Abstract
To investigate whether brassinosteroids (BRs) could be used to alleviate chill-induced inhibition of photosynthesis in cucumber (Cucumis sativus L) during chilling and subsequent recovery, the effects of exogenously applied 24-epibrassinolide (EBR) on gas exchange, chlorophyll fluorescence parameters, and antioxidant enzyme activity were studied. Cucumber plants were exposed to chilling under low light (12/8°C and 100 μmol m−2 s−1 PPFD) for 3 days and then recovered under normal temperature and high irradiance (28/18°C and 600 μmol m−2 s−1 PPFD) for 6 days. Chilling significantly decreased the net photosynthetic rate (P N) and stomatal conductance (g s), and increased rate of O2 ·− formation and H2O2 and malondialdehyde (MDA) content in cucumber leaves, but did not influence the optimal quantum yield of PSII (Fv/Fm). Chilling also decreased the effective quantum yield of PSII photochemistry (ΦPSII) and photochemical quenching (qP), but induced an increase in nonphotochemical quenching (NPQ), and the activities of superoxide dismutase (SOD) and ascorbate peroxidase (APX). High irradiance (600 μmol m−2 s−1) further aggravated the decrease in P N, g s, ΦPSII and qP, and enhanced the increase in reactive oxygen species (ROS) generation and accumulation in the first day of recovery after chilling. However, high irradiance induced a sharp decrease in Fv/Fm and NPQ, as well as the activities of SOD and APX on the first day of recovery. EBR pretreatment significantly alleviated chill-induced inhibition of photosynthesis during chilling stress and subsequent recovery period, which was mainly due to significant increases in g s, ΦPSII, qP and NPQ. EBR pretreatment also reduced ROS generation and accumulation, and increased the activities of SOD and APX during chilling and subsequent recovery. Those results suggest that EBR pretreatment alleviates the chill reduction in photosynthesis and accelerated the recovery rate mainly by increasing of the stomatal conductance, the efficiency of utilization and dissipation of leaf absorbed light, and the activity of the ROS scavenging system during chilling and subsequent recovery period.
Similar content being viewed by others
Abbreviations
- APX:
-
ascorbate peroxidase
- BRs:
-
brassinosteroids
- EBR:
-
24-epibrassinolide
- Fm′:
-
light-adapted maximum fluorescence
- Fo :
-
minimal fluorescence of dark-adapted state
- Fm :
-
maximal fluorescence of dark-adapted state
- Fv/Fm :
-
optimal quantum yield of PSII
- FM:
-
fresh mass
- g s :
-
stomatal conductance
- LT:
-
low temperature
- LTBR:
-
low temperature
- EBR:
-
pretreatment
- MDA:
-
malondialdehyde
- NT:
-
normal temperature
- NTBR:
-
normal temperature/EBR-pretreatment
- NPQ:
-
nonphotochemical quenching
- ΦPSII :
-
effective quantum yield of PSII photochemistry
- P N :
-
net photosynthetic rate
- PPFD:
-
photosynthetic photon flux density
- qP :
-
photochemical quenching coefficient
- Rubisco:
-
ribulose-1,5-bisphosphate carboxylase/oxygenase
- ROS:
-
reactive oxygen species
- SOD:
-
superoxide dismutase
References
Alam, B., Jacob, J.: Overproduction of photosynthetic electrons is associated with chilling injury in green leaves. — Photosynthetica 40: 91–95, 2002.
Ali, Q., Athar, H.R., Ashraf, M.: Modulation of growth, photosynthetic capacity and water relations in salt stressed wheat plants by exogenously applied 24-epibrassinolide. — Plant Growth Regul. 56: 107–116, 2008.
Allen, D.J., Ort, D.R.: Impact of chilling temperatures on photosynthesis in warm-climate plants. — Trends Plant Sci. 6: 36–42, 2001.
Allen, D.J., Ratner, K., Giller, Y.E., Gussakovsky, E.E., Shahak, Y., Ort, D.R.: An overnight chill induces a delayed inhibition of photosynthesis at midday in mango (Mangifera indica L.). — J. Exp. Bot. 51: 1893–1902, 2000.
Anuradha, S., Rao, S.S.R.: Application of brassinosteroids to rice seeds (Oryza sativa L.) reduced the impact of salt stress on growth, prevented photosynthetic pigment loss and increased nitrate reductase activity. — Plant Growth Regul. 40: 29–32, 2003.
Asada, K.: The water-water cycle in chloroplasts: Scavenging of active oxygens and dissipation of excess photos. — Ann. Rev. Plant Physiol. Plant Mol. Biol. 50: 601–639, 1999.
