Abstract
Silicon (Si) can stimulate plant growth and stress resistance. This study aimed at elucidating the physiological responses and molecular characterization of different NIP (nodulin 26-like intrinsic protein) genes in sugar beet. The addition of exogenous Si increased plant biomass and Si concentration in the root and shoot, implying that increased Si uptake has beneficial effects on sugar beet. The quantitative gene expression analysis showed a significant upregulation of the BvNIP5–1 gene in roots, while the BvNIP1–1, BvNIP6–1, BvNIP7–1, and BvNIP-type were unchanged following Si supplementation. It suggests that BvNIP5–1 is one of the genes localized in the plasma membrane responsible for Si uptake in sugar beet. Besides, the BvNIP5–1 gene contained promoter, transcription start site, transcription binding site, and PolyA at 800 bp, 528 bp, 557 bp, and 1637 bp, respectively. The MEME results further revealed the association of three motifs related to major intrinsic protein (MIP). In the phylogenetic tree, the BvNIP5–1 showed a close association with CqNIP5–1, AnNIP2–1 and SoNIP5–1. Interactome analysis showed functional partnership of aquaporin SIP1–2 and SIP2–1 genes with NIP genes in sugar beet. In addition, BvNIP5–1 possessed close association with several functional partners (BOR1, BOR1, NodGS, SIP1A, ACR3) and co-expressed genes (i.e., AtNIP5–1, AtBOR1, AtNodGS, AtSIP1A, AtACR3) of Arabidopsis thaliana mainly responsible for boron, arsenite, and aquaporin transport activity. NIP promoters revealed cis-regulatory elements linked to auxin, salicylic acid, and methyl jasmonate-responsive factors. These findings may advance our understanding of Si transporters underlying growth and stress tolerance in sugar beet.
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References
Islam W, Tayyab M, Khalil F, Hua Z, Huang Z, Chen H (2020) Silicon-mediated plant defense against pathogens and insect pests. Pestic Biochem Physiol 168:104641
Gaur S, Kumar J, Kumar D, Chauhan DK, Prasad SM, Srivastava PK (2020) Fascinating impact of silicon and silicon transporters in plants: a review. Ecotoxicol Environ Saf 202:110885
Ma JF, Goto S, Tamai K, Ichii M (2001) Role of root hairs and lateral roots in silicon uptake by rice. Plant Physiol 127(4):1773–1780
Ouellette S, Goyette MH, Labbé C, Laur J, Gaudreau L, Gosselin A, Dorais M, Deshmukh RK, Bélanger RR (2017) Silicon transporters and effects of silicon amendments in strawberry under high tunnel and field conditions. Front Plant Sci 8:949
Guntzer F, Keller C, Meunier JD (2012) Benefits of plant silicon for crops: a review. Agron Sustain Dev 32(1):201–213
Montpetit J, Vivancos J, Mitani-Ueno N, Yamaji N, Remus-Borel W, Belzile F, Ma FJ, Belanger RR (2012) Cloning, functional characterization and heterologous expression of TaLsi1, a wheat silicon transporter gene. Plant Mol Biol 79(1–2):35–46
Guerriero G, Hausman JF, Legay S (2016) Silicon and the plant extracellular matrix. Front Plant Sci 7:463
Kamran M, Parveen A, Ahmar S, Malik Z, Hussain S, Chattha MS, Saleem MH, Adil M, Heidari P, Chen JT (2019) An overview of hazardous impacts of soil salinity in crops, tolerance mechanisms, and amelioration through selenium supplementation. Int J Mol Sci 21(1):148
Rahman M, Ghosal A, Alam MF, Kabir AH (2016) Remediation of cadmium toxicity in field peas (Pisum sativum L.) through exogenous silicon. Ecotoxicol Environ Saf 135:165–172
Epstein E, Bloom AJ (2005) Mineral nutrition of plants: principles and perspectives. Sinauer Associates, Sunderland, MA
Zargar, S. M., Mahajan, R., Bhat, J. A., Nazir, M., Deshmukh, R., 2019. Role of silicon in plant stress tolerance: opportunities to achieve a sustainable cropping system. 3 biotech 9(3), 73
Cooke J, Leishman MR (2011) Is plant ecology more siliceous than we realise? Trends Plant Sci 16(2):61–68
Liang Y, Sun W, Zhu YG, Christie P (2007) Mechanisms of silicon-mediated alleviation of abiotic stresses in higher plants: a review. Environmental pollution (Barking, Essex: 1987) 147(2):422–428
Van Bockhaven J, De Vleesschauwer D, Höfte M (2013) Towards establishing broad-spectrum disease resistance in plants: silicon leads the way. J Exp Bot 64(5):1281–1293
