Preview

Proceedings of Universities. Applied Chemistry and Biotechnology

Advanced search

Effect of increased gene expression of alternative external NADH dehydrogenase of mitochondria of Arabidopsis thaliana on the generation of reactive oxygen in Nicotiana tabacum tobacco leaves at low temperatures

https://doi.org/10.21285/achb.943

EDN: XNVAAG

Abstract

Low temperature is an important factor limiting plant viability and productivity. Along with other stresses, low temperatures increase the generation of reactive oxygen species, which are signaling molecules that can damage cell components. As well as representing one of the main targets of oxidative damage during stress, mitochondria represent a significant source of reactive oxygen species. Plant mitochondria have a large number of enzymes providing alternative electron transport pathways, many of which are activated under stress. Our aim was to assess the effect of low positive temperatures and increased expression of the heterologous gene NDB2 (alternative external NADH dehydrogenase of mitochondria) on the generation of reactive oxygen species, which involve an alternative respiratory chain in mitochondria and the expression of stress proteins under lighting conditions in Nicotiana tabacum tobacco leaves. In the leaves of tobacco plants with increased expression of the Arabidopsis thaliana NDB2 (AtNDB2) gene, a decrease in reactive oxygen species production was observed under normal and low temperature conditions. The results indicate that the heterologous Arabidopsis thaliana NDB2 gene is involved in increasing the activity of the alternative electron transport chain in mitochondria, which reduces the level of reactive oxygen species generation and affects the content of stress proteins under normal and low-temperature exposure.

About the Authors

G. B. Borovskii
Siberian Institute of Plant Physiology and Biochemistry SB RAS
Russian Federation

Gennadii B. Borovskii, Dr. Sci. (Biology), Professor, Vice-director

132, Lermontov St., Irkutsk, 664033



E. L. Gorbyleva
Siberian Institute of Plant Physiology and Biochemistry SB RAS
Russian Federation

Elena L. Gorbyleva, Cand. Sci. (Biology), Researcher

132, Lermontov St., Irkutsk, 664033



A. I. Katyshev
Siberian Institute of Plant Physiology and Biochemistry SB RAS
Russian Federation

Alexander I. Katyshev, Cand. Sci. (Biology), Senior Researcher

132, Lermontov St., Irkutsk, 664033



N. E. Korotaeva
Siberian Institute of Plant Physiology and Biochemistry SB RAS
Russian Federation

Natalia E. Korotaeva, Cand. Sci. (Biology), Senior Researcher

132, Lermontov St., Irkutsk, 664033



E. A. Polyakova
Siberian Institute of Plant Physiology and Biochemistry SB RAS
Russian Federation

Elizaveta A. Polyakova, Postgraduate Student, Leading Engineer

132, Lermontov St., Irkutsk, 664033



D. V. Pyatrikas
Siberian Institute of Plant Physiology and Biochemistry SB RAS
Russian Federation

Darya V. Pyatrikas, Cand. Sci. (Biology), Researcher

132, Lermontov St., Irkutsk, 664033



A. V. Stepanov
Siberian Institute of Plant Physiology and Biochemistry SB RAS
Russian Federation

Alexey V. Stepanov, Cand. Sci. (Biology), Senior Researcher

132, Lermontov St., Irkutsk, 664033



I. V. Fedoseeva
Siberian Institute of Plant Physiology and Biochemistry SB RAS
Russian Federation

Irina V. Fedoseeva, Cand. Sci. (Biology), Senior Researcher

132, Lermontov St., Irkutsk, 664033



A. M. Shigarova
Siberian Institute of Plant Physiology and Biochemistry SB RAS
Russian Federation

Anastasiya M. Shigarova, Cand. Sci. (Biology), Researcher

132, Lermontov St., Irkutsk, 664033



References

1. García-Caparrós P., De Filippis L., Gul A., Hasanuzzaman M., Ozturk M., Altay V., et al. Oxidative stress and antioxidant metabolism under adverse environmental conditions: a review. The Botanical Review. 2020;87:421- 466. DOI: 10.1007/s12229-020-09231-1.

2. Bartoli C.G., Gómez F., Martínez, D.E., Guiamet J.J. Mitochondria are the main target for oxidative damage in leaves of wheat (Triticum aestivum L.). Journal of Experimental Botany. 2004;55(403):1663-1669. DOI: 10.1093/jxb/erh199.

