Multiwalled carbon nanotubes enter broccoli cells enhancing growth and water uptake of plants exposed to salinity

Journal of Nanobiotechnology - Tập 14 - Trang 1-14 - 2016
Mª Carmen Martínez-Ballesta1, Lavinia Zapata1, Najla Chalbi2, Micaela Carvajal1
1Plant Nutrition Department, Centro de Edafología y Biología Aplicada del Segura (CEBAS-CSIC), Campus Universitario de Espinardo, Murcia, Spain
2Laboratory of Extremophile Plants, Center of Biotechnology of Borj-Cedria (LEP-CBBC), Hammam-Lif, Tunisia

Tóm tắt

Carbon nanotubes have been shown to improve the germination and growth of some plant species, extending the applicability of the emerging nano-biotechnology field to crop science. In this work, exploitation of commercial multiwalled carbon nanotubes (MWCNTs) in control and 100 mM NaCl-treated broccoli was performed. Transmission electron microscopy demonstrated that MWCNTs can enter the cells in adult plants with higher accumulation under salt stress. Positive effect of MWCNTs on growth in NaCl-treated plants was consequence of increased water uptake, promoted by more-favourable energetic forces driving this process, and enhanced net assimilation of CO2. MWCNTs induced changes in the lipid composition, rigidity and permeability of the root plasma membranes relative to salt-stressed plants. Also, enhanced aquaporin transduction occurred, which improved water uptake and transport, alleviating the negative effects of salt stress. Our work provides new evidences about the effect of MWCNTs on plasma membrane properties of the plant cell. The positive response to MWCNTs in broccoli plants opens novel perspectives for their technological uses in new agricultural practices, especially when 1plants are exposed to saline environments.

Tài liệu tham khảo

Chinnamuthu CR, Boopathi PM. Nanotechnology and agroecosystem. Madras Agric J. 2009;96:17–31. Nair R, Varghese SH, Nair BG, Yoshida MY, Kumar DS. Nanoparticle material delivery to plants. Plant Sci. 2010;179:154–63. Zheng L, Hong F, Lu S, Liu C. Effect of nano-TiO2 on strength of naturally aged seeds and growth of spinach. Biol Trace Elem Res. 2005;104:83–91. Niederberger M. Nonaqueous sol-gel routes to metal oxide nanoparticles. Acc Chem Res. 2007;40:793–800. Geremias R, Fattorini D, F´avere VTD, Pedrosa RC. Bioaccumulation and toxic effects of copper in common onion Allium cepa L. Chem Ecol. 2010;26:19–26. Iijima S. Helical microtubules of graphitic carbon. Nature. 1991;354:56–8. Dresselhaus MS, Dresselhaus G, Jorio A. Unusual properties and structure of carbon nano tubes. Annu Rev Mater Res. 2004;34:247–78. Eatermadi A, Darae H, Karimkhanloo H, Koui M, Zarghami N, Akbarzadeh A, et al. Carbon nanotubes: properties, synthesis, purification, and applications. Nanoscale Res Lett. 2014;9:393. Khodakovskaya M, Dervishi E, Mahmood M, Xu Y, Li Z, Watanabe F, et al. Carbon nanotubes are able to penetrate plant seed coat and dramatically affect seed germination and plant growth. ACS Nano. 2009;3:3221–7. Khodakovskaya M, Kim B, Kim J, Alimohammdi M, Dervishi E, Mustafa T, et al. Carbon nanotubes as plant growth regulators: effects on tomato growth, reproductive system, and soil microbial community. Small. 2013;9:115–23. Ghodake G, Seo YD, Park D, Lee DS. Phytotoxicity of carbon nanotubes assessed by Brassica juncea and Phaseolus mungo. J Nanoelectron Optoe. 