Insights into molecular mechanism underlying carbon fixation inhibition of rice induced by cadmium

Xinru Zhang , Jie Chen , Jianjian Wu , Wei Wang , Lizhong Zhu

Front. Environ. Sci. Eng. ›› 2025, Vol. 19 ›› Issue (7) : 96

PDF (5416KB)
Front. Environ. Sci. Eng. ›› 2025, Vol. 19 ›› Issue (7) : 96 DOI: 10.1007/s11783-025-2016-5
RESEARCH ARTICLE

Insights into molecular mechanism underlying carbon fixation inhibition of rice induced by cadmium

Author information +
History +
PDF (5416KB)

Abstract

Cadmium (Cd) contamination poses a significant threat to the carbon fixation potential of farmland ecosystems, yet the molecular mechanisms underlying its inhibitory effects remain poorly understood. This study reveals that Cd competitively binds to ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), the key enzyme in photosynthetic carbon fixation, by displacing its native co-factor, magnesium (Mg). Both Cd2+ and Mg2+ bind to identical sites on Rubisco, forming a hexacoordinated complex with the oxygen atoms of ribulose-1,5-bisphosphate (RuBP) and key residues in Rubisco, including Asp203, His294, Glu204, and Lys201. While the binding affinity and stability of the Cd2+-Rubisco-RuBP complex are comparable to those of the Mg2+-Rubisco-RuBP complex, Cd2+ markedly shifts the catalytic activity of Rubisco from carboxylation to oxygenation. This shift results in the accumulation of 2-phosphoglycolate (2-PG), a photorespiration byproduct, by up to 11.57-fold. Consequently, the enhanced photorespiration pathway increases CO2 release, leading to a significant reduction in net CO2 fixation and ultimately inhibiting rice growth under hydroponic conditions. By elucidating the molecular mechanism through which Cd disrupts Rubisco’s dual catalytic activity, this study advances our understanding of how heavy metals impair carbon metabolism and carbon sequestration in plants, offering critical insights for mitigating Cd-induced carbon sink losses in cropland.

Graphical abstract

Keywords

Cadmium / Rice / Carbon fixation / Photorespiration / Metal-protein interaction

Highlight

● Cd2+ can competitively bind to the same active site of Rubisco as Mg2+.

● Cd2+ equipped Rubisco with high binding capacity to its substrate RuBP.

● Cd2+ shifted the catalytic activity of Rubisco from carboxylation to oxygenation.

● The accumulation of oxidation products significantly promoted photorespiration.

● Rice growth was inhibited by the decrease in the net CO2 fixation.

Cite this article

Download citation ▾
Xinru Zhang, Jie Chen, Jianjian Wu, Wei Wang, Lizhong Zhu. Insights into molecular mechanism underlying carbon fixation inhibition of rice induced by cadmium. Front. Environ. Sci. Eng., 2025, 19(7): 96 DOI:10.1007/s11783-025-2016-5

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Andersson I, Taylor T C. (2003). Structural framework for catalysis and regulation in ribulose-1,5-bisphosphate carboxylase/oxygenase. Archives of Biochemistry and Biophysics, 414(2): 130–140

[2]

Arnon D I, Hoagland D R. (1944). The investigation of plant nutrition by artificial culture methods. Biological Reviews of the Cambridge Philosophical Society, 19(2): 55–67

[3]

BahA M, Sun H Y, ChenF, ZhouJ, DaiH X, ZhangG P, Wu F B (2010). Comparative proteomic analysis of Typha angustifolia leaf under chromium, cadmium and lead stress. Journal of Hazardous Materials, 184(1−3): 191–203

[4]

Bauwe H, Hagemann M, Fernie A R. (2010). Photorespiration: players, partners and origin. Trends in Plant Science, 15(6): 330–336

[5]

Beale S I. (1999). Enzymes of chlorophyll biosynthesis. Photosynthesis Research, 60(1): 43–73

[6]

Benson A A. (2002). Paving the path. Annual Review of Plant Biology, 53(1): 1–25

[7]

Berendsen H J C, Van Der Spoel D, Van Drunen R. (1995). GROMACS: a message-passing parallel molecular dynamics implementation. Computer Physics Communications, 91(1−3): 43–56

[8]

Bradford M M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Chemistry, 72(1): 248–254

[9]

Brandis J E P, Zalesak S M, Kane M A, Michel S L J. (2021). Cadmium exchange with zinc in the non-classical zinc finger protein tristetraprolin. Inorganic Chemistry, 60(11): 7697–7707

