Biologia plantarum 65:265-272, 2021 | DOI: 10.32615/bp.2021.025
Respiration responses of wheat seedlings to treatment with trehalose under heat stress
- 1 Equipment Sharing Platform of School of Life Sciences, East China Normal University, Shanghai 200241, P.R. China
- 2 Crop Research Institute, Shandong Academy of Agricultural Sciences/National Engineering Laboratory for Wheat and Maize/Key Laboratory of Wheat Biology and Genetic Improvement in North Yellow and Huai River Valley, Ministry of Agriculture, Jinan 250100, P.R. China
Heat stress limits wheat production and trehalose can improve stress tolerance. How trehalose affects wheat respiration is unclear. In this study, we investigated the effects of exogenous trehalose on the respiration of wheat seedlings during heat stress and the subsequent recovery period. Trehalose pretreatment significantly increased the expression of the alternative oxidase genes AOX1a and AOX1c under heat stress, indicating that trehalose pretreatment increased the capacity of the alternative respiration pathway (AP) in response to heat stress. Trehalose pretreatment also enhanced the activity of the malate-oxaloacetate (Mal-OAA) shuttle and ameliorated the decrease in photosynthetic activity caused by heat stress. However, when the AP was inhibited by salicylhydroxamic acid under heat stress, both Mal-OAA shuttle activity and photosynthetic efficiency were substantially reduced in the control and trehalose pretreatment groups. In addition, trehalose pretreatment helped to maintain inner mitochondrial respiratory activity and the activity of Complex II during heat stress, particularly the coupling of oxidative phosphorylation with the Complex II electron transport chain, thereby mitigating heat-related damage to the cytochrome pathway (CP). Taken together, these results suggest that exogenous trehalose enhanced the AP and reduced damage to the CP under heat stress in wheat seedlings, thus maintaining cellular energy metabolism. Up-regulation of the AP by trehalose pretreatment may improve the heat tolerance of wheat seedlings by dissipating excess reducing equivalents transported through the Mal-OAA shuttle, thereby protecting photosynthetic performance.
Keywords: alternative respiration pathway, heat stress, malate-oxaloacetate shuttle, photosynthetic efficiency, trehalose, Triticum aestivum, wheat.
Received: December 16, 2020; Revised: April 26, 2021; Accepted: April 30, 2021; Published online: September 25, 2021 Show citation
| ACS | AIP | APA | ASA | Harvard | Chicago | Chicago Notes | IEEE | ISO690 | MLA | NLM | Turabian | Vancouver |
Supplementary files
| Download file | 6656_Luo_Suppl.pdf File size: 188.16 kB |
References
- Abdallah, M.M.-S., Abdelgawad, M.Z.A., El-Bassiouny, H.M.S.: Alleviation of the adverse effects of salinity stress using trehalose in two rice varieties. - S. Afr. J. Bot. 103: 275-282, 2016.
Go to original source... - Almeselmani, M., Viswanathan, P.S.D.: Effects of prolonged high temperature stress on respiration, photosynthesis and gene expression in wheat (Triticum aestivum L.) varieties differing in their thermotolerance. - Plant Stress 6: 25-32, 2012.
- Bartoli, C.G., Gomez, F., Gergoff, G., Guiamét, J.J., Puntarulo, S.: Up-512 regulation of the mitochondrial alternative oxidase pathway enhances 513 photosynthetic electron transport under drought conditions. - J. exp. Bot. 53: 1269-1276, 2005.
Go to original source... - Bradford, M.M.: Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. - Anal. Biochem. 72: 248-254, 1976.
Go to original source... - Dinakar, C., Vishwakarma, A., Raghavendra, A.S., Padmasree, K.: Alternative oxidase pathway optimizes photosynthesis during osmotic and temperature stress by regulating cellular ROS, malate valve and antioxidative systems. - Front. Plant Sci. 7: 68, 2016.
Go to original source... - Dutilleul, C., Driscoll, S., Cornic, G., De Paepe, R., Foyer, C.H., Noctor, G.: Functional mitochondrial complex I is required by tobacco leaves for optimal photosynthetic performance in photorespiratory conditions and during transients. - Plant Physiol. 131: 264-275, 2003.
Go to original source... - Erdal, S., Genisel, M., Turk, H., Dumlupinar, R., Demir, Y.: Modulation of alternative oxidase to enhance tolerance against cold stress of chickpea by chemical treatments. - J. Plant Physiol. 175: 95-101, 2015.
Go to original source... - Hoefnagel, M.H.N., Atkin, O.K., Wiskich, J.T.: Interdependence between chloroplasts and mitochondria in the light and the dark. - BBA - Bioenergetics 1366: 235-255, 1998.
Go to original source... - Jin, S.B.: Wheat varieties and their in distribution in China. 1st Ed. - China Agriculture Press, Beijing 1983.
- Kramer, D.M., Johnson, G., Kiirats, O., Edwards, G.E.: New fluorescence parameters for the determination of QA redox state and excitation energy fluxes. - Photosynth. Res. 79: 209, 2004.
Go to original source... - Lei, T., Sun, X., Dai, Q.-L., Zhang, F., Liang, H.-G., Lin, H.-H.: The alternative pathway in cucumber seedlings under low temperature stress was enhanced by salicylic acid. - Plant Growth Regul. 60: 35-42, 2010.
