FUNCTIONAL STATE OF MITOCHONDRIA IN VARIOUS PEA SEEDLING CULTIVARS DIFFERING IN RESISTANCE TO WATER DEFICIENCY AND INFLUENCE OF IRON TETRANITROSYL COMPLEX WITH THIOSULFATE LIGANDS ON IT

Research article
DOI:
https://doi.org/10.23649/jae.2022.4.24.07
Issue: № 4 (24), 2022
Published:
19.08.2022
PDF

Abstract

Different cultivars of plants have various ability to tolerate adverse environmental effects without a sharp decrease in growth processes and yields. The present study was carried out to study the effect of water deficiency (WD) on the morphological, biochemical and bioenergetic characteristics of two cultivars of pea seedlings differing in resistance to WD. At the same time, the effect of nitric oxide donor a tetranitrosyl iron complex with thiosulfate ligands (TNIC-thio) on the resistance of pea seedlings to insufficient moisture was studied. The functional state of the mitochondria was studied per rate respiration of mitochondria, by the level of lipid peroxidation by the spectrofluorimetry, and a fatty acid composition of mitochondrial membranes with the chromatography technique, by the study of mitochondrial morphology with the method of atomic force microscopy. Water deficiency (WD) led to the activation of lipid peroxidation, which caused swelling of mitochondria and changes in the content of C18 and C20 fatty acids (FA) in the membranes of these organelles. Wherein there was a decrease in the content of linolenic acid by 15% in the mitochondrial membranes of the less resistant cultivar, while in the resistant cultivar it decreased by only 6%. Note that in the membranes of mitochondria more resistant to water deficiency there were 3,23 times more unsaturated C20 FA. The water scarcity was accompanied by an increase in the content of these fatty acids. Differences in the FA composition of mitochondrial membranes affected the bioenergetic characteristics of mitochondria. WD caused a decrease in the maximum oxidation rates of NAD-dependent substrates by mitochondria of seedlings. At the same time, the rate of oxidation of NAD-dependent substrates and the efficiency of oxidative phosphorylation in the more resistant cultivar were higher. Treatment of pea seeds with 10-8M TNIC-thio restored the bioenergetic characteristics of mitochondria in pea seedlings of both cultivars. However, the efficiency of oxidative phosphorylation in the respiratory chain of mitochondria of the water-deficiency more resistant cultivar was 15,7% higher. The increased content of unsaturated VLCFAs in the mitochondrial membranes of pea seedlings contributes to maintaining the bioenergetic characteristics of mitochondria, and, consequently, the energy metabolism of the cell under stress conditions.

Full text is available in pdf only

References

  • Hasanuzzaman M. Exogenous nitric oxide alleviates high temperature induced oxidative stress in wheat (Triticum aestivum L.) seedlings by modulating the antioxidant defense and glyoxalase / M. Hasanuzzaman, K. Nahar, Md. M. Alam et al. // Australian J. Crop Science. – 2012. – 6(8). – pp.1314–1323.

  • Nabi S.R.B. Nitric oxide regulates plant responses to drought, salinity, and heavy metal stress / S.R.B. Nabi, R. Tayade, A. Hussain et al. // Environmental and Experimental Botany. – 2019. – 161. – pp. 120–133

  • Groß F. Nitric oxide, antioxidants and prooxidants in plant defence responses/ F. Groß, J. Durner, F. Gaupels // Front Plant Sci. – 2013. – 4.– p. 419.

  • Vanin A.F. Dinitrozilʹnyye kompleksy zheleza s tiol-soderzhashchimi ligandami: fiziko-khimiya, biologiya, meditsina [Dinitrosyl iron complexes with thiol-containing ligands: physics-chemistry, biology, medicine] /A.F. Vanin – Moskva-Izhevsk: Institut kompʹyuternykh issledovaniy, 2015. – 220 p. [in Russian]

  • Sanina N.A. Stroenie i svojstva nitrozil'nyh kompleksov zheleza s funkcional'nymi serosoderzhashchimi ligandami [Structure and properties of nitrosyl iron complexes with functional sulfur-containing ligands] / N.A. Sanina, S.M. Aldoshin // Izv. RAN. Ser. him. [News of the Russian Academy of Sciences. Chemistry Series] – 2011. – № 7. – pp. 1199–1227 [in Russian]

  • Hou Q. Lipid signalling in plant responses to abiotic stress / Q. Hou, G. Ufer, D. Bartels // Plant Cell Environ. – 2016. – 39(5). – pp.1029-48 DOI: 10.1111/pce.12666

  • Okazaki Y. Roles of lipids as signaling molecules and mitigators during stress response in plants / Y. Okazaki, K. Saito // Plant J. – 2014. – 79(4). – pp.584–596. DOI: 10.1111/tpj.12556

