Skip to main content

Advertisement

SpringerLink
Log in

Elevated atmospheric CO2 generally improved soluble sugars content in the rhizosphere soil of black locust seedlings under cadmium exposure

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Aims

Sugars in soils play vital roles in soil aggregation and microbial activity, which is easily affected by environmental factors. Here, we investigated the accumulation of total sugars and monosaccharides in the rhizosphere soil of black locust seedlings exposed to the contamination of elevated atmospheric CO2 (eCO2) and cadmium (Cd) and its driving factors.

Results

Under eCO2 + Cd compared to Cd, glucose, galactose, arabinose, mannose, and xylose concentrations in the rhizosphere soil increased and the increases were significant at 4.5 mg Cd kg−1 (p < 0.05). Glucose was the most abundant sugar. The GM/AX ratio increased (p < 0.05) under eCO2 + Cd relative to Cd, suggesting that sugars in rhizosphere soils might be mainly from microbial synthesis under eCO2 + Cd. In addition, CO2, Cd, and CO2 + Cd influenced (p < 0.05) total sugar and monosaccharide concentrations and the (galactose + mannose)/(arabinose + xylose) (GM/AX) ratio. Sugars concentrations in rhizosphere soils were affected (p < 0.05) by responses of leaf and root biomass, Cd in roots, S in leaves, leaf C/N ratio, and pH and C in rhizosphere soils to eCO2. However, the contribution of sugars in the roots to those in rhizosphere soils was not significant under elevated CO2 + Cd exposure.

Conclusions

Elevated CO2 stimulated sugar concentrations in the rhizosphere soil of black locusts exposed to Cd, which was helpful to understand the contribution of global change scenarios to sugar accumulation in the rhizosphere of plants grown in heavy metal-contaminated soils.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Bergmeyer HU (1974) Methods of enzymatic analysis, vol 3. Academic, New York, pp 212–1215

    Google Scholar 

  • Blagodatskaya E, Khomyakov N, Myachina O, Bogomolova I, Blagodatsky S, Kuzyakov Y (2014) Microbial interactions affect sources of priming induced by cellulose. Soil Biol Biochem 74:39–49

    Article  CAS  Google Scholar 

  • Bongiovanni MD, Lobartini JC (2006) Particulate organic matter, carbohydrate, humic acid contents in soil macro- and microaggregates as affected by cultivation. Geoderma 136:660–665

    Article  CAS  Google Scholar 

  • Caldeira K, Wickett ME (2005) Ocean model predictions of chemistry changes from carbon dioxide emissions to the atmosphere and ocean. J Geophys Res 110:C09S04

    Google Scholar 

  • Calfapietra C, Gielen B, Galema ANJ, Lukac M, Angelis P, Moscatelli MC, Ceulemans R, Scarascia-Mugnozza G (2003) Free-air CO2 enrichment (FACE) enhances biomass production in a short-rotation poplar plantation. Tree Physiol 23:805–814

    Article  CAS  Google Scholar 

  • Cheshire MV, Christensen BT, Sorensen LH (2010) Labeled and native sugars in particle-size fractions from soils incubated with 14Cstraw for 6 to 18 years. Eur J Soil Sci 41:29–39

    Article  Google Scholar 

  • Derrien D, Marol C, Balesdent J (2004) The dynamics of neutral sugars in the rhizosphere of wheat. An approach by C-13 pulse-labeling and GC/C/IRMS. Plant Soil 267:243–253

    Article  CAS  Google Scholar 

  • Ekmekçi Y, Tanyolaç D, Ayhan B (2008) Effects of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars. J Plant Physiol 165:600–611

    Article  Google Scholar 

  • Fischer H, Meyer A, Fischer K, Kuzyakov Y (2007) Carbohydrate and amino acid composition of dissolved organic matter leached from soil. Soil Biol Biochem 39:2926–2935

    Article  CAS  Google Scholar 

  • Gattuso JP, Gao KS, Lee K, Rost B, Schulz KG (2010) Approaches and tools to manipulate the carbonate chemistry. In: Riebesell U, Fabry VJ, Hansson L, Gattuso J-P (eds) Guide to Best Practices for Ocean Acidification Research and Data Reporting. Publications Office of the European Union, Luxembourg, pp 41–52

    Google Scholar 

  • Grandy AS, Erich MS, Porter GA (2000) Suitability of the anthrone-sulfuric acid reagent for determining water soluble carbohydrates in soil water extracts. Soil Biol Biochem 32:725–727

    Article  CAS  Google Scholar 

  • Grayston SJ, Campbell CD (1996) Functional biodiversity of microbial communities in the rhizospheres of hybrid larch (Larix eurolepis) and Sitka spruce (Picea sitchensis). Tree Physiol 16:1031–1038