2010;5:157–60. Mondal A, Basu R, Das S, Nandy P. Beneficial role of carbon nanotubes on mustard plant growth: an agricultural prospect. J Nanopart Res. 2011;13:4519–28. Safiuddin M, Gonzalez M, Cao JW, Tighe SL. State of-the-art report on use of nano-materials in concrete. Int J Pavement Eng. 2014;15:940. Begum P, Ikhtiari R, Fugetsu B. Graphene phytotoxicity in the seedling stage of cabbage, tomato, red spinach, and lettuce. Carbon. 2011;49:3907–19. Fugetsu B, Parvin B. Graphene phytotoxicity in the seedling stage of cabbage, tomato, red spinach, and lettuce. In: Bianco S, editor. Carbon nanotubes-from research to applications. CC BY-NC-SA. 2011. Liu Q, Zhao Y, Wan Y, Zheng J, Zhang X, Wang C, et al. Study of the inhibitory effect of water-soluble fullerenes on plant growth at the cellular level. ACS Nano. 2010;4:5743–8. Gao J, Wang Y, Folta KM, Krishna V, Bai W, Indeglia P, et al. Polyhydroxy fullerenes (fullerols or fullerenols): beneficial effects on growth and lifespan in diverse biological models. PLoS One. 2011;6(5):e19976. Lin S, Reppert J, Hu Q, Hudson JS, Reid ML, Ratnikova TA, et al. Uptake, translocation, and transmission of carbon nanomaterials in rice plants. Small. 2009;5:1128–32. Tiwari DK, Dasgupta-Schubert N, Villaseñor Cendejas N, Villegas J, Carreto Montoya L, García SEB. Interfacing carbon nanotubes (CNT) with plants: enhancement of growth, water and ionic nutrient uptake in maize (Zea mays) and implications for nanoagriculture. Appl Nanosci. 2014;4:577–91. Husen A. Siddiqi K Carbon and fullerene nanomaterials in plant system. J Nanobiotechnol. 2014;12:16. Khodakovskaya M, Silva K, Biris A, Dervishi E, Villagarcia H. Carbon nanotubes induce growth enhancement of tobacco cells. ACS Nano. 2012;6:2128–35. Maurel C. Plant aquaporins: novel functions and regulation properties. FEBS Lett. 2007;581:2227–36. Martínez-Ballesta MC, Rodríguez-Hernández MC, Alcaraz-López C, Mota-Cadenas C, Muries B, Carvajal M. Plant hydraulic conductivity: The aquaporins contribution. In: Elango L, editor. Hydraulic conductivity—issues, determination and applications. Rijeka: In Tech; 2011. p. 103–21. ISBN 978-953-307-288-3. Lahiani MH, Dervishi E, Chen JH, Nima Z, Gaume A, Biris AS, et al. Impact of carbon nanotube exposure to seeds of valuable crops. ACS Appl Mater Interfaces. 2013;5:7965–73. Winicov I. New molecular approaches to improving salt tolerance in crop plants. Ann Bot. 1998;82:703–10. Munns R. Comparative physiology of salt and water stress. Plant Cell Environ. 2002;25:239–50. Munns R, Tester M. Mechanisms of salinity tolerance. Annu Rev Plant Biol. 2008;59:651–81. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ. Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol. 2000;51:463–99. Carvajal M, Martinez V, Alcaraz CF. Physiological function of water channels is affected by salinity in roots of paprika pepper. Physiol Plantarum. 1999;105:95–101. Carvajal M, Cerdá A, Martínez V. Does calcium ameliorate the negative effect of NaCl on melon root water transport by regulating water channel activity? New Phytol. 2000;145:439–47. López-Perez L, Martinez-Ballesta MC, Maurel C, Carvajal M. Changes in plasma membrane lipids, aquaporins and proton pump of broccoli roots, as an adaptation mechanism to salinity. Phytochemistry. 