Hort. Sci. (Prague), 2023, 50(2):159-173 | DOI: 10.17221/28/2022-HORTSCI

Long-term high temperature stress decreases the photosynthetic capacity and induces irreversible damage in chrysanthemum seedlingsOriginal Paper

Yuanda Zhang1,2, Zaiqiang Yang1*, Peijuan Wang2*, Chao Xu1
1 Collaborative Innovation Center on Forecast and Evaluation of Meteorological Disasters, Nanjing University of Information Science and Technology, Nanjing, Jiangsu Province, P.R. China
2 Chinese Academy of Meteorological Sciences, Beijing, P.R. China

To study the effects of long-term and short-term high temperature stress and recovery on the physiological functions and appearance quality of chrysanthemums, a controlled experiment with chrysanthemums was conducted. The treatments were 25 °C for 3 days (T1D3), 25 °C for 9 days (T1D9), 41 °C for 3 days (T2D3) and 41°C for 9 days (T2D9). The results indicated that there is no significant difference between the T1D3 and T1D9 groups. Conversely, the total chlorophyll content (Chl), net photosynthetic rate (PN), and maximum quantum yield of Photosystem II (PSII) (FV/FM) under T2D3 and T2D9 decreased by 27.07%, 43.30%, 5.62%, and 44.85%, 68.22%, 8.29%, respectively. The JIP-test results showed that the T2D9-stressed plants had a lower efficiency and functional antenna size, and a higher activity of the reaction centre than T2D3. The contents of malondialdehyde, soluble protein and proline increased by 3.67 nmol/g FM, 298.75 μg/g, and 192.99 μg/g, and the antioxidant enzymes activities were inhibited significantly under T2D9. After the stress was relieved, Chl, PN, and FV/FM under T2D3 recovered to the same level as T1D3, while T2D9 did not. Furthermore, the diameter of the flowers in T2D3 showed no significant difference with the chrysanthemums under T1D3. However, the plants in T2D9 recovered poorly. Both the diameter of the flowers and the anthocyanin under T2D9 reduced significantly comparing with T1D9, indicating that the damage in the chrysanthemum seedlings caused by long-term high temperature was irreversible.

Keywords: Antioxidant enzymes; chlorophyll fluorescence; heat stress; photosynthesis; reactive oxygen species

Accepted: April 12, 2023; Prepublished online: April 12, 2023; Published: June 16, 2023  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
Zhang Y, Yang Z, Wang P, Xu C. Long-term high temperature stress decreases the photosynthetic capacity and induces irreversible damage in chrysanthemum seedlings. Hort. Sci. (Prague). 2023;50(2):159-173. doi: 10.17221/28/2022-HORTSCI.
Share...
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)
    • Open full article

