Skip to main content
Log in

Different physiological responses of C3 and C4 plants to nanomaterials

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Several studies have previously reported that nanomaterial uptake and toxicity in plants are species dependent. However, the differences between photosynthetic pathways, C3 and C4, following nanomaterial exposure are poorly understood. In the current work, wheat and rice, two C3 pathway species are compared to amaranth and maize, which utilize the C4 photosynthetic mechanism. These plants were cultured in soils which were spiked with CuO, Ag, TiO2, MWCNT, and FLG nanomaterials. Overall, the C4 plant exhibited higher resilience to NM stress than C3 plants. In particular, significant differences were observed in chlorophyll contents with rice returning a 40.9–54.2% decrease compared to 3.5–15.1% for maize. Fv/Fm levels were significantly reduced by up to 51% in rice whereas no significant reductions were observed in amaranth and maize. Furthermore, NM uptake in the C3 species was greater than that in C4 plants, a trend that was also seen in metal concentration. TEM results showed that CuO NPs altered the chloroplast thylakoid structure in rice leaves and a large number of CuO NPs were observed in the vascular sheath cells. In contrast, there were no significant changes in the chloroplasts in the vascular sheath and no significant CuO NPs were found in maize leaves. This study was the first to systematically characterize the effect of metal and carbon-based nanomaterials in soil on C3 and C4 plants, providing a new perspective for understanding the impact of nanomaterials on plants.

Graphical abstract

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

Data, associated metadata, and calculation tools are avail-able from the corresponding author Yukui Rui (ruiyukui@163.com).

References

  • Adeel M, Ma C, Ullah S, Rizwan M, Hao Y, Chen C, Jilani G, Shakoor N, Li M, Wang L, Tsang DCW, Rinklebe J, Rui Y, Xing B (2019) Exposure to nickel oxide nanoparticles insinuates physiological, ultrastructural and oxidative damage: a life cycle study on Eisenia fetida. Environ Pollut 254:113032

    Article  CAS  Google Scholar 

  • Adhikari S, Adhikari A, Ghosh S, Roy D, Azahar I, Basuli D, Hossain Z (2020) Assessment of ZnO-NPs toxicity in maize: an integrative microRNAomic approach. Chemosphere 249:20. https://doi.org/10.1016/j.chemosphere.2020.126197

    Article  CAS  Google Scholar 

  • Ahmadi N, Audebert A, Bennett MJ, Bishopp A, de Oliveira AC, Courtois B, Diedhiou A, Diévart A, Gantet P, Ghesquière A, Guiderdoni E, Henry A, Inukai Y, Kochian L, Laplaze L, Lucas M, Luu DT, Manneh B, Mo X, Muthurajan R, Périn C, Price A, Robin S, Sentenac H, Sine B, Uga Y, Véry AA, Wissuwa M, Wu P, Xu J (2014) The roots of future rice harvests. Rice 7:29. https://doi.org/10.1186/s12284-014-0029-y

    Article  Google Scholar 

  • Alkhatib R, Alkhatib B, Abdo N, Al-Eitan L, Creamer R (2019) Physio-biochemical and ultrastructural impact of (Fe3O4) nanoparticles on tobacco. BMC Plant Biol 19:253. https://doi.org/10.1186/s12870-019-1864-1

    Article  CAS  Google Scholar 

  • Baldocchi D (1994) A comparative study of mass and energy exchange rates over a closed C3 (wheat) and an open C4 (corn) crop: II. CO2 exchange and water use efficiency. Agric For Meteorol 67:291–321

    Article  Google Scholar 

  • Cao ZM, Rossi L, Stowers C, Zhang WL, Lombardini L, Ma XM (2018) The impact of cerium oxide nanoparticles on the physiology of soybean (Glycine max (L.) Merr.) under different soil moisture conditions. Environ Sci Pollut Res 25:930–939. https://doi.org/10.1007/s11356-017-0501-5

    Article  CAS  Google Scholar 

  • Conway JR, Adeleye AS, Gardea-Torresdey J, Keller AA (2015) Aggregation, dissolution, and transformation of copper nanoparticles in natural waters. Environ Sci Technol 49:2749–2756

    Article  CAS  Google Scholar 

  • Da Costa M, Sharma P (2016) Effect of copper oxide nanoparticles on growth, morphology, photosynthesis, and antioxidant response in Oryza sativa. Photosynthetica 54:110–119