2009;70:492–500. Chrispeels MJ, Crawford NM, Schroeder JI. Proteins for transport of water and mineral nutrients across the membranes of plant cells. Plant Cell. 1999;11:661–75. Witzel K, Matros A, Strickert M, Kaspar S, Peukert M, Mühling KH, et al. Salinity stress in roots of contrasting barley genotypes reveals time-distinct and genotype-specific patterns for defined proteins. Mol Plant. 2014;7:336–55. Elkahoui S, Smaoui A, Zarrouk M, Ghrir R, Limam F. Salt-induced lipid changes in Catharanthus roseus cultured cell suspension. Phytochemistry. 2004;65:1911–7. Bohn M, Lüthje S, Sperling P, Heinz E, Dörffling K. Plasma membrane lipid alterations induced by cold acclimation and abscisic acid treatment of winter wheat seedlings differing in frost resistance. J Plant Physiol. 2007;164:146–56. Chalbi N, Martinez-Ballesta MC, Youssef NB, Carvajal M. Intrinsic stability of Brassicaceae plasma membrane in relation to changes in proteins and lipids as a response to salinity. J Plant Physiol. 2015;175:148–56. Sreedharan S, Shekhawat UK, Ganapathi TR. Constitutive and stress-inducible overexpression of a native aquaporin gene (MusaPIP2;6) in transgenic banana plants signal its pivotal role in salt tolerance. Plant Mol Biol. 2015;88:41–52. Epstein E. Mineral nutrition of plants: principles and perspectives. New York: Wiley; 1972. Fitzpatrick KL, Reid RJ. The involvement of aquaglyceroporins in transport of boron in barley roots. Plant Cell Environ. 2009;32:1357–65. Tournaire-Roux C, Sutka M, Javot H, Gout E, Gerbeau P, Luu DT, et al. Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature. 2003;425:393–7. Bárzana G, Aroca R, Chaumont F, Martínez-Ballesta MC, Carvajal M, Ruiz-Lozano JM. The arbuscular mycorrhizal symbiosis increases apoplastic water flow in roots of the host plant under both well-watered and drought stress conditions. Ann Bot. 2012;109:1009–17. Muries B, Faize M, Carvajal M, Martínez-Ballesta MC. Identification and differential induction of the expression of aquaporins by salinity in broccoli plants. Mol BioSyst. 2011;7:1322–35. Santoni V, Vinh J, Pflieger D, Sommerer N, Maurel C. A proteomic study reveals novel insights into the diversity of aquaporin forms expressed in the plasma membrane of plant roots. Biochem J. 2003;373:289–96. Towbin H, Staehelin T, Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA. 1979;76:4350–4. Turner NC. Measurement of plant water status by the pressure chamber technique. Irrig Sci USA. 1988;9:289–308. Mas A, Navarro-Pedreño J, Cooke DT, James CS. Characterization and lipid composition of the plasma membrane in grape leaves. Phytochemistry. 1994;35:1249–53. López-Berenguer C, García-Viguera C, Carvajal M. Are root hydraulic conductivity responses to salinity controlled by aquaporins in broccoli plants? Plant Soil. 2006;279:13–23. Villagarcia H, Dervshi E, De Silva K, Biris A, Khodakovskaya M. Surface chemistry of carbon nanotubes impacts the growth and expression of water channel protein in tomato plants. Small. 2012;8:2328–34. Yan S, Zhao L, Li H, Zhang Q, Tan J, Huang M, et al. Single-walled carbon nanotubes selectively influence maize root tissue development accompanied by the change in the related gene expression. J Hazard Mat. 2013;246–247:110–8. Tripathi S, Sonkar SK, Sarkar S. Growth stimulation of gram (Cicer arietinum) plant by water soluble carbon nanotubes. Nanoscale. 2011;3:1176. Begum P, Fugetsu B. Phytotoxicity of multi-walled carbon nanotubes on red spinach (Amaranthus tricolor L.) and the role ascorbic acid as an antioxidant. J Hazard Mater. 