    References

    1. Aebi H. (1984): Catalase in vitro. Methods in Enzymology, 105: 121. Go to original source... Go to PubMed...
    2. Allen D.J., Ort D.R. (2001): Impacts of chilling temperatures on photosynthesis in warm-climate plants. Trends in Plant Science, 6: 36-42. Go to original source... Go to PubMed...
    3. Andrews J.R., Fryer M.J., Baker N.R. (1995): Characterization of chilling effects on photosynthetic performance of maize crops during early season growth using chlorophyll fluorescence. Journal of Experimental Botany, 46: 1195-1203. Go to original source...
    4. Arnon D.I. (1949): Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology, 24: 1-15. Go to original source... Go to PubMed...
    5. Baker N.R. (2008): Chlorophyll fluorescence: A probe of photosynthesis in vivo. Annual Review of Plant Biology, 59: 89-113. Go to original source... Go to PubMed...
    6. Begara-Morales J.C., Sánchez-Calvo B., Chaki M., Valderrama R., Mata-Pérez C., Padilla M.N., Corpas F.J., Barroso J.B. (2017): Antioxidant systems are regulated by nitric oxide-mediated post-translational modifications (NO-PTMs). Frontiers in Plant Science, 7: 152. Go to original source... Go to PubMed...
    7. Berry J.A., Bjorkman O. (2003): Photosynthetic response and adaptation to temperature in higher plants. Annual Review of Plant Physiology, 31: 491-543. Go to original source...
    8. Camejo D., Rodriguez P., Morales A., Dell'Amico J.M., Torrecillas A., Alarcon J.J. (2005): High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility. Journal of Plant Physiology, 162: 281-289. Go to original source... Go to PubMed...
    9. Cao L., Jin X.J., Zhang Y.X. (2019): Melatonin confers drought stress tolerance in soybean (Glycine max L.) by modulating photosynthesis, osmolytes, and reactive oxygen metabolism. Photosynthetica, 57: 812-819. Go to original source...
    10. Cheng X.F., Wang L., Nie L.J., Li Y.H. (2018): Chlorophyll fluorescence characteristics and antioxidant enzyme activities of chrysanthemum leaves under low temperature stress. Journal of Henan Agricultural Sciences, 47: 104-108.
    11. Cho A.R., Kim Y.J. (2021): Night temperature determines flowering time and quality of Chrysanthemum morifolium during a high day temperature. The Journal of Horticultural Science & Biotechnology, 96: 1-10. Go to original source...
    12. Chumber M., Jhanji S. (2022): Morpho-physiological and biochemical characterization of chrysanthemum varieties for early flowering under heat stress. South African Journal of Botany, 146: 603-613. Go to original source...
    13. Crafts-Brandner S.J., Law R.D. (2000): Effect of heat stress on the inhibition and recovery of the ribulose-1,5-bisphosphate carboxylase/oxygenase activation state. Planta, 212: 67-74. Go to original source... Go to PubMed...
    14. Crafts-Brandner S.J., Salvucci M.E. (2000): Rubisco activase constrains the photosynthetic potential of leaves at high temperature and CO2. Proceedings of the National Academy of Sciences of The United States of America, 97: 13430-13435. Go to original source... Go to PubMed...
    15. Dhindsa R.S., Plumb-Dhinsa P., Thorpe T.A. (1981): Leaf senescence: Correlation with increased levels of membrane permeability and lipid peroxidation and increased levels of superoxide dismutase and catalase. Journal of Experimental Botany, 32: 93-101. Go to original source...
    16. Farquhar G.D., Sharkey T.D. (1982): Stomatal conductance and photosynthesis. Annual Review of Plant Physiology, 33: 317-345. Go to original source...
    17. Fracheboud Y., Haldimann P., Leipner J., Stamp.P. (1999): Chlorophyll fluorescence as a selection tool for cold tolerance of photosynthesis in maize (Zea mays L.). Journal of Experimental Botany, 50: 1533-1540. Go to original source...
    18. Gerganova M., Popova A.V., Stanoeva D., Velitchkova M. (2017): Tomato plants acclimate better to elevated temperature and high light than to treatment with each factor separately. Plant Physiology and Biochemistry, 104: 234-241. Go to original source... Go to PubMed...
    19. Gill S.S., Tuteja N. (2010): Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry, 48: 909-930. Go to original source... Go to PubMed...
    20. Havaux M. (1993): Characterization of thermal damage to the photosynthetic electron transport system in potato leaves. Plant Science, 94: 19-33. Go to original source...