Ghareeb H, Bozso Z, Ott PG, Repenning C, Stahl F, Wydra K (2011) Transcriptome of silicon-induced resistance against Ralstonia solanacearum in the silicon non-accumulator tomato implicates priming effect. Physiol Mol Plant Pathol 75:83–89
Nwugo CC, Huerta AJ (2011) The effect of silicon on the leaf proteome of rice (Oryza sativa L.) plants under cadmium-stress. J Proteome Res 10:518–528
Zargar SM, Nazir M, Agrawal GK, Kim DW, Rakwal R (2010) Silicon in plant tolerance against environmental stressors: towards crop improvement using omics approaches. Current Proteomics 7:135–143
Hwang SJ, Hamayun M, Kim HY, Na CI, Kim KU, Shin DH, Kim SY, Lee I-J (2007) Effect of nitrogen and silicon nutrition on bioactive gibberellin and growth of rice under field conditions. J Crop Sci Biotechnol 10:281–286
Lee SK, Sohn EY, Hamayun M, Yoon JY, Lee IJ (2010) Effect of silicon on growth and salinity stress of soybean plant grown under hydroponic system. Agrofor Syst 80:333–340
Fleck AT, Nye T, Repenning C, Stahl F, Zahn M, Schenk MK (2011) Silicon enhances suberization and lignification in roots of rice (Oryza sativa). J Exp Bot 62:2001–2011
Brunings AM, Datnoff LE, Ma JF, Mitani N, Nagamura Y, Rathinasabapathi B, Kirst M (2009) Differential gene expression of rice in response to silicon and rice blast fungus Magnaporthe oryzae. Ann Appl Biol 155:161–170
Bhat, J. A., Shivaraj, S. M., Singh, P., Navadagi, D. B., Tripathi, D. K., Dash, P. K., Solanke, A. U., Sonah, H., & Deshmukh, R., 2019. Role of silicon in mitigation of heavy metal stresses in crop plants. Plants 8(3), 71
Kim, Y,H., Khan, A.L., Waqas, M., Lee, I.J. 2017. Silicon regulates antioxidant activities of crop plants under abiotic-induced oxidative stress: a review Frontiers in Plant Science 8
Martínez-Ballesta MC, Carvajal M (2016) Mutual interactions between aquaporins and membrane components. Front Plant Sci 7:1322
Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M, Ishiguro M, Murata Y, Yano M (2006) A silicon transporter in rice. Nature 440(7084):688–691
Maurel C, Boursiac Y, Luu DT, Santoni VR, Shahzad Z, Verdoucq L (2015) Aquaporins in plants. Physiol Rev 95:1321–1358
Gomes D, Agasse A, Thiebaud P, Delrot S, Geros H, Chaumont F (2009) Aquaporins are multifunctional water and solute transporters highly divergent in living organisms. Biochim Biophys Acta Biomembr 1788:1213–1228
Zangi R, Filella M (2012) Transport routes of metalloids into and out of the cell: a review of the current knowledge. Chemico Biol Interact 197:47–57
Zhao XQ, Mitani N, Yamaji N, Shen RF, Ma JF (2010) Involvement of silicon influx transporter OsNIP2;1 in selenite uptake in rice. Plant Physiol 153:1871–1877
Alexandersson E, Fraysse L, Sjövall-Larsen S, Gustavsson S, Fellert M, Karlsson M, Johanson U, Kjellbom P (2005) Whole gene family expression and drought stress regulation of aquaporins. Plant Mol Biol 59:469–484
Boursiac Y (2005) Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiol 139:790–805
Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Circular California Agricultural Experiment Station 347
Sigrist CJ, Cerutti L, de Castro E, Langendijk-Genevaux PS, Bulliard V, Bairoch A, Hulo N (2010) ROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Res 38:D161–D166
Szklarczyk D, Gable AL, Lyon D, Junge A, Wyder S, Huerta-Cepas J, Simonovic M, Doncheva NT, Morris JH, Bork P, Jensen LJ, von Mering C (2019) STRING v11: protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Res 47:D607–D613
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Peer YV, Rouze P, Rombauts S (2002) Plant CARE, a data base of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327
Khan A, Kamran M, Imran M, Al-Harrasi A, Al-Rawahi A, Al-Amri I, Lee IJ, Khan AL (2019) Silicon and salicylic acid confer high-pH stress tolerance in tomato seedlings. Sci Rep 9(1):19788
Farooq MA, Ali S, Hameed A, Ishaque W, Mahmood K, Iqbal Z (2013) Alleviation of cadmium toxicity by silicon is related to elevated photosynthesis, antioxidant enzymes; suppressed cadmium uptake and oxidative stress in cotton. Ecotoxicol Environ Saf 96:242–249
