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.
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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
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
Bates L, Waldren R, Teare I (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
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
Bhargava S, Sawant K (2013) Drought stress adaptation: metabolic adjustment and regulation of gene expression. Plant Breed 132:21–32
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
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
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
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
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
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
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
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
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
Cutler AJ, Krochko JE (1999) Formation and breakdown of ABA. Trends Plant Sci 4:472–478
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
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
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
Dutta S, Mohanty S, Tripathy BC (2009) Role of temperature stress on chloroplast biogenesis and protein import in pea. Plant Physiol 150:1050–1061
Erhardt A, Rusterholz H (1997) Effects of elevated CO2 on flowering phenology and nectar production. Acta Oecol 18:249–253
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
Foyer CH, Noctor G (2009) Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal 11:861–905
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
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
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
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
Hare P, Cress W (1997) Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regul 21:79–102
Heckenberger U, Roggatz U, Schurr U (1998) Effect of drought stress on the cytological status in Ricinus communis. J Exp Bot 49:181–189
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
Hiscox JT, Israelstam G (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334
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
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
Jones HG (2013) Plants and microclimate: a quantitative approach to environmental plant physiology, 3rd edn. Cambridge University Press, Cambridge
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
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
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
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
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
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
Meehl GA, Tebaldi C (2004) More intense, more frequent, and longer lasting heat waves in the 21st century. Science 305:994–997
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
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
Nilsen ET, Orcutt DM (1996) The physiology of plants under stress: abiotic factors. Wiley, New York
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
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
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
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
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
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
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
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
Qu A, Ding Y, Jiang Q, Zhu C (2013) Molecular mechanisms of the plant heat stress response. Biochem Biophys Res Commun 432:203–207
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
Reddy AR, Chaitanya KV, Vivekanandan M (2004) Drought-induced responses of photosynthesis and antioxidant metabolism in higher plants. J Plant Physiol 161:1189–1202
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
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
SAS Institute (2011) SAS/STAT user’s guide, version 9.3. SAS Institute, Cary
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
Sharp RE, LeNoble ME (2002) ABA, ethylene and the control of shoot and root growth under water stress. J Exp Bot 53:33–37
Sisler EC, Wood C (1988) Interaction of ethylene and CO2. Physiol Plant 73:440–444
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
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
Tubiello FN, Soussana JF, Howden SM (2007) Crop and pasture response to climate change. Proc Natl Acad Sci USA 104:19686–19690
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
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
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
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
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
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
Yu YB, Adams DO, Yang SF (1980) Inhibition of ethylene production by 2,4-dinitrophenol and high temperature. Plant Physiol 66:286–290
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
Zeppel MJ, Wilks JV, Lewis JD (2014) Impacts of extreme precipitation and seasonal changes in precipitation on plants. Biogeosciences 11:3083–3093
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
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
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.
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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
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DOI: https://doi.org/10.1007/s00425-019-03213-3