    21. Huh E.J., Shin H.K., Kim K.J., Choi S.Y. (2004): High temperature-induced flower abnormalities at bud development in chrysanthemum. Horticulture Environment and Biotechnology, 45: 345-348.
    22. Jiang Y., Huang B. (2001): Drought and heat stress injury to two cool-season turfgrasses in relation to antioxidant metabolism and lipid peroxidation. Crop Science, 41: 436-442. Go to original source...
    23. Jurczyk B., Grzesiak M., Pociecha E., Wlazło M., Rapacz M. (2019): Diverse stomatal behaviors mediating photosynthetic acclimation to low temperatures in Hordeum vulgare. Frontiers in Plant Science, 9: 1963. Go to original source... Go to PubMed...
    24. Kadir S., Sidhu G., Al-Khatib K. (2006): Strawberry (Fragaria × ananassa Duch.) growth and productivity as affected by temperature. HortScience, 41: 1423-1430. Go to original source...
    25. Kalaji H.M., Jajoo A., Oukarroum A., Brestic M., Zivcak M., Samborska I.A., Cetner M.D., Lukasik I., Goltsev V., Ladle R.J. (2017): Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiologiae Plantarum, 38: 102. Go to original source...
    26. Kalaji H.M., Baba W., Gediga K., Goltsev V., Samborska I.A., Cetner M.D., Dimitrova S., Piszcz U., Bielecki K., Karmowska K., Dankov K., Kompala-Baba A. (2018): Chlorophyll fluorescence as a tool for nutrient status identification in rapeseed plants. Photosynthesis Research, 136: 329-343. Go to original source... Go to PubMed...
    27. Kaushik D., Aryadeep R. (2014): Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Frontiers in Environmental Science, 2: 53. Go to original source...
    28. Kim M., Choi Y. (2017): A study on characteristics and changes of persistent extreme temperature events in summer and winter seasons over the Republic of Korea. Journal of Climate Research, 12: 305-320. Go to original source...
    29. Kishor P.B.K., Hong Z., Miao G.-H., Chein-An A.H., Desh Pal S.V. (1995): Overexpression of Δ1-pyrroline-5-carboxylate synthetase increases proline production and confers osmotolerance in transgenic plants. Plant Physiology, 108: 1387-1394. Go to original source... Go to PubMed...
    30. Kwak S.S., Kim S.K., Lee M.S., Jung K.H., Park I.H., Liu J.R. (1995): Acidic peroxidases from suspension-cultures of sweet potato. Phytochemistry, 39: 981-984. Go to original source...
    31. Larcher W. (1995): Photosynthesis as a tool for indicating temperature stress events. Chapter 13. In: Schulze E.-D., Caldwell M.M. (eds.): Ecophysiology of Photosynthesis. Springer Berlin Heidelberg, Springer: 261-277. Go to original source...
    32. Li J.J., Yang Z.Q. (2021): Establishment of critical nitrogen model and nitrogen nutrition diagnosis of tomato under high temperature stress. Chinese Journal of Agrometeorology, 42: 44-55.
    33. Li J.J., Yang Z.Q., Wei T.T., Huang Q.Q., Ding Y.H. (2020): Effects of high temperature and different air humidity on stomatal characteristics for tomato leaves. Northern Horticulture, 44: 23-31.
    34. Liu Y.N., Xu Q.Z., Li W.C., Yang X.H., Zheng Q., Li B., Li Z.S., Li H.W. (2019): Long-term high light stress induces leaf senescence in wheat (Triticum aestivum L.). Photosynthetica, 57: 830-840. Go to original source...
    35. Long Y.Y., Su Z.Y., Jiang Y.H., Zhang Y., Xu R.H., Yang Z.Q. (2022): The effects of low temperature and weak light on the photosynthetic characteristics of chrysanthemum and the determination of its disaster index. Chinese Journal of Ecology, 41: 1731-1739.
    36. Lu S.Y., Yang Z.Q., Zhang Y.D., Zheng H., Yang L. (2020): Effect of photoperiod on fluorescence characteristics of photosynthetic system of fresh-cut chrysanthemum leaves under high temperature. Chinese Journal of Agrometeorology, 41: 632-643.
    37. Lu T., Meng Z., Zhang G., Qi M., Sun Z., Liu Y., Li T. (2017): Sub-high temperature and high light intensity induced irreversible inhibition on photosynthesis system of tomato plant (Solanum lycopersicum L.). Frontiers in Plant Science, 8: 365. Go to original source... Go to PubMed...
    38. Luo J., Yang Z.Q., Yang L., Yuan C.H., Zhang F.Y., Li Y.C., Li C.Y. (2022): Establishment of an estimation model for chlorophyll content of strawberry leaves under high temperature conditions at seedling stage based on hyperspectral parameters. Chinese Journal of Agrometeorology, 43: 832-845.
    39. Mathur S., Allakhverdiev S.I., Jajoo A. (2011): Analysis of high temperature stress on the dynamics of antenna size and reducing side heterogeneity of Photosystem II in wheat leaves (Triticum aestivum). Biochimica et Biophysica Acta, 1807: 22-29. Go to original source... Go to PubMed...
