Skip to main content

Advertisement

Log in

Elevated carbon dioxide decreases the adverse effects of higher temperature and drought stress by mitigating oxidative stress and improving water status in Arabidopsis thaliana

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

This study revealed that elevated carbon dioxide increases Arabidopsis tolerance to higher temperature and drought stress by mitigating oxidative stress and improving water status of plants.

Abstract

Few studies have considered multiple aspects of plant responses to key components of global climate change, including higher temperature, elevated carbon dioxide (ECO2), and drought. Hence, their individual and combinatorial effects on plants need to be investigated in the context of understanding climate change impact on plant growth and development. We investigated the interactive effects of temperature, CO2, watering regime, and genotype on Arabidopsis thaliana (WT and ABA-insensitive mutant, abi1-1). Plants were grown in controlled-environment growth chambers under two temperature regimes (22/18 °C and 28/24 °C, 16 h light/8 h dark), two CO2 concentrations (400 and 700 μmol mol−1), and two watering regimes (well-watered and water-stressed) for 18 days. Plant growth, anatomical, physiological, molecular, and hormonal responses were determined. Our study provided valuable information about plant responses to the interactive effects of multiple environmental factors. We showed that drought and ECO2 had larger effects on plants than higher temperatures. ECO2 alleviated the detrimental effects of temperature and drought by mitigating oxidative stress and plant water status, and this positive effect was consistent across multiple response levels. The WT plants performed better than the abi1-1 plants; the former had higher rosette diameter, total dry mass, leaf and soil water potential, leaf moisture, proline, ethylene, trans-zeatin, isopentyladenine, and cis-zeatin riboside than the latter. The water-stressed plants of both genotypes accumulated more abscisic acid (ABA) than the well-watered plants; however, higher temperatures decreased the ability of WT plants to produce ABA in response to drought. We conclude that drought strongly, while higher temperature to a lesser extent, affects Arabidopsis seedlings, and ECO2 reduces the adverse effects of these stressors more efficiently in the WT plants than in the abi1-1 plants. Findings from this study can be extrapolated to other plant species that share similar characteristics and/or family with Arabidopsis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Abbreviations

ACO2 :

Ambient CO2

Chl:

Chlorophyll

CK:

Cytokinin

ECO2 :

Elevated CO2

MDA:

Malondialdehyde

ROS:

Reactive oxygen species

References

  • Allison I, Bindoff NL, Bindschadler RA, Cox PM, de Noblet N, England MH, Francis JE, Gruber N, Haywood AM, Karoly DJ, Kaser G, Quéré LC, Lenton TM, Mann ME, McNeil BI et al (2009) The Copenhagen diagnosis 2009: updating the world on the latest climate science. The University of New South Wales Climate Research Centre, Sydney

    Google Scholar 

  • Anjum SA, Farooq M, Xie X, Liu X, Ijaz MF (2012) Antioxidant defense system and proline accumulation enables hot pepper to perform better under drought. Sci Hortic 140:66–73

    Article  CAS  Google Scholar 

  • Bates L, Waldren R, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207

    Article  CAS  Google Scholar 

  • Bauweraerts I, Wertin TM, Ameye M, McGuire MA, Teskey RO, Steppe K (2013) The effect of heat waves, elevated [CO2] and low soil water availability on northern red oak (Quercus rubra L.) seedlings. Glob Change Biol 19:517–528

    Article  Google Scholar 

  • Bhargava S, Sawant K (2013) Drought stress adaptation: metabolic adjustment and regulation of gene expression. Plant Breed 132:21–32

    Article  CAS  Google Scholar 

  • Bray EA (2002) Abscisic acid regulation of gene expression during water-deficit stress in the era of the Arabidopsis genome. Plant Cell Environ 25:153–161

    Article  CAS  PubMed  Google Scholar 

  • Bray S, Reid DM (2002) The effect of salinity and CO2 enrichment on the growth and anatomy of the second trifoliate leaf of Phaseolus vulgaris. Can J Bot 80:349–359

