Skip to main content

Advertisement

SpringerLink
Log in

Overexpression of WssgtL3.1 gene from Withania somnifera confers salt stress tolerance in Arabidopsis

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Overexpression of Withania somnifera SGT gene (WssgtL3.1) in transgenic Arabidopsis improves various agronomic and physiological traits and alters conjugated sterol levels to mitigate the effect of salt stress.

Abstract

Sterols are essential constituents of cell membranes that are involved in several biological functions, including response to various biotic and abiotic stresses by altering membrane permeability and signaling pathways. Sterol glycosyltransferases (SGTs) are enzymes that are involved in sterol modification by converting sterols into sterol-conjugates to play essential roles in adaptive responses. However, their roles under abiotic stresses are lesser-known. Among abiotic stresses, salinity imposes serious threat to crop yield worldwide, hence the present study intends to investigate the role of WssgtL3.1-overexpressed Arabidopsis plants under salt stress indicating the crosstalk between SGT gene and salinity to develop improved crop varieties with better stress tolerance ability. The findings revealed that overexpression of WssgtL3.1 gene in A. thaliana improved the resistance against salt stress in the overexpressing lines. Transgenic lines showed significantly higher germination rate, increased plant growth with less chlorophyll damage compared to wild-type (WT) control plants. Moreover, better tolerance also correlated with enhanced osmolytes (proline and soluble sugar), better membrane integrity, decreased H2O2 production and lesser MDA accumulation and Na+/K+ ratio with more negative osmotic potential in overexpressed lines. Additionally, in sterol profiling, significant enhancement in stigmasterol was also observed in transgenic lines than WT plants. Furthermore, in expression profiling, salt responsive genes LEA 4–5, sucrose synthase, and transporter of monosaccharide (ERD) significantly upregulated in overexpressing lines as compared to WT. Thus our data strongly support the defensive role of Withania somnifera SGT gene (WssgtL3.1) against salt stress and contribute to improved salinity tolerance in plants through sterol modulation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig.7

Similar content being viewed by others

References

  • Aboobucker SI, Suza WP (2019) Why do plants convert sitosterol to stigmasterol? Front Plant Sci 10:354

    Article  Google Scholar 

  • Acosta-Motos JR, Ortuño MF, Bernal-Vicente A, Diaz-Vivancos P, Sanchez-Blanco MJ, Hernandez JA (2017) Plant responses to salt stress: adaptive mechanisms. Agronomy 7:18

    Article  Google Scholar 

  • Alexieva V, Sergiev I, Mapelli S, Karanov E (2001) The effect of drought and ultraviolet radiation on growth and stress markers in pea and wheat. Plant Cell Environ 24:1337–1344

    Article  CAS  Google Scholar 

  • Arnon DI (1949) Copper enzymes in isolated chloroplasts polyphenoloxidase in Beta Vulgaris. Plant Physiol 24:1–15

    Article  CAS  Google Scholar 

  • Bowles D, Lim EK, Poppenberger B, Vaistij FE (2006) Glycosyltransferases of lipophilic small molecules. Annu Rev Plant Biol 57:567–597. https://doi.org/10.1146/annurev.arplant.57.032905.105429

    Article  CAS  PubMed  Google Scholar 

  • Brini F 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

    Article  CAS  Google Scholar 

  • Busch F, Huner NPA, Ensminger I (2009) Biochemical constrains limit the potential of the photochemical reflectance index as a predictor of effective quantum efficiency of photosynthesis during the winter spring transition in Jack pine seedlings. Funct Plant Biol 36:1016–1026. https://doi.org/10.1071/FP08043

    Article  CAS  PubMed  Google Scholar 

  • Carillo P, Gibon Y (2011) Protocol: extraction and determination of proline. PrometheusWiki.

