Photosynthetica, 2014 (vol. 52), issue 1

Photosynthetica 2014, 52(1):96-104 | DOI: 10.1007/s11099-014-0010-4

24-epibrassinolide improves cucumber photosynthesis under hypoxia by increasing CO2 assimilation and photosystem II efficiency

Y. H. Ma1, S. R. Guo1,*
1 Key Laboratory of Southern Vegetable Crop Genetic Improvement, Ministry of Agriculture, College of Horticulture, Nanjing Agricultural University, Nanjing, China

Seedlings of the hypoxia-sensitive cucumber cultivar were hydroponically grown under hypoxia for 7 d in the presence or absence of 24-epibrassinolide (EBR, 2.1 nM). Hypoxia significantly inhibited growth, while EBR partially counteracted this inhibition. Leaf net photosynthetic rate (P N), stomatal conductance, transpiration rate, and water-use efficiency declined greatly, while the stomatal limitation value increased significantly. The maximum net photosynthetic rate was strongly reduced by hypoxia, indicating that stomatal limitation was not the only cause of the P N decrease. EBR markedly diminished the harmful effects of hypoxia on P N as well as on stomata openness. It also greatly stimulated CO2 fixation by the way of increasing the carboxylation capacity of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco), ribulose-1,5-bisphosphate regeneration, Rubisco activity, and the protection of Rubisco large subunit from degradation. Our data indicated that photosystem (PS) II was damaged by hypoxia, while EBR had the protective effect. EBR further increased nonphotochemical quenching that could reduce photodamage of the PSII reaction center. The proportion of absorbed light energy allocated for photochemical reaction (P) was reduced, while both nonphotochemical reaction dissipation of light energy and imbalanced partitioning of excitation energy between PSI and PSII increased. EBR increased P and alleviated this imbalance. The results suggest that both stomatal and nonstomatal factors limited the photosynthesis of cucumber seedlings under hypoxia. EBR alleviated the growth inhibition by improving CO2 asimilation and protecting leaves against PSII damage.

Keywords: brassinosteroids; chlorophyll content; CO2-response curve; light energy allocation; light-response curve; photosynthesis

Received: January 1, 2013; Accepted: May 20, 2013; Published: March 1, 2014Show citation

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Ma, Y.H., & Guo, S.R. (2014). 24-epibrassinolide improves cucumber photosynthesis under hypoxia by increasing CO2 assimilation and photosystem II efficiency. Photosynthetica, 52(1), 96-104. doi: 10.1007/s11099-014-0010-4.
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    References