    Article  Google Scholar 

  • Guggenberger G, Christensen BT, Zech W (1994) Land use effects on the composition of organic matter in particle-size separates of soils: I. Lignin and carbohydrate signature. Eur J Soil Sci 45:449–458

    Article  CAS  Google Scholar 

  • Gunina A, Kuzyakov Y (2015) Sugars in soil and sweets for microorganisms: review of origin, content, composition and fate. Soil Biol Biochem 90:87–100

  • Hishi T, Hirobe M, Tateno R, Takeda H (2004) Spatial and temporal patterns of water-extractable organic carbon (WEOC) of surface mineral soil in a cool temperate forest ecosystem. Soil Biol Biochem 36:1731–1737

    Article  CAS  Google Scholar 

  • Huang SP, Jia X, Zhao YH, Bai B, Chang YF (2017) Elevated CO2 benefits the soil microenvironment in the rhizosphere of Robinia pseudoacacia L. seedlings in Cd- and Pb-contaminated soils. Chemosphere 168:606–616

    Article  CAS  Google Scholar 

  • Hutsch BW, Augustin J, Merbach W (2002) Plant rhizodeposition – an important source for carbon turnover in soils. J Plant Nutr Soil Sci 165:397–407

    Article  CAS  Google Scholar 

  • IPCC (2014) Climate Change 2014: Synthesis Report. Contribution of working Groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change [Core Writing Team, Pachauri RK, Meyer LA (eds)]. IPCC, Geneva, pp 151

  • Jia X, Gao YF, Li XD, Zhao YH, Wang L, Zhang CY (2021) Effects of cadmium on soil nitrification in the rhizosphere of Robinia pseudoacacia L. seedlings under elevated atmospheric CO2 scenarios. Sci Total Environ 772:145023. https://doi.org/10.1016/j.scitotenv.2021.145023

    Article  CAS  PubMed  Google Scholar 

  • Jia X, Wang WK, Chen ZH, He YH, Liu JX (2014) Concentrations of secondary metabolites in tissues and root exudates of wheat seedlings changed under elevated atmospheric CO2 and cadmium-contaminated soils. Environ Exp Bot 107:134–143

    Article  CAS  Google Scholar 

  • Jia X, Zhao YH, Liu T, Huang SP (2016) Elevated CO2 affects secondary metabolites in Robinia pseudoacacia L. seedlings in Cd– and Pb–contaminated soils. Chemosphere 160:199–207

    Article  CAS  Google Scholar 

  • Jin CW, Du ST, Chen WW, Li GX, Zhang YS, Zheng SJ (2009) Elevated carbon dioxide improves plant iron nutrition through enhancing the iron-deficiency-induced responses under iron-limited conditions in tomato. Plant Physiol 150:272–280

    Article  CAS  Google Scholar 

  • Johnson RM, Pregitzer KS (2007) Concentration of sugars, phenolic acids, and amino acids in forest soils exposed to elevated atmospheric CO2 and O3. Soil Biol Biochem 39:3159–3166

    Article  CAS  Google Scholar 

  • Jones DL, Darrah PR (1996) Re-sorption of organic compounds by roots of Zea mays L. and its consequences in the rhizosphere. III: characteristics of sugar influx and efflux. Plant Soil 178:153–160

    Article  CAS  Google Scholar 

  • Kim S, Kang H (2011) Effects of elevated CO2 and Pb on phytoextraction and enzyme activity. Water Air Soil Poll 219:365–375

    Article  CAS  Google Scholar 

  • King JS, Hanson PJ, Bernhardt E, Deangelis P, Norby RJ, Pregitzer KS (2004) A multiyear synthesis of soil respiration responses to elevated atmospheric CO2 from four forest FACE experiments. Global Change Biol 10:1027–1042

    Article  Google Scholar 

  • Kraffczyk I, Trolldenier G, Beringer H (1984) Soluble root exudates of maize: in fluence of potassium supply and rhizosphere microorganisms. Soil Biol Biochem 16:315–322

    Article  CAS  Google Scholar 

  • Kuzyakov Y (2010) Priming effects: interactions between living and dead organic matter. Soil Biol Biochem 42:1363–1371

    Article  CAS  Google Scholar 

  • Kuzyakov Y, Domanski G (2000) Carbon input by plants into the soil. Review. J Plant Nutr Soil Sci 163:421–431

    Article  CAS  Google Scholar 

  • Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129:1–10

    Article  CAS  Google Scholar 

  • Norby RJ (1994) Issues and perspectives for investigating root responses to elevated atmospheric carbon dioxide. Plant Soil 165:9–20

    Article  CAS  Google Scholar 

  • Oades JM (1984) Soil organic matter and structural stability: mechanisms and implications for management. Plant Soil 76:319–337

