biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 66:178-187, 2022 | DOI: 10.32615/bp.2022.008

24-epibrassinolide improved chilled tomato photosynthetic performance by stabilizing electron transport chain and function of photosystem II

W.-H. HU*, X.-H. HU, C. LIU, B.-Q. WANG, X.-H. YAN
School of Life Sciences, Jinggangshan University, Ji'an, Jiangxi 343009, P.R. China

To explore the protective mechanisms of brassinosteroids in the chill-induced photoinhibition in tomato (Solanum lycopersicum), we studied the effect of foliar sprayed 24-epibrassinolide (EBR, 0.1µM) on the gas exchange, chlorophyll fluorescence characteristics, and chlorophyll a fluorescence transient in tomato seedlings under chilling stress (a temperature of 8 ℃ and an irradiance of 200 µmol m-2 s-1) for 4 d. Results showed that chilling significantly inhibited CO2 assimilation and induced photoinhibition of photosystem II (PS II). However, photosystem I (PS I) was relatively tolerant to chilling stress, which was due to the downregulation of PS II activity and increase of cyclic electron transport around PS I (CEF). Chilling led to the inactivation of PS II reaction centers (RCs) and blocked the electron transport at the PS II acceptor side, but did not affect the oxygen-evolving complex (OEC) on the donor side of PS II. Exogenous EBR could alleviate chill-induced PS II photoinhibition mainly by the increase of CO2 assimilation and thermal dissipation of excitation energy in the PS II antennae, while the protective effect of CEF was relatively smaller. This study demonstrated that EBR maintained the stability of the electron transport chain and the function of PS II in chilled tomatoes. EBR promoted the absorption (ABS/CS), trapping (TRo/CS), and electron transport (ETo/CS) per leaf area in tomatoes under chilling stress, which was due to increasing the density of active reaction centers (RC/CS), rather than the activity of active RCs.

Keywords: 24-epibrassinolide, chilling stress, electron transport chain, photosynthesis, Solanum lycopersicum.

Received: September 26, 2021; Revised: February 6, 2022; Accepted: February 25, 2022; Published online: July 29, 2022  Show citation

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HU, W.-H., HU, X.-H., LIU, C., WANG, B.-Q., & YAN, X.-H. (2022). 24-epibrassinolide improved chilled tomato photosynthetic performance by stabilizing electron transport chain and function of photosystem II. Biologia plantarum, 66, Article 178-187. https://doi.org/10.32615/bp.2022.008
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    References

    1. Ahammed, G.J., Li, X., Liu, A., Chen, S.: Brassinosteroids in plant tolerance to abiotic stress. - J. Plant Growth Regul. 39: 1451-1464, 2020. Go to original source...
    2. Allen, D.J., Ort, D.R.: Impacts of chilling temperatures on photosynthesis in warm-climate plants. - Trends Plant Sci. 6: 36-42, 2001. Go to original source...
    3. Anwar, A., Liu, Y., Dong, R., Bai, L., Yu, X., Li, Y.: The physiological and molecular mechanism of brassinosteroid in response to stress: a review. - Biol. Res. 51: 46, 2018. Go to original source...
    4. Artuso, A., Guidi, L., Soldatini, G.F., Pardossi, A., Tognoni, F.: The influence of chilling on photosynthesis and activities of some enzymes of sucrose metabolism in Lycopersicon esculentum Mill. - Acta Physiol. Plant. 22: 95-101, 2000. Go to original source...
    5. Ashraf, M., Harris, P.J.C.: Photosynthesis under stressful environments: an overview. - Photosynthetica 51: 163-190, 2013. Go to original source...
    6. Behnamnia, M., Kalantari, K.M., Rezanejad, F.: Exogenous application of brassinosteroid alleviates drought-induced oxidative stress in Lycopersicon esculentum L. - Gen. appl. Plant Physiol. 35: 22-34, 2009.
    7. Bertamini, M., Muthuchelian, K., Rubinigg, M., Zorer, R., Nedunchezhian, N.: Photoinhibition of photosynthesis in leaves of grapevine (Vitis vinifera L. cv. Riesling). Effect of chilling nights. - Photosynthetica 43: 551-557, 2005. Go to original source...