    Article  Google Scholar 

  • Das P, Barua S, Sarkar S, Chatterjee SK, Mukherjee S, Goswami L, Das S, Bhattacharya S, Karak N, Bhattacharya SS (2018) Mechanism of toxicity and transformation of silver nanoparticles: inclusive assessment in earthworm-microbe-soil-plant system. Geoderma 314:73–84

    Article  CAS  Google Scholar 

  • Evans JR (2013) Improving photosynthesis. Plant Physiol 162:1780–1793. https://doi.org/10.1104/pp.113.219006

    Article  CAS  Google Scholar 

  • Hall J, Williams LE (2003) Transition metal transporters in plants. JExB 54:2601–2613

    CAS  Google Scholar 

  • Hao Y, Fang P, Ma C, White JC, Xiang Z, Wang H, Zhang Z, Rui Y, Xing B (2019) Engineered nanomaterials inhibit Podosphaera pannosa infection on rose leaves by regulating phytohormones. Environ Res 170:1–6. https://doi.org/10.1016/j.envres.2018.12.008

    Article  CAS  Google Scholar 

  • Hao Y et al (2018) Engineered nanomaterials suppress Turnip mosaic virus infection in tobacco (Nicotiana benthamiana). Environ Sci: Nano 5:1685–1693

    CAS  Google Scholar 

  • Hernández-Prieto MA, Foster C, Watson-Lazowski A, Ghannoum O, Chen M (2019) Comparative analysis of thylakoid protein complexes in the mesophyll and bundle sheath cells from C3, C4 and C3–C4 Paniceae grasses. Physiol Plant 166:134–147

    Article  Google Scholar 

  • ISO L (2005) 10390: 2005 Soil quality–Determination of pH

  • Iziy E, Majd A, Vaezi-Kakhki MR, Nejadsattari T, Noureini SK (2019) Effects of zinc oxide nanoparticles on enzymatic and nonenzymatic antioxidant content, germination, and biochemical and ultrastructural cell characteristics of Portulaca oleracea L. Acta Soc Bot Pol 88. https://doi.org/10.5586/asbp.3639

  • Karki S, Rizal G, Quick WP (2013) Improvement of photosynthesis in rice (Oryza sativa L.) by inserting the C4 pathway. Rice 6:28 https://doi.org/10.1186/1939-8433-6-28

  • Kurepa J, Paunesku T, Vogt S, Arora H, Rabatic BM, Lu J, Wanzer MB, Woloschak GE, Smalle JA (2010) Uptake and distribution of ultrasmall anatase TiO2 Alizarin red S nanoconjugates in Arabidopsis thaliana. Nano Lett 10:2296–2302

    Article  CAS  Google Scholar 

  • Latif A, Sheng D, Sun K, Si Y, Azeem M, Abbas A, Bilal M (2020) Remediation of heavy metals polluted environment using Fe-based nanoparticles: mechanisms, influencing factors, and environmental implications. Environmental pollution (Barking, Essex : 1987) 264:114728 https://doi.org/10.1016/j.envpol.2020.114728

  • Le Van N, Ma C, Rui Y, Liu S, Li X, Xing B, Liu L (2015) Phytotoxic mechanism of nanoparticles: destruction of chloroplasts and vascular bundles and alteration of nutrient absorption. Sci Rep 5:1–13

  • Le Van N, Ma C, Shang J, Rui Y, Liu S, Xing B (2016) Effects of CuO nanoparticles on insecticidal activity and phytotoxicity in conventional and transgenic cotton. Chemosphere 144:661–670

    Article  Google Scholar 

  • Li J, Song Y, Wu K, Tao Q, Liang Y, Li T (2018) Effects of Cr2O3 nanoparticles on the chlorophyll fluorescence and chloroplast ultrastructure of soybean (Glycine max). Environ Sci Pollut Res 25:19446–19457. https://doi.org/10.1007/s11356-018-2132-x

    Article  CAS  Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Portland Press Ltd.