[10]

Busch F A, Sage R F, Farquhar G D. (2018). Plants increase CO2 uptake by assimilating nitrogen via the photorespiratory pathway. Nature Plants, 4(1): 46–54

[11]

Calvin M. (1997). Forty years of photosynthesis and related activities. Interdisciplinary Science Reviews, 22(2): 138–148

[12]

Carretero-GonzálezR, KevrekidisP G, Kevrekidis I G, MaroudasD, FrantzeskakisD J (2005). A Parrinello-Rahman approach to vortex lattices. Physics Letters , 341(1−4): 128–134

[13]

ChenJ, Le X C, ZhuL (2019). Metabolomics and transcriptomics reveal defense mechanism of rice (Oryza sativa) grains under stress of 2,2’4,4’-tetrabromodiphenyl ether. Environment International, 133(Pt A): 105154

[14]

Chen J, Wang W, Chen D J, Zhu L Z. (2023a). Benzotriazole ultraviolet stabilizers (BUVSs) as potential protein kinase antagonists in rice. Environmental Science & Technology, 57(50): 21405–21415

[15]

Chen J, Wang W, Zhu L Z. (2023b). Amino acid transporter as a potential carrier protein for the root-to-shoot translocation of polybrominated diphenyl ethers in rice. Environmental Science & Technology, 57(26): 9722–9731

[16]

Cleland W W, Andrews T J, Gutteridge S, Hartman F C, Lorimer G H. (1998). Mechanism of Rubisco: the carbamate as general base. Chemical Reviews, 98(2): 549–561

[17]

D’Alessandro A, Taamalli M, Gevi F, Timperio A M, Zolla L, Ghnaya T. (2013). Cadmium stress responses in Brassica juncea: Hints from proteomics and metabolomics. Journal of Proteome Research, 12(11): 4979–4997

[18]

Deng X, Chen Y, Yang Y, Peng L, Si L, Zeng Q. (2021). The implications of planting mode on cadmium uptake and remobilization in rice: field experiments across growth stages. Frontiers of Environmental Science & Engineering, 15(6): 137

[19]

Ditchfield R, Hehre W J, Pople J A. (1971). Self-consistent molecular-orbital methods. IX. An extended gaussian-type basis for molecular-orbital studies of organic molecules. Journal of Chemical Physics, 54(2): 724–728

[20]

Dong J Q, Zhang K, Li X, Qian Y H, Zhu H, Yuan D Q, Xu Q H, Jiang J W, Zhao D. (2017). Ultrathin two-dimensional porous organic nanosheets with molecular rotors for chemical sensing. Nature Communications, 8: 1142

[21]

Doose S, Neuweiler H, Sauer M. (2005). A close look at fluorescence quenching of organic dyes by tryptophan. ChemPhysChem, 6(11): 2277–2285

[22]

Espasa A, Lang M, Aguino C F, Sanchez-Dealcazar D, Fernandez-Blazquez J P, Sonnewald U, Cortajarena A L, Coto P B, Costa R D. (2020). Long-living and highly efficient bio-hybrid light-emitting diodes with zero-thermal-quenching biophosphors. Nature Communications, 11(1): 879

[23]

Faller P, Kienzler K, Krieger-Liszkay A. (2005). Mechanism of Cd2+ toxicity: Cd2+ inhibits photoactivation of Photosystem II by competitive binding to the essential Ca2+ site. Biochimica et Biophysica Acta. Bioenergetics, 1706(1−2): 158–164

[24]

Fernie A R, Bauwe H, Eisenhut M, Florian A, Hanson D T, Hagemann M, Keech O, Mielewczik M, Nikoloski Z, Peterhansel C. . (2013). Perspectives on plant photorespiratory metabolism. Plant Biology, 15(4): 748–753

[25]

Friedman R. (2014). Structural and computational insights into the versatility of cadmium binding to proteins. Dalton Transactions, 43(7): 2878–2887

[26]

Gaillard T. (2018). Evaluation of AutoDock and AutoDock Vina on the CASF-2013 benchmark. Journal of Chemical Information and Modeling, 58(8): 1697–1706

[27]

Genovese D, Cingolani M, Rampazzo E, Prodi L, Zaccheroni N. (2021). Static quenching upon adduct formation: a treatment without shortcuts and approximations. Chemical Society Reviews, 50(15): 8414–8427

[28]