    1. Bai, T.H., Li, C.Y., Li, C. et al.: Contrasting hypoxia tolerance and adaptation in Malus species is linked to differences in stomatal behavior and photosynthesis. - Physiol. Plantarum 147: 514-523, 2013. Go to original source...
    2. Bajguz, A., Hayat, S.: Effects of brassinosteroids on the plant responses to environmental stresses. - Plant Physiol. Biochem. 47: 1-8, 2009. Go to original source...
    3. Bertolde, F.Z., Almeida, A.-A.F., Pirovani, C.P. et al.: Physiological and biochemical responses of Theobroma cacao L. genotypes to flooding. - Photosynthetica 50: 447-457, 2012. Go to original source...
    4. Braun, G., Evron, Y., Malkin, S., Avron, M.: Proton flow through the ATP synthase in chloroplasts regulates the distribution of light energy between PS I and PS II. - FEBS Lett. 280: 57-60, 1991. Go to original source...
    5. Danon, A.: Environmentally-induced oxidative stress and its signaling. - In: EatonRye, J.J., Tripathy, B.C., Sharkey, T.D. (ed.): Advances in Photosynthesis and Respiration. Pp. 319-330. Springer, Dordrecht 2012. Go to original source...
    6. Ershova, A.N., Khripach, V.A.: Effect of epibrassinolide on lipid peroxidation in Pisum sativum at normal aeration and under oxygen deficiency. - Russ J. Plant Physiol. 43: 750-752, 1996.
    7. Fariduddin, Q., Yusuf, M., Chalkoo, S. et al.: 28-homobrassinolide improves growth and photosynthesis in Cucumis sativus L. through an enhanced antioxidant system in the presence of chilling stress. - Photosynthetica 49: 55-64, 2011. Go to original source...
    8. Gray, G.R., Savitch, L.V., Ivanov, A.G. et al.: Photosystem II excitation pressure and development of resistance to photoinhibition. (II. Adjustment of photosynthetic capacity in winter wheat and winter rye). - Plant Physiol. 110: 61-71, 1996. Go to original source...
    9. Havaux, M., Kloppstech, K.: The protective functions of carotenoid and flavonoid pigments against excess visible radiation at chilling temperature investigated in Arabidopsis npq and tt mutants. - Planta 213: 953-966, 2001. Go to original source...
    10. Hildbrand, M., Fischer, A., Feller, U.: Protein catabolism in bean leaf-disks - accumulation of a soluble fragment of ribulose-1,5-bisphosphate carboxylase/oxygenase under oxygen deficiency. - J. Exp. Bot. 45: 1197-1204, 1994. Go to original source...
    11. Holá, D.: Brassinosteroids and photosynthesis. - In: Hayat, S., Ahamad, A. (ed.): Brassinosteroids: A Class of Plant Hormone. Pp. 143-192. Springer, New York 2011. Go to original source...
    12. Hussain, M.I., Reigosa, M.J.: Allelochemical stress inhibits growth, leaf water relations, PSII photochemistry, nonphotochemical fluorescence quenching, and heat energy dissipation in three C3 perennial species. - J. Exp. Bot. 62: 4533-4545, 2011. Go to original source...
    13. Ivanov, A.G., Hurry, V., Sane, P.V. et al: Reaction centre quenching of excess light energy and photoprotection of photosystem II. - J. Plant Biol. 51: 85-96, 2008. Go to original source...
    14. Janeczko, A., Kocielniak, J., Pilipowicz, M. et al.: Protection of winter rape photosystem 2 by 24-epibrassinolide under cadmium stress. - Photosynthetica 43: 293-298, 2005. Go to original source...
    15. Jans, W.W.P., Dibor, L., Verwer, C. et al.: Effects of light and soil flooding on the growth and photosynthesis of ramin (Gonystylus bancanus) seedlings in Malaysia. - J. Tropic. Forest Sci. 24: 54-63, 2012.
    16. Jia, Y.X., Sun, J., Wang, L.P. et al: [Thermal dissipation pathway in cucumber seedling leaves under hypoxia stress.] - Chin. J. Appl. Ecol. 22: 707-712, 2011. [In Chinese]
    17. Jiang, Y.P., Cheng, F., Zhou, Y.H. et al: Brassinosteroid-induced CO2 assimilation is associated with increased stability of redox-sensitive photosynthetic enzymes in the chloroplasts in cucumber plants. - Biochem. Bioph. Res. Co. 426: 390-394, 2012. Go to original source...
    18. Kang, Y.Y., Guo, S.R., Li, J. et al.: Effect of root applied 24-epibrassinolide on carbohydrate status and fermentative enzyme activities in cucumber (Cucumis sativus L.) seedlings under hypoxia. - Plant Growth Regul. 57: 259-269, 2009. Go to original source...
    19. Kumutha, D., Ezhilmathi, K., Sairam, R.K. et al.: Waterlogging induced oxidative stress and antioxidant activity in pigeonpea genotypes. - Biol. Plantarum 53: 75-84, 2009. Go to original source...
