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Uptake of graphene enhanced the photophosphorylation performed by chloroplasts in rice plants

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Abstract

New and enhanced functions were potentially imparted to the plant organelles after interaction with nanoparticles. In this study, we found that ∼ 44% and ∼ 29% of the accumulated graphene in the rice leaves passively transported to the chloroplasts and thylakoid, respectively, significantly enhanced the fluorescence intensity of chloroplasts, and promoted about 2.4 times higher adenosine triphosphate production than that of controls. The enhancement of graphene on the photophosphorylation was ascribed to two reasons: One is that graphene facilitates the electron transfer process of photosystem II in thylakoid, and the other is that graphene protects the photosystem II against photo-bleaching by acting as a scavenger of reactive oxygen species. Overall, our work here confirmed that graphene translocating in the thylakoid promoted the photosynthetic activity of chloroplast in vivo and in vitro, providing new opportunities for designing biomimetic materials to enhance the solar energy conversion systems, especially for repairing or increasing the photosynthesis activity of the plants grown under stress environment.

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References

  1. Zhu, X. G.; Long, S. P.; Ort, D. R. Improving photosynthetic efficiency for greater yield. Annu. Rev. Plant Biol.2010, 61, 235–261.

    CAS  Google Scholar 

  2. Boghossian, A. A.; Sen, F.; Gibbons, B. M.; Sen, S.; Faltermeier, S. M.; Giraldo, J. P.; Zhang, G. T.; Zhang, J. Q.; Heller, D. A.; Strano, M. S. Application of nanoparticle antioxidants to enable hyperstable chloroplasts for solar energy harvesting. Adv. Energy Mater.2013, 3, 881–893.

    CAS  Google Scholar 

  3. Wang, Y. X.; Li, S. L.; Liu, L. B.; Lv, F. T.; Wang, S. Conjugated polymer nanoparticles to augment photosynthesis of chloroplasts. Angew. Chem., Int. Ed.2017, 56, 5308–5311.

    CAS  Google Scholar 

  4. Giraldo, J. P.; Landry, M. P.; Faltermeier, S. M.; McNicholas, T. P.; Lverson, N. M.; Boghossian, A. A.; Reuel, N. F.; Hilmer, A. J.; Sen, F.; Brew, J. A. et al. Plant nanobionics approach to augment photosynthesis and biochemical sensing. Nat. Mater.2014, 13, 400–408.

    CAS  Google Scholar 

  5. Xu, Y. Q.; Fei, J. B.; Li, G. L.; Yuan, T. T.; Li, Y.; Wang, C. L.; Li, X. B.; Li, J. B. Enhanced photophosphorylation of a chloroplast-entrapping long-lived photoacid. Angew. Chem., Int. Ed.2017, 56, 12903–12907.

    CAS  Google Scholar 

  6. Peng, C.; Tong, H.; Shen, C. S.; Sun, L. J.; Yuan, P.; He, M.; Shi, J. Y. Bioavailability and translocation of metal oxide nanoparticles in the soil-rice plant system. Sci. Total Environ.2020, 713, 136662.

    CAS  Google Scholar 

  7. Peng, C.; Zhang, H.; Fang, H. X.; Xu, C.; Huang, H. M.; Wang, Y.; Sun, L. J.; Yuan, X. F.; Chen, Y. X.; Shi, J. Y. Natural organic matter-induced alleviation of the phytotoxicity to rice (Oryza sativa L.) caused by copper oxide nanoparticles. Environ. Toxicol. Chem.2015, 34, 1996–2003.

    CAS  Google Scholar 

  8. Wu, B. Y.; Zhu, L. Z.; Le, X. C. Metabolomics analysis of TiO2 nanoparticles induced toxicological effects on rice (Oryza sativa L.). Environ. Pollut.2017, 230, 302–310.

    CAS  Google Scholar 

  9. Du, J. J.; Wang, T.; Zhou, Q. X.; Hu, X. G.; Wu, J. H.; Li, G. F.; Li, G. Q.; Hou, F.; Wu, Y. N. Graphene oxide enters the rice roots and disturbs the endophytic bacterial communities. Ecotox. Environ. Safe.2020, 192, 110304.

    CAS  Google Scholar 

  10. Zhen, H. Z.; Ji, Z. X.; Roy, K. R.; Gao, M.; Pan, Y. X.; Cai, X. M.; Wang, L. M.; Li, W.; Chang, C. H.; Kaweeteerawat, C. et al. Engineered graphene oxide nanocomposite capable of preventing the evolution of antimicrobial resistance. ACS Nano2019, 13, 11488–11499.