Hartman F C, Harpel M R. (1994). Structure, function, regulation and assembly of D-ribulose-1,5-bisphosphate carboxylase oxygenase. Annual Review of Biochemistry, 63(1): 197–232

[29]

Hibberd J M, Furbank R T. (2016). Fifty years of C4 photosynthesis. Nature, 538(7624): 177–179

[30]

KawataM, Nagashima U (2001). Particle mesh Ewald method for three−dimensional systems with two−dimensional periodicity. Chemical Physics Letters, 340(1−2): 165–172

[31]

Lakowicz J R, Weber G. (1973). Quenching of fluorescence by oxygen: a probe for structural fluctuations in macromolecules. Biochemistry, 12(21): 4161–4170

[32]

Lee C T, Yang W T, Parr R G. (1988). Development of the colle-salvetti correlation-energy formula into a functional of the electron-density. Physical Review B: Condensed Matter, 37(2): 785–789

[33]

Liang C, Xiao W, Hao H, Xiaoqing L, Chao L, Lei Z, Fashui H. (2008). Effect of Mg2+ on the structure and function of ribulose-1,5-bisphosphate carboxylase/oxygenase. Biological Trace Element Research, 121(3): 249–257

[34]

Lorimer G H. (1981). The carboxylation and oxygenation of Ribulose 1,5-bisphosphate: the primary events in photosynthesis and photorespiration. Annual Review of Plant Physiology, 32(1): 349–382

[35]

Luis A S, Briggs J, Zhang X, Farnell B, Ndeh D, Labourel A, Basle A, Cartmell A, Terrapon N, Stott K. . (2018). Dietary pectic glycans are degraded by coordinated enzyme pathways in human colonic Bacteroides. Nature Microbiology, 3(2): 210–219

[36]

Marmé N, Knemeyer J P, Sauer M, Wolfrum J. (2003). Inter- and intramolecular fluorescence quenching of organic dyes by tryptophan. Bioconjugate Chemistry, 14(6): 1133–1139

[37]

Martin-Diaconescu V, Chacon K N, Delgado-Jaime M U, Sokaras D, Weng T C, Debeer S, Blackburn N J. (2016). K beta valence to core X-ray emission studies of Cu(I) binding proteins with mixed methionine-histidine coordination. relevance to the reactivity of the M- and H-sites of peptidylglycine monooxygenase. Inorganic Chemistry, 55(7): 3431–3439

[38]

Matsumura H, Mizohata E, Ishida H, Kogami A, Ueno T, Makino A, Inoue T, Yokota A, Mae T, Kai Y. (2012). Crystal structure of rice Rubisco and implications for activation induced by positive effectors NADPH and 6-phosphogluconate. Journal of Molecular Biology, 422(1): 75–86

[39]

Najeeb U, Jilani G, Ali S, Sarwar M, Xu L, Zhou W. (2011). Insights into cadmium induced physiological and ultra-structural disorders in Juncus effusus L. and its remediation through exogenous citric acid. Journal of Hazardous Materials, 186(1): 565–574

[40]

Parmar P, Kumari N, Sharma V. (2013). Structural and functional alterations in photosynthetic apparatus of plants under cadmium stress. Botanical Studies, 54(1): 45

[41]

Paunov M, Koleva L, Vassilev A, Vangronsveld J, Goltsev V. (2018). Effects of different metals on photosynthesis: cadmium and zinc affect chlorophyll fluorescence in durum wheat. International Journal of Molecular Sciences, 19(3): 787

[42]

Rappe A K, Casewit C J, Colwell K S, Goddard W A III, Skiff W M. (1992). Skiff WM. UFF, a full periodic table force field for molecular mechanics and molecular dynamics simulations. Journal of the American Chemical Society, 114(25): 10024–10035

[43]

Shen S, Li X F, Cullen W R, Weinfeld M, Le X C. (2013). Arsenic binding to proteins. Chemical Reviews, 113(10): 7769–7792

[44]

Sigfridsson K G V, Bernát G, Mamedov F, Styring S. (2004). Molecular interference of Cd2+ with Photosystem II. Biochimica et Biophysica Acta. Bioenergetics, 1659(1): 19–31

[45]

Solymosi K, Bertrand M. (2012). Soil metals, chloroplasts, and secure crop production: a review. Agronomy for Sustainable Development, 32(1): 245–272

[46]

Tcherkez G. (2013). Modelling the reaction mechanism of ribulose-1,5-bisphosphate carboxylase/oxygenase and consequences for kinetic parameters. Plant, Cell & Environment, 36(9): 1586–1596

