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The Role of Nitric Oxide in the Arabidopsis thaliana Response to Simulated Microgravity and the Involvement of Autophagy in This Process

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Abstract

The role of nitric oxide (NO) in the response of plants to simulated microgravity has been studied. It was found that treatment of Arabidopsis thaliana seeds with NO donor sodium nitroprusside (SNP), stimulating changes in root growth parameters, leads to increased plant resistance to clinostating. After treatment of seeds with SNP, the content of endogenous NO in control plants on the sixth day of cultivation increased by 1.5 times, and it increased by 1.8 times in clinostated seed. The content of endogenous NO gradually decreased on days 9–12, which may indicate the adaptation of plants to the clinostating conditions. Using a specific DAF-FM DA fluorescent probe, an increase in NO fluorescence was found in epidermal cells of root apexes and root hairs in clinostated plants, indicating the accumulation of endogenous NO in these root tissues under stress. On the sixth day of cultivation under clinostat conditions compared with control plants, there was an increase in the accumulation of autophagosomes in the epidermal cells of the transitional zone of the root with the following decrease in this indicator on days 9–12. Seed treatment with cPTIO (NO scavenger) slightly inhibited seedling growth, and this effect was enhanced under clinostating, including a significant increase in the accumulation of autophagosomes in epidermal cells. Thus, the data obtained indicate that the regulation of endogenous NO content is an important component of intracellular signaling mechanisms that are involved in the response of plant cells to simulated microgravity.

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REFERENCES

  1. Bassham, D.C., Laporte, M., Marty, F., et al., Autophagy in development and stress responses of plants, Autophagy, 2006, vol. 2, pp. 2–11. https://doi.org/10.4161/auto.2092

    Article  CAS  PubMed  Google Scholar 

  2. Beckman, J.S., Chen, J., Ischiropoulos, H., and Crow, J.P., Oxidative chemistry of peroxynitrite, Methods Enzymol., 1994, vol. 233, pp. 229–240. https://doi.org/10.1016/s0076-6879(94)33026-3

    Article  CAS  PubMed  Google Scholar 

  3. Blume, Y.B., Krasylenko, Y.A., Demchuk, O.M., and Yemets, A.I., Tubulin tyrosine nitration regulates microtubule organization in plant cells, Front. Plant Sci., 2013, vol. 4, art. ID 530. https://doi.org/10.3389/fpls.2013.00530

    Article  PubMed  PubMed Central  Google Scholar 

  4. Cao, J.-J., Liu, C.-X., Shao, S.-J., and Zhou, J., Molecular mechanisms of autophagy regulation in plants and their applications in agriculture, Front. Plant Sci., 2021, vol. 11, art. ID 618944. https://doi.org/10.3389/fpls.2020.618944

    Article  PubMed  PubMed Central  Google Scholar 

  5. Cao, Y., Fan, X., Shen, Z., et al., Nitric oxide affects preimplantation embryonic development in a rotating wall vessel bioreactor simulating microgravity, Cell Biol. Int., 2007, vol. 31, no. 1, pp. 24–29. https://doi.org/10.1016/j.cellbi.2006.09.003

    Article  CAS  PubMed  Google Scholar 

  6. Cassia, R., Amenta, M., Fernández, M.B., et al., The role of nitric oxide in the antioxidant defense of plants exposed to UV-B radiation, in Reactive Oxygen, Nitrogen and Sulfur Species in Plants, Hasanuzzaman, M., Fotopoulos, V., Nahar, K., and Fujita, M., Eds., Wiley, 2019, pp. 555–572.

    Google Scholar 

  7. Chen, H., Dong, J., and Wang, T., Autophagy in plant abiotic stress management, Int. J. Mol. Sci., 2021, vol. 22, no. 8, art. ID 4075. https://doi.org/10.3390/ijms22084075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Correa Aragunde, M.N., Foresi, N.P., and Lamattina, L., Nitric oxide is a ubiquitous signal for maintaining redox balance in plant cells: regulation of ascorbate peroxidase as a case study, J. Exp. Bot., 2015, vol. 66, no. 10, pp. 2913–2921. https://doi.org/10.1093/jxb/erv073

    Article  CAS  PubMed  Google Scholar 

  9. Correll, M.J., Pyle, T.P., Millar, K.D.L., et al., Transcriptome analyses of Arabidopsis thaliana seedlings grown in space: implications for gravity-responsive genes, Planta, 2013, vol. 238, pp. 519–533. https://doi.org/10.1007/s00425-013-1909-x

