Login Register Cart 0
Generic placeholder image

Current Nanoscience

Editor-in-Chief

ISSN (Print): 1573-4137
ISSN (Online): 1875-6786

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Carbon Nanoparticles Promoted the Absorption of Potassium Ions by Tobacco Roots via Regulation of K+ Flux and Ion Channel Gene Expression

Author(s): Zhenjie Zhao, Huaxin Dai, Guiyao Wang, Yuhan Peng, Fu Liao, Jizhong Wu and Taibo Liang*

Volume 20, Issue 3, 2024

Published on: 26 May, 2023

Page: [390 - 398] Pages: 9

DOI: 10.2174/1573413719666230418110534

Price: $65

Abstract

Background: The regulatory effects of carbon nanomaterials (CNMs) on plant growth and their potential applications in agriculture have attracted a great deal of attention from researchers. CNMs have been shown to promote nutrient absorption and increase plant growth. However, the mechanisms by which CNMs affect plant growth and nutrient absorption are still unknown.

Methods: The tobacco seedling biomass, potassium (K+) concentration, and accumulation in hydroponic were investigated to exposure of carbon nanoparticles (CNPs). To directly observe the effect of CNPs on K+ uptake by roots, we employed a noninvasive micro-test technique (NMT) to detect the net flux of K+ on the surface of tobacco roots. The K+-depletion experiment was carried out to explore the kinetic characteristics of K+ absorption, and qRT-PCR was used to monitor the expression levels of the K+ channel gene.

Results: The results showed that tobacco seedling biomass significantly improved at 10 mg·L-1 CNP treatments, and K+ concentration and accumulation both in roots and shoots increased with 10 and 20 mg·L-1 CNPs. CNP treatments changed the flow rate of K+ from efflux to influx in tobacco roots; this was observed both in plants cultivated in a CNP-containing medium and after the addition of CNPs to previously untreated plants. A depletion test also showed that CNPs improved the K+ absorption capacity and low-K+ tolerance of tobacco seedlings.

Conclusion: CNPs enhanced the K+ absorption capacity and low-K+ tolerance of tobacco seedlings. The promotion of K+ absorption by CNPs was closely related to the activation of K+ influx channel genes and inhibition of the K+ outflow channel gene. The K+ flux response and ion channel gene expression to CNPs in plants reveal the mechanism whereby CNPs promote plant nutrient absorption.

