ReviewImpacts of elevated CO2 on plant resistance to nutrient deficiency and toxic ions via root exudates: A review
Graphical abstract
Introduction
Living plant roots exude soluble compounds into the rhizosphere referred to as root exudates (Oburger and Jones, 2018). Root exudates consist mainly of various carbon-based compounds, including low-molecular-weight (such as soluble sugars, amino acids and organic acid anions) and high-molecular-weight (such as proteins and mucilage) molecules (Jones et al., 2009). Organic anions in particular are secreted and can form complexes with nutrients (such as Mn and Zn) to enhance mobilization, or form complexes with toxic ions (such as Al3+ or heavy metals) to render them non-phyotoxic (Jones et al., 2009; Marschner, 2012).
On the other hand, the concentration of atmospheric CO2 is currently 414 μmol mol−1 (https://www.esrl.noaa.gov/gmd/ccgg/trends/, July 2020), and is predicted to reach 720 μmol mol−1 by the end of this century due to combustion of fossil fuels, deforestation and land-use changes (IPCC, 2014). Elevated CO2 (eCO2) promotes photosynthetic CO2 fixation and thus plant productivity and yield (Leakey et al., 2009; Norby and Zak, 2011). In some cases, eCO2 enhances the tolerance of plants to abiotic stresses, such as nutrient deficiency and ion toxicity through increased carbon availability of plants (AbdElgawad et al., 2016; Huang and Xu, 2015). In recent decades, a great attention has been paid to the effect of eCO2 on root exudates. It has been found that eCO2 more frequently increases the efflux of root exudates (Freeman et al., 2004; Nie et al., 2013; Phillips et al., 2006). Firstly, the increased carbon fixation under eCO2 tends to increase carbon allocation including root exudates to soils (Bhattacharyya et al., 2016; Jin et al., 2014; Rogers et al., 1995), which becomes a driving force for carbon sequestration in soils and thus contributes to the mitigation of climate change (Groenigen Kees et al., 2017; Pausch and Kuzyakov, 2017). In addition, eCO2 might promote plant performance by enhancing the plant's ability to resist abiotic stresses, to mobilise nutrients or to remediate toxic ions through increased root exudates (Jia et al., 2015; Phillips et al., 2011).
Previous studies have briefly summarized that eCO2 can increase the total efflux amount of root exudates (Nie and Pendall, 2016; Pausch and Kuzyakov, 2017). However, the collected references were insufficient to conclude the effect of eCO2 on specific compounds that are considered to be important to nutrient uptake and toxic-ion resistance. In addition, the underlying mechanisms are more frequently speculative and not well understood (Bhattacharyya et al., 2014).
In this review, we collate the findings of studies investigating the effect of eCO2 on root exudates of various plant species. Our primary aims are to determine (1) the effect size of eCO2 on efflux rates and amount of root exudates, (2) the mechanisms by which eCO2 can increase root exudates, and (3) the association of root exudates with the uptake of some specific nutrients (N, P and Fe) and resistance to toxic ions (Al and Cd) under eCO2.
Section snippets
Data collection
A literature survey was carried out using the databases of Scopus, Web of Knowledge, Google Scholar and ScienceDirect. The keywords “elevated CO2”, “elevated carbon dioxide”, “CO2 enrichment”, “climate change”, “FACE”, “rhizodeposition”, “root exudate”, “total organic carbon”, “dissolved organic carbon”, “soluble sugar”, “amino acid”, “organic acid/carboxylic acid/carboxylate”, “phenolic acid”, “citrate”, “malate” and “oxalate” were used. Dissolved organic carbon is assumed to be a measure of
Effect size of eCO2 on root exudates
Elevated CO2 did not affect efflux rate of dissolved organic C (DOC) but increased its efflux amount (Fig. 1). Despite there being no mean increase in efflux rates of DOC, some studies found that eCO2 increased efflux rates (Johansson et al., 2009; Phillips et al., 2011; van Ginkel et al., 1997), whilst others found no significant increase (Kogawara et al., 2006; Norby et al., 1987), or even decrease (Augustine et al., 2011; Hodge and Millard, 1998; Hodge et al., 1998). These indicate that the
Conclusions
This review concludes that eCO2 did not affect efflux rate of total root exudates indicated by total dissolved organic carbon despite increased total amounts of root exudates resulting from increased root growth (root biomass). Elevated CO2 increased both efflux rates and total amounts of soluble sugars, and carboxylates including citrate whilst the impacts on amino acids and malate were insignificant, likely attributed to plant species and environmental variations. We have attributed the
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
The first author received PhD scholarships from La Trobe University and the financial support from Shanghai Agriculture Applied Technology Development Program, China (2019-02-08-00-15-F01142) and the National Key Research and Development Program of China (2018YFD1100103). SJZ would acknowledge the support from the 111 project (No. B14027).
References (86)
- et al.
Effect of elevated carbon dioxide and temperature on phosphorus uptake in tropical flooded rice (Oryza sativa L.)
Eur. J. Agron.
(2014) - et al.
Elucidation of rice rhizosphere metagenome in relation to methane and nitrogen metabolism under elevated carbon dioxide and temperature using whole genome metagenomic approach
Sci. Total Environ.
(2016) - et al.
Organic acid anions: an effective defensive weapon for plants against aluminum toxicity and phosphorus deficiency in acidic soils
J. Genet. Genom.
(2016) - et al.
Mechanisms of phosphorus acquisition for ponderosa pine seedlings under high CO2 and temperature
Ann. Bot.
(1997) - et al.
Sustainable vegetable production under changing climate: the impact of elevated CO2 on yield of vegetables and the interactions with environments-A review
J. Clean. Prod.
(2020) - et al.
Elevation of atmospheric CO2 and N-nutritional status modify nodulation, nodule-carbon supply, and root exudation of Phaseolus vulgaris L
Soil Biol. Biochem.
(2007) - et al.
Characterisation and microbial utilisation of exudate material from the rhizosphere of Lolium perenne grown under CO2 enrichment
Soil Biol. Biochem.
(1998) - et al.
Altered leaf and root emissions from onion (Allium cepa L.) grown under elevated CO2 conditions
Environ. Exp. Bot.
(2004) - et al.
Concentrations of secondary metabolites in tissues and root exudates of wheat seedlings changed under elevated atmospheric CO2 and cadmium-contaminated soils
Environ. Exp. Bot.
(2014) - et al.
Increased microbial activity contributes to phosphorus immobilization in the rhizosphere of wheat under elevated CO2
Soil Biol. Biochem.
(2014)
Quantitative analysis of soluble exudates produced by ectomycorrhizal roots as a response to ambient and elevated CO2
Soil Biol. Biochem.
Concentration of sugars, phenolic acids, and amino acids in forest soils exposed to elevated atmospheric CO2 and O3
Soil Biol. Biochem.
Effects of elevated CO2 on rhizosphere characteristics of Cd/Zn hyperaccumulator Sedum alfredii
Sci. Total Environ.
Dynamics of rhizosphere properties and antioxidative responses in wheat (Triticum aestivum L.) under cadmium stress. Ecotoxicol. Environ
Saf.
Do rhizosphere priming effects enhance plant nitrogen uptake under elevated CO2?
Agric. Ecosyst. Environ.
Sampling root exudates – mission impossible?
Rhizosphere
Root morphology, excess cation uptake, and extrusion of proton and organic acid anions in Lupinus albus L. under phosphorus deficiency
Plant Sci.
Elevated atmospheric carbon dioxide concentration: effects of increased carbon input in a Lolium perenne soil on microorganisms and decomposition
Soil Biol. Biochem.
A meta-analysis of soil extracellular enzyme activities in response to global change
Soil Biol. Biochem.
Future climate CO2 levels mitigate stress impact on plants: increased defense or decreased challenge?
Front. Plant Sci.
Rhizosphere interactions, carbon allocation, and nitrogen acquisition of two perennial North American grasses in response to defoliation and elevated atmospheric CO2
Oecologia
Regulation and function of root exudates
Plant Cell Environ.
Influence of elevated carbon dioxide and temperature on belowground carbon allocation and enzyme activities in tropical flooded soil planted with rice
Environ. Monit. Assess.
Atmospheric CO2 enrichment and drought stress modify root exudation of barley
Glob. Chang. Biol.
Interactions between atmospheric CO2 concentration and phosphorus nutrition on the formation of proteoid roots in white lupin (Lupinus albus L.)
Plant Cell Environ.
Interactions between the effects of atmospheric CO2 content and P nutrition on photosynthesis in white lupin (Lupinus albus L.)
Plant Cell Environ.
Influence of rhizodeposition under elevated CO2 on plant nutrition and soil organic matter
Plant Soil
Back to acid soil fields: the citrate transporter SbMATE is a major asset for sustainable grain yield for sorghum cultivated on acid soils
G3-Genes Genom. Genet.
Elevated CO2, rhizosphere processes, and soil organic matter decomposition
Plant Soil
Root exudates as mediators of mineral acquisition in low-nutrient environments
Plant Soil
Aluminum tolerance in wheat (Triticum aestivum L.) (II. Aluminum-stimulated excretion of malic acid from root apices)
Plant Physiol.
Temporal dynamics of carbon partitioning and rhizodeposition in wheat
Plant Physiol.
Elevated CO2 (free-air CO2 enrichment) increases grain yield of aluminium-resistant but not aluminium-sensitive wheat (Triticum aestivum L.) grown in an acid soil
Ann. Bot.
The impact of elevated CO2 on acid-soil tolerance of hexaploid wheat (Triticum aestivum L.) genotypes varying in organic anion efflux
Plant Soil
Increases in the flux of carbon belowground stimulate nitrogen uptake and sustain the long-term enhancement of forest productivity under elevated CO2
Ecol. Lett.
Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2
Proc. Natl. Acad. Sci. U. S. A.
Interactions between elevated CO2 and warming could amplify DOC exports from peatland catchments
Environ. Sci. Technol.
Export of dissolved organic carbon from peatlands under elevated carbon dioxide levels
Nature
Global atmospheric change effects on terrestrial carbon sequestration: exploration with a global C- and N-cycle model (CQUESTN)
Plant Soil
Faster turnover of new soil carbon inputs under increased atmospheric CO2
Glob. Chang. Biol.
Elevated CO2 levels affects the concentrations of copper and cadmium in crops grown in soil contaminated with heavy metals under fully open-air field conditions
Environ. Sci. Technol.
Responses to iron limitation in Hordeum vulgare L. as affected by the atmospheric CO2 concentration
J. Environ. Qual.
The meta-analysis of response ratios in experimental ecology
Ecology
Cited by (40)
Elevated CO<inf>2</inf> increases soil redox potential by promoting root radial oxygen loss in paddy field
2024, Journal of Environmental Sciences (China)Modeling the carbon costs of plant phosphorus acquisition in Amazonian forests
2023, Ecological ModellingCoupled effects of elevated CO<inf>2</inf> and biochar on microbial communities of vegetated soil
2023, Journal of Environmental ManagementNutrition of plants in a changing climate
2023, Marschner's Mineral Nutrition of PlantsDifferential effects of elevated atmosphere CO<inf>2</inf> concentration on root growth in association with regulation of auxin and cytokinins under different nitrate supply
2022, Environmental and Experimental BotanyCitation Excerpt :The global atmospheric CO2 concentration has been rising steadily since the industrial revolution from approximately 280 μmol·mol-1 to currently 414 μmol·mol-1 (Dong et al., 2021).