Photosynthetica 2023, 61(2):177-189 | DOI: 10.32615/ps.2022.039

Moderate photoinhibition of PSII and oxidation of P700 contribute to chilling tolerance of tropical tree species in subtropics of China

V.S.J. SUNOJ1, Y. WEN1, A. JAJOO2, A.W. SHORT1, 3, W.H. ZENG1, N.I. ELSHEERY4, K.F. CAO1
1 State Key Laboratory for Conservation and Utilization of Subtropical Agri-Bioresources and Guangxi Key Laboratory of Forest Ecology and Conservation, College of Forestry, Guangxi University, 530004 Nanning, Guangxi, China
2 School of Life Science, Devi Ahilya University, 452017 Indore, India
4 Department of Agricultural Botany, Tanta University, 72513 Tanta, Egypt
3 Institute of Ecology and Evolution, University of Oregon, Eugene, OR 97403, USA

In the subtropics, a few tropical tree species are distributed and planted for ornamental and horticultural purposes; however, the photosynthesis of these species can be impaired by chilling. This study aimed to understand how these species respond to chilling. Light-dependent and CO2 assimilation reactions of six tropical tree species from geographically diverse areas, but grown at a lower subtropical site in China, were monitored during a chilling (≤ 10°C). Chilling induced stomatal and nonstomatal effects and moderate photoinhibition of PSII, with severe effect in Ixora chinensis. Woodfordia fruticosa was little affected by chilling, with negligible reduction of photosynthesis and PSII activity, higher cyclic electron flow (CEF), and oxidation state of P700 (P700+). Photoinhibition of PSII thus reduced electron flow to P700, while active CEF reduced oxidative damage of PSI and maintained photosynthesis during chilling. Studied parameters revealed that coupling between light-dependent and CO2 assimilation reactions was enhanced under chilling.

Additional key words: chilling; cyclic electron flow; oxidation of P700; photoinhibition; photosynthesis.

Received: May 19, 2022; Revised: June 27, 2022; Accepted: August 9, 2022; Prepublished online: September 15, 2022; Published: June 6, 2023  Show citation

ACS AIP APA ASA Harvard Chicago Chicago Notes IEEE ISO690 MLA NLM Turabian Vancouver
SUNOJ, V.S.J., WEN, Y., JAJOO, A., SHORT, A.W., ZENG, W.H., ELSHEERY, N.I., & CAO, K.F. (2023). Moderate photoinhibition of PSII and oxidation of P700 contribute to chilling tolerance of tropical tree species in subtropics of China. Photosynthetica61(SPECIAL ISSUE 2023/1), 177-189. doi: 10.32615/ps.2022.039
Download citation