    Google Scholar 

  11. Li, R. B.; Mansukhani, N. D.; Guiney, L. M.; Ji, Z. X.; Zhao, Y. C.; Chang, C. H.; French, C. T.; Miller, J. F.; Hersam, M. C.; Nel, A. E. et al. Identification and optimization of carbon radicals on hydrated graphene oxide for ubiquitous antibacterial coatings. ACS Nano2016, 10, 10966–10980.

    CAS  Google Scholar 

  12. Chen, L. Y.; Wang, C. L.; Li, H. L.; Qu, X. L.; Yang, S. T.; Chang, X. L. Bioaccumulation and toxicity of 13C-skeleton labeled graphene oxide in wheat. Environ. Sci. Technol.2017, 51, 10146–10153.

    CAS  Google Scholar 

  13. Guo, X. K.; Dong, S. P.; Petersen, E. J.; Gao, S. X.; Huang, Q. G.; Mao, L. Biological uptake and depuration of radio-labeled graphene by Daphnia magna. Environ. Sci. Technol.2013, 47, 12524–12531.

    CAS  Google Scholar 

  14. Huang, C.; Xia, T.; Niu, J. F.; Yang, Y.; Lin, S. J.; Wang, X. K; Yang, G. Q.; Mao, L.; Xing, B. S. Transformation of 14C-Labeled graphene to 14CO2 in the shoots of a rice plant. Angew. Chem., Int. Ed.2018, 57, 9759–9763.

    CAS  Google Scholar 

  15. Novoselov, K. S.; Geim, A. K.; Morozov, S. V.; Jiang, D.; Zhang, Y.; Dubonos, S. V.; Grigorieva, I. V.; Firsov, A. A. Electric field effect in atomically thin carbon films. Science2004, 306, 666–669.

    CAS  Google Scholar 

  16. Liu, C. H.; Chang, Y. C.; Norris, T. B.; Zhong, Z. H. Graphene photodetectors with ultra-broadband and high responsivity at room temperature. Nat. Nanotechnol.2014, 9, 273–278.

    CAS  Google Scholar 

  17. Li, W.; Wu, S. S.; Zhang, H. R.; Zhang, X. J.; Zhuang, J. L.; Hu, C. F.; Liu, Y. L.; Lei, B. F.; Ma, L.; Wang, X. J. Enhanced biological photosynthetic efficiency using light-harvesting engineering with dual-emissive carbon dots. Adv. Funct. Mater.2018, 28, 1804004.

    Google Scholar 

  18. Lonergan, T. A.; Sargent, M. L. Regulation of the photosynthesis rhythm in Euglena gracilis II. Involvement of electron flow through both photosystems. Plant Physiol.1979, 64, 99–103.

    CAS  Google Scholar 

  19. Gould, P. D.; Diza, P.; Hogben, C.; Kusakina, J.; Salem, R.; Hwrtwell, J.; Hall, A. Delayed fluorescence as a universal tool for the measurement of circadian rhythms in higher plants. Plant J.2009, 58, 893–901.

    CAS  Google Scholar 

  20. Cai, P.; Li, G. L.; Yang, Y.; Su, X. O.; Zhang, Z. F. Co-assembly of thylakoid and graphene oxide as a photoelectrochemical composite film for enhanced mediated electron transfer. Colloids Surf. A2018, 555, 37–42.

    CAS  Google Scholar 

  21. Fang, X.; Sokol, K. P.; Heidary, N.; Kandiel, T. A.; Zhang, J. Z.; Reisner, E. Structure-activity relationships of hierarchical three-dimensional electrodes with photosystem II for semiartificial photosynthesis. Nano Lett.2019, 19, 1844–1850.

    CAS  Google Scholar 

  22. Calkins, J. O.; Umasankar, Y.; O'Neill, H.; Ramasamy, R. P. High photo-electrochemical activity of thylakoid-carbon nanotube composites for photosynthetic energy conversion. Energy Environ. Sci.2013, 6, 1891–1900.

    CAS  Google Scholar 

  23. Ventrella, A.; Catucci, L.; Agostiano, A. Effect of aggregation state, temperature and phospholipids on photobleaching of photosynthetic pigments in spinach Photosystem II core complexes. Bioelectrochemistry2008, 73, 43–48.

