Journal Home > Volume 17 , Issue 2
Nano Research 2024, 17(2): 734-742 https://doi.org/10.1007/s12274-023-6362-y
Review Article | Issue | Published: 12 December 2023

Synthetic brochosomes: Design, synthesis, and applications

Show Author's Information Lin Wang1,2,  Jinsol Choi1,2,  Tak-Sing Wong1,2,3( )
Department of Mechanical Engineering, The Pennsylvania State University, University Park, PA 16802, USA
Materials Research Institute, The Pennsylvania State University, University Park, PA 16802, USA
Department of Biomedical Engineering, The Pennsylvania State University, University Park, PA 16802, USA
Keywords:
energy harvesting, photocatalyst, surface-enhanced Raman scattering, superhydrophobicity, antireflection, synthetic brochosomes, leafhopper
Topics:
Biomimetic materials
Cite this article:
Wang L, Choi J, Wong T-S. Synthetic brochosomes: Design, synthesis, and applications. Nano Research, 2024, 17(2): 734-742. https://doi.org/10.1007/s12274-023-6362-y
Download citation
EndNote(RIS)
BibTeX

314

Views

24

Downloads

Citations

2

Crossref

1

WoS

2

Scopus

0

CSCD

Abstract Full text About this article

Brochosomes, which are nanoscopic buckyball-shaped granules produced by leafhoppers, are one of the most intricate structures discovered in nature. Various functions of brochosomes have been proposed but only a few have been experimentally validated due to the challenge of fabricating their synthetic counterparts. Advancements in micro- and nanofabrication have recently led to the emergence of synthetic brochosomes, opening up new possibilities for innovative applications. This review explores the early discovery of natural brochosomes and their geometrical features, followed by the recent progress in fabricating synthetic brochosomes and their applications. Perspectives on future applications and challenges in the scalable manufacturing of synthetic brochosomes are discussed.


menu
Abstract
Full text
Outline
About this article

Synthetic brochosomes: Design, synthesis, and applications

Show Author's information Lin Wang1,2, Jinsol Choi1,2, Tak-Sing Wong1,2,3( )
Department of Mechanical Engineering, The Pennsylvania State University, University Park, PA 16802, USA
Materials Research Institute, The Pennsylvania State University, University Park, PA 16802, USA
Department of Biomedical Engineering, The Pennsylvania State University, University Park, PA 16802, USA

Abstract

Brochosomes, which are nanoscopic buckyball-shaped granules produced by leafhoppers, are one of the most intricate structures discovered in nature. Various functions of brochosomes have been proposed but only a few have been experimentally validated due to the challenge of fabricating their synthetic counterparts. Advancements in micro- and nanofabrication have recently led to the emergence of synthetic brochosomes, opening up new possibilities for innovative applications. This review explores the early discovery of natural brochosomes and their geometrical features, followed by the recent progress in fabricating synthetic brochosomes and their applications. Perspectives on future applications and challenges in the scalable manufacturing of synthetic brochosomes are discussed.

Keywords: energy harvesting, photocatalyst, surface-enhanced Raman scattering, superhydrophobicity, antireflection, synthetic brochosomes, leafhopper

References(67)

[1]

Tulloch, G. S.; Shapiro, J. E.; Cochran, G. W. The occurrence of ultramicroscopic bodies with leafhoppers and mosquitoes. Bull. Brooklyn Entomol. Soc. 1952, 47, 41–42.
DOI Google Scholar
[2]

Tulloch, G. S.; Shapiro, J. E. Brochosomes. Bull. Brooklyn Entomol. Soc. 1953, 48, 57.
Google Scholar
[3]

Tulloch, G. S.; Shapiro, J. E. Brochosomes and leafhoppers. Science 1954, 120, 232–232.
DOI Google Scholar
[4]

Rakitov, R. A. Secretion of brochosomes during the ontogenesis of a leafhopper, Oncometopia orbona (F) (Insecta, Homoptera, Cicadellidae). Tissue Cell 2000, 32, 28–39.
DOI Google Scholar
[5]

Rakitov, R. A. Secretory products of the Malpighian tubules of Cicadellidae (Hemiptera, Membracoidea): An ultrastructural study. Int. J. Insect Morphol. Embryol. 1999, 28, 179–193.
DOI Google Scholar
[6]