    8. Brüggemann, W., Klaucke, S., Maas-Kantel, K.: Long-term chilling of young tomato plants under low light. V. kinetic and molecular properties of two key enzymes of the Calvin cycle in Lycopersicon esculentum Mill and L. peruvianum Mill. - Planta 194: 160-168, 1994. Go to original source...
    9. Caffagni, A., Pecchioni, N., Francia, E., Pagani, D., Milc, J.: Candidate gene expression profiling in two contrasting tomato cultivars under chilling stress. - Biol. Plant. 58: 283-295, 2014. Go to original source...
    10. Che, X., Ding, R., Li, Y., Zhang, Z., Gao, H., Wang, W.: Mechanism of long-term toxicity of CuO NPs to microalgae. - Nanotoxicology 12: 923-939, 2018. Go to original source...
    11. Chen, S., Strasser, R.J., Qiang, S.: In vivo assessment of effect of phytotoxin tenuazonic acid on PS II reaction centers. - Plant Physiol. Biochem. 84: 10-21, 2014. Go to original source...
    12. Cui, L., Cao, K., Zou, Z.: Effects of exogenous 24-epibrassinolide on photosynthesis and ATP synthase B subunit of tomato under low temperature/poor light. - Pak. J. Bot. 49: 57-62, 2017.
    13. Cui, L., Zou, Z., Zhang, J., Zhao, Y., Yan, F.: 24-epibrassinolide enhances plant tolerance to stress from low temperatures and poor light intensities in tomato (Lycopersicon esculentum Mill.). - Funct. integr. Genomics 16: 29-35, 2016. Go to original source...
    14. Ding, F., Wang, M., Zhang, S., An, X.: Changes in SBPase activity influence photosynthetic capacity, growth, and tolerance to chilling stress in transgenic tomato plants. - Sci. Rep. 6: 32741, 2016. Go to original source...
    15. Fang, P.P., Yan, M.Y., Chi, C., Wang, M.Q., Zhou, Y.H., Zhou, J., Shi, K., Xia, X.J., Foyer, C.H., Yu, J.Q.: Brassinoteroids act as a positive regulator of photoprotection in response to chilling stress. - Plant Physiol. 180: 2061-2076, 2019. Go to original source...
    16. Guo, Y., Liu, W., Wang, H., Wang, X., Chen, S.: Action mode of the mycotoxin patulin as a novel natural photosystem II inhibitor. - J. Agr. Food Chem. 69: 7313-7323, 2021. Go to original source...
    17. 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. Go to original source...
    18. Hu, W.H., Wu, Y., Zeng, J.Z., He, L., Zeng, Q.M.: Chill-induced inhibition of photosynthesis was alleviated by 24-epibrassinolide pretreatment in cucumber during chilling and subsequent recovery. - Photosynthetica 48: 537-544, 2010. Go to original source...
    19. Hu, W.H., Yan, X.H., Xiao, Y.A., Zeng, J.J., Qi, H.J., Ogweno, J.Q.: 24-Epibrassinolide alleviate drought-induced inhibition of photosynthesis in CaPS Icum annuum. - Sci. Hort. 150: 232-237, 2013. Go to original source...
    20. Hu, W.H., Zhou, Y.H., Du, Y.S., Xia, X.J., Yu, J.Q.: Differential response of photosynthesis in greenhouse- and field-ecotypes of tomato to long-term chilling under low light. - J. Plant Physiol. 163: 1238-1246, 2006. Go to original source...
    21. Huang, W., Yang, Y.J., Hu, H., Zhang, S.B.: Moderate photoinhibition of photosystem II protects photosystem I from photodamage at chilling stress in tobacco leaves. - Front. Plant Sci. 7: 182, 2016. Go to original source...
    22. Huang, W., Zhang, S.B., Cao, K.F.: The different effects of chilling stress under moderate light intensity on photosystem II compared with photosystem I and subsequent recovery in tropical tree species. - Photosynth. Res. 103: 175-182, 2010. Go to original source...
