DOI QR코드

DOI QR Code

Molecular Characterization of Silicon (Si) Transporter Genes, Insights into Si-acquisition Status, Plant Growth, Development, and Yield in Alfalfa

  • Md Atikur Rahman (Grassland and Forage Division, National Institute of Animal Science, RDA) ;
  • Sang-Hoon Lee (Grassland and Forage Division, National Institute of Animal Science, RDA) ;
  • Yowook Song (Grassland and Forage Division, National Institute of Animal Science, RDA) ;
  • Hyung Soo Park (Grassland and Forage Division, National Institute of Animal Science, RDA) ;
  • Jae Hoon Woo (Grassland and Forage Division, National Institute of Animal Science, RDA) ;
  • Bo Ram Choi (Grassland and Forage Division, National Institute of Animal Science, RDA) ;
  • Ki-Won Lee (Grassland and Forage Division, National Institute of Animal Science, RDA)
  • Received : 2023.06.22
  • Accepted : 2023.06.28
  • Published : 2023.09.30

Abstract

Silicon (Si) has the potential to improve plant growth and stress tolerance. The study aimed to explore Si-involving plant responses and molecular characterization of different Si-responsive genes in alfalfa. In this study, the exogenous supplementation of Si enhanced plant growth, and biomass yield. Si-acquisition in alfalfa root and shoot was higher in Si-supplemented compared to silicon deficient (-Si) plants, implying Si-acquisition has beneficial on alfalfa plants. As a consequence, the quantum efficiency of photosystem II (Fv/Fm) was significantly increased in silicon-sufficient (+Si) plants. The quantitative gene expression analysis exhibited a significant upregulation of the Lsi1, Lsi2, Lsi3, NIP5;1, and NIP6;1 genes in alfalfa roots, while BOR1, BOR4, NIP2, and NIP3 showed no significant variation in their expression. The MEME results further noticed the association of four motifs related to the major intrinsic protein (MIP). The interaction analysis revealed that NIP5;1 and Lsi1 showed a shared gene network with NIP2, BOR1, and BOR4, and Lsi2, Lsi3 and NIP3-1, respectively. These results suggest that members of the major intrinsic proteins (MIPs) family especially Lsi1, Lsi2, Lsi3, NIP5;1, and NIP6;1 genes helped to pass water and other neutral solutes through the cell membrane and those played significant roles in Si uptake and transport in plants. Together, these insights might be useful for alfalfa breeding and genome editing approaches for alfalfa improvement.

Keywords

Acknowledgement

This study was supported by the RDA Fellowship Program of the National Institute of Animal Science, and Cooperative Research Program for Agriculture Science and Technology Development (Project No. PJ01592501), Rural Development Administration, Republic of Korea.