Rakitov, R. A. Powdering of egg nests with brochosomes and related sexual dimorphism in leafhoppers (Hemiptera: Cicadellidae). Zool. J. Linn. Soc. 2004, 140, 353–381.
DOI Google Scholar
[7]

de Azevedo-Filho, W. S.; Carvalho, G. S. Brochosomes-for-eggs of the Proconiini (Hemiptera: Cicadellidae, Cicadellinae) species associated with orchards of Citrus sinensis (L) Osbeck in Rio Grande do Sul, Brazil. Neotrop. Entomol. 2005, 34, 387–394.
DOI Google Scholar
[8]

de Azevedo Filho, W. S.; Botton, M.; Paladini, A.; Carvalho, G. S.; Ringenberg, R.; Lopes, J. R. S. Egg brochosomes of proconiini (Hemiptera: Cicadellidae, Cicadellinae) species associated with cultivation of grapevines. Sci. Agric. 2008, 65, 209–213.
DOI Google Scholar
[9]

Day, M. F.; Briggs, M. The origin and structure of brochosomes. J. Ultrastruct. Res. 1958, 2, 239–244.
DOI Google Scholar
[10]

Smith, D. S.; Littau, V. C. Cellular specialization in the excretory epithelia of an insect, Macrosteles fascifrons Stål (Homoptera). J. Biophys. Biochem. Cytol. 1960, 8, 103–133.
DOI Google Scholar
[11]

Gouranton, J.; Maillet, P. L. Origine et structure des brochosomes. J. Microscopie 1967, 6, 53–64.
Google Scholar
[12]

Rakitov, R.; Moysa, A. A.; Kopylov, A. T.; Moshkovskii, S. A.; Peters, R. S.; Meusemann, K.; Misof, B.; Dietrich, C. H.; Johnson, K. P.; Podsiadlowski, L. et al. Brochosomins and other novel proteins from brochosomes of leafhoppers (Insecta, Hemiptera, Cicadellidae). Insect Biochem. Mol. Biol. 2018, 94, 10–17.
DOI Google Scholar
[13]

Rakitov, R. A. Post-moulting behaviour associated with Malpighian tubule secretions in leafhoppers and treehoppers (Auchenorrhyncha: Membracoidea). Eur. J. Entomol. 1996, 93, 167–184.
Google Scholar
[14]

Storey, H. H.; Nichols, R. F. W. Defaecation by a Jassid species. Proc. Roy. Entomol. Soc. Lond. Ser. A Gen. Entomol. 1937, 12, 149–150.
DOI Google Scholar
[15]

Vidano, C.; Arzone, A. “Wax-area” in cicadellids and its connection with brochosomes from Malpighian tubules. Mitt. Schweiz. Entomol. Ges. 1984, 57, 444–445.
Google Scholar
[16]

Dong, H. Y.; Huang, M. Analysis of the anointing and grooming behavior of several adult insects in Typhlocybinae (Hemiptera: Cicadellidae). J. Insect Behav. 2013, 26, 540–549.
DOI Google Scholar
[17]

Navone, P. Origine, struttura e funzioni di escreti e secreti entomatici di aspetto ceroso distribuiti sul corpo mediante zampe. Ann. Fac. Sci. Agr. Univ. Stud. Torino 1987, 14, 237–294.
DOI Google Scholar
[18]

Rakitov, R.; Gorb, S. N. Brochosomal coats turn leafhopper (Insecta, Hemiptera, Cicadellidae) integument to superhydrophobic state. Proc. Roy. Soc. B: Biol. Sci. 2013, 280, 20122391.
DOI Google Scholar
[19]

Rakitov, R.; Gorb, S. N. Brochosomes protect leafhoppers (Insecta, Hemiptera, Cicadellidae) from sticky exudates. J. Roy. Soc. Interface 2013, 10, 20130445.
DOI Google Scholar
[20]

Arzone, A. Brocosomi: Origine, forma, funzione. Atti Accad. Naz. Ital. Entomol. Rc. 1986, 34, 59–71.
DOI Google Scholar
[21]

Mayse, M. A. Observations on the occurrence of chalky deposits on forewings of Oncometopia orbona (F) (Homoptera: Cicadellidae). J. Ark. Acad. Sci. 1981, 35, 84–86.
Google Scholar
[22]

Hix, R. Egg-laying and brochosome production observed in glassy-winged sharpshooter. Calif. Agric. 2001, 55, 19–22.
DOI Google Scholar
[23]

Humphrey, E. C.; Dworakowska, I. The natural history of brochosomes in Yakuza ganunga (Hemiptera, Auchenorrhyncha, Cicadellidae, Typhlocybinae, Erythroneurini). Denisia 2002, 4, 433–454.
Google Scholar
[24]