Supplementary files

Download fileSunoj_2928_supplement.docx

File size: 650.21 kB

References

  1. Agrawal D., Allakhverdiev S.I., Jajoo A.: Cyclic electron flow plays an important role in protection of spinach leaves under high temperature stress. - Russ. J. Plant Physiol. 63: 210-215, 2016. Go to original source...
  2. Allakhverdiev S.I.: Recent progress in the studies of structure and function of photosystem II. - J. Photoch. Photobio. B 104: 1-8, 2011. Go to original source...
  3. 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...
  4. Allen D.J., Ratner K., Giller Y.E. et al.: An overnight chill induces a delayed inhibition of photosynthesis at midday in mango (Mangifera indica L.). - J. Exp. Bot. 51: 1893-902, 2000. Go to original source...
  5. Asada K.: Production and scavenging of reactive oxygen species in chloroplasts and their functions. - Plant Physiol. 141: 391-396, 2006. Go to original source...
  6. Baker N.R., Harbinson J., Kramer D.M.: Determining the limitations and regulation of photosynthetic energy transduction in leaves. - Plant Cell Environ. 30: 1107-1125, 2007. Go to original source...
  7. 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. 54c: 645-657, 1999. Go to original source...
  8. Belgio E., Kapitonova E., Chmeliov J. et al.: Economic photoprotection in photosystem II that retains a complete light-harvesting system with slow energy traps. - Nat. Commun. 5: 4433, 2014. Go to original source...
  9. Bukhov N.G., Carpentier R.: Heterogeneity of photosystem II reaction centers as influenced by heat treatment of barley leaves. - Physiol. Plantarum 110: 279-285, 2000. Go to original source...
  10. Derks A., Schaven K., Bruce D.: Diverse mechanisms for photoprotection in photosynthesis. Dynamic regulation of photosystem II excitation in response to rapid environmental change. - BBA-Bioenergetics 1847: 468-485, 2015. Go to original source...
  11. Elsheery N.I., Sunoj V.S.J., Wen Y. et al.: Foliar application of nanoparticles mitigates the chilling effect on photosynthesis and photoprotection in sugarcane. - Plant Physiol. Bioch. 149: 50-60, 2020. Go to original source...
  12. Elsheery N.I., Wilske B., Cao K.F.: The effect of night chilling on gas exchange and chlorophyll fluorescence of two mango cultivars growing under two irradiances. - Acta Bot. Yunnan. 30: 447-456, 2008. Go to original source...
  13. Elsheery N.I., Wilske B., Zhang J.L., Cao K.F.: Seasonal variations in gas exchange and chlorophyll fluorescence in the leaves of five mango cultivars in southern Yunnan, China. - J. Hortic. Sci. Biotech. 82: 855-862, 2007. Go to original source...
  14. Foyer C.H., Shigeoka S.: Understanding oxidative stress and antioxidant functions to enhance photosynthesis. - Plant Physiol. 155: 93-100, 2011. Go to original source...
  15. Gao S., Wang G.: The enhancement of cyclic electron flow around photosystem I improves the recovery of severely desiccated Porphyra yezoensis (Bangiales, Rhodophyta). - J. Exp. Bot. 12: 4349-4358, 2012. Go to original source...
  16. Genty B., Briantais J.M., Baker N.R.: The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. - BBA-Gen. Subjects 990: 87-92, 1989. Go to original source...
  17. Gratani L., Catoni R., Varone L.: Morphological, anatomical and physiological leaf traits of Q. ilex, P. latifolia, P. lentiscus, and M. communis and their response to Mediterranean climate stress factors. - Bot. Stud. 54: 35, 2013. Go to original source...
  18. Guidi L., Lo Piccolo E., Landi M.: Chlorophyll fluorescence, photoinhibition and abiotic stress: Does it make any difference the fact to be a C3 or C4 species? - Front. Plant Sci. 10: 174, 2019. Go to original source...
  19. Huang W., Hu H., Zhang S.: Photosynthesis and photosynthetic electron flow in the alpine evergreen species Quercus guyavifolia in winter. - Front. Plant Sci. 7: 1511, 2016b. Go to original source...
