Skip to main content
Log in

Myo-inositol phosphate synthase improves heat stress tolerance by ethylene-mediated modulation of chlorophyll content and photosynthetic efficiency

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

L-myo-inositol phosphate synthase (MIPS; EC 5.5.1.4) encodes the enzyme synthesizing Myo-inositol for plant growth and development. Myo-inositol and its phosphate derivatives are involved in various physiological functions ranging from cell wall synthesis, chromatin remodeling, signal transduction, and providing stress responses. In the present study, we report that MIPS regulates chlorophyll content and photosynthesis efficiency via the ethylene signaling pathway. We have used Triticum aestivum MIPS-A (TAMIPS-A) for the present study and characterized it by mutant complementation and overexpression studies in Arabidopsis. TaMIPS-A overexpressing Arabidopsis transgenics were analyzed physiologically under thermal stress conditions. Analysis of overexpression TaMIPS-A transgenics under control and thermal stress conditions revealed them to have enhanced photosynthetic potential under heat stress. When TaMIPS-A overexpression (OE) Arabidopsis transgenics are supplemented with either ACC, the ethylene precursor, or AgNO3, the ethylene signaling inhibitor indicated that MIPS regulates the photosynthetic efficiency and chlorophyll content via the ethylene signaling pathway under control and thermal stress. Expression analysis of essential genes involved in the ethylene biosynthetic and signaling pathway corroborated.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

Data availability

Data sharing not applicable to this article as no datasets were generated or analysed during the current study.

References

  • Aminaka R, Taira Y, Kashino Y, Koike H, Satoh K (2006) Acclimation to the growth temperature and thermosensitivity of photosystem II in a mesophilic cyanobacterium, Synechocystis sp. PCC6803. Plant Cell Physiol 47:1612–1621

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berry JA, Bjorkman O (1980) Photosynthetic response and adaptation to temperature in higher plants. Annu Rev Plant Physiol 31:491–543

    Article  Google Scholar 

  • Beyer EM (1976) A potent inhibitor of ethylene action in plants. Plant Physiol 58(3):268–271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ceusters J, Van de Poel B (2018) Ethylene exerts species-specific and age-dependent control of photosynthesis. Plant Physiol 176:2601–2612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang SH, Lu LS, Wang NN, Chang YY (2008) Negative feedback regulation of system-1 ethylene production by the tomato 1-aminocyclopropane-1-carboxylate synthase 6 gene promoter. Plant Sci 175:149–160

    Article  CAS  Google Scholar 

  • Ciardi JA, Deikman J, Orzolek MD (1997) Increased ethylene synthesis enhances chilling tolerance in tomatoes. Physiol Plant 101:333–340

    Article  CAS  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  PubMed  Google Scholar 

  • Donahue JL, Alford SR, Torabinejad J, Kerwin RE, Nourbakhsh A, Ray WK, Hernick M, Huang X, Lyons BM, Hein PP, Gillaspy GE (2010) The Arabidopsis thaliana myo-inositol 1-phosphate synthase1 gene is required for Myo-inositol synthesis and suppression of cell death. Plant Cell 22:888–903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gautam H, Fatma M, Sehar Z, Iqbal N, Albaqami M, Khan NA (2022) Exogenously sourced ethylene positively modulates photosynthesis, carbohydrate metabolism, and antioxidant defense to enhance heat tolerance in rice. Int J Mol Sci 23(3):1031

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hiscox JD, Israelstam GF (1979) A method for the extraction of chlorophyll from leaf tissue without maceration. Can J Bot 57:1332–1334

    Article  CAS  Google Scholar 

  • Joshi R, Ramanarao MV, Baisakh N (2013) Arabidopsis plants constitutively overexpressing a myo-inositol 1-phosphate synthase gene (SaINO1) from the halophyte smooth cordgrass exhibit an enhanced level of tolerance to salt stress. Plant Physiol Biochem 65:61–66

    Article  CAS  PubMed  Google Scholar 

  • Khurana N, Sharma N, Khurana P (2017) Overexpression of a heat stress-inducible, wheat myo-inositol-1-phosphate synthase 2 (TaMIPS2) confers tolerance to various abiotic stresses in Arabidopsis thaliana. Agri Gene 6:24–30

    Article  Google Scholar 

  • Kumar D, Yusuf MA, Singh P, Sardar M, Sarin NB (2014) Histochemical detection of superoxide and H2O2 accumulation in Brassica juncea Seedlings. Bio-Protoc 4(8):e1108

    Article  Google Scholar 

  • Lackey KH, Pope PM, Johnson MD (2003) Expression of 1L-myo-inositol-1-phosphate synthase in organelles. Plant Physiol 132:2240–2247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Latrasse D, Jégu T, Meng PH, Mazubert C, Hudik E, Delarue M, Charon C, Crespi M, Hirt H, Raynaud C, Bergounioux C, Benhamed M (2013) Dual function of MIPS1 as a metabolic enzyme and transcriptional regulator. Nucleic Acids Res 41:2907–2917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loewus FA, Murthy PPN (2000) myo-Inositol metabolism in plants. Plant Sci 150:1–19

    Article  CAS  Google Scholar 

  • Mamedov M, Hayashi H, Murata N (1993) Effects of glycine betaine and unsaturation of membrane lipids on the heat stability of photosynthetic electron-transport and phosphorylation reactions in Synechocystis PCC6803. Biochim Biophys Acta 1142:1–5