Swain, R. B. Notes on the oviposition and life-history of the leafhopper Oncometopia undata Fabr. (Homoptera: Cicadellidae). Entomol. News 1936, 47, 264–266.
DOI Google Scholar
[25]

Yang, S. K.; Sun, N.; Stogin, B. B.; Wang, J.; Huang, Y.; Wong, T. S. Ultra-antireflective synthetic brochosomes. Nat. Commun. 2017, 8, 1285.
DOI Google Scholar
[26]

Shih, M. S.; Chen, H. Y.; Li, P. C.; Yang, H. T. Broadband omnidirectional antireflection coatings inspired by embroidered ball-like structures on leafhoppers. Appl. Surf. Sci. 2020, 532, 147397.
DOI Google Scholar
[27]

Riley, C. V.; Howard, L. O. The glassy-winged sharpshooter. Insect Life 1893, 5, 150–154.
DOI Google Scholar
[28]

Rakitov, R. A. The covering formed by brochosomes on the cuticle of leafhoppers (Homoptera, Cicadellidae). Entomol. Rev. 1995, 74, 90–103.
Google Scholar
[29]

Lei, C. W.; Chen, R. Y.; Yang, H. T. Leafhopper wing-inspired broadband omnidirectional antireflective embroidered ball-like structure arrays using a nonlithography-based methodology. Langmuir 2020, 36, 5296–5302.
DOI Google Scholar
[30]

Si, Y. S.; Huang, T. Q.; Xie, H. Q.; Chen, M. Synthesis of biomimetic brochosome-shaped microspheres via droplets assembly strategy. Chem. Mater. 2022, 34, 7271–7279.
DOI Google Scholar
[31]
Pan, Q.; Zhang, H. F.; Yang, Y. P.; Cheng, C. W. 3D brochosomes-like TiO2/WO3/BiVO4 arrays as photoanode for photoelectrochemical hydrogen production. Small 2019 , 15, 1900924.
DOI
[32]

Zhu, K.; Yang, K.; Zhang, Y. Z.; Yang, Z. Y.; Qian, Z. T.; Li, N.; Li, L.; Jiang, G. H.; Wang, T. Y.; Zong, S. F. et al. Wearable SERS sensor based on omnidirectional plasmonic nanovoids array with ultra-high sensitivity and stability. Small 2022, 18, 2201508.
DOI Google Scholar
[33]

Zhao, W. D.; Zhang, Y. X.; Yang, J. J.; Li, J. M.; Feng, Y.; Quan, M. H.; Yang, Z.; Xiao, S. Y. Synergistic plasmon resonance coupling and light capture in ordered nanoarrays as ultrasensitive and reproducible SERS substrates. Nanoscale 2020, 12, 18056–18066.
DOI Google Scholar
[34]

Si, Y. S.; Huang, T. Q.; Li, Q. J.; Huang, Y. T.; Gao, S. P.; Chen, M.; Wu, L. M. Hierarchical macro-mesoporous polymeric carbon nitride microspheres with narrow bandgap for enhanced photocatalytic hydrogen production. Adv. Mater. Interfaces 2018, 5, 1801241.
DOI Google Scholar
[35]

Liu, Z. Q.; Li, W.; Sheng, W. B.; Liu, S. Y.; Li, R.; Li, Q.; Li, D. Y.; Yu, S.; Li, M.; Li, Y. S. et al. Tunable hierarchically structured meso-macroporous carbon spheres from a solvent-mediated polymerization-induced self-assembly. J. Am. Chem. Soc. 2023, 145, 5310–5319.
DOI Google Scholar
[36]

Clapham, P. B.; Hutley, M. C. Reduction of lens reflexion by the “moth eye” principle. Nature 1973, 244, 281–282.
DOI Google Scholar
[37]

Miller, W. H.; Bernard, G. D.; Allen, J. L. The optics of insect compound eyes. Science 1968, 162, 760–767.
DOI Google Scholar
[38]

Shavit, K.; Wagner, A.; Schertel, L.; Farstey, V.; Akkaynak, D.; Zhang, G.; Upcher, A.; Sagi, A.; Yallapragada, V. J.; Haataja, J. et al. A tunable reflector enabling crustaceans to see but not be seen. Science 2023, 379, 695–700.
DOI Google Scholar
[39]

Li, Y. F.; Zhang, J. H.; Yang, B. Antireflective surfaces based on biomimetic nanopillared arrays. Nano Today 2010, 5, 117–127.
DOI Google Scholar
[40]