    Article  CAS  PubMed  Google Scholar 

  10. de Angeli, A., Thomine, S., Frachisse, J-M., et al., Anion channels and transporters in plant cell membranes, FEBS Lett., 2007, vol. 581, no. 12, pp. 2367–2374. https://doi.org/10.1016/j.febslet.2007.04.003

    Article  CAS  PubMed  Google Scholar 

  11. Fancy, N.N., Bahlmann, A-K., and Loake, G.J., Nitric oxide function in plant abiotic stress, Plant, Cell Environ., 2017, vol. 40, pp. 462–472. https://doi.org/10.1111/pce.12707

    Article  CAS  Google Scholar 

  12. Gilroy, S., Białasek, M., Suzuki, N., et al., ROS, calcium, and electric signals: key mediators of rapid systemic signaling in plants, Plant Physiol., 2016, vol. 171, no. 3, pp. 1606–1615. https://doi.org/10.1104/pp.16.00434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Hu, X., Neill, S.J., Tang, Z., and Cai, W., Nitric oxide mediates gravitropic bending in soybean roots, Plant Physiol., 2005, vol. 137, no. 2, pp. 663–670. https://doi.org/10.1104/pp.104.054494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Khan, M., Al Azawi, T.N.I., Pande, A., et al., The role of nitric oxide-induced ATILL6 in growth and disease resistance in Arabidopsis thaliana, Front. Plant Sci., 2021, vol. 12, art. ID 685156. https://doi.org/10.3389/fpls.2021.685156

    Article  PubMed  PubMed Central  Google Scholar 

  15. Klein-Nulend, J., Bacabac, R.G., Veldhuijzen, J.P., Van Loon, J.J.W.A., Microgravity and bone cell mechanosensitivity, Adv. Space Res., 2003, vol. 32, no. 8, pp. 1551–1559. https://doi.org/10.1016/S0273-1177(03)90395-4

    Article  CAS  PubMed  Google Scholar 

  16. Krasylenko, Yu.A., Yemets, A.I., Sheremet, Ya.A., and Blume, Ya.B., Nitric oxide as a critical factor for Arabidopsis microtubules perceptions of UV-B irradiation, Physiol. Plant, 2012, vol. 145, no. 4, pp. 505–515. https://doi.org/10.1111/j.1399-3054.2011.01530.x

    Article  CAS  PubMed  Google Scholar 

  17. Krasylenko, Yu.A., Yemets, A.I., and Blume, Ya.B., Cell mechanisms of nitric oxide signaling in plants under abiotic stress conditions, in Mechanism of Plant Hormone Signaling Under Stress: A Functional Genomic Frontier, Pandey, G., Ed., Wiley-Blackwell, 2017, vol. 1, pp. 371–398. https://doi.org/10.1002/9781118889022.ch15

    Book  Google Scholar 

  18. Kruse, C.P.S. and Wyatt, S.E., Nitric oxide, gravity response, and a unified schematic of plant signaling, Plant Sci., 2022, vol. 314, art. ID 111105. https://doi.org/10.1016/j.plantsci.2021.111105

    Article  CAS  PubMed  Google Scholar 

  19. Lin. J. and Wang, L., Oxidative stress in oocytes and embryo development: implications for in vitro systems, Antioxid. Redox Signaling, 2021, vol. 34, no. 17, pp. 1394–1406. https://doi.org/10.1089/ars.2020.8209

    Article  CAS  Google Scholar 

  20. Lytvyn, D.I., Raynaud, C., Yemets, A.I., et al., Involvement of inositol biosynthesis and nitric oxide in the mediation of UV-B induced oxidative stress, Front. Plant Sci., 2016, vol. 7, art. ID 430. https://doi.org/10.3389/fpls.2016.00430

    Article  PubMed  PubMed Central  Google Scholar 

  21. Lytvyn, D.I., Olenieva, V.D., Yemets, A.I., and Blume, Ya.B., Histochemical analysis of tissue-specific α-tubulin acetylation as a response to autophagy induction by different stress factors in Arabidopsis thaliana, Cytol. Genet., 2018, vol. 52, pp. 245–252. https://doi.org/10.3103/S0095452718040059

    Article  Google Scholar 

  22. Mohd Amnan, M.A., Pua, T.-L., Lau, S.-E., et al., Osmotic stress in banana is relieved by exogenous nitric oxide, PeerJ, 2021, vol. 9, art. ID e10879. https://doi.org/10.7717/peerj.10879

