK, Boschung J et al (eds) Climate change 2013. The Physical science basis. Contribution of Working Group I to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, New York
Johnson SN, Ryalls JMW, Karley AJ (2014) Global climate change and crop resistance to aphids: contrasting responses of lucerne genotypes to elevated atmospheric carbon dioxide. Ann Appl Biol 165:62–72
Kopka J, Schauer N, Krueger S, Birkemeyer C, Usadel B, Bergmuller E, Dörmmann P, Gibon Y, Stiii M, Willmitzer L, Fernie AR, Steinhauser D (2005) GMD@CSB.DB: the golm metabolome database. Bioinformatics 21:1635–1638
Kostiainen K, Jalkanen H, Kaakinen S, Saranpaeae P, Vapaavuori E (2006) Wood properties of two silver birch clones exposed to elevated CO2 and O3. Glob Chang Biol 12:1230–1240
Kreuzwieser J, Hauberg J, Howell KA, Carroll A, Rennenberg H, Millar AH, Whelan J (2009) Differential response of grey poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiol 14:461–473
Leakey ADB, Ainsworth EA, Bernacchi CJ, Rogers A, Long SP, Ort DR (2009) Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. J Exp Bot 60:2859–2876
Li Q, Chen J, Moorhead DL (2012a) Respiratory carbon losses in a managed oak forest ecosystem. For Ecol Manag 279:1–10
Li T, Di Z, Han X, Yang X (2012b) Elevated CO2 improves root growth and cadmium accumulation in the hyperaccumulator Sedum alfredii. Plant Soil 354:325–334
Liu X, Kozovits AR, Grams TE, Blaschke H, Rennenberg H, Matyssek R (2004) Competition modifies effects of enhanced ozone/carbon dioxide concentrations on carbohydrate and biomass accumulation in juvenile Norway spruce and European beech. Tree Physiol 24:1045–1055
Long SP, Ainsworth EA, Rogers A, Ort DR (2004) Rising atmospheric carbon dioxide: plants FACE the future. Ann Rev Plant Biol 55:591–628
Loreto F, Velikova V (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol 127:781–787
Luo ZB, Janz D, Jiang X, Göbel C, Wildhagen H, Tan Y, Rennenberg H, Feussner I, Polle A (2009) Upgrading root physiology for stress tolerance by ectomycorrhizas: insights from metabolite and transcriptional profiling into reprogramming for stress anticipation. Plant Physiol 151:1902–1917
Maestre FT, Reynolds JF (2007) Biomass responses to elevated CO2, soil heterogeneity and diversity: an experimental assessment with grassland assemblages. Oecologia 151:512–520
Matros A, Amme S, Kettig B, Buck-Sorlin GH, Sonnewald U, Mock HP (2006) Growth at elevated CO2 concentrations leads to modified profiles of secondary metabolites in tobacco cv. SamsunNN and to increased resistance against infection with potato virus Y. Plant Cell Environ 29:126–137
Meuriot F, Decau ML, Morvan-Bertrand A, Prud’Homme MP, Gastal F, Simon JC, Volenec JJ, Avice JC (2005) Contribution of initial C and N reserves in Medicago sativa recovering from defoliation: impact of cutting height and residual leaf area. Funct Plant Biol 32:321–334
Mishra AK, Rai R, Agrawal SB (2013) Individual and interactive effects of elevated carbon dioxide and ozone on tropical wheat (Triticumae stivum L.) cultivars with special emphasis on ROS generation and activation of antioxidant defence system. Indian J Biochem Biophys 50:39–149
Munné-Bosch S, Queval G, Foyer CH (2014) The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiol 28:1705–1722
Murayama S, Saigusa N, Chan D, Yamamoto S, Kondo H, Eguchi Y (2003) Temporal variations of atmospheric CO2 concentration in a temperate deciduous forest in central Japan. Tellus B Chem Phys Meteorol 55:232–243