  • Chaturvedi P, Misra P, Tuli R (2011) Sterol glycosyltransferases—the enzymes that modify sterols. Appl Biochem Biotechnol 165:47–68. https://doi.org/10.1007/s12010-011-9232-0

    Article  CAS  PubMed  Google Scholar 

  • Chaturvedi P, Mishra M, Akhtar N, Gupta P, Mishra P, Tuli R (2012) Sterol glycosyltransferases-identification of members of gene family and their role in stress in Withania somnifera. Mol Biol Rep 39:9755–9764. https://doi.org/10.1007/s11033-012-1841-3

    Article  CAS  PubMed  Google Scholar 

  • Chauhan PS, Lata C, Tiwari S, Chauhan AS, Mishra SK, Agrawal L, Chakrabarty D, Nautiyal CS (2019) Transcriptional alterations reveal Bacillus amyloliquefaciens-rice cooperation under salt stress. Sci Rep 9(1):1–3

    Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  Google Scholar 

  • Cooke DT, Burden RS (1990) Lipid modulation of plasma membrane-bound ATPases. Physiol Plant 78:153–159

    Article  CAS  Google Scholar 

  • DeBolt S, Scheible WR, Schrick K, Auer M, Beisson F, Bischoff V, Bouvier-Navé P, Carroll A, Hematy K, Li Y, Milne J (2009) Mutations in UDP-glucose: sterol glucosyltransferase in Arabidopsis cause transparent testa phenotype and suberization defect in seeds. Plant Physiol 151(1):78–87

    Article  CAS  Google Scholar 

  • Deuticke B, Haest C (1987) Lipid modulation of transport proteins in vertebrate cell membranes. Annu Rev Physiol 49:221–235

    Article  CAS  Google Scholar 

  • El-Beltagi HS, Mohamed HI (2013) Reactive oxygen species, lipid peroxidation and antioxidative defense mechanism. Not Bot Horti Agrobo 41:44–57

    Article  CAS  Google Scholar 

  • Ferrer A, Altabella T, Arró M, Boronat A (2017) Emerging roles for conjugated sterols in plants. Prog Lipid Res 67:27–37

    Article  CAS  Google Scholar 

  • Grille S, Zaslawski A, Thiele S, Plat J, Warnecke D (2010) The functions of steryl glycosides come to those who wait: recent advances in plants, fungi, bacteria and animals. Prog Lipid Res 49:262–288

    Article  CAS  Google Scholar 

  • Hassanein R, Hashem H, Khalil R (2012) Stigmasterol treatment increases salt stress tolerance of faba bean plants by enhancing antioxidant systems. Plant Omics 5:476

    CAS  Google Scholar 

  • Hayford MB, Medford JI, Hoffman NL, Rogers SG, Klee HJ (1988) Development of a plant transformation selection system based on expression of genes encoding gentamicin acetyltransferases. Plant physiol 86:1216–1222

    Article  CAS  Google Scholar 

  • Huang X, Wang G, Shen Y, Huang Z (2012) The wheat gene TaST can increase the salt tolerance of transgenic Arabidopsis. Plant Cell Rep 31:339–347

    Article  CAS  Google Scholar 

  • Kasuga M, Miura S, Shinozaki K, Yamaguchi-Shinozaki K (2004) A combination of the Arabidopsis DREB1A gene and stress-inducible rd29A promoter improved drought- and low-temperature stress tolerance in tobacco by gene transfer. Plant Cell Physiol 45:346–350

    Article  CAS  Google Scholar 

  • Lara JA, Burciaga-Monge A, Chávez A, Revés M, Lavilla R, Arró M, Boronat A, Altabella T, Ferrer A (2018) Identification and characterization of sterol acyltransferases responsible for steryl ester biosynthesis in tomato. Front Plant Sci 9:588

    Article  Google Scholar 

  • Li W, Li M, Zhang W, Welti R, Wang X (2004) The plasma membrane–bound phospholipase Dδ enhances freezing tolerance in Arabidopsis thaliana. Nat Biotechnol 22:427–433

    Article  Google Scholar 

  • Li Y, He N, Hou J, Xu L, Liu C, Zhang J, Wang Q, Zhang X, Wu X (2018) Factors influencing leaf chlorophyll content in natural forests at the biome scale. Front Ecol Evol 6:64

    Article  CAS  Google Scholar 

  • Lim EK, Bowles DJ (2004) A class of plant glycosyltransferases involved in cellular homeostasis. EMBO J 23:2915–2922. https://doi.org/10.1038/sj.emboj.76002957600295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu W-H, Ding B, Ruan X-M, Xu H-T, Yang J, Liu S-M (2007) Analysis of free and conjugated phytosterols in tobacco by an improved method using gas chromatography–flame ionization detection.J. Chromatogr A 1163:304–311