  20. Huang W., Quan X., Zhang S.B., Liu T.: In vivo regulation of proton motive force during photosynthetic induction. - Environ. Exp. Bot. 148: 109-116, 2018. Go to original source...
  21. Huang W., Yang Y.J., Hu H. et al.: Sustained diurnal stimulation of cyclic electron flow in two tropical tree species Erythrophleum guineense and Khaya ivorensis. - Front. Plant Sci. 7: 1068, 2016a. Go to original source...
  22. Huang W., Zhang S.B., Cao K.F.: Stimulation of cyclic electron flow during recovery after chilling-induced photoinhibition of PSII. - Plant Cell Physiol. 51: 1922-1928, 2010a. Go to original source...
  23. 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, 2010b. Go to original source...
  24. 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...
  25. Huang W., Zhang S.B., Xu J.C., Liu T.: Plasticity in roles of cyclic electron flow around photosystem I at contrasting temperatures in the chilling-sensitive plant Calotropis gigantea. - Environ. Exp. Bot. 141: 145-153, 2017. Go to original source...
  26. Huang W., Zhang S.B., Zhang J.L., Hu H.: Photoinhibition of photosystem I under high light in the shade-established tropical tree species Psychotria rubra. - Front. Plant Sci. 6: 801, 2015. Go to original source...
  27. Jalili A., Jamzad Z., Thompson K. et al.: Climate change, unpredictable cold waves and possible brakes on plant migration. - Global Ecol. Biogeogr. 19: 642-648, 2010. Go to original source...
  28. Joliot P., Johnson G.N.: Regulation of cyclic and linear electron flow in higher plants. - P. Natl. Acad. Sci. USA 108: 13317-13322, 2011. Go to original source...
  29. Joliot P., Joliot A.: Cyclic electron flow in C3 plants. - BBA-Bioenergetics 1757: 362-368, 2006. Go to original source...
  30. Jurczyk B., Grzesiak M., Pociecha E. et al.: Diverse stomatal behaviors mediating photosynthetic acclimation to low temperatures in Hordeum vulgare. - Front. Plant Sci. 9: 1963, 2019. Go to original source...
  31. Kadota K., Furutani R., Makino A. et al.: Oxidation of P700 induces alternative electron flow in photosystem I in wheat leaves. - Plants-Basel 8: 152, 2019. Go to original source...
  32. Khatoon M., Inagawa K., Pospí¹il P. et al.: Quality control of photosystem II: Thylakoid unstacking is necessary to avoid further damage to the D1 protein and to facilitate D1 degradation under light stress in spinach thylakoids. - J. Biol. Chem. 284: 25343-25352, 2009. Go to original source...
  33. Klughammer C., Schreiber U.: An improved method, using saturating light pulses, for the determination of photosystem-I quantum yield via P700+ absorbance changes at 830 nm. - Planta 192: 261-268, 1994. Go to original source...
  34. Klughammer C., Schreiber U.: Complementary PSII quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the Saturation Pulse method. - PAM Appl. Notes 1: 27-35, 2008.
  35. Kono M., Terashima I.: Elucidation of photoprotective mecha­nisms of PSI against fluctuating light photoinhibition. - Plant Cell Physiol. 57: 1405-1414, 2016. Go to original source...
  36. Körner C.: Plant adaptation to cold climates. - F1000Research 5: 2769, 2016. Go to original source...
  37. Kou J., Takahashi S., Oguchi R. et al.: Estimation of the steady-state cyclic electron flux around PSI in spinach leaf discs in white light, CO2-enriched air and other varied conditions. - Funct. Plant Biol. 4: 1018-1028, 2013. Go to original source...
  38. 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: 209-218, 2004. Go to original source...
  39. Kubo S., Masumura T., Saito Y. et al.: Cyclic electron flow around PSI functions in the photoinhibited rice leaves. - Soil Sci. Plant Nutr. 57: 105-113, 2011. Go to original source...
  40. Li Y., Liu J., Zhou G. et al.: Warming effects on photosynthesis of subtropical tree species: a translocation experiment along an altitudinal gradient. - Sci. Rep.-UK 6: 24895, 2016. Go to original source...