    Article  Google Scholar 

  • Burgos A, Szymanski J, Seiwert B, Degenkolbe T, Hannah MA, Giavalisco P, Willmitzer L (2011) Analysis of short-term changes in the Arabidopsis thaliana glycerolipidome in response to temperature and light. Plant J 66:656–668

    Article  CAS  PubMed  Google Scholar 

  • Ceulemans R, Van Praet L, Jiang XN (1995) Effects of CO2 enrichment, leaf position and clone on stomatal index and epidermal cell density in poplar (Populus). New Phytol 131:99–107

    Article  Google Scholar 

  • Chappelle EW, Kim MS, McMurtrey JE III (1992) Ratio analysis of reflectance spectra (RARS): an algorithm for the remote estimation of the concentrations of chlorophyll a, chlorophyll b, and carotenoids in soybean leaves. Remote Sens Environ 39:239–247

    Article  Google Scholar 

  • Christmann A, Weiler EW, Steudle E, Grill E (2007) A hydraulic signal in root-to-shoot signaling of water shortage. Plant J 52:167–174

    Article  CAS  PubMed  Google Scholar 

  • Cossu M, Murgia L, Ledda L, Deligios PA, Sirigu A, Chessa F, Pazzona A (2014) Solar radiation distribution inside a greenhouse with south-oriented photovoltaic roofs and effects on crop productivity. Appl Energy 133:89–100

    Article  Google Scholar 

  • Cui L, Li J, Fan Y, Xu S, Zhang Z (2006) High temperature effects on photosynthesis, PSII functionality and antioxidant activity of two Festuca arundinacea cultivars with different heat susceptibility. Bot Stud 47:61–69

    CAS  Google Scholar 

  • Cui M, Lin Y, Zu Y, Efferth T, Li D, Tang Z (2015) Ethylene increases accumulation of compatible solutes and decreases oxidative stress to improve plant tolerance to water stress in Arabidopsis. J Plant Biol 58:193–201

    Article  CAS  Google Scholar 

  • Cutler AJ, Krochko JE (1999) Formation and breakdown of ABA. Trends Plant Sci 4:472–478

    Article  CAS  PubMed  Google Scholar 

  • De Meutter J, Tytgat T, Witters E, Gheysen G, Van Onckelen H, Gheysen G (2003) Identification of cytokinins produced by the plant parasitic nematodes Heterodera schachtii and Meloidogyne incognita. Mol Plant Pathol 4:271–277

    Article  PubMed  Google Scholar 

  • Dodd IC, Davies WJ (2010) Hormones and the regulation of water balance. In: Davies PJ (ed) Plant hormones, 3rd edn. Springer, Dordrecht, pp 519–548

    Chapter  Google Scholar 

  • Duan H, Amthor JS, Duursma RA, O’grady AP, Choat B, Tissue DT (2013) Carbon dynamics of eucalypt seedlings exposed to progressive drought in elevated [CO2] and elevated temperature. Tree Physiol 33:779–792

    Article  CAS  PubMed  Google Scholar 

  • Dutta S, Mohanty S, Tripathy BC (2009) Role of temperature stress on chloroplast biogenesis and protein import in pea. Plant Physiol 150:1050–1061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erhardt A, Rusterholz H (1997) Effects of elevated CO2 on flowering phenology and nectar production. Acta Oecol 18:249–253

    Article  Google Scholar 

  • Farrow SC, Emery RN (2012) Concurrent profiling of indole-3-acetic acid, abscisic acid, and cytokinins and structurally related purines by high-performance-liquid-chromatography tandem electrospray mass spectrometry. Plant Methods 8:42

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905

    Article  CAS  PubMed  Google Scholar 

  • Franks PJ, Adams MA, Amthor JS, Barbour MM, Berry JA, Ellsworth DS, Farquhar GD, Ghannoum O, Lloyd J, McDowell N (2013) Sensitivity of plants to changing atmospheric CO2 concentration: from the geological past to the next century. New Phytol 197:1077–1094