    Article  CAS  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668

    Article  CAS  PubMed  Google Scholar 

  • Meng PH, Raynaud C, Tcherkez G, Blanchet S, Massoud K, Domenichini S, Henry Y, Soubigou-Taconnat L, Lelarge-Trouverie C, Saindrenan P, Renou JP, Bergounioux C (2009) Crosstalks between myo-inositol metabolism, programmed cell death, and basal immunity in Arabidopsis. Plos One 4:1–15

    Article  Google Scholar 

  • Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot 64:3983–3998

    Article  CAS  PubMed  Google Scholar 

  • Pahwa K, Ghai N, Kaur J, Singh I, Singh S, Dhingra M (2017) Influence of ethylene and cobalt chloride on photosynthetic parameters and pedicel anatomy of pigeon pea (Cajanus cajan L.) genotypes. J Environ Biol 38:367–374

    Article  Google Scholar 

  • Patra B, Ray S, Richter A, Majumder L (2010) Enhanced salt tolerance of transgenic tobacco plants by co-expression of PcINO1 and McIMT1 is accompanied by the increased level of Myo-inositol and methylated inositol. Protoplasma 245:143–152

    Article  CAS  PubMed  Google Scholar 

  • Sharma DK, Andersen SB, Ottosen C-O, Rosenqvist E (2015) Wheat cultivars selected for high Fv/Fm under heat stress maintain high photosynthesis, total chlorophyll, stomatal conductance, transpiration and dry matter. Physiol Plantarum 153:284–298

    Article  CAS  Google Scholar 

  • Sharma N, Chaudhary C, Khurana P (2020a) Wheat Myo-inositol phosphate synthase influences plant growth and stress responses via ethylene mediated signaling. Sci Rep 10:10766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sharma N, Chaudhary C, Khurana P (2020b) Role of myo-inositol during skotomorphogenesis in Arabidopsis. Sci Rep 10:17329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Slesak I, Libik M, Karpinska B, Karpinski S, Miszalski Z (2007) The role of hydrogen peroxide in regulation of plant metabolism and cellular signalling in response to environmental stresses. Acta Biochim Pol 54(1):39–50

    Article  CAS  PubMed  Google Scholar 

  • Tan J, Wang C, Xiang B et al (2013) Hydrogen peroxide and nitric oxide mediated cold- and dehydration-induced myo-inositol phosphate synthase that confers multiple resistances to abiotic stresses. Plant, Cell Environ 36:288–299

    Article  CAS  PubMed  Google Scholar 

  • Tholen D, Pons TL, Voesenek LACJ, Poorter H (2007) Ethylene insensitivity results in down-regulation of Rubisco expression and photosynthetic capacity in tobacco. Plant Physiol 144:1305–1315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tholen D, Pons TL, Voesenek LACJ, Poorter H (2008) The role of ethylene perception in the control of photosynthesis. Plant Signal Behav 3:108–109

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu YS, Yang CY (2019) Ethylene-mediated signaling confers thermotolerance and regulates transcript levels of heat shock factors in rice seedlings under heat stress. Bot Stud 60:23

    Article  PubMed  PubMed Central  Google Scholar 

  • Zacarias L, Reid MS (1990) Role of growth regulators in the senescence of Arabidopsis thaliana leaves. Physiol Plant 80:549–554

    Article  CAS  Google Scholar 

  • Zhuo C, Wang T, Lu S et al (2013) A cold-responsive galactinol synthase gene from Medicago falcata (MfGolS1) is induced by myo-inositol and confers multiple tolerances to abiotic stresses. Physiol Plant 149:67–78

    Article  CAS  PubMed  Google Scholar 

  • Ali, N., Paul, S., Gayen, D., Sarkar, S.N., Datta, S.K., and Datta, K. (2013). RNAi mediated down-regulation of myo-inositol-3-phosphate synthase to generate low phytate rice. Rice (N. Y). 6:12.

  • Sun X., Zhao T., Gan S., Ren X., Fang L., Karungo S. K., Wang Y., Chen L., Li S., Xin H. (2016). Ethylene positively regulates cold tolerance in grapevine by modulating the expression of ethylene response factor 057. Sci Rep. 6.

  • Zhai H., Wang F., Si Z., et al (2016). A myo-inositol-1-phosphate synthase gene , IbMIPS1 , enhances salt and drought tolerance and stem nematode resistance in transgenic sweet potato. 592–602.

Download references

Funding

NS received a UGC fellowship from the University Grant Commission, Government of India. PK received financial support from the Department of Biotechnology, Government of India (BT/PR8406/AGIII/103/879/2013), and the JC Bose fellowship award, Science and Engineering Research Board, Government of India.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Paramjit Khurana.

Additional information

Handling Editor: Néstor Carrillo

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 (PDF 395 KB)

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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sharma, N., Shree, B. & Khurana, P. Myo-inositol phosphate synthase improves heat stress tolerance by ethylene-mediated modulation of chlorophyll content and photosynthetic efficiency. Protoplasma 260, 1097–1107 (2023). https://doi.org/10.1007/s00709-022-01835-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-022-01835-1

Keywords

Navigation