    23. Huang, W., Zhang, S.B., Cao, K.F.: Cyclic electron flow plays an important role in photoprotection of tropical trees illuminated at temporal chilling temperature. - Plant Cell Physiol. 52: 297-305, 2011. Go to original source...
    24. Jiang, D.X., Chu, X., Li, M. Hou, J.J., Chen, G.X.: Exogenous spermidine enhances salt-stressed rice photosynthetic performance by stabilizing structure and function of chloroplast and thylakoid membranes. - Photosynthetica 58: 61-71, 2002. Go to original source...
    25. Kee, S.C., Martin, B., Ort, D.R.: The effects of chilling in the dark and in the light on photosynthesis of tomato: electron transfer reactions. - Photosynth. Res. 8: 41-51, 1986. Go to original source...
    26. Kolomeichuk, L.V., Efimova, M.V., Zlobin, I.E., Kreslavski, V.D., Murgan, O.K., Kovtun, I.S., Khripach, V.A., Kuznetsov, V.V., Allakhverdiev, S.I.: 24-epibrassinolide alleviates the toxic effects of NaCl on photosynthetic processes in potato plants. - Photosynth. Res. 146: 151-163, 2020. Go to original source...
    27. Krishna, P.: Brassinoteroid-mediated stress responses. - J. Plant Growth Regul. 22: 289-297, 2003. Go to original source...
    28. Lang, J., Barták, M., Hájek, J., Váczi, P., Zikmundová, B.: Chilling effects on primary photosynthetic processes in Medicago sativa: acclimatory changes after short- and long-term exposure to low temperatures. - Biologia 75: 1105-1114, 2020. Go to original source...
    29. Li, J., Yang, P., Gan, Y., Yu, J., Xie, J.: Brassinosteroid alleviates chilling-induced oxidative stress in pepper by enhancing antioxidation systems and maintenance of photosystem II. - Acta Physiol. Plant. 37: 222, 2015. Go to original source...
    30. Li, J.W., Zhang, S.-B.: Differences in the responses of photosystems I and II in Cymbidium siense and C. tracyanum to long-term chilling stress. - Front. Plant Sci. 6: 1097, 2015. Go to original source...
    31. Li, Q., Chen, L.S., Jiang, H.X., Tang, N., Lin, A.H., Yang, G.H.: Effects of manganese-excess on CO2 assimilation, ribulose-1,5-bisphosphate carboxylase/oxygenase, carbohydrates and photosynthetic electron transport of leaves, and antioxidant systems of leaves and roots in Citrus grandis seedlings. - BMC Plant Biol. 10: 42, 2010. Go to original source...
    32. Mlinarić, S., Cesar, V., Lepeduą, H.: Antioxidative response and photosynthetic regulatory mechanisms in common fig leaves after short-term chilling stress. - Ann. appl. Biol. 178: 315-327, 2021. Go to original source...
    33. Mumtaz, M.A., Munir, S., Liu, G., Chen, W., Wang, Y., Yu, H., Mahmood, S., Ahiakpa, J.K., Tamim, S.A., Zhang, Y.: Altered brassinolide sensitivity1 transcriptionally inhibits chlorophyll synthesis and photosynthesis capacity in tomato. - Plant Growth Regul. 92: 417-426, 2020. Go to original source...
    34. Munekage, Y., Hashimoto, M., Miyake, C., Tomizawa, K.I., Endo, T., Tasaka, M., Shikanai, T.: Cyclic electron flow around photosystem I is essential for photosynthesis. - Nature 429: 579-582, 2004. Go to original source...
    35. 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, 2007. Go to original source...
    36. Ort, D.R., Baker, N.R.: A photoprotective for O2 as an alternative electron sink in photosynthesis. - Curr. Opin. Plant Biol. 5: 193-198, 2002. Go to original source...
    37. Park, E.J., Jeknić, Z., Sakamoto, A., DeNoma, J., Yuwansiri, R., Murata, N., Chen, T.H.H.: Genetic engineering of glycinebetaine synthesis in tomato protects seeds, plants, and flowers from chilling damage. - Plant J. 40: 474-487, 2004. Go to original source...