[47]

Tcherkez G. (2016). The mechanism of Rubisco-catalysed oxygenation. Plant, Cell & Environment, 39(5): 983–997

[48]

Wang K, Bastos A, Ciais P, Wang X, Rodenbeck C, Gentine P, Chevallier F, Humphrey V W, Huntingford C, O’Sullivan M. . (2022). Regional and seasonal partitioning of water and temperature controls on global land carbon uptake variability. Nature Communications, 13(1): 3469

[49]

Wang P, Chen H, Kopittke P M, Zhao F J. (2019). Cadmium contamination in agricultural soils of China and the impact on food safety. Environmental Pollution, 249: 1038–1048

[50]

Warburg O. (1956). Respiratory impairment in cancer cells. Science, 124(3215): 269–270

[51]

Willick I R, Plaxton W C, Lolle S J, Macfie S M. (2019). Transcriptional and post-translational upregulation of phospho-enolpyruvate carboxylase in Arabidopsis thaliana (L. Heynh) under cadmium stress. Environmental and Experimental Botany, 164: 29–39

[52]

Wright M H, Sieber S A. (2016). Chemical proteomics approaches for identifying the cellular targets of natural products. Natural Product Reports, 33(5): 681–708

[53]

Wu X, Yang X, Geng X, Ji X, Zhang X, Yue H, Li G, Sang N. (2022). Bisphenol A analogs induce cellular dysfunction in human trophoblast cells in a thyroid hormone receptor-dependent manner: in silico and in vitro analyses. Environmental Science & Technology, 56(12): 8384–8394

[54]

Xiao Z G, Loughlin F, George G N, Howlett G J, Wedd A G. (2004). C-terminal domain of the membrane copper transporter Ctr1 from Saccharomyces cerevisia binds four Cu(I) ions as a cuprous-thiolate polynuclear cluster: sub-femtomolar Cu(I) affinity of three proteins involved in copper trafficking. Journal of the American Chemical Society, 126(10): 3081–3090

[55]

Xu Y, Fu X, Sharkey T D, Shachar-Hill Y, Walker A B J. (2021). The metabolic origins of non-photorespiratory CO2 release during photosynthesis: a metabolic flux analysis. Plant Physiology, 186(1): 297–314

[56]

Yamori W. (2016). Photosynthetic response to fluctuating environments and photoprotective strategies under abiotic stress. Journal of Plant Research, 129(3): 379–395

[57]

Yang Q, Li Z, Lu X, Duan Q, Huang L, Bi J. (2018). A review of soil heavy metal pollution from industrial and agricultural regions in China: pollution and risk assessment. Science of the Total Environment, 642: 690–700

[58]

Zhang X, Chen J, Wang W, Zhu L. (2024). Photosynthetic mechanisms of carbon fixation reduction in rice by cadmium and polycyclic aromatic hydrocarbons. Environmental Pollution, 344: 123436

[59]

Zhang X, Liu N, Lu H, Zhu L. (2022a). Molecular mechanism of organic pollutant-induced reduction of carbon fixation and biomass yield in Oryza sativa L. Environmental Science & Technology, 56(7): 4162–4172

[60]

Zhang Y, Piao S, Sun Y, Rogers B M, Li X, Lian X, Liu Z, Chen A, Peñuelas J. (2022b). Future reversal of warming-enhanced vegetation productivity in the Northern Hemisphere. Nature Climate Change, 12(6): 581–586

[61]

Zhou H, Zhu W, Yang W T, Gu J F, Gao Z X, Chen L W, Du W Q, Zhang P, Peng P Q, Liao B H. (2018). Cadmium uptake, accumulation, and remobilization in iron plaque and rice tissues at different growth stages. Ecotoxicology and Environmental Safety, 152: 91–97

[62]

Zhu Z, Piao S, Myneni R B, Huang M, Zeng Z, Canadell J G, Ciais P, Sitch S, Friedlingstein P, Arneth A. . (2016). Greening of the Earth and its drivers. Nature Climate Change, 6(8): 791–795

[63]

Zou M, Zhou S, Zhou Y, Jia Z, Guo T, Wang J. (2021). Cadmium pollution of soil-rice ecosystems in rice cultivation dominated regions in China: a review. Environmental Pollution, 280: 116965

RIGHTS & PERMISSIONS

Higher Education Press 2025

AI Summary AI Mindmap
PDF (5416KB)

Supplementary files

FSE-25051-OF-ZXR_suppl_1

527

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/