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Changes in Invertase Activities during Hardening to Hypothermia of Nicotiana tabacum L. and Arabidopsis thaliana Heynh. (L.)

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Abstract

Changes in invertase activities were studied upon hardening of chilling-sensitive (Nicotiana tabacum L.) and cold-resistant (Arabidopsis thaliana Heynh. (L.)) plants to hypothermia. In tobacco plants, the activity of cytoplasmic and vacuolar invertases was found to decrease by 20% during hardening, while the activity of cell wall invertase increased almost twofold. In arabidopsis, the activity of all three types of invertases increased more than twofold during hardening. The hardened tobacco plants showed a 20% increase in sugar content, while the relative content of sucrose and hexoses (fructose and glucose) in sugars did not change after hardening and equaled approximately 50% each. During hardening of arabidopsis plants, the sugar content increased 2.5 fold, whereas the proportion of sucrose in the total sugar content decreased (from 44 to 24%) and the proportion of hexoses increased (from 56 to 76%). It was proposed that the increase in activity of cell wall invertase in both plant species suppressed the outflow of assimilates and facilitated the accumulation of photosynthates in mesophyll cells of tobacco and arabidopsis leaves. The decrease in activity of cytoplasmic and vacuolar invertases in N. tabacum restricted the formation of hexoses in cells and reduced the efficiency of cold hardening in tobacco plants. More than a twofold increase in the content of soluble carbohydrates in arabidopsis was mainly caused by hexose accumulation, which was due to the increased activity of cytoplasmic and vacuolar invertases and ensured high efficiency of A. thaliana hardening to hypothermia.

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REFERENCES

  1. Larcher, W., Physiological Plant Ecology: Ecophysiology and Stress Physiology of Functional Groups, Berlin: Springer-Velag, 2003, p. 513.

    Book  Google Scholar 

  2. Trunova, T.I., Rastenie i nizkotemperaturnyi stress. 64‑e Timiryazevskie chteniya (Plants and Low-Temperature Stress: 64th Timiryazev’s Readings), Moscow: Nauka, 2007.

  3. Tarkowski, L.P. and van den Ende, W., Cold tolerance triggered by soluble sugars: a multifaceted countermeasure, Front. Plant Sci., 2015, vol. 6, art. ID 203. https://doi.org/10.3389/fpls.2015.00203

    Article  PubMed  PubMed Central  Google Scholar 

  4. Sturm, A., Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning, Plant Physiol., 1999, vol. 121, p. 1. https://doi.org/10.1104/pp.121.1.1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Deryabin, A.N., Burakhanova, E.A., and Trunova, T.I., Apoplastic sugars and cell wall invertase are involved in formation of the tolerance of cold-resistant potato plants to hypothermia, Dokl. Biochem. Biophys., 2015, vol. 465, p. 366.

    Article  CAS  Google Scholar 

  6. Qian, W., Xiao, B., Wang, L., Hao, X., Yue, C., Cao, H., Wang, Y., Li, N., Yu, Y., Zeng, J., Yang, Y., and Wang, X., CsINV5, a tea vacuolar invertase gene enhances cold tolerance in transgenic Arabidopsis, BMC Plant Biol., 2018, vol. 18, art. ID 228. https://doi.org/10.1186/s12870-018-1456-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Weiszmann, J., Furtauer, L., Weckwerth, W., and Nagele, T., Vacuolar sucrose cleavage prevents limitation of cytosolic carbohydrate metabolism and stabilizes photosynthesis under abiotic stress, FEBS J., 2018, vol. 285, p. 4082. https://doi.org/10.1111/febs.14656

    Article  CAS  PubMed  Google Scholar 

  8. Xiang, L., Le Roy, K., Bolouri-Moghaddam, M.R., Vanhaecke, M., Lammens, W., Rolland, F., and van den Ende, W., Exploring the neutral invertase—oxidative stress defence connection in Arabidopsis thaliana, J. Exp. Bot., 2011, vol. 62, p. 3849. https://doi.org/10.1093/jxb/err069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Deryabin, A.N., Dubinina, I.M., Burakhanova, E.A., Astakhova, N.V., Sabelnikova, E.P., and Trunova, T.I., Influence of yeast-derived invertase gene expression in potato plants on membrane lipid peroxidation at low temperature, J. Therm. Biol., 2005, vol. 30, p. 73. https://doi.org/10.1016/j.jtherbio.2004.07.002

    Article  CAS  Google Scholar 

  10. Sasaki, H., Ichimura, K., Imada, S., and Yamaki, S., Sucrose synthase and sucrose phosphate synthase, but not acid invertase, are regulated by cold acclimation and deacclimation in cabbage seedlings, J. Plant Physiol., 2001, vol. 158, p. 847.

    Article  CAS  Google Scholar 

  11. Turkina, M.V. and Sokolova, S.V., Methods for the determination of monosaccharides and oligosaccharides, in Biokhimicheskie metody v fiziologii rastenii (Biochemical Methods in Plant Physiology), Pavlinova, O.A., Ed., Moscow: Nauka, 1971.

  12. Klimov, S.V., Cold hardening of plants is a result of maintenance of an increased photosynthesis/respiration ratio at low temperature, Biol. Bull. (Moscow), 2003, vol. 30, p. 48.

    Article  Google Scholar 

  13. Trunova, T.I., Astakhova, N.V., Deryabin, A.N., and Sabel’nikova, E.P., Ultrastructural organization of chloroplasts of the leaves of potato plants transformed with the yeast invertase gene at normal and low temperature, Dokl. Biol. Sci., 2003, vol. 389, p. 176.