    40. Maxwell K., Johnson G. (2000): Chlorophyll fluorescence - a practical guide. Journal of Experimental Botany, 51: 659-668. Go to original source...
    41. Mittler R. (2017): ROS are good. Trends in Plant Science, 22: 11-19. Go to original source... Go to PubMed...
    42. Munné-Bosch S., Pintó-Marijuan M. (2017): Free radicals, oxidative stress and antioxidants. In: Thomas B., Murphy D.J., Murray B.G. (eds.): Encyclopedia of Applied Plant Sciences. 2nd Ed. Amsterdam, Elsevier Academic: 16-19. Go to original source...
    43. Nakano Y., Takase T., Sumitomo K., Suzuki S., Tsuda-Kawamura K., Hisamatsu T. (2020): Delay of flowering at high temperature in chrysanthemum: Duration of darkness and transitions in lighting determine daily peak heat sensitivity. The Horticulture Journal, 89: 255. Go to original source...
    44. Nozaki K., Fukai S. (2008): Effects of high temperature on floral development and flowering in spray chrysanthemum. Journal of Applied Horticulture, 10: 8-14. Go to original source...
    45. Oren-Shamir M., Nissim-Levi A. (1999): Temperature and gibberellin effects on growth and anthocyanin pigmentation in Photinia leaves. Journal of Horticultural Science and Biotechnology, 74: 355-360. Go to original source...
    46. Pinto-Marijuan M., Munne-Bosch S. (2014): Photo-oxidative stress markers as a measure of abiotic stress-induced leaf senescence: advantages and limitations. Journal of Experimental Botany, 65: 3845-3857. Go to original source... Go to PubMed...
    47. Salvucci M.E., Osteryoung K.W., Crafts-Brandner S.J., Vierling E. (2001): Exceptional sensitivity of rubisco activase to thermal denaturation in vitro and in vivo. Plant Physiology, 127: 1053-1064. Go to original source...
    48. Sánchez F., Manzanares M., Andres E., Tenorio J.L., Ayerbe L. (1998): Turgor maintenance, osmotic adjustment and soluble sugar and proline accumulation in 49 pea cultivars in response to water stress. Field Crops Research (Netherlands), 59: 225-235. Go to original source...
    49. Seliem M.K., Hafez Y.M., El-Ramady H. (2020): Using nano-selenium in reducing the negative effects of high temperature stress on Chrysanthemum morifolium Ramat. Journal of Sustainable Agricultural Sciences, 46: 47-59. Go to original source...
    50. Shaked-Sachray L., Weiss D., Reuveni M., Nissim-Levi A., Oren-Shamir M. (2002): Increased anthocyanin accumulation in aster flowers at elevated temperatures due to magnesium treatment. Physiologia Plantarum, 114: 559-565. Go to original source... Go to PubMed...
    51. Shi J.Q., Liu Y.Q., Wang Y.L., Yang Z.Q. (2022): Effects of nitrogen application on fluorescence characteristics of cucumber in fruit growth stage under high temperature stress. Acta Agriculurae Boreali-Sinica, 37: 84-95.
    52. Singh S.P., Singh P. (2015): Effect of temperature and light on the growth of algae species: A review. Renewable and Sustainable Energy Reviews, 50: 431-444. Go to original source...
    53. Strasser R.J., Srivastava A., Tsimilli-Michael M. (2000): The fluorescence transient as a tool to characterize and screen photosynthetic samples. Chapter 25. In: Probing Photosynthesis Mechanisms Regulation & Adaptation. London, Taylor & Francis: 443-480.
    54. Su Z.Y., Yang Z.Q., Long Y.Y., Zhang Y., Jiang Y.H., Xu R.H. (2022): Effect of light supplementation frequency on photosynthetic characteristics of tomato seedling leaves under weak light. Chinese Journal of Agrometeorology, 43: 720-731.
    55. Sun X., Guo J., Zheng C. (2013): Study on heat damage and vegetative recovery of chrysanthemum. Journal of Shandong Agricultural University ( Natural Science), 44: 6-11.
    56. Takahashi S., Murata N. (2008): How do environmental stresses accelerate photoinhibition? Trends in Plant Science, 13: 178-182. Go to original source... Go to PubMed...
    57. Tsikas D. (2017): Assessment of lipid peroxidation by measuring malondialdehyde (MDA) and relatives in biological samples: Analytical and biological challenges. Analytical Biochemistry, 524: 13-30. Go to original source... Go to PubMed...
    58. Whitham S., Dinesh-Kumar S.P., Choi D., Hehl R., Corr C., Baker B. (1994): The product of the tobacco mosaic virus resistance gene N: Similarity to toll and the interleukin-1 receptor. Cell, 78: 1101-1115. Go to original source... Go to PubMed...
