Skip to main content
SpringerLink
Log in

Enhanced RuBisCO activity and promoted dicotyledons growth with degradable carbon dots

  • Research Article
  • Published:
Nano Research Aims and scope Submit manuscript

Abstract

The ∼ 5 nm degradable carbon dots (CDs) were synthesized directly from carbon rod by a one-step electrochemical method at room temperature. The as-prepared CDs can effectively enhance the ribulose bisphosphate carboxylase oxygenase (RuBisCO) activity, and then promote the dicotyledons growth (soybean, tomato, eggplant and so on) and finally increase their yields. Here, we used Arabidopsis thaliana and Trifolium repens L. as model plants to systematically study the beneficial effects of CDs on plant growth. These include: (i) accelerating seed germination; (ii) enlarging root elongation; (iii) increasing metal ions absorption and delivery; (iv) improving enzymes activity; (v) enhancing the carbohydrate content; (vi) degradation into plant hormone analogues and CO2; and finally (vii) enhancing the grain production by about 20%.

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

Similar content being viewed by others

References

  1. Hamilton, A.; Hamilton, P. Plant Conservation: An Ecosystem Approach; Earthscan: London, 2006.

    Google Scholar 

  2. Kesler, S. E.; Simon, A. C. Mineral Resources, Economics and the Environment; Cambridge University: Cambridge, 2015.

    Book  Google Scholar 

  3. Zheng, L.; Hong, F. S.; Lu, S. P.; Liu, C. Effect of nano-TiO2 on strength of naturally aged seeds and growth of spinach. Biol. Trace Elem. Res. 2005, 104, 83–91.

    Article  Google Scholar 

  4. Hong, F. S.; Zhou, J.; Liu, C.; Yang, F.; Wu, C.; Zheng, L.; Yang, P. Effect of nano-TiO2 on photochemical reaction of chloroplasts of spinach. Biol. Trace Elem. Res. 2005, 105, 269–279.

    Article  Google Scholar 

  5. Gao, F. Q.; Hong, F. S.; Liu, C.; Zheng, L.; Su, M. Y.; Wu, X.; Yang, F.; Wu, C.; Yang, P. Mechanism of nano-anatase TiO2 on promoting photosynthetic carbon reaction of spinach: Inducing complex of rubisco-rubisco activase. Biol. Trace Elem. Res. 2006, 111, 239–253.

    Article  Google Scholar 

  6. Zheng, L.; Su, M. Y.; Liu, C.; Chen, L.; Huang, H.; Wu, X.; Liu, X. Q.; Yang, F.; Gao, F. Q.; Hong, F. S. Effects of nanoanatase TiO2 on photosynthesis of spinach chloroplasts under different light illumination. Biol. Trace Elem. Res. 2007, 119, 68–76.

    Article  Google Scholar 

  7. Gao, F. Q.; Liu, C.; Qu, C. X.; Zheng, L.; Yang, F.; Su, M. Y.; Hong, F. S. Was improvement of spinach growth by nano-TiO2 treatment related to the changes of rubisco activase? BioMetals 2008, 21, 211–217.

    Article  Google Scholar 

  8. Ma, L. L.; Liu, C.; Qu, C. X.; Yin, S. T.; Liu, J.; Gao, F. Q.; Hong, F. H. Rubisco activase mRNA expression in spinach: Modulation by nanoanatase treatment. Biol. Trace Elem. Res. 2008, 122, 168–178.

    Article  Google Scholar 

  9. Wang, X. M.; Gao, F. Q.; Ma, L. L.; Liu, J.; Yin, S. T.; Yang, P.; Hong, F. S. Effects of nano-anatase on ribulose-1, 5-bisphosphate carboxylase/oxygenase mRNA expression in spinach. Biol. Trace Elem. Res. 2008, 126, 280–289.

    Article  Google Scholar 

  10. Su, M. Y.; Liu, J.; Yin, S. T.; Ma, L. L.; Hong, F. S. Effects of nanoanatase on the photosynthetic improvement of chloroplast damaged by linolenic acid. Biol. Trace Elem. Res. 2008, 124, 173–183.