« Previous Next »
Graphical Abstract

[1]
Maathuis, F.J.M. Physiological functions of mineral macronutrients. Curr. Opin. Plant Biol., 2009, 12(3), 250-258.
[http://dx.doi.org/10.1016/j.pbi.2009.04.003] [PMID: 19473870]
[2]
Wang, Y.; Wu, W.H. Potassium transport and signaling in higher plants. Annu. Rev. Plant Biol., 2013, 64(1), 451-476.
[http://dx.doi.org/10.1146/annurev-arplant-050312-120153] [PMID: 23330792]
[3]
Ashley, M.K.; Grant, M.; Grabov, A. Plant responses to potassium deficiencies: A role for potassium transport proteins. J. Exp. Bot., 2006, 57(2), 425-436.
[http://dx.doi.org/10.1093/jxb/erj034] [PMID: 16364949]
[4]
Amtmann, A.; Hammond, J.P.; Armengaud, P.; White, P.J. Nutrient sensing and signaling in plants: Potassium and phosphorus. Adv. Bot. Res., 2005, 43, 209-257.
[http://dx.doi.org/10.1016/S0065-2296(05)43005-0]
[5]
Epstein, E.; Rains, D.W.; Elzam, O.E. Resolution of dual mechanisms of potassium absorption by barley roots. Proc. Natl. Acad. Sci. USA, 1963, 49(5), 684-692.
[http://dx.doi.org/10.1073/pnas.49.5.684] [PMID: 16591089]
[6]
Ragel, P.; Raddatz, N.; Leidi, E.O.; Quintero, F.J.; Pardo, J.M. Regulation of K+ nutrition in plants. Front. Plant Sci., 2019, 10, 281.
[http://dx.doi.org/10.3389/fpls.2019.00281] [PMID: 30949187]
[7]
Maathuis, F.J.M.; Sanders, D. Mechanisms of potassium absorption by higher plant roots. Physiol. Plant., 1996, 96(1), 158-168.
[http://dx.doi.org/10.1111/j.1399-3054.1996.tb00197.x]
[8]
Hosseinzadeh, K.; Mardani, M.R.; Paikar, M.; Hasibi, A.; Tavangar, T.; Nimafar, M.; Ganji, D.D.; Shafii, M.B. Investigation of second grade viscoelastic non-Newtonian nanofluid flow on the curve stretching surface in presence of MHD. Results Engineer., 2023, 17, 100838.
[http://dx.doi.org/10.1016/j.rineng.2022.100838]
[9]
El-Saadony, M.T.; Saad, A.M.; Soliman, S.M.; Salem, H.M.; Desoky, E.S.M.; Babalghith, A.O.; El-Tahan, A.M.; Ibrahim, O.M.; Ebrahim, A.A.M.; Abd El-Mageed, T.A.; Elrys, A.S.; Elbadawi, A.A.; El-Tarabily, K.A.; AbuQamar, S.F. Role of nanoparticles in enhancing crop tolerance to abiotic stress: A comprehensive review. Front. Plant Sci., 2022, 13, 946717.
[http://dx.doi.org/10.3389/fpls.2022.946717] [PMID: 36407622]
[10]
Zhao, L.; Lu, L.; Wang, A.; Zhang, H.; Huang, M.; Wu, H.; Xing, B.; Wang, Z.; Ji, R. Nanobiotechnology in agriculture: Use of nanomaterials to promote plant growth and stress tolerance. J. Agric. Food Chem., 2020, 68(7), 1935-1947.
[http://dx.doi.org/10.1021/acs.jafc.9b06615] [PMID: 32003987]
[11]
Patel, D.K.; Kim, H.B.; Dutta, S.D.; Ganguly, K.; Lim, K.T. Carbon nanotubes-based nanomaterials and their agricultural and biotechnological applications. Materials, 2020, 13(7), 1679.
[http://dx.doi.org/10.3390/ma13071679] [PMID: 32260227]
[12]
Srivastava, A.; Singh, R. Nanoparticles for sustainable agriculture and their effect on plants. Curr. Nanosci., 2021, 17(1), 58-69.
[http://dx.doi.org/10.2174/1573413716999200403152439]
[13]
Usman, M.; Farooq, M.; Wakeel, A.; Nawaz, A.; Cheema, S.A.; Rehman, H.; Ashraf, I.; Sanaullah, M. Nanotechnology in agriculture: Current status, challenges and future opportunities. Sci. Total Environ., 2020, 721, 137778.
[http://dx.doi.org/10.1016/j.scitotenv.2020.137778] [PMID: 32179352]
[14]
Lahiani, M.H.; Dervishi, E.; Chen, J.; 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(16), 7965-7973.
[http://dx.doi.org/10.1021/am402052x] [PMID: 23834323]
[15]
Verma, S.K.; Das, A.K.; Gantait, S.; Kumar, V.; Gurel, E. Applications of carbon nanomaterials in the plant system: A perspective view on the pros and cons. Sci. Total Environ., 2019, 667, 485-499.
[http://dx.doi.org/10.1016/j.scitotenv.2019.02.409] [PMID: 30833247]
[16]
Saxena, M.; Maity, S.; Sarkar, S. Carbon nanoparticles in ‘biochar’ boost wheat (Triticum aestivum) plant growth. RSC Advances, 2014, 4(75), 39948-39954.