Oliveira KR, Souza Junior JP, Bennett SJ, Checchio MV, Alves RC, Felisberto G, Prado RM, Gratão PL (2020) Exogenous silicon and salicylic acid applications improve tolerance to boron toxicity in field pea cultivars by intensifying antioxidant defence systems. Ecotoxicol Environ Saf 201:110778
Kong W, Yang S, Wang Y, Bendahmane M, Fu X (2017) Genome-wide identification and characterization of aquaporin gene family in Beta vulgaris. PeerJ 5:e3747
Pommerrenig B, Diehn TA, Bienert GP (2015) Metalloido-porins: essentiality of Nodulin 26-like intrinsic proteins in metalloid transport. Plant Sci 238:212–227
Deshmukh RK, Vivancos J, Guérin V, Sonah H, Labbé C, Belzile F, Bélanger RR (2013) Identification and functional characterization of silicon transporters in soybean using comparative genomics of major intrinsic proteins in Arabidopsis and rice. Plant Mol Biol 83:303–315
Wang Y, Li R, Li D, Jia X, Zhou D, Li J, Lyi SM, Hou S, Huang Y, Kochian LV, Liu J (2017) NIP1;2 is a plasma membrane-localized transporter mediating aluminum uptake, translocation, and tolerance in Arabidopsis. Proc Natl Acad Sci U S A 114(19):5047–5052
Wong A, Gehring C, Irving HR (2015) Conserved functional motifs and homology modeling to predict hidden moonlighting functional sites. Frontiers Bioeng Biotech 3:82
Tyerman SD, Niemietz CM (2002) Plant aquaporins: multifunctional water and solute channels with expanding roles. Plant Cell Environ 25:173–194
Johanson, U., Danielson, J., 2010. Phylogeny of major intrinsic proteins, plant aquaporins: roles in water homeostasis, nutrition, and signaling processes. Bienert GP, Jahn TP. (Eds), MIPs and their role in the exchange of metalloids (1st edition), Landes bioscience springer, New York, pp. 19-31
Abascal F, Irisarri I, Zardoya R (2014) Diversity and evolution of membrane intrinsic proteins. Biochim Biophys Acta 1840(5):1468–1481
Sato R, Maeshima M (2019) The ER-localized aquaporin SIP2;1 is involved in pollen germination and pollen tube elongation in Arabidopsis thaliana. Plant Mol Biol 100(3):335–349
Mousavi SR, Niknejad Y, Fallah H, Tari DB (2020) Methyl jasmonate alleviates arsenic toxicity in rice. Plant Cell Rep 39(8):1041–1060
Nair, A., Thulasiram, H. V., Bhargava, S., 2020. Role of jasmonate in modulation of mycorrhizae-induced resistance against fungal pathogens. Methods in molecular biology (Clifton, N.J.), 2085, 109–115
Kurowska MM, Daszkowska-Golec A, Gajecka M, Kościelniak P, Bierza W, Szarejko I (2020) Methyl Jasmonate affects photosynthesis efficiency, expression of HvTIP genes and nitrogen homeostasis in barley. Int J Mol Sci 21(12):4335
Tripathi, D. K., Rai, P., Guerriero, G., Sharma, S., Corpas, F. J., & Singh, V. P. (2020). Silicon induces adventitious root formation in rice (Oryza sativa L.) under arsenate stress with the involvement of nitric oxide and indole-3-acetic acid. Journal of experimental botany, eraa488
Rai KK, Pandey N, Rai SP (2020) Salicylic acid and nitric oxide signaling in plant heat stress. Physiol Plant 168(2):241–255
Huda, A.K.M.N., Swaraz, A.M., Reza, M.A., Haque, M.A., Kabir, A.H., 2016. Remediation of chromium toxicity through exogenous salicylic acid in Rice (Oryza sativa L.). water air soil Pollut 227, 278
Shen C, Yue R, Sun T, Zhang L, Yang Y, Wang H (2015) OsARF16, a transcription factor regulating auxin redistribution, is required for iron deficiency response in rice (Oryza sativa L.). Plant Sci 231:148–158
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We are grateful to the University of Rajshahi, Bangladesh.
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MAR performed ICP-MS and qPCR analysis. AFMMH and MI performed bioinformatics analysis. MSA performed plant phenotype experiments. KL edited the manuscript. AHK prepared the draft manuscript and supervised the whole work.
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Rahman, M.A., Haque, A.M., Akther, M.S. et al. The NIP Genes in Sugar Beet: Underlying Roles in Silicon Uptake and Growth Improvement. Silicon 14, 3551–3562 (2022). https://doi.org/10.1007/s12633-021-01133-0
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DOI: https://doi.org/10.1007/s12633-021-01133-0