    59. Xu C., Yang Z., Wang M., Zhang X., Zheng Q., Li J., Huang H., Wang L., Zou Y. (2019): Effects of low temperature on photosynthesis and antioxidant enzyme activities of panax notoginseng during seeding stage. International Journal of Agriculture and Biology, 21: 1279-1286.
    60. Xu C., Gao R., Wang M.T., Yang Z.Q., Han W., Zheng S.H. (2020a): Fuzzy comprehensive evaluation and model establishment of the effect of high temperature in the seedling stage on the nutritional quality of strawberry fruit. Chinese Journal of Agrometeorology, 41: 785-793.
    61. Xu C., Wang M.T., Yang Z.Q., Han W., Zheng S.H. (2020b): Effect of high temperature in seedling stage on phenological stage of strawberry and its simulation. Chinese Journal of Agrometeorology, 41: 644-654.
    62. Xu C., Wang M.T., Yang Z.Q., Zheng Q.T. (2020c): Low temperature and low irradiation induced irreversible damage of strawberry seedlings. Photosynthetica, 58: 156-164. Go to original source...
    63. Xu C., Shen M.Y., Wang M.T., Yang Z.Q., Han W., Zheng S.H. (2021a): Modification of strawberry dry matter accumulation model under short-term high temperature conditions at seedling stage. Chinese Journal of Agrometeorology, 42: 572-582.
    64. Xu C., Wang M.T., Yang Z.Q., Han W., Zheng S.H. (2021b): Effects of high temperature on photosynthetic physiological characteristics of strawberry seedlings in greenhouse and construction of stress level. Chinese Journal of Applied Ecology, 32: 231-240.
    65. Xue S.J., Yang Z.Q., Li J. (2018): Effect of high-temperature on the quality of pakchoi and its simulation. Chinese Journal of Eco-Agriculture, 25: 1042-1051.
    66. Yamamoto Y., Kai S., Ohnishi A., Tsumura N., Ishikawa T., Hori H., Morita N., Ishikawa Y. (2014): Quality control of PSII: Behavior of PSII in the highly crowded grana thylakoids under excessive light. Plant and Cell Physiology, 55: 1206-1215. Go to original source... Go to PubMed...
    67. Yang L., Yang Z.Q., Chen J.J., Huang C.R. (2022): The distribution of high temperature and high humidity disasters for facility tomato in Fujian Province. Chinese Journal of Ecology, 41: 1149-1155.
    68. Yang Z.Q., Xu C., Wang M.T., Zhao H.L., Umutoni M.A. (2019): Enhancing the thermotolerance of tomato seedlings by heat shock treatment. Photosynthetica, 57: 1184-1192. Go to original source...
    69. Yang L., Yang Z.Q., Zhang Y.D., Zheng H., Lu S.Y. (2020): Mechanism analysis on photosynthetic attenuation in chrysanthemum leaves under low light condition. Chinese Journal of Agrometeorology, 41: 707-718.
    70. Yusuf M.A., Kumar D., Rajwanshi R., Strasser R.J., Tsimilli-Michael M., Govindjee, Sarin N.B. (2010): Overexpression of γ-tocopherol methyl transferase gene in transgenic Brassica juncea plants alleviates abiotic stress: Physiological and chlorophyll a fluorescence measurements. Biochimica et Biophysica Acta (BBA) - Bioenergetics, 1797: 1428-1438. Go to original source... Go to PubMed...
    71. Zhang F.Y., Yang Z.Q., Yang L., Luo J., Li Y.C., Li C.Y. (2022): Effects of high temperature and humidity on photosynthetic characteristics and protective enzyme activities of cucumber leaves at seedling stage. Northern Horticulture, 16: 1-8.
    72. Zhang S., Zhang D., Xu X., Liao Y., Shen S., Yin D. (2005): Study on the mechanism and forecasting method of high temperature disaster in summer in the large cities of the Yangtze River Basin. Journal of Nanjing Institude of Meteorology, 28: 840-846.
    73. Zhang Y., Yang Z., Lu S., Yang L., Zheng H. (2021): Response of photosynthetic characteristics of leaves of protected chrysanthemum variety "Jinbeidahong" to high temperature stress. Northen Horticulture, 6: 72-80.
    74. Zhang Z., Zhu L., Song A., Wang H., Chen S., Jiang J., Chen F. (2020): Chrysanthemum (Chrysanthemum morifolium) CmICE2 conferred freezing tolerance in Arabidopsis. Plant Physiology and Biochemistry, 146: 31-41. Go to original source... Go to PubMed...
    75. Zheng H., Wang D., Yang Z.Q., Zhang Y.D., Lu S.Y., Yang L. (2021): Effects of high temperature and humidity on photosynthetic characteristics and protective enzyme activities of cucumber leaves in greenhouse. Northern Horticulture, 45: 48-55.
    76. Zhou Y., Zhu S., Hua J., Liu Y., Xiang J., Ding W. (2018): Spatio-temporal distribution of high temperature heat wave in Nanjing. Journal of Geo-information Science, 20: 1613-1621.

    This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.


    Return to the content