Abstract
Key message
NtTAS14-like1 enhances osmotic tolerance through coordinately activating the expression of osmotic- and ABA-related genes.
Abstract
Osmotic stress is one of the most important limiting factors for tobacco (Nicotiana tabacum) growth and development. Dehydrin proteins are widely involved in plant adaptation to osmotic stress, but few of these proteins have been functionally characterized in tobacco. Here, to identify genes required for osmotic stress response in tobacco, an encoding dehydrin protein gene NtTAS14-like1 was isolated based on RNA sequence data. The expression of NtTAS14-like1 was obviously induced by mannitol and abscisic acid (ABA) treatments. Knock down of NtTAS14-like1 expression reduced osmotic tolerance, while overexpression of NtTAS14-like1 conferred tolerance to osmotic stress in transgenic tobacco plants, as determined by physiological analysis of the relative electrolyte leakage and malonaldehyde accumulation. Further expression analysis by quantitative real-time PCR indicated that NtTAS14-like1 participates in osmotic stress response possibly through coordinately activating osmotic- and ABA-related genes expression, such as late embryogenesis abundant (NtLEA5), early responsive to dehydration 10C (NtERD10C), calcium-dependent protein kinase 2 (NtCDPK2), ABA-responsive element-binding protein (NtAREB), ABA-responsive element-binding factor 1 (NtABF1), dehydration-responsive element-binding genes (NtDREB2A), xanthoxin dehydrogenase/reductase (NtABA2), ABA-aldehyde oxidase 3 (NtAAO3), 9-cis-epoxycarotenoid dioxygenase (NtNCED3). Together, this study will facilitate to improve our understandings of molecular and functional properties of plant TAS14 proteins and to improve genetic evidence on the involvement of the NtTAS14-like1 in osmotic stress response of tobacco.
Similar content being viewed by others
Data availability
All data supporting the findings of this study are available within this paper.
Abbreviations
- ABA:
-
Abscisic acid
- DREB:
-
Dehydration-responsive element-binding genes
- NCED:
-
9-cis-Epoxycarotenoid dioxygenase
- ABA2:
-
Xanthoxin dehydrogenase/reductase
- AAO3:
-
ABA-aldehyde oxidase 3
- DHN proteins:
-
Dehydrins
- LEA:
-
Late embryogenesis abundant
- VIGS:
-
Virus-induced gene silencing
- EL:
-
Relative electrolyte leakage
- MDA:
-
Malonaldehyde
- DS:
-
Drought stress
- AREB:
-
ABA-responsive element-binding protein
- ERD10C:
-
Early responsive to dehydration 10C
- WT:
-
Wild type
- ABF1:
-
ABA-responsive element-binding factor 1
- qRT-PCR:
-
Quantitative real-time PCR
- RNA-seq:
-
RNA sequence
- CDPK2:
-
Calcium-dependent protein kinase 2
References
Agarwal PK, Agarwal P, Reddy MK, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274. https://doi.org/10.1007/s00299-006-0204-8
Agarwal PK, Shukla PS, Gupta K, Jha B (2013) Bioengineering for salinity tolerance in plants: state of the art. Mol Biotechnol 54:102–123. https://doi.org/10.1007/s12033-012-9538-3
Asano T, Hayashi N, Kikuchi S, Ohsugi R (2012) CDPK-mediated abiotic stress signaling. Plant Signal Behav 7:817–821. https://doi.org/10.4161/psb.20351
Bahrami-Rad S, Hajiboland R (2017) Effect of potassium application in drought-stressed tobacco (Nicotiana rustica L.) plants: comparison of root with foliar application. Ann Agric Sci 62:121–130. https://doi.org/10.1016/j.aoas.2017.08.001
Brini F, Hanin M, Lumbreras V et al (2007) Overexpression of wheat dehydrin DHN-5 enhances tolerance to salt and osmotic stress in Arabidopsis thaliana. Plant Cell Rep 26:2017–2026. https://doi.org/10.1007/s00299-007-0412-x
Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560. https://doi.org/10.1093/aob/mcn125
Chen K, Li G, Bressan R et al (2020) Abscisic acid dynamics, signaling, and functions in plants. J Integr Plant Biol 62:25–54. https://doi.org/10.1111/jipb.12899
Chinnusamy V, Gong Z, Zhu JK (2008) Abscisic acid-mediated epigenetic processes in plant development and stress responses. J Integr Plant Biol 50:1187–1195. https://doi.org/10.1111/j.1744-7909.2008.00727.x
Dong H, Wu C, Luo C et al (2020) Overexpression of MdCPK1a gene, a calcium dependent protein kinase in apple, increase tobacco cold tolerance via scavenging ROS accumulation. PLoS ONE 15:e0242139. https://doi.org/10.1371/journal.pone.0242139