3. Liberatore K.L., Dukowic-Schulze S., Miller M.E., Chen C., Kianian S.F. 2016. The role of mitochondria in plant development and stress tolerance. Free Radical Biology and Medicine. 2016;100:238-256. DOI: 10.1016/j.freeradbiomed.2016.03.033.

4. Sachdev S., Ansari S.A., Ansari M.I., Fujita M., Hasanuzzaman M. Abiotic stress and reactive oxygen species: generation, signaling, and defense mechanisms. Antioxidants. 2021;10(2):277. DOI: 10.3390/antiox10020277.

5. Møller I.M., Rasmusson A.G., Van Aken O. Plant mitochondria – past, present and future. The Plant Journal. 2021;108(4):912-959. DOI: 10.1111/tpj.15495.

6. Bailey C.D., Carr T.G., Harris S.A., Hughes C.E. Characterization of angiosperm nrDNA polymorphism, paralogy, and pseudogenes. Molecular Phylogenetics and Evolution. 2003;29(3):435-455. DOI: 10.1016/j.ympev.2003.08.021.

7. Saha B., Borovskii G., Panda S.K. Alternative oxidase and plant stress tolerance. Plant Signaling & Behavior. 2016;11(12). DOI: 10.1080/15592324.2016.1256530.

8. Garmash E.V. Role of mitochondrial alternative oxidase in the regulation of cellular homeostasis during development of photosynthetic function in greening leaves. Plant Biology. 2021;23(2):221-228. DOI: 10.1111/plb.13217.

9. Elhafez D., Murcha M.W., Clifton R., Soole K.L., Day D.A., Whelan J. Characterization of mitochondrial alternative NAD(P)H dehydrogenases in Arabidopsis: intraorganelle location and expression. Plant & Cell Physiology. 2006;47(1):43-54. DOI: 10.1093/pcp/pci221.

10. Clifton R., Lister R., Parker K.L. Sappl P.G., Elhafez D., Millar A.H., et al. Stress-induced co-expression of alternative respiratory chain components in Arabidopsis thaliana. Plant Molecular Biology. 2005;58:193-212. DOI: 10.1007/s11103-005-5514-7.

11. Wanniarachchi V.R., Dametto L., Sweetman C., Shavrukov Y., Day D.A., et al. Alternative respiratory pathway component genes (AOX and ND) in rice and barley and their response to stress. International Journal of Molecular Sciences. 2018;19(3):915. DOI: 10.3390/ijms19030915.

12. Popov V.N., Syromyatnikov M.Y., Fernie A.R., Chakraborty S., Gupta K.J., Igamberdiev A.U. The uncoupling of respiration in plant mitochondria: keeping reactive oxygen and nitrogen species under control. Journal of Experimental Botany. 2021;72(3):793-807. DOI: 10.1093/jxb/eraa510.

13. Yerlikaya B.A., Ates D., Abudureyimu B., Aksoy E. Effect of climate change on abiotic stress response gene networks in Arabidopsis thaliana. In: Prakash C.S., Fiaz S., Fahad S. (eds). Principles and practices of OMICS and genome editing for crop improvement. Cham: Springer; 2022, p. 149-172. DOI: 10.1007/978-3-030-96925-7_6.

14. Sweetman C., Waterman C.D., Rainbird B.M., Smith P.M.C., Jenkins C.D., Day D.A., et al. AtNDB2 is the main external NADH dehydrogenase in mitochondria and is important for tolerance to environmental stress. Plant Physiology. 2019;181(2):774-788. DOI: 10.1104/pp.19.00877.

15. Alizadeh R., Kumleh H.H., Rezadoost M.H. The simultaneous activity of cytosolic and mitochondrial antioxidant mechanisms in neutralizing the effect of drought stress in soybean. Plant Physiology Reports. 2023;28(1):78-91. DOI: 10.1007/s40502-022-00704-6.

16. Korotaeva N.E., Shigarova A.M., Katyshev A.I., Fedoseeva I.V., Fedyaeva A.V., Sauchyn D.V., et al. Effect of expression of the NDB2 heterologous gene of Arabidopsis thaliana on growth and respiratory activity of Nicotiana tabacum. Russian Journal of Plant Physiology. 2023;70:93. DOI: 10.1134/S1021443723600885.