  • Liu Y, Yue L, Wang C, Zhu X, Wang Z, Xing B (2020) Photosynthetic response mechanisms in typical C3 and C4 plants upon La2O3 nanoparticle exposure. Environ Sci Nano

  • McManus P, Hortin J, Anderson AJ, Jacobson AR, Britt DW, Stewart J, McLean JE (2018) Rhizosphere interactions between copper oxide nanoparticles and wheat root exudates in a sand matrix: influences on copper bioavailability and uptake 37:2619-2632 https://doi.org/10.1002/etc.4226

  • Nayyar H (2003) Accumulation of osmolytes and osmotic adjustment in water-stressed wheat (Triticum aestivum) and maize (Zea mays) as affected by calcium and its antagonists. Environ Exp Bot 50:253–264. https://doi.org/10.1016/s0098-8472(03)00038-8

    Article  CAS  Google Scholar 

  • Nayyar H, Gupta D (2006) Differential sensitivity of C-3 and C-4 plants to water deficit stress: Association with oxidative stress and antioxidants. Environ Exp Bot 58:106–113. https://doi.org/10.1016/j.envexpbot.2005.06.021

    Article  CAS  Google Scholar 

  • Pal A, Swain SS, Das AB, Mukherjee AK, Chand PK (2013) Stable germ line transformation of a leafy vegetable crop amaranth (Amaranthus tricolor L.) mediated by Agrobacterium tumefaciens In Vitro Cellular & Developmental Biology-Plant 49:114-128

  • Peng C-L, Lin Z-F, Lin G-Z (2000) Superoxide production rate and photosynthetic feature in leaves of some plant species under photooxidation. Acta Phytophysiol Sin 26:81–87

    CAS  Google Scholar 

  • Perreault F, Popovic R, Dewez D (2014) Different toxicity mechanisms between bare and polymer-coated copper oxide nanoparticles in Lemna gibba. Environ Pollut 185:219–227

    Article  CAS  Google Scholar 

  • Rico CM, Majumdar S, Duarte-Gardea M, Peralta-Videa JR, Gardea-Torresdey JL (2011) Interaction of nanoparticles with edible plants and their possible implications in the food chain. J Agric Food Chem 59:3485–3498

    Article  CAS  Google Scholar 

  • Rui MM, Ma C, Tang X, Yang J, Jiang F, Pan Y, Xiang Z, Hao Y, Rui Y, Cao W, Xing B (2017) Phytotoxicity of silver nanoparticles to peanut (Arachis hypogaea L.): physiological responses and food safety. ACS Sustain Chem Eng 5:6557–6567. https://doi.org/10.1021/acssuschemeng.7b00736

    Article  CAS  Google Scholar 

  • RUSSELL RS, Shorrocks V (1959) The relationship between transpiration and the absorption of inorganic ions by intact plants. JExB 10:301–316

    Google Scholar 

  • Sanzari I, Leone A, Ambrosone A (2019) Nanotechnology in plant science: to make a long story short. Front Bioeng Biotechnol 7:12. https://doi.org/10.3389/fbioe.2019.00120

    Article  Google Scholar 

  • Uzilday B, Turkan I, Ozgur R, Sekmen AH (2014) Strategies of ROS regulation and antioxidant defense during transition from C-3 to C-4 photosynthesis in the genus Flaveria under PEG-induced osmotic stress. J Plant Physiol 171:65–75. https://doi.org/10.1016/j.jplph.2013.06.016

    Article  CAS  Google Scholar 

  • Uzilday B, Turkan I, Sekmen AH, Ozgur R, Karakaya HC (2012) Comparison of ROS formation and antioxidant enzymes in Cleome gynandra (C-4) and Cleome spinosa (C-3) under drought stress. Plant Sci 182:59–70. https://doi.org/10.1016/j.plantsci.2011.03.015

    Article  CAS  Google Scholar 

  • Wang Y, Chang CH, Ji Z, Bouchard DC, Nisbet RM, Schimel JP, Gardea-Torresdey JL, Holden PA (2017) Agglomeration determines effects of carbonaceous nanomaterials on soybean nodulation, dinitrogen fixation potential, and growth in soil. ACS Nano 11:5753–5765. https://doi.org/10.1021/acsnano.7b01337

    Article  CAS  Google Scholar 

  • Wang Z, Xie X, Zhao J, Liu X, Feng W, White JC, Xing B (2012) Xylem- and phloem-based transport of CuO nanoparticles in maize (Zea mays L.). Environ Sci Technol 46:4434–4441. https://doi.org/10.1021/es204212z