    Article  CAS  Google Scholar 

  • Pan X, Song W, Zhang D (2010) Earthworms (Eisenia foetida, Savigny) mucus as complexing ligand for imidacloprid. Biol Fert Soils 46:845–850

    Article  Google Scholar 

  • Pérez-de-Mora A, Burgos P, Madejón E, Cabrera F, Jaeckel P, Schloter M (2006) Microbial community structure and function in a soil contaminated by heavy metals: effects of plant growth and different amendments. Soil Biol Biochem 38:327–341

    Article  Google Scholar 

  • Suslov MA (2020) Dynamics of intercellular water transfer in the roots of intact Zea mays L. plants under elevated concentrations of atmospheric CO2. Plant Physiol Bioch 151:516–525

    Article  CAS  Google Scholar 

  • Tanaka H, Hamada R, Kondoh A, Sakagami K (1990) Determination of component sugars in soil organic matter by HPLC. Zentralbl Mikrobiol 145:621–628

    Article  CAS  Google Scholar 

  • Tian L, Dell E, Shi W (2010) Chemical composition of dissolved organic matter in agroecosystems: correlations with soil enzyme activity and carbon and nitrogen mineralization. Appl Soil Ecol 46:426–435

    Article  Google Scholar 

  • Vu JCV, Gesch RW, Pennanen AH, Allen LHJ, Boote KJ, Bowes G (2001) Soybean photosysnthesis, Rubisco, and carbohydrate enzymes function at supraoptimal temperatures in elevated CO2. J Plant Physiol 158:295–307

    Article  CAS  Google Scholar 

  • Wang L, Jia X, Zhao YH, Zhang CY, Gao YF, Li XD, Cao KM, Zhang NJ (2021) Effects of elevated CO2 on arbuscular mycorrhizal fungi associated with Robinia pseudoacacia L. grown in cadmium-contaminated soils. Sci Total Environ 768:144453. https://doi.org/10.1016/j.scitotenv.2020.144453

    Article  CAS  PubMed  Google Scholar 

  • Warembourg FR, Estelrich HD (2000) Towards a better understanding of carbon flow in the rhizosphere: a time-dependent approach using carbon-14. Biol Fert Soils 30:528–534

    Article  CAS  Google Scholar 

  • Xu WH, Huang H, Wang AH, Xiong ZT, Wang ZY (2006) Advance in studies on activation of heavy metal by root exudates and mechanism. Ecol Environ 15:184–189 (in Chinese)

    Google Scholar 

  • Yang YR, Song YY, Scheller HV, Ghosh A, Ban YH, Chen H, Tang M (2015) Community structure of arbuscular mycorrhizal fungi associated with Robinia pseudoacacia in uncontaminated and heavy metal contaminated soils. Soil Biol Biochem 86:146–158

    Article  CAS  Google Scholar 

  • Zak DR, Pregitzer KS, King JS, Holmes WE (2000) Elevated atmospheric CO2, fine roots and the response of soil microorganisms: a review and hypothesis. New Phytol 147:201–222

    Article  CAS  Google Scholar 

  • Zhang CY, Jia X, Zhao YH, Wang L, Cao KM, Zhang NJ, Gao YF, Wang ZW (2021) The combined effects of elevated atmospheric CO2 and cadmium exposure on flavonoids in the leaves of Robinia pseudoacacia L seedlings. Ecotox Environ Safe 210:111878. https://doi.org/10.1016/j.ecoenv.2020.111878

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was jointly supported by the National Natural Science Foundation of China (grant Nos. 31870582 and 31270665) and the Project Supported by Shaanxi Key Laboratory of Land Consolidation of China (Program No. 2019TD-01).

Author information

Authors and Affiliations

  1. Key Laboratory of Subsurface Hydrology and Ecological Effects in Arid Region of Ministry of Education, Shaanxi Key Laboratory of Land Consolidation, School of Water and Environment, Chang’an University, No. 126, Yanta Road, Xi’an, 710054, People’s Republic of China

    Xia Jia, Jiamin Zhao, Ningjing Zhang, Chunyan Zhang, Lu Wang & Kemeng Cao

  2. School of Land Engineering, Chang’an University, Xi’an, 710054, People’s Republic of China

    Yonghua Zhao & Yunfeng Gao

Authors
  1. Xia Jia
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jiamin Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ningjing Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yonghua Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chunyan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kemeng Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yunfeng Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xia Jia.

Additional information

Responsible Editor: Juan Barcelo.

Publisher's note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 117 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jia, X., Zhao, J., Zhang, N. et al. Elevated atmospheric CO2 generally improved soluble sugars content in the rhizosphere soil of black locust seedlings under cadmium exposure. Plant Soil 468, 197–209 (2021). https://doi.org/10.1007/s11104-021-05129-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-021-05129-y

Keywords

Search

Navigation