Barth, C., Krause, G.H.: Inhibition of photosystems I and II in chilling-sensitive and chilling-tolerant plants under light and low-temperature stress. — Z. Naturforsch. C. 54: 645–657, 1999.
Berry, J., Björkman, O.: Photosynthetic response and adaptation to temperature in higher plants. — Annu. Rev. Plant Physiol. Plant Mol. Biol. 31: 491–543, 1980.
Bradford, M.M.: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. — Anal. Biochem. 72: 248–254, 1976.
Brüggemann, W., van der Kooij, T.A.W., van Hasselt, P.R.: Long-term chilling of young tomato plants under low light and subsequent recovery. II. Chlorophyll fluorescence, carbon metabolism and activity of ribulose-1,5-bisphosphate carboxylase/oxygenase. — Planta 186: 179–187, 1992.
Demmig-Adams, B., Adams, W.W.,III, Barker, D.H., Logan, B.A., Bowling, D.R., Verhoeven, A.S.: Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation. — Physiol. Plant. 98: 253–264, 1996.
Ershova, A.N., Khripach, V.A: Effects of epibrassinolide on lipid peroxidation in Pisum sativum at normal aeration and under oxygen deficiency. — Russ. J. Plant Physiol. 43: 750–752, 1996.
Feng, Y.L., Cao, K.F.: Photosynthesis and photoinhibition after night chilling in seedlings of two tropical tree species grown under three irradiances. — Photosynthetica 43: 567–574, 2005.
Foyer, C.H., Lelandais, M., Kunert, K.J.: Photooxidative stress in plants. — Physiol. Plant. 92: 696–717, 1994.
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 Physiol. Biochem. 40: 659–668, 2002.
Giannopolitis, C.N., Ries, S.K.: Superoxide dismutase. I. Occurrences in higher plants. — Plant Physiol. 59: 309–414, 1977.
Hodges, D.M., DeLong, J.M., Forney, C.F., Prange, R.K.: Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidative in plant tissues containing anthocyanin and other interfering compounds. — Planta 207: 606–611, 1999.
Hu, W.H., Shi, K., Song, X.S., Xia, X.J., Zhou, Y.H., Yu, J.Q.: Different effects of chilling on respiration in leaves and roots of cucumber (Cucumis sativus). — Plant Physiol. Biochem. 44: 837–843, 2006.
Hu, W.H., Song, X.S., Shi, K., Xia, X.J., Zhou, Y.H., Yu, J.Q.: Changes in electron transport, superoxide dismutase and ascorbate peroxidase isoenzymes in chloroplasts and mitochondria of cucumber leaves as influenced by chilling. — Photosynthetica 46: 581–588, 2008.
Janda, T., Szalai, G., Páldi, E.: Chlorophyll fluorescence and anthocyanin content in chilled maize plants after return to a non-chilling temperature under various irradiances. — Biol. Plant. 38: 625–627, 1996.
Jung, S., Steffen, K.L., Lee, H.J.: Comparative photoinhibition of a high and a low altitude ecotype of tomato (Lycopersicon hirsutum) to chilling stress under high and low light condition. — Plant Sci. 134: 69–77, 1998.
Khripach, V., Zhabinskii, V., de Groot, A.: Twenty years of brassinosteroids: Steroidal plant hormones warrant better crops for the XXI century. — Ann. Bot. 86: 441–447, 2000.
Kościelniak, J., Biesaga-Kościelniak, J.: Photosynthesis and non-photochemical excitation quenching components of chlorophyll excitation in maize and field bean during chilling at different photon flux density. — Photosynthetica 44: 174–180, 2006.
Krishna, P.: Brassinoteroid-mediated stress responses. — J. Plant Growth Regul. 22: 289–297, 2003.
Li, L., van Staden, J., Jager, A.K.: Effects of plant growth regulators on the antioxidant system in seedlings of two maize cultivars subjected to water stress. — Plant Growth Regul. 25: 81–87, 1998.
Liu, Y.J., Zhao, Z.G., Si, J., Di, C.X., Han, J., An, L.Z.: 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.
Martin, B., Ort, D.R.: The recovery of photosynthesis in tomato subsequent to chilling exposure. — Photosynth. Res. 6: 121–132, 1985.
Mazzora, L.M., Núňez, M., Hechavarria, M., Coll, F., Sánchez-Blanco, M.J.: Influence of brassinosteroids on antioxidant enzyme activity in tomato under different temperatures. — Biol. Plant. 45: 593–596, 2002.