Newman JA, Abner ML, Dado RG, Gibson DJ, Brookings A, Parsons AJ (2003) Effects of elevated CO2, nitrogen and fungal endophyte-infection on tall fescue: growth, photosynthesis, chemical composition and digestibility. Glob Chang Biol 9:425–437
Nixon KC (2006) Global and Neotropical distribution and diversity of oak (genus Quercus) and oak forests. In: Kappelle M (ed) Ecology and conservation of Neotropical montane oak forests. Ecological studies, vol 185. Springer, Berlin, pp 3–13
Nösberger J, Long SP, Norby RJ, Stitt M, Hendrey GR, Blum H (eds) (2006) Managed ecosystems and CO2: case studies, processes, and perspectives, vol 187. Springer, Berlin
Novriyanti E, Watanabe M, Kitao M, Utsugi H, Uemura A, Koike T (2012) High nitrogen and elevated CO2 effects on the growth, defense and photosynthetic performance of two eucalypt species. Environ Pollut 170:124–130
Overdieck D, Fenselau K (2009) Elevated CO2 concentration and temperature effects on the partitioning of chemical components along juvenile Scots pine stems (Pinus sylvestris L.). Trees 23:771–786
Palmroth S, Katul GG, Maier CA, Ward E, Manzoni S, Vico G (2013) On the complementary relationship between marginal nitrogen and water-use efficiencies among Pinus taeda leaves grown under ambient and CO2-enriched environments. Ann Bot 111:467–477
Peever TL, Higgins VJ (1989) Electrolyte leakage, lipoxygenase, and lipid peroxidation induced in tomato leaf tissue by specific and nonspecific elicitors from Cladosporium fulvum. Plant Physiol 90:867–875
Penuelas J, Sardans J, Estiarte M, Ogaya R, Carnicer J, Coll M, Barbeta A, Rivas-Ubach A, Llusia J, Garbulsky M, Filella I (2013) Evidence of current impact of climate change on life: a walk from genes to the biosphere. Glob Chang Biol 19:2303–2338
Polle A, McKee I, Blaschke L (2001) Altered physiological and growth responses to elevated [CO2] in offspring from holm oak (Quercus ilex L.) mother trees with lifetime exposure to naturally elevated [CO2]. Plant Cell Environ 24:1075–1083
Pongratz J, Caldeira K (2012) Attribution of atmospheric CO2 and temperature increases to regions: importance of preindustrial land use change. Environ Res Lett 7:034001
Pritchard SG, Rogers HH (2000) Spatial and temporal deployment of crop roots in CO2-enriched atmospheres. New Phytol 147:55–71
Ryalls JM, Moore BD, Riegler M, Gherlenda AN, Johnson SN (2014) Amino acid-mediated impacts of elevated carbon dioxide and simulated root herbivory on aphids are neutralized by increased air temperatures. J Exp Bot 66:613–623
Salazar-Parra C, Aguirreolea J, Sánchez-Díaz M, Irigoyen JJ, Morales F (2012) Climate change (elevated CO2, elevated temperature and moderate drought) triggers the antioxidant enzymes’ response of grapevine cv. Tempranillo, avoiding oxidative damage. Physiol Plant 144:99–110
Schwanz P, Polle A (1998) Antioxidative systems, pigment and protein contents in leaves of adult Mediterranean oak species (Quercus pubescens and Q. ilex) with lifetime exposure to elevated CO2. New Phytol 140:411–423
Schwanz P, Kimball BA, Idso SB, Hendrix DL, Polle A (1996) Antioxidants in sun and shade leaves of sour orange trees (Citrus aurantium) after long-term acclimation to elevated CO2. J Exp Bot 47:1941–1950
Singh A, Agrawal M (2015) Effects of ambient and elevated CO2 on growth, chlorophyll fluorescence, photosynthetic pigments, antioxidants, and secondary metabolites of Catharanthus roseus (L.) G Don. grown under three different soil N levels. Environ Sci Pollut Res 22:3936–3946
Staudt M, Joffre R, Rambal S, Kesselmeier J (2001) Effect of elevated CO2 on monoterpene emission of young Quercus ilex trees and its relation to structural and ecophysiological parameters. Tree Physiol 21:437–445