    20. Ladygin, V.G.: The effect of root hypoxia and iron deficiency on the photosynthesis, biochemical composition, and structure of pea chloroplasts. - Russ. J. Plant Physiol. 51: 28-40, 2004. Go to original source...
    21. Li, X.-G., Meng, Q.-W., Jiang, G.-Q. Zou, Q.: The susceptibility of cucumber and sweet pepper to chilling under low irradiance is related to energy dissipation and water-water cycle. - Photosynthetica 41: 259-265, 2003. Go to original source...
    22. Lichtenthaler, H.K., Gitelson, A., Lang, M.: Non-destructive determination of chlorophyll content of leaves of a green and an aurea mutant of tobacco by reflectance measurements. - J. Plant Physiol. 148: 483-493, 1996. Go to original source...
    23. Liu, Y.J., Zhao, Z.G., Si, J. et al.: Brassinosteroids alleviate chilling-induced oxidative damage by enhancing antioxidant defense system in suspension cultured cells of Chorispora bungeana. - Plant Growth Regul. 59: 207-214, 2009. Go to original source...
    24. Long, S.P., Bernacchi, C.J.: Gas exchange measurements, what can they tell us about the underlying limitations to photosynthesis? Procedures and sources of error. - J. Exp. Bot. 54: 2393-2401, 2003. Go to original source...
    25. Morard, P., Lacoste, L., Silvestre, J.: Effect of oxygen deficiency on mineral nutrition of excised tomato roots. - J. Plant Nutr. 27: 613-626, 2004. Go to original source...
    26. Nishiyama, Y., Yamamoto, H., Allakhverdiev, S.I. et al.: Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. - EMBO J. 20: 5587-5594, 2001. Go to original source...
    27. Ogweno, J.O., Song, X.S., Shi, K. et al.: Brassinosteroids alleviate heat-induced inhibition of photosynthesis by increasing carboxylation efficiency and enhancing antioxidant systems in Lycopersicon esculentum. - J. Plant Growth Regul. 27: 49-57, 2008. Go to original source...
    28. Olivella, C., Biel, C., Sevé, R., Vendrell, M.: Hormonal and physiological responses of Gerbera jamesonii to flooding stress. - HortScience 35: 222-225, 2000. Go to original source...
    29. Pezeshki, S.R.: Responses of bald cypress (Taxodium-distichum) seedlings to hypoxia: leaf protein content, ribulose-1,5-bisphosphate carboxylase/oxygenase activity and photosynthesis. - Photosynthetica 30: 59-68, 1994.
    30. Piñol, R., Simón, E.: Effect of 24-epibrassinolide on chlorophyll fluorescence and photosynthetic CO2 assimilation in Vicia faba plants treated with the photosynthesis-inhibiting herbicide terbutryn. - J. Plant Growth Regul. 28: 97-105, 2009. Go to original source...
    31. Sairam, R.K., Kumutha, D., Ezhilmathi, K. et al.: Physiology and biochemistry of waterlogging tolerance in plants. - Biol. Plantarum 52: 401-412, 2008. Go to original source...
    32. Schreiber, U., Bilger, W., Hormann, H., Neubauer, C.: Chlorophyll fluorescence as a diagnostic tool: Basics and some aspects of practical relevance. - In: Raghavendra, A.S. (ed.): Photosynthesis: a Comprehensive Treatise. Pp. 320-336. Cambridge University Press, Cambridge 1998.
    33. Smethurst, C.F., Garnett, T., Shabala, S.: Nutritional and chlorophyll fluorescence responses of lucerne (Medicago sativa) to waterlogging and subsequent recovery. - Plant Soil 270: 31-45, 2005. Go to original source...
    34. Takahashi, S., Murata, N.: How do environmental stresses accelerate photoinhibition? - Trends Plant Sci. 13: 178-182, 2008. Go to original source...
    35. Tournaire-Roux, C., Sutka, M., Javot, H. et al.: Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. - Nature 425: 393-397, 2003. Go to original source...
    36. Xia, X.-J., Huang, L.-F., Zhou, Y.-H. et al.: Brassinosteroids promote photosynthesis and growth by enhancing activation of Rubisco and expression of photosynthetic genes in Cucumis sativus. - Planta 230: 1185-1196, 2009. Go to original source...
    37. Yu, J.Q., Huang, L.F., Hu, W.H. et al.: A role for brassinosteroids in the regulation of photosynthesis in Cucumis sativus, - J. Exp. Bot. 55: 1135-1143, 2004. Go to original source...
    38. Yuan, L.Y., Shu, S., Sun, J., Guo, S.R. et al.: Effects of 24-epibrassinolide on the photosynthetic characteristics, antioxidant system, and chloroplast ultrastructure in Cucumis sativus L. under Ca(NO3)2 stress. - Photosynth. Res. 112: 205-214, 2012. Go to original source...

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