    Article  CAS  Google Scholar 

  • Madina BR, Sharma LK, Chaturvedi P, Sangwan RS, Tuli R (2007) Purification and characterization of a novel glucosyltransferase specific to 27beta-hydroxy steroidal lactones from Withania somnifera and its role in stress responses. Biochim Biophys Acta 1774:1199–1207. https://doi.org/10.1016/j.bbapap.2007.06.015

    Article  CAS  PubMed  Google Scholar 

  • Mishra MK, Chaturvedi P, Singh R, Singh G, Sharma LK, Pandey V, Kumari N, Misra P (2013) Overexpression of WsSGTL1 gene of Withania somnifera enhances salt tolerance, heat tolerance and cold acclimation ability in transgenic Arabidopsis plants. PLoS ONE 8(4):e63064

    Article  CAS  Google Scholar 

  • Mishra MK, Singh G, Tiwari S, Singh R, Kumari N, Misra P (2015) Characterization of Arabidopsis sterol glycosyltransferase TTG15/UGT80B1 role during freeze and heat stress. Plant Signal Behav 10:e1075682. https://doi.org/10.1080/15592324.2015.1075682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mishra MK, Srivastava M, Singh G, Tiwari S, Niranjan A, Kumari N, Misra P (2017) Overexpression of Withania somnifera SGTL1 gene resists the interaction of fungus Alternaria brassicicola in Arabidopsis thaliana. Physiol Mol Plant Pathol 97:11–19

    Article  CAS  Google Scholar 

  • Pandey V, Niranjan A, Atri N, Chandrashekhar K, Mishra MK, Trivedi PK, Misra P (2014) WsSGTL1 gene from Withania somnifera, modulates glycosylation profile, antioxidant system and confers biotic and salt stress tolerance in transgenic tobacco. Planta 239:1217–1231. https://doi.org/10.1007/s00425-014-2046-x

    Article  CAS  PubMed  Google Scholar 

  • Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349

    Article  CAS  Google Scholar 

  • Ramirez-Estrada K, Castillo N, Lara JA, Arró M, Boronat A, Ferrer A, Altabella T (2017) Tomato UDP-glucose sterol glycosyltransferases: a family of developmental and stress regulated genes that encode cytosolic and membrane-associated forms of the enzyme Front. Plant Sci 8:984

    Google Scholar 

  • Rogowska A, Szakiel A (2020) The role of sterols in plant response to abiotic stress. Phytochem Rev 19:1525–1538

    Article  CAS  Google Scholar 

  • Rudell DR, Buchanan DA, Leisso RS, Whitaker BD, Mattheis JP, Zhu Y, Varanasi V (2011) Ripening, storage temperature, ethylene action, and oxidative stress alter apple peel phytosterol metabolism. Phytochemistry 72:1328–1340

    Article  CAS  Google Scholar 

  • Saema S, Rahman LU, Singh R, Niranjan A, Ahmad IZ, Misra P (2016) Ectopic overexpression of WsSGTL1, a sterol glucosyltransferase gene in Withania somnifera, promotes growth, enhances glycowithanolide and provides tolerance to abiotic and biotic stresses. Plant Cell Rep 35:195–211. https://doi.org/10.1007/s00299-015-1879-510.1007/s00299-015-1879-5

    Article  CAS  PubMed  Google Scholar 

  • Schreiber U (2004) Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: an overview. Chlorophyll a fluorescence. Springer, Berlin, pp 279–319

    Chapter  Google Scholar 

  • Sharma LK, Madina BR, Chaturvedi P, Sangwan RS, Tuli R (2007) Molecular cloning and characterization of one member of 3beta-hydroxy sterol glucosyltransferase gene family in Withania somnifera. Arch Biochem Biophys 460:48–55. https://doi.org/10.1016/j.abb.2007.01.024

    Article  CAS  PubMed  Google Scholar 

  • Singh R, Pandey N, Naskar J, Shirke PA (2015) Physiological performance and differential expression profiling of genes associated with drought tolerance in contrasting varieties of two Gossypium species. Protoplasma 252:423–438