17. Borovskii G.B., Gorbyleva E.L., Katyshev A.I., Korotaeva N.E., Polyakova E.A., Pyatrikas D.V., et al. Effect of the overexpression of external alternative NADH dehydrogenase gene in Arabidopsis on the resistance of transformed tobacco plants to negative temperatures. Proceedings of Universities. Applied Chemistry and Biotechnology. 2023;13(4):516-522. (In Russian). DOI: 10.21285/2227-2925-2023-13-4-516-522. EDN: FNBXUJ.

18. Velikova V., Yordanov I., Edreva A. Oxidative stress and some antioxidant systems in acid rain-treated bean plants: protective role of exogenous polyamines. Plant Science. 2000;151(1):59-66. DOI: 10.1016/S0168-9452(99)00197-1.

19. Foyer C.H., Vanacker H., Gomez L.D., Harbinson J. Regulation of photosynthesis and antioxidant metabolism in maize leaves at optimal and chilling temperatures: review. Plant Physiology and Biochemistry. 2002;40(6-8):659- 668. DOI: 10.1016/S0981-9428(02)01425-0.

20. Foyer C.H., Noctor G. Redox regulation in photosynthetic organisms: signaling, acclimation and practical implications. Antioxidants & Redox Signaling. 2009;11(4):861-905. DOI: 10.1089/ars.2008.2177.

21. Igamberdiev A.U., Bykova N.V. Mitochondria in photosynthetic cells: coordinating redox control and energy balance. Plant Physiology. 2023;191(4):2104- 2119. DOI: 10.1093/plphys/kiac541.

22. Shameer S., Ratcliffe, R.G., Sweetlove L.J. Leaf energy balance requires mitochondrial respiration and export of chloroplast NADPH in the light. Plant Physiology. 2019;180(4):1947-1961. DOI: 10.1104/pp.19.00624.

23. Gandin A., Duffes C., Day D.A., Cousins A.B. The absence of alternative oxidase AOX1a results in altered response of photosynthetic carbon assimilation to increasing CO2 in Arabidopsis thaliana. Plant and Cell Physiology. 2012;53(9):1627-1637. DOI: 10.1093/pcp/pcs107.

24. Cheng D., Gao H., Zhang L. Upregulation of mitochondrial alternative oxidase pathway protects photosynthetic apparatus against photodamage under chilling stress in Rumex K-1 leaves. Photosynthetica. 2020;58(5):1116-1121. DOI: 10.32615/ps.2020.060.

25. Cheng D.D., Zhang L.T. Mitochondrial alternative oxidase pathway acts as an electron sink during photosynthetic induction in Rumex K-1 leaves. Photosynthetica. 2021;59(4):615-624. DOI: 10.32615/ps.2021.047.

26. Garmash E.V., Velegzhaninov I.O., Ermolina K.V., Rybak A.V., Malyshev R.V. Altered levels of AOX1a expression result in changes in metabolic pathways in Arabidopsis thaliana plants acclimated to low dose rates of ultraviolet B radiation. Plant Science. 2020;291:110332. DOI: 10.1016/j.plantsci.2019.110332.

27. Liu Y.-J., Norberg F.E.B., Szilágyi A., De Paepe R., Åkerlund H.-E., Rasmusson A.G. The mitochondrial external NADPH dehydrogenase modulates the leaf NADPH/ NADP+ ratio in transgenic Nicotiana sylvestris. Plant & Cell Physiology. 2008;49(2):251-263. DOI: 10.1093/pcp/pcn001.

28. Jethva J., Lichtenauer S., Schmidt-Schippers R., Steffen-Heins A., Poschet G., Wirtz M., et al. Mitochondrial alternative NADH dehydrogenases NDA1 and NDA2 promote survival of reoxygenation stress in Arabidopsis by safeguarding photosynthesis and limiting ROS generation. New Phytologist. 2023;238(1):96-112. DOI: 10.1111/nph.18657.