Tausz M, Olszyk DM, Monschein S, Tingey DT (2004) Combined effects of CO2 and O3 on antioxidative and photoprotective defense systems in needles of ponderosa pine. Biol Plant 48:543–548
Teng N, Jin B, Wang Q, Hao H, Ceulemans R, Kuang T, Lin J (2009) No detectable maternal effects of elevated CO2 on Arabidopsis thaliana over 15 generations. PLoS One 4:e6035
Top SM, Filley TR (2014) Effects of elevated CO2 on the extractable amino acids of leaf litter and fine roots. New Phytol 202:1257–1266
Updegraff DM (1969) Semimicro determination of cellulose in biological materials. Anal Biochem 32:420–424
Vaz M, Cochard H, Gazarini L, Graça J, Chaves MM, Pereira JS (2012) Cork oak (Quercus suber L.) seedlings acclimate to elevated CO2 and water stress: photosynthesis, growth, wood anatomy and hydraulic conductivity. Trees 26:1145–1157
Vivin P, Guehl JM (1997) Changes in carbon uptake and allocation patterns in Quercus robur seedlings in response to elevated CO2 and water stress: an evaluation with 13C labelling. Annal Sci Forest 54:597–610
Vurro E, Bruni R, Bianchi A, di Toppi LS (2009) Elevated atmospheric CO2 decreases oxidative stress and increases essential oil yield in leaves of Thymus vulgaris grown in a mini-FACE system. Environ Exp Bot 65:99–106
Wagner S, Berg P, Schädler G, Kunstmann H (2013) High resolution regional climate model simulations for Germany: part II—projected climate changes. Clim Dyn 40:415–427
Winter H, Lohaus G, Heldt HW (1992) Phloem transport of amino acids in relation to their cytosolic levels in barley leaves. Plant Physiol 99:996–1004
Wu G, Chen F, Ge F (2007) Effects of elevated CO2 on the growth and foliar chemistry of transgenic Bt cotton. J Integr Plant Biol 49:1361–1369
Xu Z, Jiang Y, Zhou G (2015) Response and adaptation of photosynthesis, respiration, and antioxidant systems to elevated CO2 with environmental stress in plants. Front Plant Sci 6:701
Yu J, Chen L, Xu M, Huang B (2012) Effects of elevated CO2 on physiological responses of tall fescue to elevated temperature, drought stress, and the combined stresses. Crop Sci 52:1848
Zhang FF, Wang YL, Huang ZZ, Zhu XC, Zhang FJ, Chen FD, Fang WM, Teng NJ (2012) Effects of CO2 enrichment on growth and development of Impatiens hawkeri. Sci World J 12:2012
Zhu C, Xu X, Wang D, Zhu J, Liu G, Seneweera S (2016) Elevated atmospheric [CO2] stimulates sugar accumulation and cellulose degradation rates of rice straw. GCB Bioenerg 8:579–587
Zinta G, AbdElgawad H, Domagalska MA, Vergauwen L, Knapen D, Nijs I, Janssens IA, Beemster GT, Asard H (2014) Physiological, biochemical, and genome-wide transcriptional analysis reveals that elevated CO2 mitigates the impact of combined heat wave and drought stress in Arabidopsis thaliana at multiple organizational levels. Glob Chang Biol 20:3670–3685
Zonge YZ, Shangguan ZP (2016) Increased sink capacity enhances C and N assimilation under drought and elevated CO2 conditions in maize. J Integr Agric 15:2775–2785
Acknowledgements
This study was part of the APEK project (NO. 2047441501) funded by the Bundesministerium für Ernährung und Landwirtschaft (BMEL) and the Bundesminesterium für Umwelt, Naturschaft, Bau und Reaktorsicherheit (BMUB) based on the decision of the German Federal Parliament.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Arab, L., Seegmueller, S., Kreuzwieser, J. et al. Atmospheric pCO2 impacts leaf structural and physiological traits in Quercus petraea seedlings. Planta 249, 481–495 (2019). https://doi.org/10.1007/s00425-018-3016-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-018-3016-5