    Article  CAS  PubMed  Google Scholar 

  • Gammans M, Mérel P, Ortiz-Bobea A (2017) Negative impacts of climate change on cereal yields: statistical evidence from France. Environ Res Lett 12:054007

    Article  CAS  Google Scholar 

  • Gillespie KM, Rogers A, Ainsworth EA (2011) Growth at elevated ozone or elevated carbon dioxide concentration alters antioxidant capacity and response to acute oxidative stress in soybean (Glycine max). J Exp Bot 62:2667–2678

    Article  CAS  PubMed  Google Scholar 

  • Guo Y, Jia W, Song J, Wang D, Chen M, Wang B (2012) Thellungilla halophila is more adaptive to salinity than Arabidopsis thaliana at stages of seed germination and seedling establishment. Acta Physiol Plant 34:1287–1294

    Article  CAS  Google Scholar 

  • Hare P, Cress W (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102

    Article  CAS  Google Scholar 

  • Heckenberger U, Roggatz U, Schurr U (1998) Effect of drought stress on the cytological status in Ricinus communis. J Exp Bot 49:181–189

    Article  CAS  Google Scholar 

  • Hirayama T, Shinozaki K (2010) Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant J 61:1041–1052

    Article  CAS  PubMed  Google Scholar 

  • Hiscox JT, Israelstam G (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334

    Article  CAS  Google Scholar 

  • Houpis JL, Surano KA, Cowles S, Shinn JH (1988) Chlorophyll and carotenoid concentrations in two varieties of Pinus ponderosa seedlings subjected to long-term elevated carbon dioxide. Tree Physiol 4:187–193

    Article  CAS  PubMed  Google Scholar 

  • Jia J, Zhou J, Shi W, Cao X, Luo J, Polle A, Luo Z (2017) Comparative transcriptomic analysis reveals the roles of overlapping heat-/drought-responsive genes in poplars exposed to high temperature and drought. Sci Rep 7:43215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones HG (2013) Plants and microclimate: a quantitative approach to environmental plant physiology, 3rd edn. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Kirnak H, Kaya C, Tas I, Higgs D (2001) The influence of water deficit on vegetative growth, physiology, fruit yield and quality in eggplants. Bulg J Plant Physiol 27:34–46

    Google Scholar 

  • Kurepin LV, Qaderi MM, Back TG, Reid DM, Pharis RP (2008) A rapid effect of applied brassinolide on abscisic acid concentrations in Brassica napus leaf tissue subjected to short-term heat stress. Plant Growth Regul 55:165–167

    Article  CAS  Google Scholar 

  • Larkindale J, Knight MR (2002) Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 128:682–695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lenka SK, Lohia B, Kumar A, Chinnusamy V, Bansal KC (2009) Genome-wide targeted prediction of ABA responsive genes in rice based on over-represented cis-motif in co-expressed genes. Plant Mol Biol 69:261–271

    Article  CAS  PubMed  Google Scholar 

  • Li L, McCormack ML, Ma C, Kong D, Zhang Q, Chen X, Zeng H, Niinemets Ü, Guo D (2015) Leaf economics and hydraulic traits are decoupled in five species-rich tropical-subtropical forests. Ecol Lett 18:899–906

    Article  CAS  PubMed  Google Scholar 

  • Limin Y, Mei H, Guangsheng Z, Jiandong L (2007) The changes in water-use efficiency and stoma density of Leymus chinensis along Northeast China transect. Acta Ecol Sin 27:16–23

    Article  Google Scholar 

  • Meehl GA, Tebaldi C (2004) More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305:994–997

    Article  CAS  PubMed  Google Scholar 

  • Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant Cell Environ 33:453–467

    Article  CAS  PubMed  Google Scholar 

  • Minitab Inc (2014) Minitab® Release 17. Statistical software for Windows®. Minitab Inc, State College