    38. Qian, T., Zheng, X., Yang, J., Xu, Y., Lu, S.: Optimal utilization of light energy in semiclosed greenhouse using three-dimensional cucumber model. - Sci. Programming Towards a Smart World 2020: 8855063, 2020. Go to original source...
    39. Saibo, N.J.M., Lourenço, T., Oliveira, M.M.: Transcription factors and regulation of photosynthetic and related metabolism under environmental stresses. - Ann. Bot. 103: 609-623, 2009. Go to original source...
    40. Sasse, J.M.: Physiological actions of brassinosteroids: an update. - J. Plant Growth Regul. 22: 276-288, 2003. Go to original source...
    41. Sharma, I., Ching, E., Saini, S., Bhardwaj, R., Pati, P.K.: Exogenous application of brassinosteroid offers tolerance to salinity by altering stress responses in rice variety Pusa Basmati-1. - Plant Physiol. Biochem. 69: 17-26, 2013. Go to original source...
    42. Shu, S., Tang, Y., Yuan, Y., Sun, J., Zhong, M., Guo, S.: The role of 24-epibrassinolide in the regulation of photosynthetic characteristics and nitrogen metabolism of tomato seedlings under a combined low temperature and weak light stress. - Plant Physiol. Biochem. 107: 344-353, 2016. Go to original source...
    43. Strasser, R.J., Tsimilli-Michael, M., Srivastava, A.: Analysis of the chlorophyll a fluorescence transient. - In: Pagageorgiou G.C., Govindjee (ed.): Chlorophyll Fluorescence: A Signature of Photosynthesis. Pp. 321-362. Kluwer Academic Publishers, Dordrecht 2004. Go to original source...
    44. Strasser, R.J., Srivastava, A., Govindjee: Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteria. - Photochem. Photobiol. 61: 32-42, 1995. Go to original source...
    45. Sun, Y., He, Y., Irfan, A.R., Liu, X., Yu, Q., Zhang, Q., Yang, D.: Exogenous brassinolide enhances the growth and cold resistance of maize (Zea mays L.) seedlings under chilling stress. - Agronomy 10: 488, 2020. Go to original source...
    46. Taiz, L., Zeiger, E.: Plant Physiology. 5th Edition. Sinauer Associates, Sunderland 2010.
    47. Takagi, D., Amako, K., Hashiguchi, M., Fukaki, H., Ishizaki, K., Goh, T., Fukao, Y., Sano, R., Kurata, T., Demura, T., Sawa, S., Miyake, C.: Chloroplastic ATP synthase builds up a proton motive force preventing production of reactive oxygen species in photosystem I. - Plant J. 91: 306-324, 2017. Go to original source...
    48. Takahashi, S., Badger, M.R.: Photoprotection in plants: a new light on photosystem II damage. - Trends Plant Sci. 16: 1360-1385, 2011. Go to original source...
    49. Tang, X.D., An, B.Y., Cao, D.M., Xu, R., Wang, S.Y., Zhang, Z.D., Liu, X.J., Sun, X.G.: Improving photosynthetic capacity, alleviating photosynthetic inhibition and oxidative stress under low-temperature stress with exogenous hydrogen sulfide in blueberry seedlings. - Front. Plant Sci. 11: 108, 2020. Go to original source...
    50. Tsimilli-Michael, M.: Revisiting JIP-test: an educative review on concepts, assumptions, approximations, definitions and terminology. - Photosynthetica 57: 90-107, 2019.
    51. Wu, X.X., Ding, H.D., Chen, J.L., Zhu, Z.W., Zha, D.S.: Amelioration of oxidative damage in Solanum melongena seedlings by 24-epibrassinolide during chilling stress and recovery. - Biol. Plant. 59: 350-356, 2015. Go to original source...
    52. Xia, X.J., Huang, L.F., Zhou, Y.H., Mao, W.H., Shi, K., Wu, J.X., Asami, T., Chen, Z., Yu, J.Q.: Brassinosteroids promote photosynthesis and growth by enhancing activation of Rubisco and expression of photosynthetic genes in Cucumis sativus. - Planta 230: 1185-1196, 2009a. Go to original source...