References

  1. Das, U., Rahman, M.A., Ela, E.J., Lee, K.W. and Kabir, A.H. 2021. Sulfur triggers glutathione and phytochelatin accumulation causing excess Cd bound to the cell wall of roots in alleviating Cd-toxicity in alfalfa. Chemosphere. 262:128361.
  2. Epstein, E. and Bloom, A. 2005. Mineral nutrition of plants: Principles and perspectives. Journal of Plant Physiology. 162:1380-1381. https://doi.org/10.1016/j.jplph.2005.06.002
  3. Gomes, D., Agasse, A., Thiebaud, P., Delrot, S., Geros, H. and Chaumont, F. 2009. Aquaporins are multifunctional water and solute transporters highly divergent in living organisms. Biochimica et Biophysica Acta (BBA)-Biomembranes. 1788:1213-1228. https://doi.org/10.1016/j.bbamem.2009.03.009
  4. Guerriero, G., Hausman, J.F. and Legay, S. 2016. Silicon and the plant extracellular matrix. Frontiers in Plant Science. 7:463.
  5. Hajiboland, R. 2022. Silicon-mediated cold stress tolerance in plants. In: H. Etesami, A.H. Al Saeedi, H. El-Ramady, M. Fujita, M. Pessarakli and M. Anwar Hossain (Eds.), Silicon and nano-silicon in environmental stress management and crop quality improvement. Academic Press. pp. 161-180.
  6. Haque, A.F.M.M., Rahman, M.A., Das, U., Rahman, M.M., Elseehy, M.M., El-Shehawi, A.M., Parvez, M.S. and Kabir, A.H. 2022. Changes in physiological responses and MTP (metal tolerance protein) transcripts in soybean (Glycine max) exposed to differential iron availability. Plant Physiology and Biochemistry. 179:1-9. https://doi.org/10.1016/j.plaphy.2022.03.007
  7. Haque, A.F.M.M., Tasnim, J., El-Shehawi, A.M., Rahman, M.A., Parvez, M.S., Ahmed, M.B. and Kabir, A.H. 2021. The Cd-induced morphological and photosynthetic disruption is related to the reduced Fe status and increased oxidative injuries in sugar beet. Plant Physiology and Biochemistry. 166:448-458. https://doi.org/10.1016/j.plaphy.2021.06.020
  8. Hoagland, D.R. and Arnon, D.I. 1950. The water-culture method for growing plants without soil. California Agricultural Experiment Station. 347:32.
  9. Huff, H.R. 2001. Silicon. In: K.H.J. Buschow, R.W. Cahn, M.C. Flemings, B. Ilschner, E.J. Kramer, S. Mahajan and P. Veyssiere (Eds.), Encyclopedia of materials: Science and technology. Elsevier. Oxford. pp. 8486-8497.
  10. Imtiaz, M., Rizwan, M.S., Mushtaq, M.A., Ashraf, M., Shahzad, S.M., Yousaf, B., Saeed, D.A., Rizwan, M., Nawaz, M.A., Mehmood, S. and Tu, S. 2016. Silicon occurrence, uptake, transport and mechanisms of heavy metals, minerals and salinity enhanced tolerance in plants with future prospects: A review. Journal of Environmental Management. 183:521-529. https://doi.org/10.1016/j.jenvman.2016.09.009
  11. Joudmand, A. and Hajiboland, R. 2019. Silicon mitigates cold stress in barley plants via modifying the activity of apoplasmic enzymes and concentration of metabolites. Acta Physiologiae Plantarum. 41:29.
  12. Kabir, A.H., Das, U., Rahman, M.A. and Lee, K.W. 2021. Silicon induces metallochaperone-driven cadmium binding to the cell wall and restores redox status through elevated glutathione in Cd-stressed sugar beet. Physiologia Plantarum. 173:352-368. https://doi.org/10.1111/ppl.13424
  13. Kabir, A.H., Ela, E.J., Bagchi, R., Rahman, M.A., Peiter, E. and Lee, K.W. 2023. Nitric oxide acts as an inducer of strategy-I responses to increase Fe availability and mobilization in Fe-starved broccoli (Brassica oleracea var. oleracea). Plant Physiology and Biochemistry. 194:182-192. https://doi.org/10.1016/j.plaphy.2022.11.018
  14. Lee, K.W., Rahman, M.A., Kim, K.Y., Choi, G.J., Cha, J.Y., Cheong, M.S., Shohael, A.M., Jones, C. and Lee, S.H. 2018. Overexpression of the alfalfa DnaJ-like protein (MsDJLP) gene enhances tolerance to chilling and heat stresses in transgenic tobacco plants. Turkish Journal of Biology. 42:12-22. https://doi.org/10.3906/biy-1705-30
  15. Livak, K.J. and Schmittgen, T.D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods. 25:402-408. https://doi.org/10.1006/meth.2001.1262
  16. Ma, J.F. and Yamaji, N. 2008. Functions and transport of silicon in plants. Cellular and molecular life sciences: Cellular and Molecular Life Sciences. 65:3049-3057. https://doi.org/10.1007/s00018-008-7580-x
  17. Ma, J.F., Goto, S., Tamai, K. and Ichii, M. 2001. Role of root hairs and lateral roots in silicon uptake by rice. Plant Physiology. 127:1773-1780. https://doi.org/10.1104/pp.010271