    CAS  Google Scholar 

  24. Zhang, H.; Liu, H.; Tian, Z. Q.; Lu, D. L.; Yu, Y.; Cestellos-Blanco, S.; Sakimoto, K. K.; Yang, P. D. Bacteria photosensitized by intracellular gold nanoclusters for solar fuel production. Nat. Nanotechnol.2018, 13, 900–905.

    CAS  Google Scholar 

  25. Liu, J. G.; Mei, C. C.; Cai, H.; Wang, M. X. Relationships between subcellular distribution and translocation and grain accumulation of Pb in different rice cultivars. Water Air Soil Pollut.2015, 226, 93.

    Google Scholar 

  26. Li, G. L.; Fei, J. B.; Xu, Y. Q.; Li, Y.; Li, J. B. Bioinspired assembly of hierarchical light-harvesting architectures for improved photophosphorylation. Adv. Funct. Mater.2018, 28, 1706557.

    Google Scholar 

  27. Chen, Z. W.; De Queiros Silveira, G.; Ma, X. D.; Xie, Y. S.; Wu, Y. A.; Barry, E.; Rajh, T.; Fry, H. C.; Laible, P. D.; Rozhkova, E. A. Light-gated synthetic protocells for plasmon-enhanced chemiosmotic gradient generation and ATP synthesis. Angew. Chem., Int. Ed.2019, 58, 4896–4900.

    CAS  Google Scholar 

  28. Xu, Y. Q.; Fei, J. B.; Li, G. L.; Yuan, T. T.; Xu, X.; Wang, C. L.; Li, J. B. Optically matched semiconductor quantum dots improve photophosphorylation performed by chloroplasts. Angew. Chem., Int. Ed.2018, 57, 6532–6535.

    CAS  Google Scholar 

  29. Feng, X. Y.; Jia, Y.; Cai, P.; Fei, J. B.; Li, J. B. Coassembly of photosystem II and ATPase as artificial chloroplast for light-driven ATP synthesis. ACS Nano2016, 10, 556–561.

    CAS  Google Scholar 

  30. Suga, M.; Akita, F.; Hirata, K.; Ueno, G.; Murakami, H.; Nakajima, Y.; Shimizu, T.; Yamashita, K.; Yamamoto, M.; Ago, H. et al. Native structure of photosystem II at 1.95 Å resolution viewed by femtosecond X-ray pulses. Nature2015, 517, 99–103.

    CAS  Google Scholar 

  31. Shen, J. R. The structure of photosystem II and the mechanism of water oxidation in photosynthesis. Annu. Rev. Plant Biol.2015, 66, 23–48.

    CAS  Google Scholar 

  32. Jagendorf, A. T.; Uribe, E. ATP formation caused by acid-base transition of spinach chloroplasts. Proc. Natl. Acad. Sci. USA1966, 55, 170–177.

    CAS  Google Scholar 

  33. Kanazawa, A.; Kramer, D. M. In vivo modulation of nonphotochemical exciton quenching (NPQ) by regulation of the chloroplast ATP synthase. Proc. Natl. Acad. Sci. USA2002, 99, 12789–12794.

    CAS  Google Scholar 

  34. Kopnov, F.; Cohen-Ofri, I.; Noy, D. Electron transport between photosystem II and photosystem I encapsulated in sol-gel glasses. Angew. Chem., Int. Ed.2011, 50, 12347–12350.

    CAS  Google Scholar 

  35. Goltsev, V.; Zaharieva, I.; Chernev, P.; Strasser, R. J. Delayed fluorescence in photosynthesis. Photosynth. Res.2009, 101, 217–232.

    CAS  Google Scholar 

  36. Buchta, J.; Grabolle, M.; Dau, H. Photosynthetic dioxygen formation studied by time-resolved delayed fluorescence measurements-method, rationale, and results on the activation energy of dioxygen formation. Biochim. Biophys. Acta2007, 1767, 565–574.

    CAS  Google Scholar 

  37. Yeh, T. F.; Teng, C. Y.; Chen, S. J.; Teng, H. Nitrogen-doped graphene oxide quantum dots as photocatalysts for overall water-splitting under visible light illumination. Adv. Mater.2014, 26, 3297–3303.

    CAS  Google Scholar 

  38. Zou, H. Y.; He, B. W.; Kuang, P. Y.; Yu, J. G.; Fan, K. NixSy nanowalls/nitrogen-doped graphene foam is an efficient trifunctional catalyst for unassisted artificial photosynthesis. Adv. Funct. Mater.2018, 28, 1706917.