    Article  Google Scholar 

  11. Yang, F.; Hong, F. S.; You, W. J.; Liu, C.; Gao, F. Q.; Wu, C.; Yang, P. Influence of nano-anatase TiO2 on the nitrogen metabolism of growing spinach. Biol. Trace Elem. Res. 2006, 110, 179–190.

    Article  Google Scholar 

  12. Shah, V.; Belozerova, I. Influence of metal nanoparticles on the soil microbial community and germination of lettuce seeds. Water, Air, Soil Pollut. 2009, 197, 143–148.

    Article  Google Scholar 

  13. Husen, A.; Siddiqi, K. S. Carbon and fullerene nanomaterials in plant system. J. Nanobiotechnology 2014, 12, 16.

    Article  Google Scholar 

  14. Qu, G. B.; Bai, Y. H.; Zhang, Y.; Jia, Q.; Zhang, W. D.; Yan, B. The effect of multiwalled carbon nanotube agglomeration on their accumulation in and damage to organs in mice. Carbon 2009, 47, 2060–2069.

    Article  Google Scholar 

  15. Liu, Q. L.; Chen, B.; Wang, Q. L.; Shi, X. L.; Xiao, Z. Y.; Lin, J. X.; Fang, X. H. Carbon nanotubes as molecular transporters for walled plant cells. Nano Lett. 2009, 9, 1007–1010.

    Article  Google Scholar 

  16. Kang, S.; Herzberg, M.; Rodrigues, D. F.; Elimelech, M. Antibacterial effects of carbon nanotubes: Size does matter! Langmuir 2008, 24, 6409–6413.

    Article  Google Scholar 

  17. Tripathi, S.; Sonkar, S. K.; Sarkar, S. Growth stimulation of gram (Cicer arietinum) plant by water soluble carbon nanotubes. Nanoscale 2011, 3, 1176–1181.

    Article  Google Scholar 

  18. Sonkar, S. K.; Roy, M.; Babar, D. G.; Sarkar, S. Water soluble carbon nanoonions from wood wool as growth promoters for gram plants. Nanoscale 2012, 4, 7670–7675.

    Article  Google Scholar 

  19. Tripathi, K. M.; Bhati, A., Singh, A.; Sonker, A. K.; Sarkar, S.; Sonkar, S. K. Sustainable changes in the contents of metallic micronutrients in first generation gram seeds imposed by carbon nano-onions: Life cycle seed to seed study. ACS Sustainable Chem. Eng. 2017, 5, 2906–2916.

    Article  Google Scholar 

  20. Villagarcia, H.; Dervishi, E.; De Silva, K.; Biris, A. S.; Khodakovskaya, M. V. Surface chemistry of carbon nanotubes impacts the growth and expression of water channel protein in tomato plants. Small 2012, 8, 2328–2334.

    Article  Google Scholar 

  21. Lahiani, M. H.; Dervishi, E.; Chen, J. H.; Nima, Z.; Gaume, A.; Biris, A. S.; Khodakovskaya, M. V. Impact of carbon nanotube exposure to seeds of valuable crops. ACS Appl. Mater. Interfaces 2013, 5, 7965–7973.

    Article  Google Scholar 

  22. Lahiani, M. H.; Dervishi, E.; Ivanov, I.; Chen, J. H.; Khodakovskaya, M. Comparative study of plant responses to carbon-based nanomaterials with different morphologies. Nanotechnology 2016, 27, 265102.

    Article  Google Scholar 

  23. Kole, C.; Kole, P.; Randunu, K. M.; Choudhary, P.; Podila, R.; Ke, P. C.; Rao, A. M.; Marcus, R. K. Nanobiotechnology can boost crop production and quality: First evidence from increased plant biomass, fruit yield and phytomedicine content in bitter melon (Momordica charantia). BMC Biotechnol. 2013, 13, 37.

    Article  Google Scholar 

  24. Saxena, M.; Maity, S.; Sarkar, S. Carbon nanoparticles in “biochar” boost wheat (Triticum aestivum) plant growth. RSC Adv. 2014, 4, 39948–39954.