2012;243:212–22. Sidiqui MH, Al-Whaibi MH, Firoz M, Al-Khaishany MY. Role of nanoparticles in plants. In: Sidiqui MH, Al-Whaibi MH, Firoz M, editors. Nanotechnology and plant sciences. Springer; 2015. p. 19–35. doi:10.1007/978-3-319-14502-0_2. Zaghdoud C, Mota-Cadenas C, Carvajal M, Muries B, Ferchichi A, Martínez-Ballesta MC. Elevated CO2 alleviates negative effects of salinity on broccoli (Brassica oleracea L. var Italica) plants by modulating water balance through aquaporins abundance. Environ Exp Bot. 2013;95:12–24. Martinez-Ballesta MC, Diaz R, Martinez V, Carvajal M. Different blocking effect of HgCl2 and NaCl on aquaporins of pepper plants. J Plant Physiol. 2003;160:1487–92. Carvajal M, Cooke DT, Clarkson DT. High temperature effects on hydraulic conductance and plasma membrane fluidity of nutrient deprived wheat roots. Plant Cell Environ. 1996;19:1110–4. Niemietz CM, Tyerman SD. New potent inhibitors of aquaporins: silver and gold compounds inhibit aquaporins of plant and human origin. FEBS Lett. 2002;531:443–7. Al-Qurainy F. Effects of sodium azide on growth and yield traits of Eruca sativa (L.). World Appl Sci J. 2009;7:220–6. Smirnova E, Gustev A, Zayteseva O, Sheina O, Tkachev A, Kuznesova E, et al. Uptake and accumulation of multiwalled carbon nanotubes change the morphometric and biochemical characteristics of Onobrychis arenaria seedlings. Front Chem Sci Eng. 2012;6:132–8. Liu Q, Chen B, Wang Q, Shi X, Xiao Z, Lin J, Fang X. Carbon nanotubes as molecular transporters for walled plant cells. Nano Lett. 2009;9:1007–10. Serag MF, Kaji N, Habuchi S, Bianco A, Baba Y. Nanobiotechnology meets plant cell biology: carbon nanotubes as organelle targeting nanocarriers. RSC Adv. 2013;3:4856–62. Chen G, Qiu J, Liu Y, Jiang R, Cai S, Liu Y, et al. Carbon nanotubes act as contaminant carriers and translocate within plants. Sci Rep. 2015;5:15682. Serag MF, Braeckmans K, Habuchi S, Kaji N, Bianco A, Baba Y. Spatio temporal visualization of subcellular dynamics of carbon nanotubes. Nano Lett. 2012;12:6145–51. Serag MF, Kaji N, Gaillard C, Okamoto Y, Terasaka K, Jabasini M, et al. Trafficking and subcellular localization of multiwalled carbon nanotubes in plant cells. ACS Nano. 2011;5:493–9. Giraldo JP, Landry MP, Faltermeier SM, McNicholas TP, Iverson NM, Boghossian AA, et al. Plant nanobionics approach to augment photosynthesis and biochemical sensing. Nat Mater. 2014;13:400–8. Silva C, Aranda FJ, Ortiz A, Carvajal M, Martínez V, Teruel JA. Root plasma membrane lipid changes in relation to water transport in pepper: a response to NaCl and CaCl2 treatment. Plant Biol. 2007;50:650–7. Basyuni M, Baba S, Kinjo Y, Oku H. Salinity increases the triterpenoid content of a salt secretor and a non salt secretor mangrove. Aquat Bot. 2012;97:17–23. Ryaz AB, Panstruga R. Lipid rafts in plants. Planta. 2005;223:5–19. Guimaraes FVA, Lacerda CF, Marques EC, Miranda MRA, Abreu CEB, Prisco JT, et al. Calcium can moderate changes on membrane structure and lipid composition in cowpea plants under salt stress. Plant Growth Reg. 2011;65:55–63. Levental I, Grzybek M, Simons K. Raft domains of variable properties and compositions in plasma membrane vesicles. Proc Natl Acad Sci USA. 2011;108:11411–6. Chevalier AS, Chaumont F. Trafficking of plant plasma membrane aquaporins: multiple regulation levels and complex sorting signals. Plant Cell Physiol. 2014;56:819–29.