  41. Li Y., Sunoj V.S.J., Short A.W. et al.: Correlations between allocation to foliar phosphorus fractions and maintenance of photosynthetic integrity in six mangrove populations as affected by chilling. - New Phytol. 232: 2267-2282, 2021. Go to original source...
  42. Liu X., Zhou Y., Xiao J., Bao F.: Effects of chilling on the structure, function and development of chloroplasts. - Front Plant Sci. 9: 1715, 2018. Go to original source...
  43. Mathur S., Sunoj V.S.J., Elsheery N.I. et al.: Regulation of photosystem II heterogeneity and photochemistry in two cultivars of C4 crop sugarcane under chilling stress. - Front. Plant Sci. 12: 627012, 2021. Go to original source...
  44. Mau A.C., Reed S.C., Wood T.E., Cavaleri M.A.: Temperate and tropical forest canopies are already functioning beyond their thermal thresholds for photosynthesis. - Forests 9: 47, 2018. Go to original source...
  45. Maxwell K., Johnson G.N.: Chlorophyll fluorescence - a practical guide. - J. Exp. Bot. 51: 659-668, 2000. Go to original source...
  46. Miyake C.: Alternative electron flows (water-water cycle and cyclic electron flow around PSI) in photosynthesis: Molecular mechanisms and physiological functions. - Plant Cell Physiol. 51: 1951-1963, 2010. Go to original source...
  47. Miyake C.: Molecular mechanism of oxidation of P700 and suppression of ROS production in photosystem I in response to electron-sink limitations in C3 plants. - Antioxidants 9: 230, 2020. Go to original source...
  48. Miyake C., Horiguchi S., Makino A. et al.: Effects of light intensity on cyclic electron flow around PSI and its relationship to non-photochemical quenching of Chl fluorescence in tobacco leaves. - Plant Cell Physiol. l46: 1819-1830, 2005b. Go to original source...
  49. Miyake C., Miyata M., Shinzaki Y., Tomizawa K.: CO2 response of cyclic electron flow around PSI (CEF-PSI) in tobacco leaves: Relative electron fluxes through PSI and PSII determine the magnitude of non-photochemical quenching (NPQ) of Chl fluorescence. - Plant Cell Physiol. 46: 629-637, 2005a. Go to original source...
  50. Miyake C., Shinzaki Y., Miyata M., Tomizawa K.: Enhancement of cyclic electron flow around PSI at high light and its contribution to the induction of non-photochemical quenching of Chl fluorescence in intact leaves of tobacco plants. - Plant Cell Physiol. 45: 1426-1433, 2004. Go to original source...
  51. Mohanty P., Allakhverdiev S.I., Murata N.: Application of low temperatures during photoinhibition allows characterization of individual steps in photodamage and the repair of photosystem II. - Photosynth. Res. 94: 217-224, 2007. Go to original source...
  52. Müller P., Li X.-P., Niyogi K.K.: Non-photochemical quenching. A response to excess light energy. - Plant Physiol. 125: 1558-1566, 2001. Go to original source...
  53. Murata N., Allakhverdiev S.I., Nishiyama Y.: The mechanism of photoinhibition in vivo: Re-evaluation of the roles of catalase, α-tocopherol, non-photochemical quenching, and electron transport. - BBA-Bioenergetics 1817: 1127-1133, 2012. Go to original source...
  54. Murata N., Takahashi S., Nishiyama Y., Allakhverdiev S.I.: Photoinhibition of photosystem II under environmental stress. - BBA-Bioenergetics 1767: 414-421, 2007. Go to original source...
  55. Murchie E.H., Niyogi K.K.: Manipulation of photoprotection to improve plant photosynthesis. - Plant Physiol. 155: 86-92, 2011. Go to original source...
  56. Neto M.C.L., Cerqueira J.V.A., da Cunha J.R. et al.: Cyclic electron flow, NPQ and photorespiration are crucial for the establishment of young plants of Ricinus communis and Jatropha curcas exposed to drought. - Plant Biol. 19: 650-659, 2017. Go to original source...
  57. Oxborough K., Baker N.R.: Resolving chlorophyll a fluorescence images of photosynthetic efficiency into photochemical and non-photochemical components - calculation of qP and Fv'/Fm' without measuring Fo'. - Photosynth. Res. 54: 135-142, 1997. Go to original source...