    Article  Google Scholar 

  25. Li, H. T.; He, X. D.; Kang, Z. H.; Huang, H.; Liu, Y.; Liu, J. L.; Lian, S. Y.; Tsang, C. H. A.; Yang, X. B.; Lee, S. T. Water-soluble fluorescent carbon quantum dots and photocatalyst design. Angew. Chem., Int. Ed. 2010, 49, 4430–4434.

    Article  Google Scholar 

  26. Li, H.; Guo, S. J.; Li, C. X.; Huang, H.; Liu, Y.; Kang, Z. H. Tuning laccase catalytic activity with phosphate functionalized carbon dots by visible light. ACS Appl. Mater. Interfaces 2015, 7, 10004–10012.

    Article  Google Scholar 

  27. Abu-Ghosh, S.; Kumar, V. B.; Fixler, D.; Dubinsky, Z.; Gedanken, A.; Iluz, D. Nitrogen-doped carbon dots prepared from bovine serum albumin to enhance algal astaxanthin production. Algal Res. 2017, 23, 161–165.

    Article  Google Scholar 

  28. Liu, X. J.; Liu, L. T.; Hu, X. J.; Zhou, S. Y.; Ankri, R.; Fixler, D.; Xie, Z. Multimodal bioimaging based on gold nanorod and carbon dot nano-hybrids as a novel tool for atherosclerosis detection. Nano Res. 2018, 11, 1262–1273.

    Article  Google Scholar 

  29. Niu, Y. F.; Ling, G.; Wang, L.; Guan, S. Y.; Xie, Z.; Barnoy, E. A.; Zhou, S. Y.; Fixler, D. Gold rod-polyethylene glycol-carbon dot nanohybrids as phototheranostic probes. Nanomaterials 2018, 8, 706.

    Article  Google Scholar 

  30. Guo, S. J.; Zhao, S. Q.; Wu, X. Q.; Li, H.; Zhou, Y. J.; Zhu, C.; Yang, N. J.; Jiang, X.; Gao, J.; Bai, L. et al. A Co3O4-CDots-C3N4 three component electrocatalyst design concept for efficient and tunable CO2 reduction to syngas. Nat. Commun. 2017, 8, 1828.

    Article  Google Scholar 

  31. Liu, J.; Liu, Y.; Liu, N. Y.; Han, Y. Z.; Zhang, X.; Huang, H.; Lifshitz, Y.; Lee, S. T.; Zhong, J.; Kang, Z. H. Metal-free efficient photocatalyst for stable visible water splitting via a two-electron pathway. Science 2015, 347, 970–974.

    Article  Google Scholar 

  32. Yu, H.; Du, L. B.; Guan, L. M.; Zhang, K.; Li, Y. Y.; Zhu, H. J.; Sun, M. T.; Wang, S. H. A ratiometric fluorescent probe based on the pi-stacked graphene oxide and cyanine dye for sensitive detection of bisulfite. Sens. Actuators B: Chem. 2017, 247, 823–829.

    Article  Google Scholar 

  33. Yan, Y. H.; Yu, H.; Zhang, K.; Sun, M. T.; Zhang, Y. J.; Wang, X. K.; Wang, S. H. Dual-emissive nanohybrid of carbon dots and gold nanoclusters for sensitive determination of mercuric ions. Nano Res. 2016, 9, 2088–2096.

    Article  Google Scholar 

  34. Ge, H. W.; Zhang, K.; Yu, H.; Yue, J.; Yu, L.; Chen, X. F.; Hou, T. X.; Alamry, K. A.; Marwani, H. M.; Wang, S. H. Sensitive and selective detection of antibiotic d-penicillamine based on a dual-mode probe of fluorescent carbon dots and gold nanoparticles. J. Fluoresc. 2018, 28, 1405–1412.

    Article  Google Scholar 

  35. Li, H.; Kong, W. Q.; Liu, J.; Liu, N. Y.; Huang, H.; Liu, Y.; Kang, Z. H. Fluorescent N-doped carbon dots for both cellular imaging and highly-sensitive catechol detection. Carbon 2015, 91, 66–75.