Go to original source... - Liu, M.J., Sun, X.J., Zhang, Z.S., Liu, Y.T., Gao, H.Y.: Quantitative research of plant mitochondrial respiration state and its application in plant biology. - Plant Physiol. 50: 111-116, 2014.
- Luo, Y., Li, F., Wang, G.P., Yang, X.H., Wang, W.: Exogenously-supplied trehalose protects thylakoid membranes of winter wheat from heat-induced damage. - Biol. Plant. 54: 495-501, 2010.
Go to original source... - Luo, Y., Li, W.M., Wang, W.: Trehalose: protector of antioxidant enzymes or reactive oxygen species scavenger under heat stress? - Environ. exp. Bot. 63: 378-384, 2008.
Go to original source... - Meng, X., Zhang, Z., Gao, H.Y., Yang, C., Meng, Q.W.: Temperature rise enhances photoprotection in cucumber leaves via mitochondrial alternative oxidase (AOX) pathway. - J. Plant. Physiol. 49: 63-69, 2013.
- Millar, A.H., Leaver, C.J.: The cytotoxic lipid peroxidation product, 4-hydroxy-2-nonenal, specifically inhibits decarboxylating dehydrogenases in the matrix of plant mitochondria. - FEBS Lett. 481: 117-121, 2000.
Go to original source... - Møller, I.M.: Plant mitochondria a oxidative stress: electron transport, NADPH turnover, and metabolism of reactive oxygen species. - Annu. Rev. Plant. Physiol. Plant. mol. Biol. 52: 561-591, 2001.
Go to original source... - Noguchi, K., Yoshida, K. Interaction between photosynthesis and respiration in illuminated leaves. - Mitochondrion 8: 87-99, 2008.
Go to original source... - Rurek, M., Woyda-Ploszczyca, A.M., Jarmuszkiewicz, W.: Biogenesis of mitochondria in cauliflower (Brassica oleracea var. botrytis) curds subjected to temperature stress and recovery involves regulation of the complexome, respiratory chain activity, organellar translation and ultrastructure. - BBA 1847: 399, 2015.
Go to original source... - Sampedro, J.G., Cortés, P., Muñoz-Clares, R.A., Fernández, A., Uribe, S.: Thermal inactivation of the plasma membrane H+-ATPase from Kluyveromyces lactis. Protection by trehalose. - BBA 1544: 64-73, 2001.
Go to original source... - Schluepmann, H., Van, D.A., Aghdasi, M., Wobbes, B., Paul, M., Smeekens, S.: Trehalose mediated growth inhibition of Arabidopsis seedlings is due to trehalose-6-phosphate accumulation. - Plant. Physiol. 135: 879-890, 2004.
Go to original source... - Schreiber, U. Pulse-Amplitude-Modulation (PAM) Fluorometry and Saturation Pulse Method: An Overview. - Springer, Dordrecht 2004.
- Valenti, D., Vacca, R.A., De Pinto, M.C., De, G.L., Marra, E., Passarella, S.: In the early phase of programmed cell death in tobacco bright yellow 2 cells the mitochondrial adenine nucleotide translocator, adenylate kinase and nucleoside diphosphate kinase are impaired in a reactive oxygen species-dependent manner. - BBA 1767: 66-78, 2007.
Go to original source... - Vanlerberghe. G.C., McIntosh, L.: Alternative oxidase: from gene to function. - Annu. Rev. Plant. Physiol. Plant. mol. Biol. 48: 703-734, 1997.
Go to original source... - Wahid, A., Gelani, S., Ashraf, M., Foolad, M.R.: Heat tolerance in plants: an overview. - Environ. exp. Bot. 61: 199-223, 2007.
Go to original source... - Wang, F., Wang, X., Zhao, C., Wang, J., Li, P., Dou, Y., Bi, Y.: Alternative pathway is involved in the tolerance of highland barley to the low-nitrogen stress by maintaining the cellular redox homeostasis. - Plant Cell Rep. 35: 317-328, 2016.
Go to original source... - Yip, J.Y., Vanlerberghe, G.C.: Mitochondrial alternative oxidase acts to dampen the generation of active oxygen species during a period of rapid respiration induced to support a high rate of nutrient uptake. - Physiol. Plant. 112: 327-333, 2001.
Go to original source... - Yoshida, K., Terashima, I., Noguchi, K.: Up-regulation of mitochondrial alternative oxidase concomitant with chloroplast over-reduction by excess light. - Plant Cell Physiol. 48: 606, 2007.
Go to original source... - Zhang, L.T., Zhang, Z.S., Gao, H.Y., Meng, X.L., Yang, C., Liu, J.G., Meng, Q.W.: The mitochondrial alternative oxidase pathway protects the photosynthetic apparatus against photodamage in Rumex K-1 leaves. - BMC Plant Biol. 12: 40, 2012.
Go to original source... - Zhang, Y., Marcillat, O., Giulivi, C., Ernster, L., Davies, K.J. The oxidative inactivation of mitochondrial electron transport chain components and ATPase. - J. biol. Chem. 265: 16330, 1990.
Go to original source...