Raut, H. K.; Ganesh, V. A.; Nair, A. S.; Ramakrishna, S. Anti-reflective coatings: A critical, in-depth review. Energy Environ. Sci. 2011, 4, 3779–3804.
DOI Google Scholar
[41]

Banerjee, P.; Burks, G. R.; Bialik, S. B.; Nassr, M.; Bello, E.; Alleyne, M.; Freeman, B. D.; Barrick, J. E.; Schroeder, C. M.; Milliron, D. J. Nanostructure-derived antireflectivity in leafhopper brochosomes. Adv. Photonics Res. 2023, 4, 2200343.
DOI Google Scholar
[42]

Quéré, D. Wetting and roughness. Annu. Rev. Mater. Res. 2008, 38, 71–99.
DOI Google Scholar
[43]

Cassie, A. B. D.; Baxter, S. Wettability of porous surfaces. Trans. Faraday Soc. 1944, 40, 546–551.
DOI Google Scholar
[44]

Cassie, A. B. D.; Baxter, S. Large contact angles of plant and animal surfaces. Nature 1945, 155, 21–22.
DOI Google Scholar
[45]

Ding, Q. Q.; Kang, Y. L.; Li, W. L.; Sun, G. F.; Liu, H.; Li, M.; Ye, Z. R.; Zhou, M.; Zhou, J. G.; Yang, S. K. Bioinspired brochosomes as broadband and omnidirectional surface-enhanced Raman scattering substrates. J. Phys. Chem. Lett. 2019, 10, 6484–6491.
DOI Google Scholar
[46]

Liu, H.; Xu, C.; Xia, Q. D.; Ying, Y. B.; Li, Q.; Zhao, X. Y.; Zhang, Y. J.; Yang, S. K. Tailorable and angle-independent colors from synthetic brochosomes. ACS Nano 2023, 17, 2257–2265.
DOI Google Scholar
[47]

Hua, C. Z.; Cheng, Z. Q.; Ma, Y. C.; He, H. Y.; Xu, G.; Liu, Y.; Yang, S. K.; Han, G. R. Enhanced electrochromic tungsten oxide by bio-inspired brochosomes. J. Electrochem. Soc. 2021, 168, 042503.
DOI Google Scholar
[48]

Skliutas, E.; Lebedevaite, M.; Kabouraki, E.; Baldacchini, T.; Ostrauskaite, J.; Vamvakaki, M.; Farsari, M.; Juodkazis, S.; Malinauskas, M. Polymerization mechanisms initiated by spatio-temporally confined light. Nanophotonics 2021, 10, 1211–1242.
DOI Google Scholar
[49]

Kelly, B. E.; Bhattacharya, I.; Heidari, H.; Shusteff, M.; Spadaccini, C. M.; Taylor, H. K. Volumetric additive manufacturing via tomographic reconstruction. Science 2019, 363, 1075–1079.
DOI Google Scholar
[50]

Tumbleston, J. R.; Shirvanyants, D.; Ermoshkin, N.; Janusziewicz, R.; Johnson, A. R.; Kelly, D.; Chen, K.; Pinschmidt, R.; Rolland, J. P.; Ermoshkin, A. et al. Continuous liquid interface production of 3D objects. Science 2015, 347, 1349–1352.
DOI Google Scholar
[51]

Han, F.; Gu, S. Y.; Klimas, A.; Zhao, N.; Zhao, Y. X.; Chen, S. C. Three-dimensional nanofabrication via ultrafast laser patterning and kinetically regulated material assembly. Science 2022, 378, 1325–1331.
DOI Google Scholar
[52]

Klaus-Joerger, T.; Joerger, R.; Olsson, E.; Granqvist, C. G. Bacteria as workers in the living factory: Metal-accumulating bacteria and their potential for materials science. Trends Biotechnol. 2001, 19, 15–20.
DOI Google Scholar
[53]

Kolinko, I.; Lohße, A.; Borg, S.; Raschdorf, O.; Jogler, C.; Tu, Q.; Pósfai, M.; Tompa, É.; Plitzko, J. M.; Brachmann, A. et al. Biosynthesis of magnetic nanostructures in a foreign organism by transfer of bacterial magnetosome gene clusters. Nat. Nanotechnol. 2014, 9, 193–197.
DOI Google Scholar
[54]

Choi, Y.; Park, T. J.; Lee, D. C.; Lee, S. Y. Recombinant Escherichia coli as a biofactory for various single- and multi-element nanomaterials. Proc. Natl. Acad. Sci. USA 2018, 115, 5944–5949.
DOI Google Scholar
[55]