    53. Xia, X.J., Wang, Y.J., Zhou, Y.H., Tao, Y., Mao, W.H., Shi, K., Asami, T., Chen, Z., Yu, J.Q.: Reactive oxygen species are involved in brassinosteroids-induced stress tolerance in Cucumis sativus. - Plant Physiol. 150: 801-814, 2009b. Go to original source...
    54. Xia, X.J., Zhou, Y., Ding, J., Shi, K., Asami, T., Chen, Z., Yu, J.: Induction of systemic stress tolerance by brassinosteroid in Cucumis sativus. - New Phytol. 191: 706-720, 2011. Go to original source...
    55. Xiao, F., Zhang, Y.L., Yang, Y.L., Zhang, W.F.: Downregulation of PS II activity and increased cyclic electron transport in cotton prevents PS I from photoinhibition due to night chilling. - Photosynthetica 57: 523-532, 2019. Go to original source...
    56. Yamori, W., Sakata, N., Suzuki, Y., Shikanai, T., Makino, A.: Cyclic electron flow around photosystem I via chloroplast NAD(P)H dehydrogenase (NDH) complex performs a significant physiological role during photosynthesis and plant growth at low temperature in rice. - Plant J. 68: 966-976, 2011. Go to original source...
    57. Yamori, W., Shikanai, T.: Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth. - Annu. Rev. Plant Biol. 67: 81-106, 2016. Go to original source...
    58. Ye, Z.P.: A new model for relationship between irradiance and the rate of photosynthesis in Oryza sativa. - Photosynthetica 45: 637-640, 2007. Go to original source...
    59. 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. Go to original source...
    60. Yu, J.Q., Matsui, Y.: Effects of roots exudates and allelochemicals on ion uptake by cucumber seedlings. - J. chem. Ecol. 23: 817-827, 1997. Go to original source...
    61. Zhang, F.H., Lu, K., Gu, Y.Y., Zhang, L., Li, W.Y., Li, Z.: Effects of low-temperature stress and brassinolide application on the photosynthesis and leaf structure of tung tree seedlings. - Front. Plant Sci. 10: 1767, 2020a. Go to original source...
    62. Zhang, J.F., Li, J., Xie, J.M., Yu, J.H., Tang, C.N.: Changes in photosynthesis and carotenoid composition of pepper (CaPS Icum annuum L.) in response to low-light and low temperature combined with low-light stress. - Photosynthetica 58: 125-136, 2020b. Go to original source...
    63. Zhang, L.T., Xu, R., Liu, J.G.: Efficacy of botanical pesticide for rotifer extermination during the cultivation of NannochloroPS Is oculate probed by chlorophyll a fluorescence transient. - Photosynthetica 58: 156-162, 2020c. Go to original source...
    64. Zhang, Y.P., Zhu, X.H., Ding, H.D., Yang, S.J., Chen, Y.Y.: Foliar application of 24-epibrassinolide alleviates high-temperature-induced inhibition of photosynthesis in seedlings of two melon cultivars. - Photosynthetica 51: 341-349, 2013. Go to original source...
    65. Zhao, M., Yang, L., Wang, J., Xie, S., Zheng, Y., Nie, L., Zhu, S., Hou, J., Chen, G., Wang, C.: Transcriptome analysis reveals a positive effect of brassinosteroids on the photosynthetic capacity of wucai under low temperature. - BMC Genomics 20: 810, 2019. Go to original source...
    66. Zhao, Y., Yu, H., Zhou, J.M., Smith, S.M., Li, J.: Malate circulation: linking chloroplast metabolism to mitochondrial ROS. - Trends Plant Sci. 25: 446-454, 2020. Go to original source...
    67. 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. Go to original source...
    68. Zushi, K., Kajiwara, S., Matsuzoe, N.: Chlorophyll a fluorescence OJIP transient as a tool to characterize and evaluate response to heat and chilling stress in tomato leaf and fruit. - Sci. Hort. 148: 39-46, 2012. Go to original source...

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