  18. Ma, J.F., Tamai, K., Yamaji, N., Mitani, N., Konishi, S., Katsuhara, M., Ishiguro, M., Murata, Y. and Yano, M. 2006. A silicon transporter in rice. Nature. 440:688-691. https://doi.org/10.1038/nature04590
  19. Maurel, C., Boursiac, Y., Luu, D.T., Santoni, V., Shahzad, Z. and Verdoucq, L. 2015. Aquaporins in plants. Physiological Reviews. 95:1321-1358. https://doi.org/10.1152/physrev.00008.2015
  20. Moradi, P., Vafaee, Y., Mozafari, A.A. andTahir, N.A.R. 2022. Silicon nanoparticles and methyl jasmonate improve physiological response and increase expression of stress-related genes in strawberry cv. Paros under salinity stress. Silicon. 14:10559-10569. https://doi.org/10.1007/s12633-022-01791-8
  21. Park, J.H. and Saier Jr, M.H. 1996. Phylogenetic characterization of the MIP family of transmembrane channel proteins. The Journal of Membrane Biology. 153:171-180. https://doi.org/10.1007/s002329900120
  22. Rahman, M.A., Ahmed, M.B., Alotaibi, F., Alotaibi, K.D., Ziadi, N., Lee, K.W. and Kabir, A.H. 2021. Growth and physiological impairments in Fe-starved alfalfa are associated with the downregulation of Fe and S transporters along with redox imbalance. Chemical and Biological Technologies in Agriculture. 8:36.
  23. Rahman, M.A., Bagchi, R., El-Shehawi, A.M., Elseehy, M.M., Anee, S.A., Lee, K.W. and Kabir, A.H. 2022. Physiological and molecular characterization of strategy-I responses and expression of Fe-transporters in Fe-deficient soybean. South African Journal of Botany. 147:942-950. https://doi.org/10.1016/j.sajb.2022.03.052
  24. Rahman, M.A., Haque, A.F.M.M., Akther, M.S., Islam, M., Lee, K.W. and Kabir, A.H. 2022. The NIP genes in sugar beet: underlying roles in silicon uptake and growth improvement. Silicon. 14:3551-3562. https://doi.org/10.1007/s12633-021-01133-0
  25. Rahman, M.A., Kabir, A.H., Mandal, A., Roy, S.K., Song, Y., Ji, H.C. and Lee, K.W. 2020. Glutathione restores Hg-induced morpho-physiological retardations by inducing phytochelatin and oxidative defense in alfalfa. Biology. 9.
  26. Rahman, M.A., Lee, S.H., Ji, H.C., Kabir, A.H., Jones, C.S. and Lee, K.W. 2018. Importance of mineral nutrition for mitigating aluminum toxicity in plants on acidic soils: Current status and opportunities. International Journal of Molecular Sciences. 19:3073.
  27. Rahman, M.A., Woo, J.H., Lee, S.H., Park, H.S., Kabir, A.H., Raza, A., El Sabagh, A. and Lee, K.W. 2022c. Regulation of Na+/H+ exchangers, Na+/K+ transporters, and lignin biosynthesis genes, along with lignin accumulation, sodium extrusion, and antioxidant defense, confers salt tolerance in alfalfa. Frontiers in Plant Science. 13:1041764.
  28. Rastogi, A., Yadav, S., Hussain, S., Kataria, S., Hajihashemi, S., Kumari, P., Yang, X. and Brestic, M., 2021. Does silicon really matter for the photosynthetic machinery in plants...? Plant Physiology and Biochemistry. 169:40-48. https://doi.org/10.1016/j.plaphy.2021.11.004
  29. Raza, A., Salehi, H., Rahman, M.A., Zahid, Z., Haghjou, M.M., Najafi-Kakavand, S., Charagh, S., Osman, H.S., Albaqami, M., Zhuang, Siddique, K.H. and Zhuang, W. 2022. Plant hormones and neurotransmitter interactions mediate antioxidant defenses under induced oxidative stress in plants. Frontiers in Plant Science. 13:961872.
  30. Sabir, F., Gomes, S., Loureiro-Dias, M.C., Soveral, G. and Prista, C. 2020. Molecular and functional characterization of grapevine nips through heterologous expression in aqy-null Saccharomyces cerevisiae. International Journal of Molecular Sciences. 21.
  31. Sigrist, C.J., Cerutti, L., de Castro, E., Langendijk-Genevaux, P.S., Bulliard, V., Bairoch, A. and Hulo, N. 2010. PROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Research. 38:D161-166. https://doi.org/10.1093/nar/gkp885
  32. Szklarczyk, D., Gable, A.L., Lyon, D., Junge, A., Wyder, S., Huerta-Cepas, J., Simonovic, M., Doncheva, N.T., Morris, J.H., Bork, P., Jensen, L.J. and Mering, C.von. 2019. STRING v11: Protein-protein association networks with increased coverage, supporting functional discovery in genome-wide experimental datasets. Nucleic Acids Research. 47:D607-D613. https://doi.org/10.1093/nar/gky1131
  33. Xu, W., Dai, W., Yan, H., Li, S., Shen, H., Chen, Y., Xu, H., Sun, Y., He, Z. and Ma, M. 2015. Arabidopsis NIP3;1 Plays an important role in arsenic uptake and root-to-shoot translocation under arsenite stress conditions. Moleluclar Plant. 8:722-733. https://doi.org/10.1016/j.molp.2015.01.005