  • Naudts K, Van den Berge J, Janssens IA, Nijs I, Ceulemans R (2013) Combined effects of warming and elevated CO2 on the impact of drought in grassland species. Plant Soil 369:497–507

    Article  CAS  Google Scholar 

  • Nilsen ET, Orcutt DM (1996) The physiology of plants under stress: abiotic factors. Wiley, New York

    Google Scholar 

  • Noble A, Kisiala A, Galer A, Clysdale D, Emery RJN (2014) Euglena gracilis (Euglenophyceae) produces abscisic acid and cytokinins and responds to their exogenous application singly and in combination with other growth regulators. Eur J Phycol 49:244–254

    Article  CAS  Google Scholar 

  • Oliveira VF, Silva EA, Carvalho MA (2016) Elevated CO2 atmosphere minimizes the effect of drought on the Cerrado species Chrysolaena obovata. Front Plant Sci 7:1–15

    Google Scholar 

  • Piñero MC, Houdusse F, Garcia-Mina JM, Garnica M, Del Amor FM (2014) Regulation of hormonal responses of sweet pepper as affected by salinity and elevated CO2 concentration. Physiol Plant 151:375–389

    Article  CAS  PubMed  Google Scholar 

  • Qaderi MM, Reid DM (2005) Growth and physiological responses of canola (Brassica napus) to UV-B and CO2 under controlled environment conditions. Physiol Plant 125:247–259

    Article  CAS  Google Scholar 

  • Qaderi MM, Reid DM (2009) Crop responses to elevated carbon dioxide and temperature. In: Singh SN (ed) Climate change and crops. Springer, New York, pp 1–18

    Google Scholar 

  • Qaderi MM, Kurepin LV, Reid DM (2006) Growth and physiological responses of canola (Brassica napus) to three components of global climate change: temperature, carbon dioxide and drought. Physiol Plant 128:710–721

    Article  CAS  Google Scholar 

  • Qaderi MM, Lynch AL, Godin VJ, Reid DM (2013) Single and interactive effects of temperature, carbon dioxide, and watering regime on the invasive weed black knapweed (Centaurea nigra). Ecoscience 20:328–338

    Article  Google Scholar 

  • Qaderi MM, Godin VJ, Reid DM (2015) Single and combined effects of temperature and red: far-red light ratio on evening primrose (Oenothera biennis). Botany 93:475–483

    Article  Google Scholar 

  • Qu A, Ding Y, Jiang Q, Zhu C (2013) Molecular mechanisms of the plant heat stress response. Biochem Biophys Res Commun 432:203–207

    Article  CAS  PubMed  Google Scholar 

  • Quesnelle PE, Emery RN (2007) cis-Cytokinins that predominate in Pisum sativum during early embryogenesis will accelerate embryo growth in vitro. Botany 85:91–103

    Google Scholar 

  • Reddy AR, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161:1189–1202

    Article  CAS  Google Scholar 

  • Rizhsky L, Liang H, Shuman J, Shulaev V, Davletova S, Mittler R (2004) When defense pathways collide. The response of Arabidopsis to a combination of drought and heat stress. Plant Physiol 134:1683–1696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roy J, Picon-Cochard C, Augusti A, Benot ML, Thiery L, Darsonville O, Landais D, Piel C, Defossez M, Devidal S, Escape C, Ravel O, Fromin N, Volaire F, Milcu A et al (2016) Elevated CO2 maintains grassland net carbon uptake under a future heat and drought extreme. Proc Natl Acad Sci USA 113:6224–6229

    Article  CAS  PubMed  Google Scholar 

  • SAS Institute (2011) SAS/STAT user’s guide, version 9.3. SAS Institute, Cary

    Google Scholar 

  • Sekiya N, Yano K (2008) Stomatal density of cowpea correlates with carbon isotope discrimination in different phosphorus, water and CO2 environments. New Phytol 179:799–807