Mittler, R.: Oxidative stress, antioxidants and stress tolerance. — Trends Plant Sci. 7: 405–410, 2002.
Nakano, Y., Asada, K.: Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplast. — Plant Cell Physiol. 22: 876–880, 1981.
Ogweno, J.O., Song, X.S., Shi, K., Hu, W.H., Mao, W.H., Zhou, Y.H., Yu, J.Q., Nogués, S.: 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.
Ort, D.R., Baker, N.R.: A photoprotective role for O2 as an alternative electron sink in photosynthesis? — Curr. Opin. Plant Biol. 5: 193–198, 2002.
Powles, S.B.: Photoinhibition of photosynthesis induced by visible light. — Annu. Rev. Plant Physiol. Plant Mol. Biol. 35: 15–44, 1984.
Shahbaz, M., Ashraf, M., Athar, H.R.: Does exogenous application of 24-epibrassinolide ameliorate salt induced growth inhibition in wheat (Triticum aestivum L.)? — Plant Growth Regul. 55: 51–64, 2008.
Szalai, G., Janda, T., Paldi, E., Szigeti, Z.: Role of light in the development of post-chilling symptoms in maize. — J. Plant Physiol. 148: 378–383, 1996.
von Caemmerer, S., Farquhar, G.D.: Some relationships between the biochemistry of photosynthesis and the gas exchange of leaves. — Planta 153: 376–387, 1981.
Weng, J.-H., Jhaung, L.-H., Jiang, J.-Y., Lai, G.-M., Liao, T.-S.: Down-regulation of photosystem 2 efficiency and spectral reflectance in mango leaves under very low irradiance and varied chilling treatments. — Photosynthetica 44: 248–254, 2006.
Xia, X.J., Wang, Y.J., Zhou, Y.H., Tao, Y., Mao, W.H., Shi, K., Asami, T., Chen, Z.X., Yu, J.Q.: Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. — Plant Physiol. 150: 801–814, 2009.
Yu, J.Q., Huang, L.F., Hu, W.H., Zhou, Y.H., Mao, W.H., Ye, S.F., Nogués, S.: A role for brassinosteroids in the regulation of photosynthesis in Cucumis sativus. — J. Exp. Bot. 55: 1135–1143, 2004.
Yu, J.Q., Matsui, Y.: Effects of root exudates and allelochemicals on ion uptake by cucumber seedlings. — J. Chem. Ecol. 23: 817–827, 1997.
Yu, J.Q., Zhou, Y.H., Huang, L.F., Allen, D.J.: Chill-induced inhibition of photosynthesis: genotypic variation within Cucumis sativus. — Plant Cell Physiol. 43: 1182–1188, 2002a.
Yu, J.Q., Zhou, Y.H., Ye, S.F., Huang, L.F.: 24-epibrassinolide and abscisic acid protect cucumber seedling form chilling injury. — J. Hort. Sci. Biotechnol. 77: 430–473, 2002b.
Zhang, M.C., Zhai, Z.X., Tian, X.L., Duan, L.S., Li, Z.H.: Brassinolide alleviated the adverse effect of water deficits on photosynthesis and the antioxidant of soybean (Glycine max L.). — Plant Growth Regul. 56: 257–264, 2008.
Zhou, Y.H., Huang, L.F., Zhang, Y.L., Shi, K., Yu, J.Q., Nogués, S.: Chill-induced decrease in capacity of RuBP carboxylation and associated H2O2 accumulation in cucumber leaves are alleviated by grafting onto figleaf gourd. — Ann. Bot. 100: 839–848, 2007.
Zhou, Y.H., Yu, J.Q., Huang, L.F., Nogués, S.: The relationship between CO2 assimilation, photosynthetic electron transport and water-water cycle in chill-exposed cucumber leaves under low light and subsequent recovery. — Plant Cell Environ. 27: 1503–1514, 2004.
Acknowledgments
This work was supported by the National Key Technology R&D Program (2008BADA6B02), National Natural Science Foundation of China (30860175), Program for New Century Excellent Talents in University in the China (NCET-08-0703) and Natural Science Foundation of Jiangxi Province (2007GZN1666).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Hu, W.H., Wu, Y., Zeng, J.Z. et al. Chill-induced inhibition of photosynthesis was alleviated by 24-epibrassinolide pretreatment in cucumber during chilling and subsequent recovery. Photosynthetica 48, 537–544 (2010). https://doi.org/10.1007/s11099-010-0071-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11099-010-0071-y