Du X, Zhao X, Li X et al (2013) Overexpression of TaSRK2C1, a wheat SNF1-related protein kinase 2 gene, increases tolerance to dehydration, salt, and low temperature in transgenic tobacco. Plant Mol Biol Report 31:810–821. https://doi.org/10.1007/s11105-012-0548-x
Estrada-Melo AC, Ma C, Reid MS, Jiang CZ (2015) Overexpression of an ABA biosynthesis gene using a stress-inducible promoter enhances drought resistance in petunia. Hortic Res 2:1–9. https://doi.org/10.1038/hortres.2015.13
Fang Y, Xiong L (2015) General mechanisms of drought response and their application in drought resistance improvement in plants. Cell Mol Life Sci 72:673–689. https://doi.org/10.1007/s00018-014-1767-0
Finkelstein R, Gibson S (2002) ABA and sugar interactions regulating development: cross-talk or voices in a crowd. Curr Opin Plant Biol 5:26–32. https://doi.org/10.1016/s1369-5266(01)00225-4
Frey A, Effroy D, Lefebvre V et al (2012) Epoxycarotenoid cleavage by NCED5 fine-tunes ABA accumulation and affects seed dormancy and drought tolerance with other NCED family members. Plant J 70:501–512. https://doi.org/10.1111/j.1365-313X.2011.04887.x
Gao Y, Han D, Jia W et al (2020) Molecular characterization and systematic analysis of NtAP2/ERF in tobacco and functional determination of NtRAV-4 under drought stress. Plant Physiol Biochem 156:420–435. https://doi.org/10.1016/j.plaphy.2020.09.027
Godoy JA, Pardo JM, Pintor-Toro JA (1990) A tomato cDNA inducible by salt stress and abscisic acid: nucleotide sequence and expression pattern. Plant Mol Biol 15:695–705. https://doi.org/10.1007/BF00016120
Godoy JA, Lunar R, Torres-schumann S et al (1994) Expression, tissue distribution and subcellular localization of dehydrin TAS14 in salt-stressed tomato plants. Plant Mol Biol 26:1921–1934
Hu R, Zhu X, Xiang S et al (2016) Comparative transcriptome analysis revealed the genotype specific cold response mechanism in tobacco. Biochem Biophys Res Commun 469:535–541. https://doi.org/10.1016/j.bbrc.2015.12.040
Hu Z, Huang X, Amombo E et al (2020) The ethylene responsive factor CdERF1 from bermudagrass (Cynodon dactylon) positively regulates cold tolerance. Plant Sci 294:110432. https://doi.org/10.1016/j.plantsci.2020.110432
Hu Z, Yan W, Yang C et al (2022) Integrative analysis of transcriptome and metabolome provides insights into the underlying mechanism of cold stress response and recovery in two tobacco cultivars. Environ Exp Bot 200:104920. https://doi.org/10.1016/j.envexpbot.2022.104920
Hu Z, He Z, Li Y et al (2023) Transcriptomic and metabolic regulatory network characterization of drought responses in tobacco. Front Plant Sci 13:1067076. https://doi.org/10.3389/fpls.2022.1067076
Jha RK, Mishra A (2022) Introgression of SbERD4 gene encodes an early-responsive dehydration-stress protein that confers tolerance against different types of abiotic stresses in transgenic tobacco. Cells. https://doi.org/10.3390/cells11010062
Kamarudin ZS, Yusop MR, Ismail MR et al (2019) LEA gene expression assessment in advanced mutant rice genotypes under drought stress. Int J Genomics 2019:8406036. https://doi.org/10.1155/2019/8406036
Lata C, Prasad M (2011) Role of DREBs in regulation of abiotic stress responses in plants. J Exp Bot 62:4731–4748. https://doi.org/10.1093/jxb/err210
Leng P, Yuan B, Guo Y, Chen P (2014) The role of abscisic acid in fruit ripening and responses to abiotic stress. J Exp Bot 65:4577–4588. https://doi.org/10.1093/jxb/eru204
Li X, Liu Q, Feng H et al (2020) Dehydrin MtCAS31 promotes autophagic degradation under drought stress. Autophagy 16:862–877. https://doi.org/10.1080/15548627.2019.1643656
Livak KJ, Schmittgen TD (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
Muñoz-Mayor A, Pineda B, Garcia-Abellán JO et al (2012) Overexpression of dehydrin tas14 gene improves the osmotic stress imposed by drought and salinity in tomato. J Plant Physiol 169:459–468. https://doi.org/10.1016/j.jplph.2011.11.018
Premachandra GS, Saneoka H, Fujita K, Ogata S (1992) Leaf water relations, osmotic adjustment, cell membrane stability, epicuticular wax load and growth as affected by increasing water deficits in sorghum. J Exp Bot 43:1569–1576