    Article  CAS  Google Scholar 

  • Xiong T, Dumat C, Dappe V, Vezin H, Schreck E, Shahid M, Pierart A, Sobanska S (2017) Copper oxide nanoparticle foliar uptake, phytotoxicity, and consequences for sustainable urban agriculture. Environ Sci Technol 51:5242–5251. https://doi.org/10.1021/acs.est.6b05546

    Article  CAS  Google Scholar 

  • Yang J, Jiang F, Ma C, Rui Y, Rui M, Adeel M, Cao W, Xing B (2018) Alteration of crop yield and quality of wheat upon exposure to silver nanoparticles in a life cycle study. J Agric Food Chem 66:2589–2597

    Article  CAS  Google Scholar 

  • Ye Z-P, Ling Y, Yu Q, Duan HL, Kang HJ, Huang GM, Duan SH, Chen XM, Liu YG, Zhou SX (2020) Quantifying light response of leaf-scale water-use efficiency and its interrelationships with photosynthesis and stomatal conductance in C3 and C4 species. Front Plant Sci 11:374. https://doi.org/10.3389/fpls.2020.00374

    Article  Google Scholar 

  • Ze YG, Liu C, Wang L, Hong MM, Hong FS (2011) The regulation of TiO2 nanoparticles on the expression of light-harvesting complex II and photosynthesis of chloroplasts of Arabidopsis thaliana. Biol Trace Elem Res 143:1131–1141. https://doi.org/10.1007/s12011-010-8901-0

    Article  CAS  Google Scholar 

  • Zhang P, Ma Y, Zhang Z, He X, Zhang J, Guo Z, Tai R, Zhao Y, Chai Z (2012) Biotransformation of ceria nanoparticles in cucumber plants. ACS Nano 6:9943–9950. https://doi.org/10.1021/nn303543n

    Article  CAS  Google Scholar 

  • Zhang P, Ma Y, Xie C, Guo Z, He X, Valsami-Jones E, Lynch I, Luo W, Zheng L, Zhang Z (2019) Plant species-dependent transformation and translocation of ceria nanoparticles. Environ Sci Nano 6:60–67. https://doi.org/10.1039/c8en01089g

    Article  CAS  Google Scholar 

  • Zhang P, Guo Z, Zhang Z, Fu H, White JC, Lynch I (2020) Nanomaterial transformation in the soil–plant system: implications for food safety and application in agriculture. Small 16(21):e2000705. https://doi.org/10.1002/smll.202000705

  • Zhao X, Han L, Xiao J, Wang L, Liang T, Liao X (2020) A comparative study of the physiological and biochemical properties of tomato (Lycopersicon esculentum M.) and maize (Zea mays L.) under palladium stress. Sci Total Environ 705:135938 https://doi.org/10.1016/j.scitotenv.2019.135938

Download references

Funding

This work was supported by National Key R&D Program of China (2017YFD0801103, 2017YFD0801300), NSFC-Guangdong Joint Fund U1401234, National Natural Science Foundation of China 41371471, National Natural Science Foundation of China 41130526, National innovation and entrepreneurship program for undergraduate (202010019081), and Undergraduate Research Program supported by Yantai Institute of China agricultural university (U20191001).

Author information

Authors and Affiliations

Authors

Contributions

Tonghao Bai designed the experiments, analyzed the data, and drafted the paper. Peng Zhang analyzed the data and revised the paper. Zhiling Guo, Andrew J. Chetwynd, Mei Zhang, and Yukui Rui reviewed and edited manuscript. Muhammad Adeel, Mingshu Li, Ruize Gao, and Jianwei Li helped to perform the experiments. Kerui Guo and Yi Hao helped to get TEM images of nanoparticles. All authors have given approval to the final version of the manuscript.

Corresponding authors

Correspondence to Peng Zhang or Yukui Rui.

Ethics declarations

Ethical approval

Not applicable.

Consent to participate

Not applicable.

Consent to publish

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Additional information

Responsible Editor: Gangrong Shi

Publisher’s note

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

Supplementary Information

ESM 1

(DOCX 3173 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bai, T., Zhang, P., Guo, Z. et al. Different physiological responses of C3 and C4 plants to nanomaterials. Environ Sci Pollut Res 28, 25542–25551 (2021). https://doi.org/10.1007/s11356-021-12507-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-12507-7

Keywords

Navigation