    Article  Google Scholar 

  36. Lu, F.; Song, Y. X.; Huang, H.; Liu, Y.; Fu, Y. J.; Huang, J.; Li, H.; Qu, H. H.; Kang, Z. H. Fluorescent carbon dots with tunable negative charges for bio-imaging in bacterial viability assessment. Carbon 2017, 120, 95–102.

    Article  Google Scholar 

  37. Ge, J. C.; Lan, M. H.; Zhou, B. J.; Liu, W. M.; Guo, L.; Wang, H.; Jia, Q. Y.; Niu, G. L.; Huang, X.; Zhou, H. Y. et al. A graphene quantum dot photodynamic therapy agent with high singlet oxygen generation. Nat. Commun. 2014, 5, 4596.

    Article  Google Scholar 

  38. Lim, S. Y.; Shen, W.; Gao, Z. Q. Carbon quantum dots and their applications. Chem. Soc. Rev. 2015, 44, 362–381.

    Article  Google Scholar 

  39. Jermyn, M. A. Increasing the sensitivity of the anthrone method for carbohydrate. Anal. Biochem. 1975, 68, 332–335.

    Article  Google Scholar 

  40. Loewus, F. A. Improvement in anthrone method for determination of carbohydrates. Anal. Chem. 1952, 24, 219.

    Article  Google Scholar 

  41. Hohl, H.; Stumm, W. Interaction of Pb2+ with hydrous γ-Al2O3. J. Colloid Interface Sci. 1976, 55, 281–288.

    Article  Google Scholar 

  42. Crocker, M.; Herold, R. H. M.; Sonnemans, M. H. W.; Emeis, C. A.; Wilson, A. E.; Van Der Moolen, J. N. Studies on the acidity of mordenite and ZSM 5. 1. Determination of broensted acid site concentrations in mordenite and ZSM 5 by conductometric titration. J. Phys. Chem. 1993, 97, 432–439.

    Article  Google Scholar 

  43. Hunt, J. P.; Taube, H. The photochemical decomposition of hydrogen peroxide. Quantum yields, tracer and fractionation effects. J. Am. Chem. Soc. 1952, 74, 5999–6002.

    Article  Google Scholar 

  44. Zhao, Y.; Allen, B. L.; Star, A. Enzymatic degradation of multiwalled carbon nanotubes. J. Phys. Chem. A 2011, 115, 9536–9544.

    Article  Google Scholar 

  45. Lan, Y.; Mott, K. A. Determination of apparent K m values for ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) activase using the spectrophotometric assay of rubisco activity. Plant Physiol. 1991, 95, 604–609.

    Article  Google Scholar 

  46. Chong, Y.; Ma, Y. F.; Shen, H.; Tu, X. L.; Zhou, X.; Xu, J. Y.; Dai, J. W.; Fan, S. J.; Zhang, Z. J. The in vitro and in vivo toxicity of graphene quantum dots. Biomaterials 2014, 35, 5041–5048.

    Article  Google Scholar 

  47. Ming, H.; Ma, Z.; Liu, Y.; Pan, K. M.; Yu, H.; Wang, F.; Kang, Z. H. Large scale electrochemical synthesis of high quality carbon nanodots and their photocatalytic property. Dalton Trans. 2012, 41, 9526–9531.

    Article  Google Scholar 

  48. Li, H.; Zhang, M. L.; Song, Y. X.; Wang, H. B.; Liu, C. A.; Fu, Y. J.; Huang, H.; Liu, Y.; Kang, Z. H. Multifunctional carbon dot for lifetime thermal sensing, nucleolus imaging and antialgal activity. J. Mater. Chem. B 2018, 6, 5708–5717.

    Article  Google Scholar 

  49. Khodakovskaya, M.; Dervishi, E.; Mahmood, M.; Xu, Y.; Li, Z. R.; Watanabe, F.; Biris, A. S. Carbon nanotubes are able to penetrate plant seed coat and dramatically affect seed germination and plant growth. ACS Nano 2009, 3, 3221–3227.

