Photosynthetica 2019, 57(3):857-865 | DOI: 10.32615/ps.2019.081

Influence of shading on photosynthesis and antioxidative activities of enzymes in apple trees

Y.J. LIU1,5, W. ZHANG1,5, Z.B. WANG1, L. MA1, Y.P. GUO1,2, X.L. REN1, L.X. MEI1
1 College of Horticulture, Northwest A&F University, Yangling, Shaanxi, China
2 Key Laboratory of Horticulture Plant Biology and Germplasm Innovation in Northwest China, Ministry of Agriculture, Northwest A&F University, Yangling, Shaanxi, China

This study investigated the effects of shading on photosynthesis in 3-year-old potted apple trees. The trees were grown either in full sunlight or in a shade environment with about 50% of sunlight filtered through black plastic nets. Under the shade conditions, the net photosynthetic rate (PN), the stomatal conductance, the transpiration rate, and the intercellular CO2 concentration decreased before midday, which was due to low light energy but the PN of the shaded trees increased relative to the control trees during the afternoon. In addition, the concentrations of chlorophyll (Chl) a, b, and total Chl increased in the shaded trees. In shaded apple trees, the photochemical efficiency increased. There was a lower content of reactive oxygen species and activities of antioxidant enzymes. The results showed that moderate shading can improve the total photosynthetic efficiency, which is mainly attributed to alleviation of photodamage and low accumulation of reactive oxygen species.

Keywords: chlorophyll fluorescence; gas exchange; Malus domestica; photoinhibition.