    Article  CAS  Google Scholar 

  • Singh G, Tiwari M, Singh SP, Singh S, Trivedi PK, Misra P (2016) Silencing of sterol glycosyltransferases modulates the withanolide biosynthesis and leads to compromised basal immunity of Withania somnifera. Sci Rep 6:25562. https://doi.org/10.1038/srep25562

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stein O, Granot D (2019) An overview of sucrose synthases in plants. Front Plant Sci 10:95

    Article  Google Scholar 

  • Summermatter K, Sticher L, Métraux J-P (1995) Systemic responses in Arabidopsis thaliana infected and challenged with Pseudomonas syringae pv. syringae. Plant Physiol 108:1379–1385

    Article  CAS  Google Scholar 

  • Sun Y-G, Wang B, Jin S-H, Qu X-X, Li Y-J, Hou B-K (2013) Ectopic expression of Arabidopsis glycosyltransferase UGT85A5 enhances salt stress tolerance in tobacco. PLoS ONE 8:e59924

    Article  CAS  Google Scholar 

  • Surjus A, Durand M (1996) Lipid changes in soybean root membranes in response to salt treatment. J Exp Bot 47:17–23. https://doi.org/10.1093/Jxb/47.1.17

    Article  CAS  Google Scholar 

  • Tapken W, Murphy AS (2015) Membrane nanodomains in plants: capturing form, function, and movement. J Exp Bot 66:1573–1586

    Article  CAS  Google Scholar 

  • Tiwari S, Lata C, Chauhan PS, Nautiyal CS (2016) Pseudomonas putida attunes morphophysiological, biochemical and molecular responses in Cicer arietinum L. during drought stress and recovery. Plant Physiol Biochem 99:108–117. https://doi.org/10.1016/j.plaphy.2015.11.001

    Article  CAS  PubMed  Google Scholar 

  • Tiwari S, Prasad V, Chauhan PS, Lata C (2017) Bacillus amyloliquefaciens confers tolerance to various abiotic stresses and modulates plant response to phytohormones through osmoprotection and gene expression regulation in rice. Front Plant Sci 8:1510

    Article  Google Scholar 

  • Tiwari S, Gupta SC, Chauhan PS, Lata C (2020) An OsNAM gene plays important role in root rhizobacteria interaction in transgenic Arabidopsis through abiotic stress and phytohormone crosstalk. Plant cell rep. https://doi.org/10.1007/s00299-020-02620-1

    Article  PubMed  Google Scholar 

  • Xiong L, Zhu JK (2002) Molecular and genetic aspects of plant responses to osmotic stress. Plant Cell Environ 25:131–139

    Article  CAS  Google Scholar 

  • Zhang H, Mao X, Wang C, Jing R (2010) Overexpression of a common wheat gene TaSnRK2. 8 enhances tolerance to drought, salt and low temperature in Arabidopsis. PLoS ONE 5:e16041

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The Director, Council of Scientific and Industrial Research-National Botanical Research Institute, is gratefully acknowledged by authors for providing the facilities. ST acknowledges CSIR-SRF for providing financial support to carry out the research work.

Author information

Author notes

  1. Manoj Kumar Mishra and Shalini Tiwari equal contribution.

Authors and Affiliations

  1. Department of Botany, University of Lucknow, Lucknow, 226007, India

    Manoj Kumar Mishra

  2. CSIR-National Botanical Research Institute, Rana Pratap Marg, Lucknow, 226001, India

    Shalini Tiwari & Pratibha Misra

Authors
  1. Manoj Kumar Mishra
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shalini Tiwari
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pratibha Misra
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MKM conceived and designed research. MKM and ST conducted experiments and analyzed data. MKM and ST wrote the manuscript. PM improvised the language of manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Manoj Kumar Mishra.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Communicated by Aryadeep Roychoudhury.

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.

Supplementary file1 (DOCX 1254 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mishra, M.K., Tiwari, S. & Misra, P. Overexpression of WssgtL3.1 gene from Withania somnifera confers salt stress tolerance in Arabidopsis. Plant Cell Rep 40, 2191–2204 (2021). https://doi.org/10.1007/s00299-021-02666-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-021-02666-9

Keywords

Search

Navigation