[http://dx.doi.org/10.1039/C4RA06535B]
[17]
Li, S.M.; Ma, C.; Li, L.H.; Zhang, A.Y.; Han, X.; Wang, F.; Wang, D.; Zheng, C.; Mao, R. Effect of nano-carbon on nitrogen absorption, root activity and soil enzyme of maize. J. Northeast Agric. Univ., 2014, 45, 14-18.
[18]
Shekhawat, G.S.; Mahawar, L.; Rajput, P.; Rajput, V.D.; Minkina, T.; Singh, R.K. Role of engineered carbon nanoparticles (CNPs) in promoting growth and metabolism of Vigna radiata (L.) Wilczek: Insights into the biochemical and physiological responses. Plants, 2021, 10(7), 1317.
[http://dx.doi.org/10.3390/plants10071317] [PMID: 34203538]
[19]
Wang, G.; Xiao, Y.; Peng, F.; Zhang, Y.; Gao, H.; Sun, X.; Yue, H.E. Effects of nano-carbon on nitrogen absorption, utilization and plant growth of strawberry. J. Soil Water Conserv., 2018, 32(5), 335-340, 351.
[20]
Hu, Y.; Zhang, P.; Zhang, X.; Liu, Y.; Feng, S.; Guo, D.; Nadezhda, T.; Song, Z.; Dang, X. Multi-Wall carbon nanotubes promote the growth of Maize (Zea mays) by regulating carbon and nitrogen metabolism in leaves. J. Agric. Food Chem., 2021, 69(17), 4981-4991.
[http://dx.doi.org/10.1021/acs.jafc.1c00733] [PMID: 33900073]
[21]
Tiwari, D.K.; Dasgupta-Schubert, N.; Villaseñor Cendejas, L.M.; Villegas, J.; Montoya, C.L.; García, B.S.E. 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(5), 577-591.
[http://dx.doi.org/10.1007/s13204-013-0236-7]
[22]
Khodakovskaya, M.V.; de Silva, K.; Nedosekin, D.A.; Dervishi, E.; Biris, A.S.; Shashkov, E.V.; Galanzha, E.I.; Zharov, V.P. Complex genetic, photothermal, and photoacoustic analysis of nanoparticle-plant interactions. Proc. Natl. Acad. Sci. USA, 2011, 108(3), 1028-1033.
[http://dx.doi.org/10.1073/pnas.1008856108] [PMID: 21189303]
[23]
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(10), 4519-4528.
[http://dx.doi.org/10.1007/s11051-011-0406-z]
[24]
Joshi, A.; Kaur, S.; Dharamvir, K.; Nayyar, H.; Verma, G. Multi-walled carbon nanotubes applied through seed-priming influence early germination, root hair, growth and yield of bread wheat (Triticum aestivum L.). J. Sci. Food Agric., 2018, 98(8), 3148-3160.
[http://dx.doi.org/10.1002/jsfa.8818] [PMID: 29220088]
[25]
Chen, L.; Yang, J.; Li, X.; Liang, T.; Nie, C.; Xie, F.; Liu, K.; Peng, X.; Xie, J. Carbon nanoparticles enhance potassium uptake via upregulating potassium channel expression and imitating biological ion channels in BY-2 cells. J. Nanobiotechnology, 2020, 18(1), 21.
[http://dx.doi.org/10.1186/s12951-020-0581-0] [PMID: 31992314]
[26]
Wu, H.; Shabala, L.; Shabala, S.; Giraldo, J.P. Hydroxyl radical scavenging by cerium oxide nanoparticles improves Arabidopsis salinity tolerance by enhancing leaf mesophyll potassium retention. Environ. Sci. Nano, 2018, 5(7), 1567-1583.
[http://dx.doi.org/10.1039/C8EN00323H]
[27]
Luo, J.; Qin, J.; He, F.; Li, H.; Liu, T.; Polle, A.; Peng, C.; Luo, Z.B. Net fluxes of ammonium and nitrate in association with H+ fluxes in fine roots of Populus popularis. Planta, 2013, 237(4), 919-931.
[http://dx.doi.org/10.1007/s00425-012-1807-7] [PMID: 23179443]
[28]
Jeworutzki, E.; Roelfsema, M.R.G.; Anschütz, U.; Krol, E.; Elzenga, J.T.M.; Felix, G.; Boller, T.; Hedrich, R.; Becker, D. Early signaling through the Arabidopsis pattern recognition receptors FLS2 and EFR involves Ca2+-associated opening of plasma membrane anion channels. Plant J., 2010, 62(3), 367-378.
[http://dx.doi.org/10.1111/j.1365-313X.2010.04155.x] [PMID: 20113440]
[29]
Niu, M.; Bao, C.; Zhan, J.; Yue, X.; Zou, J.; Su, N.; Cui, J. Plasma membrane-localized protein BcHIPP16 promotes the uptake of copper and cadmium in planta. Ecotoxicol. Environ. Saf., 2021, 227, 112920.
[http://dx.doi.org/10.1016/j.ecoenv.2021.112920] [PMID: 34678630]