    Article  PubMed  PubMed Central  Google Scholar 

  23. Mugnai, S., Pandolfi, C., Masi, E., et al., Oxidative stress and NO signalling in the root apex as an early response to changes in gravity conditions, BioMed. Res. Int., 2014, vol. 2014, art. ID 834134. https://doi.org/10.1155/2014/834134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Mur, L.A.J., Mandon, J., Persijn, S., et al., Nitric oxide in plants: an assessment of the current state of knowledge, AoB Plants, 2013, vol. 5, art. ID pls052. https://doi.org/10.1093/aobpla/pls052

    Article  CAS  PubMed  Google Scholar 

  25. Nasir, N.N.M., Ho, C.-L., Lamasudin, D.U., and Saidi, N.B., Nitric oxide improves tolerance to Fusarium oxysporum f. sp. cubense Tropical Race 4 in banana, Physiol. Mol. Plant Pathol., 2020, vol. 111, art. ID 101503. https://doi.org/10.1016/j.pmpp.2020.101503

    Article  CAS  Google Scholar 

  26. Olenieva, V., Lytvyn, D., Yemets, A., et al., Tubulin acetylation accompanies autophagy development induced by different abiotic stimuli in Arabidopsis thaliana, Cell Biol. Int., 2019, vol. 43, no. 9, pp. 1056–1064. https://doi.org/10.1002/cbin.10843

    Article  CAS  PubMed  Google Scholar 

  27. París, R., Vazquez, M.M., Graziano, M., et al., Distribution of endogenous NO regulates early gravitropic response and PIN2 localization in Arabidopsis roots, Front. Plant Sci., 2018, vol. 9, art. ID 495. https://doi.org/10.3389/fpls.2018.00495

    Article  PubMed  PubMed Central  Google Scholar 

  28. Paul, A.-L., Zupanska, A.K., Schultz, E.R., and Ferl, R.J., Organ-specific remodeling of the Arabidopsis transcriptome in response to spaceflight, BMC Plant Biol., 2013, vol. 13, art. ID 112. https://doi.org/10.1186/1471-2229-13-112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Pedroso, M.C. and Durzan, D.J., Effect of different gravity environments on DNA fragmentation and cell death in Kalanchoë leaves, Ann. Bot., 2000, vol. 86, no. 5, pp. 983–994. https://doi.org/10.1006/anbo.2000.1260

    Article  CAS  PubMed  Google Scholar 

  30. Plohovska, S.H., Krasylenko, Y.A., and Yemets, A.I., Nitric oxide modulates actin filament organization in Arabidopsis thaliana primary root cells at low temperatures, Cell Biol. Int., 2019, vol. 43, no. 9, pp. 1020–1030. https://doi.org/10.1002/cbin.10931

    Article  CAS  PubMed  Google Scholar 

  31. Rizzo, A.M., Montorfano, G., Negroni, M., et al., Simulated microgravity induce glutathione antioxidant pathwayin Xenopus laevis embryos, Cell Biol. Int., 2009, vol. 33, no. 8, pp. 893–898. https://doi.org/10.1016/j.cellbi.2009.04.015

    Article  CAS  PubMed  Google Scholar 

  32. Sarath, G., Bethke, P.C., Jones, R., et al., Nitric oxide accelerates seed germination in warm-season grasses, Planta, 2006, vol. 223, pp. 1154–1164. https://doi.org/10.1007/s00425-005-0162-3

    Article  CAS  PubMed  Google Scholar 

  33. Siamwala, J.H., Reddy, S.H., Majumder, S., et al., Simulated microgravity perturbs actin polymerization to promote nitric oxide-associated migration in human immortalized Eahy926 cells, Protoplasma, 2010, vol. 242, pp. 3–12. https://doi.org/10.1007/s00709-010-0114-z

    Article  CAS  PubMed  Google Scholar 

  34. Strohm, A., Baldwin, K., and Masson, P., Multiple roles for membrane-associated protein trafficking and signaling in gravitropism, Front. Plant Sci., 2012, vol. 3, art. ID 274. https://doi.org/10.3389/fpls.2012.00274

    Article  PubMed  PubMed Central  Google Scholar 

  35. Sun, H., Feng, F., Liu, J., and Zhao, Q., Nitric oxide affects rice root growth by regulating auxin transport under nitrate supply, Front. Plant Sci., 2018, vol. 9, art. ID 659. https://doi.org/10.3389/fpls.2018.00659

    Article  PubMed  PubMed Central  Google Scholar 

  36. Wang, Z., Ma, R., Zhao, M., et al., NO and ABA Interaction regulates tuber dormancy and sprouting in potato, Front. Plant Sci., 2020, vol. 11, art. ID 311. https://doi.org/10.3389/fpls.2020.00311