    Article  CAS  Google Scholar 

  14. Klimov, S.V., Popov, V.N., Dubinina, I.M., Burakhanova, E.A., and Trunova, T.I., The decreased cold-resistance of chilling-sensitive plants is related to suppressed CO2 assimilation in leaves and sugar accumulation in roots, Russ. J. Plant Physiol., 2002, vol. 49, p. 776.

    Article  CAS  Google Scholar 

  15. Xin, Z. and Browse, J., Cold comfort farm: the acclimation of plants to freezing temperatures, Plant Cell Environ., 2000, vol. 23, p. 893.

    Article  Google Scholar 

  16. Zuther, E., Schulz, E., Childs, L.H., and Hincha, D.K., Clinal variation in the non-acclimated and cold–acclimated freezing tolerance of Arabidopsis thaliana accessions, Plant Cell Environ., 2012, vol. 35, p. 1860. https://doi.org/10.1111/j.1365-3040.2012.02522.x

    Article  CAS  PubMed  Google Scholar 

  17. Ashworth, E.N. and Pearce, R.S., Extracellular freezing in leaves of freezing-sensitive species, Planta, 2002, vol. 214, p. 798.

    Article  CAS  Google Scholar 

  18. Ma, Y., Zhang, Y., Lu, J., and Shao, H., Roles of plant soluble sugars and their responses to plant cold stress, Afr. J. Biotechnol., 2009, vol. 8, p. 2004.

    CAS  Google Scholar 

  19. Sicher, R., Carbon partitioning and the impact of starch deficiency on the initial response of Arabidopsis to chilling temperatures, Plant Sci., 2011, vol. 181, p. 167. https://doi.org/10.1016/j.plantsci.2011.05.005

    Article  CAS  PubMed  Google Scholar 

  20. Barau, J., Grandis, A., de Andrade Carvalho, V.M., Teixeira, G.S., Zaparoli, G.H.A., Scatolin do Rio, M.A., Rincones, J., Buckeridge, M.S., and Guimarães Pereira G.A., Apoplastic and intracellular plant sugars regulate developmental transitions in witches broom disease of cacao, J. Exp. Bot., 2015, vol. 66, p. 1325. https://doi.org/10.1093/jxb/eru485

    Article  CAS  PubMed  Google Scholar 

  21. Roitsch, T. and González, M.-C., Function and regulation of plant invertases: sweet sensations, Trends Plant Sci., 2004, vol. 9, p. 606.

    Article  CAS  Google Scholar 

  22. Gamalei, Yu.V., Floema lista (Leaf Phloem), St. Petersburg: Nauka, 1990.

  23. Gamalei, Yu.V., Pakhomova, M.V., and Syutkina, A.V., Ecological aspects of assimilate transport. I. Temperature, Fiziol. Rast., 1992, vol. 39, p. 1068.

    Google Scholar 

  24. Chikov, V.I. and Bakirova, G.G., Role of the apoplast in the control of assimilate transport, photosynthesis, and plant productivity, Russ. J. Plant Physiol., 2004, vol. 51, p. 420.

    Article  CAS  Google Scholar 

  25. Livingston, D.P. and Henson, C.A., Apoplastic sugars, fructans, fructan exohydrolase, and invertase in winter oat: responses to second-phase cold hardening, Plant Physiol., 1998, vol. 116, p. 403. https://doi.org/10.1104/pp.116.1.403

    Article  CAS  PubMed Central  Google Scholar 

  26. Reyes-Díaz, M., Ulloa, N., Zúñiga-Feest, A., Gutiérrez, A., Gidekel, M., Alberdi, M., Corcuera, L.J., and Bravo, L.A., Arabidopsis thaliana avoids freezing by supercooling, J. Exp. Bot., 2006, vol. 57, p. 3687.

    Article  Google Scholar 

  27. Gupta, A.K. and Kaur, N., Sugar signaling and gene expression in relation to carbohydrate metabolism under abiotic stresses in plants, J. Biosci., 2005, vol. 30, p. 761.

    Article  CAS  Google Scholar 

  28. Moore, B., Zhou, L., Rolland, F., Hall, Q., Cheng, W.H., and Liu, Y.X., Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling, Science, 2003, vol. 300, p. 332.

    Article  CAS  Google Scholar 

  29. Wilhelm, K.S. and Thomashow, M.F., Arabidopsis thaliana cor15b, an apparent homologue of cor15a, is strongly responsive to cold and ABA, but not drought, Plant Mol. Biol., 1993, vol. 23, p. 1073.

    Article  CAS  Google Scholar 

  30. Jang, J.C., Leόn, P., and Sheen, J., Hexokinase as a sugar sensor in higher plants, Plant Cell, 1997, vol. 9, p. 5.

    CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This work was supported by the Ministry of Education and Science of the Russian Federation (State Assignment no. 121040800153-1 “Mechanisms of Plant Adaptation to the Factors of Aridization of the Global Climate and Anthropogenic Pollution of the Environment”).

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Correspondence to V. N. Popov.

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Conflict of interests. The authors declare that they have no conflicts of interest.

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Translated by A. Bulychev

Abbreviations: HXK1—hexokinase 1.

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Popov, V.N., Astakhova, N.V. Changes in Invertase Activities during Hardening to Hypothermia of Nicotiana tabacum L. and Arabidopsis thaliana Heynh. (L.). Russ J Plant Physiol 68, 1218–1226 (2021). https://doi.org/10.1134/S1021443721050149

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