[30]
Chen, L.; Wang, H.; Li, X.; Nie, C.; Liang, T.; Xie, F.; Liu, K.; Peng, X.; Xie, J. Highly hydrophilic carbon nanoparticles: Uptake mechanism by mammalian and plant cells. RSC Advances, 2018, 8(61), 35246-35256.
[http://dx.doi.org/10.1039/C8RA06665E] [PMID: 35547047]
[31]
Hoagland, D.R.; Arnon, D.I. The water-culture method for growing plants without soil. California Agricultural Experiment Station Circular, 1950, 347, 1-32.
[32]
Xu, X.; Du, X.; Wang, F.; Sha, J.; Chen, Q.; Tian, G.; Zhu, Z.; Ge, S.; Jiang, Y. Effects of potassium levels on plant growth, accumulation and distribution of carbon, and nitrate metabolism in apple dwarf rootstock seedlings. Front. Plant Sci., 2020, 11, 904.
[http://dx.doi.org/10.3389/fpls.2020.00904] [PMID: 32655607]
[33]
Xu, R.R.; Qi, S.D.; Lu, L.T.; Chen, C.T.; Wu, C.A.; Zheng, C.C.A. DExD/H box RNA helicase is important for K+ deprivation responses and tolerance in Arabidopsis thaliana. FEBS J., 2011, 278(13), 2296-2306.
[http://dx.doi.org/10.1111/j.1742-4658.2011.08147.x] [PMID: 21535471]
[34]
Ma, W.; Yang, G.; Xiao, Y.; Zhao, X.; Wang, J. ABA-dependent K+ flux is one of the important features of the drought response that distinguishes Catalpa from two different habitats. Plant Signal. Behav., 2020, 15(4), 1735755.
[http://dx.doi.org/10.1080/15592324.2020.1735755] [PMID: 32141360]
[35]
Xu, J.; Li, H.D.; Chen, L.Q.; Wang, Y.; Liu, L.L.; He, L.; Wu, W.H. A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell, 2006, 125(7), 1347-1360.
[http://dx.doi.org/10.1016/j.cell.2006.06.011] [PMID: 16814720]
[36]
Drew, M.C.; Saker, L.R.; Barber, S.A.; Jenkins, W. Changes in the kinetics of phosphate and potassium absorption in nutrient-deficient barley roots measured by a solution-depletion technique. Planta, 1984, 160(6), 490-499.
[http://dx.doi.org/10.1007/BF00411136] [PMID: 24258775]
[37]
Core, R.; Rdct, R.; Team, R.; Team, R. A language and environment for statistical computing. Computing, 2015, 1, 12-21.
[38]
Claassen, N.; Barber, S.A. A method for characterizing the relation between nutrient concentration and flux into roots of intact plants. Plant Physiol., 1974, 54(4), 564-568.
[http://dx.doi.org/10.1104/pp.54.4.564] [PMID: 16658929]
[39]
Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Δ Δ C(T). Method. Methods, 2001, 25(4), 402-408.
[http://dx.doi.org/10.1006/meth.2001.1262] [PMID: 11846609]
[40]
Zhang, K.; Chen, Y.P.; Zhang, T.T.; Zhao, Y.; Shen, Y.; Huang, L.; Gao, X.; Guo, J.S. The logistic growth of duckweed (Lemna minor) and kinetics of ammonium uptake. Environ. Technol., 2014, 35(5), 562-567.
[http://dx.doi.org/10.1080/09593330.2013.837937] [PMID: 24645435]
[41]
Nielsen, N.E.; Barber, S.A. Differences among genotypes of corn in the kinetics of P uptake. Agron. J., 1978, 70(5), 695-698.
[http://dx.doi.org/10.2134/agronj1978.00021962007000050001xa]
[42]
Khodakovskaya, M.V.; de Silva, K.; Biris, A.S.; Dervishi, E.; Villagarcia, H. Carbon nanotubes induce growth enhancement of tobacco cells. ACS Nano, 2012, 6(3), 2128-2135.
[http://dx.doi.org/10.1021/nn204643g] [PMID: 22360840]
[43]
Yuan, Z.; Zhang, Z.; Wang, X.; Li, L.; Cai, K.; Han, H. Novel impacts of functionalized multi-walled carbon nanotubes in plants: promotion of nodulation and nitrogenase activity in the rhizobium-legume system. Nanoscale, 2017, 9(28), 9921-9937.
[http://dx.doi.org/10.1039/C7NR01948C] [PMID: 28678233]
[44]
Sano, T.; Becker, D.; Ivashikina, N.; Wegner, L.H.; Zimmermann, U.; Roelfsema, M.R.G.; Nagata, T.; Hedrich, R. Plant cells must pass a K+ threshold to re-enter the cell cycle. Plant J., 2007, 50(3), 401-413.
[http://dx.doi.org/10.1111/j.1365-313X.2007.03071.x] [PMID: 17425714]
[45]
Dai, X.Y.; Su, Y.R.; Wei, W.X.; Wu, J.S.; Fan, Y.K. Effects of top excision on the potassium accumulation and expression of potassium channel genes in tobacco. J. Exp. Bot., 2009, 60(1), 279-289.