Iravani, S.; Varma, R. S. Biofactories: Engineered nanoparticles via genetically engineered organisms. Green Chem. 2019, 21, 4583–4603.
DOI Google Scholar
[56]

Edwards, D. A.; Hanes, J.; Caponetti, G.; Hrkach, J.; Ben-Jebria, A.; Eskew, M. L.; Mintzes, J.; Deaver, D.; Lotan, N.; Langer, R. Large porous particles for pulmonary drug delivery. Science 1997, 276, 1868–1872.
DOI Google Scholar
[57]

Mitchell, M. J.; Billingsley, M. M.; Haley, R. M.; Wechsler, M. E.; Peppas, N. A.; Langer, R. Engineering precision nanoparticles for drug delivery. Nat. Rev. Drug Discov. 2021, 20, 101–124.
DOI Google Scholar
[58]

Mukherjee, R.; Krishnan, R.; Lu, T. M.; Koratkar, N. Nanostructured electrodes for high-power lithium ion batteries. Nano Energy 2012, 1, 518–533.
DOI Google Scholar
[59]

Wang, Y.; Huang, X. L.; Liu, H. W.; Qiu, W. L.; Feng, C.; Li, C.; Zhang, S. H.; Liu, H. K.; Dou, S. X.; Wang, Z. M. Nanostructure engineering strategies of cathode materials for room-temperature Na-S batteries. ACS Nano 2022, 16, 5103–5130.
DOI Google Scholar
[60]

Jain, R.; Lakhnot, A. S.; Bhimani, K.; Sharma, S.; Mahajani, V.; Panchal, R. A.; Kamble, M.; Han, F. D.; Wang, C. S.; Koratkar, N. Nanostructuring versus microstructuring in battery electrodes. Nat. Rev. Mater. 2022, 7, 736–746.
DOI Google Scholar
[61]

Chen, G. Y.; Seo, J.; Yang, C. H.; Prasad, P. N. Nanochemistry and nanomaterials for photovoltaics. Chem. Soc. Rev. 2013, 42, 8304–8338.
DOI Google Scholar
[62]

Liu, L. X.; Luo, C. H.; Zhang, J. H.; He, X.; Shen, Y.; Yan, B.; Huang, Y.; Xia, F.; Jiang, L. Synergistic effect of bio-inspired nanochannels: Hydrophilic DNA probes at inner wall and hydrophobic coating at outer surface for highly sensitive detection. Small 2022, 18, 2201925.
DOI Google Scholar
[63]

Yang, X.; Wang, J. H.; Gao, Z. F.; Zhang, W. Q.; Zhu, H.; Song, Y. J.; Wang, Q.; Liu, M. J.; Jiang, L.; Huang, Y. et al. An orthogonal dual-regulation strategy for sensitive biosensing applications. Natl. Sci. Rev. 2022, 9, nwac048.
DOI Google Scholar
[64]

Huang, Y.; Liu, L. X.; Yang, X.; Zhang, X. Y.; Yan, B.; Wu, L.; Feng, P. J.; Lou, X. D.; Xia, F.; Song, Y. L. et al. A diverse micromorphology of photonic crystal chips for multianalyte sensing. Small 2021, 17, 2006723.
DOI Google Scholar
[65]

Jakšić, Z.; Obradov, M.; Jakšić, O. Brochosome-inspired metal-containing particles as biomimetic building blocks for nanoplasmonics: Conceptual generalizations. Biomimetics 2021, 6, 69.
DOI Google Scholar
[66]

Zhang, X. G.; Zhang, X. L.; Luo, C. L.; Liu, Z. Q.; Chen, Y. Y.; Dong, S. L.; Jiang, C. Z.; Yang, S. K.; Wang, F. B.; Xiao, X. H. Volume-enhanced Raman scattering detection of viruses. Small 2019, 15, 1805516.
DOI Google Scholar
[67]

Yang, S. K.; Dai, X. M.; Stogin, B. B.; Wong, T. S. Ultrasensitive surface-enhanced Raman scattering detection in common fluids. Proc. Natl. Acad. Sci. USA 2016, 113, 268–273.
DOI Google Scholar
Publication history
Copyright
Acknowledgements

Publication history

Received: 05 June 2023
Revised: 22 November 2023
Accepted: 23 November 2023
Published: 12 December 2023
Issue date: February 2024

Copyright

© Tsinghua University Press 2023

Acknowledgements

Acknowledgements

This work was supported by the Office of Naval Research Award (Nos. N00014-20-1-2095 and N00014-23-1-2173, Program manager: Dr. Kristy L. Hentchel).

Return