    Article  CAS  PubMed  Google Scholar 

  • Sharp RE, LeNoble ME (2002) ABA, ethylene and the control of shoot and root growth under water stress. J Exp Bot 53:33–37

    Article  CAS  PubMed  Google Scholar 

  • Sisler EC, Wood C (1988) Interaction of ethylene and CO2. Physiol Plant 73:440–444

    Article  CAS  Google Scholar 

  • Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) (2013) 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, New York

    Google Scholar 

  • Teng N, Wang J, Chen T, Wu X, Wang Y, Lin J (2006) Elevated CO2 induces physiological, biochemical and structural changes in leaves of Arabidopsis thaliana. New Phytol 172:92–103

    Article  CAS  PubMed  Google Scholar 

  • Tubiello FN, Soussana JF, Howden SM (2007) Crop and pasture response to climate change. Proc Natl Acad Sci USA 104:19686–19690

    Article  PubMed  Google Scholar 

  • Verslues PE, Bray EA (2005) Role of abscisic acid (ABA) and Arabidopsis thaliana ABA-insensitive loci in low water potential-induced ABA and proline accumulation. J Exp Bot 57:201–212

    Article  CAS  PubMed  Google Scholar 

  • Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14

    Article  CAS  PubMed  Google Scholar 

  • Weber H, Chételat A, Reymond P, Farmer EE (2004) Selective and powerful stress gene expression in Arabidopsis in response to malondialdehyde. Plant J 37:877–888

    Article  CAS  PubMed  Google Scholar 

  • Yan K, Chen W, Zhang G, Xu S, Liu Z, He X, Wang L (2010) Elevated CO2 ameliorated oxidative stress induced by elevated O3 in Quercus mongolica. Acta Physiol Plant 32:375–385

    Article  CAS  Google Scholar 

  • Yeung EC (2015) A guide to the study of plant structure with emphasis on living specimens. In: Yeung E, Stasolla C, Sumner M, Huang B (eds) Plant microtechniques and protocols. Springer International Publishing, Cham, pp 3–22

    Chapter  Google Scholar 

  • Yong JWH, Wong SC, Letham DS, Hocart CH, Farquhar GD (2000) Effects of elevated [CO2] and nitrogen nutrition on cytokinins in the xylem sap and leaves of cotton. Plant Physiol 124:767–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu YB, Adams DO, Yang SF (1980) Inhibition of ethylene production by 2,4-dinitrophenol and high temperature. Plant Physiol 66:286–290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 52:1848–1858

    Article  CAS  Google Scholar 

  • Zeppel MJ, Wilks JV, Lewis JD (2014) Impacts of extreme precipitation and seasonal changes in precipitation on plants. Biogeosciences 11:3083–3093

    Article  Google Scholar 

  • Zhu J, Fu X, Koo YD, Zhu JK, Jenney FE, Adams MW, Zhu Y, Shi H, Yun DJ, Hasegawa PM, Bressan RA (2007) An enhancer mutant of Arabidopsis salt overly sensitive 3 mediates both ion homeostasis and the oxidative stress response. Mol Cell Biol 27:5214–5224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 Change Biol 20:3670–3685

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported by the Natural Sciences and Engineering Research Council (NSERC) of Canada through a Discovery grant and by Mount Saint Vincent University through an Internal Research grant to MMQ. A graduate scholarship from Yarmouk University, Irbid, Jordan to MIAG is greatly acknowledged. We appreciate useful comments on the manuscript from two anonymous referees.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mirwais M. Qaderi.

Ethics declarations

Conflict of interest

The authors have no conflict of interest to declare.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abo Gamar, M.I., Kisiala, A., Emery, R.J.N. et al. Elevated carbon dioxide decreases the adverse effects of higher temperature and drought stress by mitigating oxidative stress and improving water status in Arabidopsis thaliana. Planta 250, 1191–1214 (2019). https://doi.org/10.1007/s00425-019-03213-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-019-03213-3

Keywords

Navigation