[http://dx.doi.org/10.1093/jxb/ern285] [PMID: 19112172]
[46]
Gaymard, F.; Pilot, G.; Lacombe, B.; Bouchez, D.; Bruneau, D.; Boucherez, J.; Michaux-Ferrière, N.; Thibaud, J.B.; Sentenac, H. Identification and disruption of a plant shaker-like outward channel involved in K+ release into the xylem sap. Cell, 1998, 94(5), 647-655.
[http://dx.doi.org/10.1016/S0092-8674(00)81606-2] [PMID: 9741629]
[47]
Zhang, Y.; Qin, L.J.; Zhao, D.; Zhao, D.G. Improvement of drought-stress in NtHAK1-overexpressing Nicotiana tabacum. Chih Wu Sheng Li Hsueh T’ung Hsun, 2017, 53, 1444-1452.
[48]
Mukherjee, A.; Majumdar, S.; Servin, A.D.; Pagano, L.; Dhankher, O.P.; White, J.C. Carbon nanomaterials in agriculture: A critical review. Front. Plant Sci., 2016, 7, 172.
[http://dx.doi.org/10.3389/fpls.2016.00172] [PMID: 26941751]
[49]
Tripathi, S.; Sonkar, S.K.; Sarkar, S. Growth stimulation of gram (Cicer arietinum) plant by water soluble carbon nanotubes. Nanoscale, 2011, 3(3), 1176-1181.
[http://dx.doi.org/10.1039/c0nr00722f] [PMID: 21253651]
[50]
Khodakovskaya, M.V.; Kim, B.S.; Kim, J.N.; Alimohammadi, M.; Dervishi, E.; Mustafa, T.; Cernigla, C.E. Carbon nanotubes as plant growth regulators: effects on tomato growth, reproductive system, and soil microbial community. Small, 2013, 9(1), 115-123.
[http://dx.doi.org/10.1002/smll.201201225] [PMID: 23019062]
[51]
Stampoulis, D.; Sinha, S.K.; White, J.C. Assay-dependent phytotoxicity of nanoparticles to plants. Environ. Sci. Technol., 2009, 43(24), 9473-9479.
[http://dx.doi.org/10.1021/es901695c] [PMID: 19924897]
[52]
Liu, C.; Guo, Z.; Yao, Y.X.; Du, Y.P. Functional identification of grape potassium ion transporter VviHKT1;7 under salt stress. Zhongguo Nong Ye Ke Xue, 2021, 54, 1952-1963.
[53]
Liu, Y.; Bai, L.; Sun, M.; Wang, J.; Li, S.; Miao, L.; Yan, Y.; He, C.; Yu, X.; Li, Y. Adaptation of cucumber seedlings to low temperature stress by reducing nitrate to ammonium during it’s transportation. BMC Plant Biol., 2021, 21(1), 189.
[http://dx.doi.org/10.1186/s12870-021-02918-6] [PMID: 33874888]
[54]
Zangooee, M.R.; Hosseinzadeh, K.; Ganji, D.D. Hydrothermal analysis of hybrid nanofluid flow on a vertical plate by considering slip condition. Theor. Appl. Mech. Lett., 2022, 12(5), 100357.
[http://dx.doi.org/10.1016/j.taml.2022.100357]
[55]
Najafabadi, F.M.; Rostami, T.H.; Hosseinzadeh, K.; Ganji, D. D. Hydrothermal study of nanofluid flow in channel by RBF method with exponential boundary conditions. Proc IMechE Part E: J Process Mechanical Engineering, 2022. 09544089221133909. [Epub a head of print].
[http://dx.doi.org/10.1177/09544089221133909]
[56]
Zhao, Z.; Hu, L.; Chen, Q.; Dai, H.; Meng, X.; Yin, Q.; Liang, T. iTRAQ-Based comparative proteomic analysis provides insights into tobacco callus response to carbon nanoparticles. Plant Mol. Biol. Report., 2022, 40, 556-565.
[57]
Véry, A.A.; Sentenac, H. Molecular mechanisms and regulation of K+ transport in higher plants. Annu. Rev. Plant Biol., 2003, 54(1), 575-603.
[http://dx.doi.org/10.1146/annurev.arplant.54.031902.134831] [PMID: 14503004]
[58]
Sinnige, M.P.; ten Hoopen, P.; van den Wijngaard, P.W.J.; Roobeek, I.; Schoonheim, P.J.; Mol, J.N.M.; de Boer, A.H. The barley two-pore K+-channel HvKCO1 interacts with 14-3-3 proteins in an isoform specific manner. Plant Sci., 2005, 169(3), 612-619.
[http://dx.doi.org/10.1016/j.plantsci.2005.05.013]
[59]
He, C.; Cui, K.; Duan, A.; Zeng, Y.; Zhang, J. Genome-wide and molecular evolution analysis of the Poplar KT/HAK/KUP potassium transporter gene family. Ecol. Evol., 2012, 2(8), 1996-2004.
[http://dx.doi.org/10.1002/ece3.299] [PMID: 22957200]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy