Review
Impacts of elevated CO2 on plant resistance to nutrient deficiency and toxic ions via root exudates: A review

https://doi.org/10.1016/j.scitotenv.2020.142434Get rights and content

Highlights

  • Elevated CO2 (eCO2) increases total efflux of root exudates from root systems.

  • Elevated CO2 increases efflux rates of soluble sugars, carboxylates and citrate.

  • Increased root exudation enhances nutrient uptake under eCO2.

  • Contributions of root exudates to toxic-ion resistance under eCO2 need further validation.

Abstract

Elevated atmospheric CO2 (eCO2) concentration can increase root exudation into soils, which improves plant tolerance to abiotic stresses. This review used a meta-analysis to assess effect sizes of eCO2 on both efflux rates and total amounts of some specific root exudates, and dissected whether eCO2 enhances plant's resistance to nutrient deficiency and ion toxicity via root exudates. Elevated CO2 did not affect efflux rates of total dissolved organic carbon, a measure of combined root exudates per unit of root biomass or length, but increased the efflux amount of root systems per plant by 31% which is likely attributed to increased root biomass (29%). Elevated CO2 increased efflux rates of soluble-sugars, carboxylates, and citrate by 47%, 111%, and 16%, respectively, but did not affect those of amino acids and malate. The increased carbon allocation to roots, increased plant requirements of mineral nutrients, and heightened detoxification responses to toxic ions under eCO2 collectively contribute to the increased efflux rates despite lacking molecular evidence. The increased efflux rates of root exudates under eCO2 were closely associated with improved nutrient uptake whilst less studies have validated the associations between root exudates and resistance to toxic ions of plants when grown under eCO2. Future studies are required to reveal how climate change (eCO2) affect the efflux of specific root exudates, particularly organic anions, the corresponding nutrient uptake and toxic ion resistance from plant molecular biology and soil microbial ecology perspectives.

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).

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