    Article  PubMed  PubMed Central  Google Scholar 

  37. Xiao, Y., Liu, Y., and Wang, G., Involvement of nitric oxide in the mechanism of biochemical alterations induced by simulated microgravity in Microcystis aeruginosa, Adv. Space Res., 2012, vol. 49, no. 5, pp. 850–858. https://doi.org/10.1016/j.asr.2011.11.003

    Article  CAS  Google Scholar 

  38. Xiong, J., Li, Y., and Nie, J., Effects of simulated microgravity on nitric oxide level in cardiac myocytes and its mechanism, Sci. China, Ser. C: Life Sci., 2003, vol. 46, no. 3, pp. 302–309. https://doi.org/10.1360/03yc9032

    Article  CAS  Google Scholar 

  39. Yemets, A.I., Krasylenko, Yu.A., and Blume, Ya.B., Nitric oxide and UV-B radiation, in Nitric Oxide Action in Abiotic Stress Responses in Plants, Khan, M.N., Mobin, M., Mohammad, F., and Corpas, F.J., Eds., Springer-Verlag, 2015, pp. 141–154. https://doi.org/10.1007/978-3-319-17804-2_9

    Book  Google Scholar 

  40. Yemets, A., Shadrina, R., Horyunova, I., et al., Development of autophagy in plant cells under microgravity: the role of microtubules and atg8 proteins in autophagosome formation, in Space Research in Ukraine 2018–2020, Fedorov, O., Ed., Akademperiodyka, 2021, pp. 79–84.

    Google Scholar 

  41. Yun, B.-W., Feechan, A., Yin, M., et al., S-nitrosylation of NADPH oxidase regulates cell death in plant immunity, Nature, 2011, vol. 478, no. 7368, pp. 264–268. https://doi.org/10.1038/nature10427

    Article  CAS  PubMed  Google Scholar 

  42. Yun, B.-W., Skelly, M.J., Yin, M., et al., Nitric oxide and S‑nitrosoglutathione function additively during plant immunity, New Phytol., 2016, vol. 211, no. 2, pp. 516–526. https://doi.org/10.1111/nph.13903

    Article  CAS  PubMed  Google Scholar 

  43. Zhan, N., Wang, C., Chen, L., et al., S-nitrosylation targets GSNO reductase for selective autophagy during hypoxia responses in plants, Mol. Cell, 2018, vol. 71, no. 1, pp. 142–154. https://doi.org/10.1016/j.molcel.2018.05.024

    Article  CAS  PubMed  Google Scholar 

  44. Zhang, Y., Su, J., Cheng, D., et al., Nitric oxide contributes to methane-induced osmotic stress tolerance in mung bean, BMC Plant Biol., 2018, vol. 18, art. ID 207. https://doi.org/10.1186/s12870-018-1426-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Shadrina, R.Y., Yemets, A.I., and Blume, Ya.B., Autophagy development as an adaptive response to microgravity conditions in Arabidopsis thaliana, Factors Exp. Evol. Organisms, 2019, vol. 25, pp. 327–332. https://doi.org/10.7124/FEEO.v25.1186

  46. Shadrina, R.Y., Horiunova, I.I., Blume, Ya.B., and Yemets, A.I., Autophagosome formation and transcriptional activity of atg8 genes in Arabidopsis root cells during the development of autophagy under microgravity conditions, Rep. Nat. Akad. Nauk Ukr., 2020, vol. 9, pp. 77–85. https://doi.org/10.15407/dopovidi2020.09.077

    Article  CAS  Google Scholar 

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ACKNOWLEDGMENTS

This research has been financially supported by the project “Development of the concept of regulation of development and stress resistance of plants for their adaptation to space flight conditions by attracting cellular and biological resources” of the targeted comprehensive program of the National Academy of Sciences of Ukraine for scientific space research for 2018–2022 (state registration number 01118U003742).

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This study did not receive any certain grant from financial organs in governmental, commercial, or noncommercial sectors.

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Correspondence to Ya. B. Blume.

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The authors declare that they have no conflicts of interest. This article does not contain any studies involving animals or human participants performed by any of the authors.

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Translated by V. Mittova

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Plokhovska, S.H., Shadrina, R.Y., Kravets, O.A. et al. The Role of Nitric Oxide in the Arabidopsis thaliana Response to Simulated Microgravity and the Involvement of Autophagy in This Process. Cytol. Genet. 56, 244–252 (2022). https://doi.org/10.3103/S0095452722030100

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