Rabara RC, Tripathi P, Reese RN et al (2015) Tobacco drought stress responses reveal new targets for Solanaceae crop improvement Tobacco drought stress responses reveal new targets for Solanaceae crop improvement. BMC Genomics. https://doi.org/10.1186/s12864-015-1575-4
Riyazuddin R, Nisha N, Singh K et al (2022) Involvement of dehydrin proteins in mitigating the negative effects of drought stress in plants. Plant Cell Rep 41:519–533. https://doi.org/10.1007/s00299-021-02720-6
Rizhsky L, Liang H, Mittler R (2002) The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiol 130:1143–1151. https://doi.org/10.1104/pp.00685
Saavedra L, Svensson J, Carballo V et al (2006) A dehydrin gene in Physcomitrella patens is required for salt and osmotic stress tolerance. Plant J 45:237–249. https://doi.org/10.1111/j.1365-313X.2005.02603.x
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Sun Y, Liu L, Sun S et al (2021) AnDHN, a dehydrin protein from Ammopiptanthus nanus, mitigates the negative effects of drought stress in plants. Front Plant Sci 12:1–15. https://doi.org/10.3389/fpls.2021.788938
Szlachtowska Z, Rurek M (2023) Plant dehydrins and dehydrin-like proteins: characterization and participation in abiotic stress response. Front Plant Sci 14:1213188. https://doi.org/10.3389/fpls.2023.1213188
Tommasini L, Svensson JT, Rodriguez EM et al (2008) Dehydrin gene expression provides an indicator of low temperature and drought stress: transcriptome-based analysis of barley (Hordeum vulgare L.). Funct Integr Genomics 8:387–405. https://doi.org/10.1007/s10142-008-0081-z
Ullah A, Manghwar H, Shaban M et al (2018) Phytohormones enhanced drought tolerance in plants: a coping strategy. Environ Sci Pollut Res 25:33103–33118. https://doi.org/10.1007/s11356-018-3364-5
Wang H, Li N, Li H et al (2023) Overexpression of NtGCN2 improves drought tolerance in tobacco by regulating proline accumulation, ROS scavenging ability, and stomatal closure. Plant Physiol Biochem 198:107665. https://doi.org/10.1016/j.plaphy.2023.107665
Xu J, Zhou Y, Xu Z et al (2020) Combining physiological and metabolomic analysis to unravel the regulations of coronatine alleviating water stress in tobacco (Nicotiana tabacum L.). Biomolecules. https://doi.org/10.3390/biom10010099
Yamaguchi-Shinozaki K, Shinozaki K (1994) A novel cis-acting element in an arabidopsis gene is involved in responsiveness to drought, low-temperature, or high-salt stress. Plant Cell 6:251–264. https://doi.org/10.2307/3869643
Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803. https://doi.org/10.1146/annurev.arplant.57.032905.105444
Yuan C, Li C, Yan L, Jackson AO, Liu Z, Han C, Yu J, Li D (2011) A high throughput Barley Stripe Mosaic Virus vector for virus induced gene silencing in monocots and dicots. PLoS ONE 6(10):e26468. https://doi.org/10.1371/journal.pone.0026468
Zandkarimi H, Ebadi A, Salami SA et al (2015) Analyzing the expression profile of AREB/ABF and DREB/CBF genes under drought and salinity stresses in grape (Vitis vinifera L.). PLoS ONE 10:1–16. https://doi.org/10.1371/journal.pone.0134288
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273. https://doi.org/10.1146/annurev.arplant.53.091401.143329
Funding
This work was supported by the Science and Technology Program of Hunan Provincial Tobacco Corporation (Grant Nos: HN2021KJ02, HN2021KJ04, 19-23Aa01) and the National Natural Science Foundation of China (Grant No 32201459).
Author information
Authors and Affiliations
Contributions
XH and RH conceived and designed the experiments. XH, ZH and YL performed most of the experiments. JY, SS, XL, and PY performed some of the experiments. XH and ZH wrote the manuscript. RH, YL, CX, and CL gave advices and revised the manuscript. All authors read and approved the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no conflict of interest related to this study. The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Communicated by Marcelo Menossi.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Hu, Z., Li, Y., Yang, J. et al. The positive impact of the NtTAS14-like1 gene on osmotic stress response in Nicotiana tabacum. Plant Cell Rep 43, 25 (2024). https://doi.org/10.1007/s00299-023-03118-2
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00299-023-03118-2