  • Taylor N.L. Differential Impact of Environmental Stresses on the Pea Mitochondrial Proteome / N.L. Taylor, J.L Heazlewood, D.A. Day et al. // Mol Cell Proteomics. – 2005. – 4(8). – pp. 1122–1133. DOI: 10.1074/mcp.M400210–MCP200

  • Møller I.M. Plant mitochondria – past, present and future / I.M. Møller, A.G. Rasmusson, O.V. Aken // The Plant Journal. – 2021. – 108. – pp. 912–959 DOI: 10.1111/tpj.15495

  • Lakomkin V.L. Long-lasting hypotensive action of stable preparations of dinitrosyl-iron complexes with thiol-containing ligands in conscious normotensive and hypertensive rat / V.L. Lakomkin, A.F. Vanin, A.A. Timoshin et al // Nitric Oxide. – 2007. – 16(4). – pp. 413–418

  • Popov V.N. Vliyaniye ingibitorov elektronnogo transporta na obrazovaniye aktivnykh form kisloroda pri okislenii suktsinata mitokhondriyami gorokha [The effect of electron transport inhibitors on the formation of reactive oxygen species during the oxidation of succinate by pea mitochondria] / V.N. Popov, E.K. Ruge, A.A Starkov // Biokhimiya [Biochemistry]. – 2003. – 68(7). – pp. 910–916 [in Russian]

  • Fletcher B.I. Measurement of fluorescent lipid peroxidation products in biological systems and tissues / B.I. Fletcher, C.D. Dillard., A.L. Tappel // Anal. Biochem. – 1973. – 52. – pp. 1–9

  • Carreau J.P. Adaptation of Macroscale Method to the Microscale for Fatty Acid Methyl Trans esterification of Biological Lipid Extracts / J.P Carreau., J.P Dubacq // J. Chromatogr. – 1979. – 151. – pp. 384−390.

  • Wang J. Fatty Acid Determination in Chicken Egg Yolk.A Comparison of Different Methods/ J. Wang, H. Sunwoo, G. Cherian et al // Poultry. Science. – 2000. – 79. – pp.1168−1171

  • Golovina R.V. Thermodynamic Evaluation Interaction of Fatty Acid Methyl Esters with Polar and Nonpolar Stationary Phases, Based on Their Retention Indices Chromatographia / R.V. Golovina, T.E. Kuzmenko // Chromatography. – 1977. – 10. – pp. 545−546.

  • Zhang L. Characterization of mitochondrial dynamics and subcellular localization of ROS reveal that HsfA2 alleviates oxidative damage caused by heat stress in Arabidopsis / L. Zhang, D. Xing, C. Gao // J. Exp. Bot. – 2009. – 60. – pp. 2073–2091. DOI: 10.1093/jxb/erp078.

  • Mata-Pérez C. Transcriptomic profiling of linolenic acid-responsive genes in ROS signaling from RNA-seq data in Arabidopsis/ C. Mata-Pérez, B. Sánchez-Calvo, J.C. Begara-Morales et al // Frontiers in Plant Science. – 2015. – 6. – p.122. DOI: 10.3389/fpls.2015.00122

  • He M. Plant Unsaturated Fatty Acids: Multiple Roles in Stress Response / M. He, N. Zh. Ding // Front. Plant Sci. – 2020. – 11. – p. 562785. DOI: 10.3389/fpls.2020.562785

  • Batsale M. Biosynthesis and Functions of Very-Long-Chain Fatty Acids in the Responses of Plants to Abiotic and Biotic Stresses / M. Batsale, D. Bahammou, L Fouillen et al. // Cells. – 2021. – 10(6). – p. 1284. DOI: 10.3390/cells10061284

  • Zhukov A.V. Very-long-chain fatty acids (VLCFAs) in plant response to stress / A.V. Zhukov, M. Shumskaya // Functional Plant Biology. – 2020 – 47(8). – pp. 695–703 DOI: 10.1071/FP19100

  • Popov V.N. Izmeneniya soderzhaniya i zhirnokislotnogo sostava lipidov list'ev i kornej tabaka pri nizkotemperaturnom zakalivanii [Changes in the content and fatty acid composition of lipids of tobacco leaves and roots during low-temperature hardening] / Popov V.N., Antipina O.V., Pchelkin V.P. et al. // Fiziologiya rastenij [Plant physiology]. – 2012. – 59. – pp. 203–208 [in Russian]

  • Zhigacheva I.V. Iron-Sulfur-Nitrosyl Complex Increases the Resistance of Pea Seedling to Water Deficiency/ I.V. Zhigacheva, V.I. Binyukov, E.M. Mil et al. // Current Chemical Biology. – 2020. – 14(3). – pp. 203–215 DOI: 10.2174/2212796814999200907162619