  58. Raven J.A.: Speedy small stomata? - J. Exp. Bot. 65: 1415-1424, 2014. Go to original source...
  59. Rutherford A.W., Krieger-Liszkay A.: Herbicide-induced oxidative stress in photosystem II. - Trends Biochem. Sci. 26: 648-653, 2001. Go to original source...
  60. Rymbai H., Laxman R.H., Dinesh M.R. et al.: Diversity in leaf morphology and physiological characteristics among mango (Mangifera indica) cultivars popular in different agro-climatic regions of India. - Sci. Hortic.-Amsterdam 176: 189-193, 2014. Go to original source...
  61. Shaku K., Shimakawa G., Hashiguchi M., Miyake C.: Reduction-induced suppression of electron flow (RISE) in the photosynthetic electron transport system of Synechococcus elongatus PCC 7942. - Plant Cell Physiol. 57: 1443-1453, 2016. Go to original source...
  62. Shimakawa G., Miyake C.: Oxidation of P700 ensures robust photosynthesis. - Front. Plant. Sci. 9: 1617, 2018. Go to original source...
  63. Someralo S., Krause G.H.: Photoinhibition at chilling tempera­tures and effects of freezing stress on cold acclimated spinach leaves in the field. A fluorescence study. - Physiol. Plantarum 79: 617-622, 1990. Go to original source...
  64. Sonoike K.: Degradation of psa B gene product, the reaction center subunit of photosystem I, is caused during photoinhibition of photosystem I: possible involvement of active oxygen species. - Plant Sci. 115: 157-164, 1996. Go to original source...
  65. Sonoike K.: Photoinhibition of photosystem I. - Physiol. Plantarum 142: 56-64, 2011. Go to original source...
  66. Takagi D., Ishizaki K., Hanawa H. et al.: Diversity of strategies for escaping reactive oxygen species production within photosystem I among land plants: P700 oxidation system is prerequisite for alleviating photoinhibition in photosystem I. - Physiol. Plantarum 161: 56-74, 2017. Go to original source...
  67. Takahashi S., Milward S.E., Fan D.Y. et al.: How does cyclic electron flow alleviate photoinhibition in Arabidopsis? - Plant Physiol. 149: 1560-1567, 2009. Go to original source...
  68. Tikkanen M., Mekala N.R., Aro E.M.: Photosystem II photoinhibition-repair cycle protects Photosystem I from irreversible damage. - BBA-Bioenergetics 1837: 210-215, 2014. Go to original source...
  69. Wen Y., Qin D.W., Leng B. et al.: The physiological cold tolerance of warm-climate plants is correlated with their latitudinal range limit. - Biol. Lett. 14: 20180277, 2018. Go to original source...
  70. West K.R., Wiskich J.T.: Photosynthetic control by isolated pea chloroplasts. - Biochem. J. 109: 527-532, 1968. Go to original source...
  71. Wu J., Nadeem M., Galagedara L. et al.: Effects of chilling stress on morphological, physiological, and biochemical attributes of silage corn genotypes during seedling establishment. - Plants-Basel 11: 1217, 2022. Go to original source...
  72. 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...
  73. Yang Y.J., Chang W., Huang W. et al.: The effects of chilling-light stress on photosystems I and II in three Paphiopedilum species. - Bot. Stud. 58: 53, 2017. Go to original source...
  74. Zhang S., Scheller H.V.: Photoinhibition of photosystem I at chilling temperature and subsequent recovery in Arabidopsis thaliana. - Plant Cell Physiol. 45: 1595-1602, 2004. Go to original source...
  75. Zheng C., Tang J., Chen J. et al.: Mechanisms on inhibition of photosynthesis in Kandelia obovata due to extreme cold events under climate change. - Ecol. Process. 5: 20, 2016. Go to original source...
  76. Zheng X.-T., Chen Y.-L., Zhang X.-H. et al.: ANS-deficient Arabidopsis is sensitive to high light due to impaired anthocyanin photoprotection. - Funct. Plant Biol. 46: 756-765, 2019. Go to original source...
  77. Zivcak M., Brestic M., Kunderlikova K. et al.: Repetitive light pulse-induced photoinhibition of photosystem I severely affects CO2 assimilation and photoprotection in wheat leaves. - Photosynth. Res. 126: 449-463, 2015. Go to original source...