    Google Scholar 

  39. Pankratov, D.; Zhao, J. M.; Nur, M. A.; Shen, F.; Leech, D.; Chi, Q. J.; Pankratova, G.; Gorton, L. The influence of surface composition of carbon nanotubes on the photobioelectrochemical activity of thylakoid bioanodes mediated by osmium-complex modified redox polymer. Electrochim. Acta2019, 310, 20–25.

    CAS  Google Scholar 

  40. Gao, C.; Huang, Q. X.; Lan, Q. P.; Feng, Y.; Tang, F.; Hoi Maggie, P. M.; Zhang, J. X.; Lee Mimon, M. Y.; Wang, R B. A user-friendly herbicide derived from photo-responsive supramolecular vesicles. Nat. Commun.2018, 9, 2967.

    Google Scholar 

  41. Vass, I.; Styring, S.; Hundal, T.; Koivuniemi, A.; Aro, E.; Adnersson, B. Reversible and irreversible intermediates during photoinhibition of photosystem II. Stable reduced QA species promote chlorophyll triplet formation. Proc. Natl. Acad. Sci. USA1992, 89, 1408–1412.

    CAS  Google Scholar 

  42. Keren, N.; Berg, A.; Van Kan, P. J. M.; Levanon, H.; Ohad, I. Mechanism of photosystem II photoinactivation and D1 protein degradation at low light: The role of back electron flow. Proc. Natl. Acad. Sci. USA1997, 94, 1579–1584.

    CAS  Google Scholar 

  43. Kusama, Y.; Inoue, S.; Jimbo, H.; Takaichi, S.; Sonoike, K.; Hihara, Y.; Nishiyama, Y. Zeaxanthin and echinenone protect the repair of photosystem II from inhibition by singlet oxygen in Synechocystis sp. PCC 6803. Plant. Cell. Physiol.2015, 56, 906–916.

    CAS  Google Scholar 

  44. Zavafer, A.; Chow, W. S.; Cheah, M. H. The action spectrum of photosystem II photoinactivation in visible light. J. Photochem. Photobiol. B2015, 152, 247–260.

    CAS  Google Scholar 

  45. Qiao, Y.; Zhang, P. P.; Wang, C. M.; Ma, L. Y.; Su, M. Reducing X-ray induced oxidative damages in fibroblasts with graphene oxide. Nanomaterials2014, 4, 522–534.

    Google Scholar 

  46. Qiu, Y.; Wang, Z. Y.; Owens, A. C. E.; Kulaots, I.; Chen, Y. T.; Kane, A. B.; Hurt, R. H. Antioxidant chemistry of graphene-based materials and its role in oxidation protection technology. Nanoscale2014, 6, 11744–11755.

    CAS  Google Scholar 

  47. Xia, W.; Xue, H. R.; Wang, J. W.; Wang, T.; Song, L.; Guo, H.; Fan, X. L.; Gong, H.; He, J. P. Functionlized graphene serving as free radical scavenger and corrosion protection in gamma-irradiated epoxy composites. Carbon2016, 101, 315–323.

    CAS  Google Scholar 

  48. Gao, M.; Wang, Z. Z.; Zheng, H. Z.; Wang, L.; Xu, S. J.; Liu, X.; Li, W.; Pan, Y. X.; Wang, W. L.; Cai, X. M. et al. Two-dimensional tin selenide (SnSe) nanosheets capable of mimicking key dehydrogenases in cellular metabolism. Angew. Chem., Int. Ed.2020, 59, 3618–3623.

    CAS  Google Scholar 

  49. Cai, X. M.; Dong, J.; Liu, J.; Zheng, H. Z.; Kaweeteerawat, C.; Wang, F. J.; Ji, Z. X.; Li, R. B. Multi-hierarchical profiling the structure-activity relationships of engineered nanomaterials at nano-bio interfaces. Nat. Commun.2018, 9, 4416.

    Google Scholar 

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Acknowledgements

We acknowledge the financial support from the National Natural Science Foundation of China (No. 21677074) and the Fundamental Research Funds for the Central Universities (No. 021114380082).

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Correspondence to Liang Mao.

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Lu, K., Shen, D., Dong, S. et al. Uptake of graphene enhanced the photophosphorylation performed by chloroplasts in rice plants. Nano Res. 13, 3198–3205 (2020). https://doi.org/10.1007/s12274-020-2862-1

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