29. Borovskii G.B., Korotaeva N.E., Katyshev A.I., Fedoseeva I.V., Fedyaeva A.V., Kondakova M.A., et al. The overexpression of the Arabidopsis NDB2 gene in tobacco plants affects the expression of genes encoding the alternative mitochondrial electron transport pathways and stress proteins. In: Plant Genetics, Genomics, Bioinformatics, and Biotechnology: abstracts of the 6th International scientific conference. 14–18 June 2021, Novosibirsk. Novosibirsk: Institute of Cytology and Genetics SB RAS; 2021, p. 42. DOI: 10.18699/PlantGen2021-026. EDN: NKNKPO.

30. Elkelish A., Qari S.H., Mazrou Y.S., Abdelaal K.A., Hafez Y.M., Abu-Elsaoud A.M., et al. Exogenous ascorbic acid induced chilling tolerance in tomato plants through modulating metabolism, osmolytes, antioxidants, and transcriptional regulation of catalase and heat shock proteins. Plants. 2020;9(4):431. DOI: 10.3390/plants9040431.

31. Yurina N.P. Heat shock proteins in plant protection from oxidative stress. Molecular Biology. 2023;57:951- 964. DOI: 10.1134/S0026893323060201.

32. Kumar R., Khungar L., Shimphrui R., Tiwari L.D., Tripathi G., Sarkar N.K., et al. AtHsp101 research sets course of action for the genetic improvement of crops against heat stress. Journal of Plant Biochemistry and Biotechnology. 2020;29:715-732. DOI: 10.1007/s13562-020-00624-2.

33. Tiwari L.D., Kumar R., Sharma V., Sahu A.K., Sahu B., Naithani S.C., et al. Stress and development phenotyping of Hsp101 and diverse other Hsp mutants of Arabidopsis thaliana. Journal of Plant Biochemistry and Biotechnology. 2021;30:889-905. DOI: 10.1007/s13562-021-00706-9.

34. McLoughlin F., Basha E., Fowler M.E., Kim M., Bordowitz J., Katiyar-Agarwal S., et al. Class I and II small heat shock proteins together with HSP101 protect protein translation factors during heat stress. Plant Physiology. 2016;172(2):1221-1236. DOI: 10.1104/pp.16.00536.

35. Kim D.H., Xu Z.-Y., Na Y.J., Yoo Y.-J., Lee J., Sohn E.-J., et al. Small heat shock protein Hsp17.8 functions as an AKR2A cofactor in the targeting of chloroplast outer membrane proteins in Arabidopsis. Plant Physiology. 2011;157(1):132-146. DOI: 10.1104/pp.111.178681.

36. Leaden L., Busi M.V., Gomez-Casati D.F. The mitochondrial proteins AtHscB and AtIsu1 involved in Fe–S cluster assembly interact with the Hsp70-type chaperon AtHscA2 and modulate its catalytic activity. Mitochondrion. 2014;19:375-381. DOI: 10.1016/j.mito.2014.11.002.

37. Myouga F., Motohashi R., Kuromori T., Nagata N., Shinozaki K. An Arabidopsis chloroplast-targeted Hsp101 homologue, APG6, has an essential role in chloropl ast development as well as heat-stress response. The Plant Journal. 2006;48(2):249-60. DOI: 10.1111/j.1365-313X.2006.02873.x.

38. Oh S.E., Yeung C., Babaei-Rad R., Zhao R. Cosuppression of the chloroplast localized molecular chaperone HSP90.5 impairs plant development and chloroplast biogenesis in Arabidopsis. BMC Research Notes. 2014;7:643. DOI: 10.1186/1756-0500-7-643.


Review

For citations:


Borovskii G.B., Gorbyleva E.L., Katyshev A.I., Korotaeva N.E., Polyakova E.A., Pyatrikas D.V., Stepanov A.V., Fedoseeva I.V., Shigarova A.M. Effect of increased gene expression of alternative external NADH dehydrogenase of mitochondria of Arabidopsis thaliana on the generation of reactive oxygen in Nicotiana tabacum tobacco leaves at low temperatures. Proceedings of Universities. Applied Chemistry and Biotechnology. 2024;14(4):514-524. (In Russ.) https://doi.org/10.21285/achb.943. EDN: XNVAAG

Views: 125


Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.


ISSN 2227-2925 (Print)
ISSN 2500-1558 (Online)