    Article  Google Scholar 

  50. Wilson, A. T.; Calvin, M. The Photosynthetic cycle. CO2 dependent transients. J. Am. Chem. Soc. 1955, 77, 5948–5957.

    Article  Google Scholar 

  51. Walker, D. A. Three phases of chloroplast research. Nature 1970, 226, 1204–1208.

    Article  Google Scholar 

  52. Lin, M. T.; Occhialini, A.; Andralojc, P. J.; Parry, M. A. J.; Hanson, M. R. A faster rubisco with potential to increase photosynthesis in crops. Nature 2014, 513, 547–550.

    Article  Google Scholar 

  53. Wong, S. W.; Cowan, I. R.; Farquhar, G. D. Stomatal conductance correlates with photosynthetic capacity. Nature 1979, 282, 424–426.

    Article  Google Scholar 

  54. Kotchey, G. P.; Hasan, S. A.; Kapralov, A. A.; Ha, S. H.; Kim, K.; Shvedova, A. A.; Kagan, V. E.; Star, A. A natural vanishing act: The enzyme-catalyzed degradation of carbon nanomaterials. Acc. Chem. Res. 2012, 45, 1770–1781.

    Article  Google Scholar 

  55. Allen, B. L.; Kotchey, G. P.; Chen, Y. N.; Yanamala, N. V. K.; Klein-Seetharaman, J.; Kagan, V. E.; Star, A. Mechanistic investigations of horseradish peroxidase-catalyzed degradation of single-walled carbon nanotubes. J. Am. Chem. Soc. 2009, 131, 17194–17205.

    Article  Google Scholar 

  56. Went, F. W.; Thimann, K. V. Phytohormones; The Macmillan Company: New York, 1937.

    Google Scholar 

  57. Nurunnabi, M.; Khatun, Z.; Huh, K. M.; Park, S. Y.; Lee, D. Y.; Cho, K. J.; Lee, Y. K. In vivo biodistribution and toxicology of carboxylated graphene quantum dots. ACS Nano 2013, 7, 6858–6867.

    Article  Google Scholar 

Download references

Acknowledgements

This work is supported by the National MCF Energy R&D Program (No. 2018YFE0306105), the National Natural Science Foundation of China (Nos. 51725204, 51572179, 21771132, and 21471106), the Natural Science Foundation of Jiangsu Province (No. BK20161216), Collaborative Innovation Center of Suzhou Nano Science & Technology, the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD), and the 111 Project.

Author information

Authors and Affiliations

  1. Institute of Functional Nano & Soft Materials (FUNSOM), Jiangsu Key Laboratory for Carbon-Based Functional Materials & Devices, Joint International Research Laboratory of Carbon-Based Functional Materials and Devices, Soochow University, Suzhou, 215123, China

    Hao Li, Yang Liu, Jun Zhong, Yeshayahu Lifshitz, Shuit-Tong Lee & Zhenhui Kang

  2. School of biology & basic medical sciences, Soochow university, Suzhou, 215123, China

    Jian Huang

  3. College of Life Science and Oceanography, Shenzhen Key Laboratory of Marine Bioresources and Ecology, Shenzhen University, Shenzhen, 518060, China

    Yong Wang & Shuiming Li

  4. School of Basic Medical Sciences, Beijing University of Chinese Medicine, Beijing, 100029, China

    Fang Lu

  5. Department of Materials Science and Engineering, Technion, Israel Institute of Technology, Haifa, 3200003, Israel

    Yeshayahu Lifshitz

Authors
  1. Hao Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jian Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fang Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jun Zhong
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Shuiming Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yeshayahu Lifshitz
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Shuit-Tong Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Zhenhui Kang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Yang Liu, Yeshayahu Lifshitz or Zhenhui Kang.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, H., Huang, J., Liu, Y. et al. Enhanced RuBisCO activity and promoted dicotyledons growth with degradable carbon dots. Nano Res. 12, 1585–1593 (2019). https://doi.org/10.1007/s12274-019-2397-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12274-019-2397-5

Keywords

Search

Navigation