Received: May 8, 2018; Accepted: August 1, 2018; Prepublished online: July 12, 2019; Published: July 23, 2019Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
LIU, Y.J., ZHANG, W., WANG, Z.B., MA, L., GUO, Y.P., REN, X.L., & MEI, L.X. (2019). Influence of shading on photosynthesis and antioxidative activities of enzymes in apple trees. Photosynthetica, 57(3), 857-865. doi: 10.32615/ps.2019.081.
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. Adams W.W., Muller O., Cohu C.M., Demmig-Adams B.: May photoinhibition be a consequence, rather than a cause, of limited plant productivity? - Photosynth. Res. 117: 31-44, 2013. Go to original source...
    2. Aebi H.: Catalase in vitro. - Methods Enzymol. 105: 12-126, 1984. Go to original source...
    3. Allorent G., Tokutsu R., Roach T. et al.: A dual strategy to cope with high light in Chlamydomonas reinhardtii. - Plant Cell 25: 545-557, 2013. Go to original source...
    4. Apel K., Hirt H.: Reactive oxygen species: Metabolism, oxidative stress, and signal transduction. - Annu. Rev. Plant Biol. 55: 373-399, 2004. Go to original source...
    5. Araus J.L., Amaro T., Voltas J. et al.: Chlorophyll fluorescence as a selection criterion for grain yield in durum wheat under Mediterranean conditions. - Field Crop. Res. 55: 209-223, 1998. Go to original source...
    6. Aro E.M., Virgin I., Andersson B.: Photoinhibition of photo-system II. Inactivation, protein damage and turnover. - Biochim. Biophys. Acta 1143: 113-134, 1993. Go to original source...
    7. Asada K.: The water-water cycle an alternative photon and electron sinks. - Philos. T. Roy. Soc. London B. 355: 1419-1431, 2000. Go to original source...
    8. Asada K.: Production and scavenging of reactive oxygen species in chloroplasts and their functions. - Plant Physiol. 141: 391-396, 2006. Go to original source...
    9. Baig M.J., Anand A., Mandal P.K., Bhatt R.K.: Irradiance in-fluences contents of photosynthetic pigments and proteins in tropical grasses and legumes. - Photosynthetica 43: 47-53, 2005. Go to original source...
    10. Baker N.R., Rosenqvist E.: Applications of chlorophyll fluores-cence can improve crop production strategies: an examination of future possibilities. - J. Exp. Bot. 55: 1607-1621, 2004. Go to original source...
    11. Barber J., Morris E., Buchel C.: Revealing the structure of the photosystem II chlorophyll binding proteins, CP43 and CP47. - Biochim. Biophys. Acta 1459: 239-247, 2000. Go to original source...
    12. Baxter A., Mittler R., Suzuki N.: ROS as key players in plant stress signalling. - J. Exp. Bot. 65: 1229-1240, 2014. Go to original source...
    13. Blot N., Mella-Flores D., Six C. et al.: Light history influences the response of the marine Cyanobacterium synechococcus sp. WH7803 to oxidative stress. - Plant Physiol. 156: 1934-1954, 2011.
    14. Rodríquez-Calcerrada J.R., Pardos J.A., Gil L. et al.: Light response in seedlings of a temperate (Quercus petraea) and a sub-Mediterranean species (Quercus pyrenaica): contrasting ecological strategies as potential keys to regeneration per-formance in mixed marginal populations. - Plant Ecol. 195: 273-285, 2008. Go to original source...
    15. Campbell D.A., Hossain Z., Cockshutt A.M. et al.: Photosystem II protein clearance and FtsH function in the diatom Thalassiosira pseudonana. - Photosynth. Res. 115: 43-54, 2013. Go to original source...
    16. Carmo-Silva A.E., Salvucci M.E.: The temperature response of CO2 assimilation, photochemical activities and Rubisco activation in Camelina sativa, a potential bioenergy crop with limited capacity for acclimation to heat stress. - Planta 236: 1433-1445, 2012. Go to original source...
    17. Carpentier R.: Effect of high-temperature stress on the photo-synthetic apparatus. - In: Pessarakli M. (ed.): Handbook of Plant and Crop Stress. Pp. 337-348. Marcel Dekker Inc., New York 1999. Go to original source...
    18. Dai Y., Shen Z., Liu Y.: Effects of shade treatments on the photosynthetic capacity, chlorophyll fluorescence, and chlorophyll content of Tetrastigma hemsleyanum Diels et Gilg. - Environ. Exp. Bot. 65: 177-182, 2009. Go to original source...
    19. Dat J., Vandenabeele S., Vranová E. et al.: Dual action of the active oxygen species during plant stress responses. - Cell Mol. Life Sci. 57: 779-795, 2000. Go to original source...
    20. Deng Y., Li C., Shao Q. et al.: Differential responses of double petal and multi petal jasmine to shading: I. Photosynthetic characteristics and chloroplast ultrastructure. - Plant Physiol. Bioch. 55: 93-102, 2012. Go to original source...
    21. Dhindsa R.S., Plumb-Dhindsa P., Thorpe T.A.: Leaf senescence: correlated with increased levels of membrane permeability and lipid peroxidation and decreased levels of superoxide dismutase and catalase. - J. Exp. Bot. 32: 93-101, 1981. Go to original source...
    22. Egley G.H., Paul R.N., Vaughn K.C., Duke S.O.: Role of peroxidase in the development of water impermeable seed coats in Sida spinosa L. - Planta 157: 224-232, 1983. Go to original source...
    23. Foyer C.H., Shigeoka S.: Understanding oxidative stress and antioxidant functions to enhance photosynthesis. - Plant Physiol. 155: 93-100, 2011. Go to original source...
    24. Genty B., Briantais J.M., Baker N.R.: The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. - Biochim. Biophys. Acta 990: 87-92, 1989. Go to original source...
    25. Georgea A.P., Hiekeb S., Rasmussenc T., Lüddersb P.: Early shading reduces fruit yield and late shading reduces quality in low-chill peach (Prunus persica (L.) Batsch) in subtropical Australia. - J. Hortic. Sci. 71: 561-571, 1996. Go to original source...
    26. Glenn D.M.: Particle film mechanisms of action that reduce the effect of environmental stress in ʻEmpireʼ apple - J. Am. Soc. Hortic. Sci. 134: 314-321, 2009. Go to original source...
    27. Goh C.H., Ko S.M., Koh S. et al.: Photosynthesis and environments: Photoinhibition and repair mechanisms in plants. - J. Plant. Biol. 55: 93-101, 2012. Go to original source...
    28. Green B.R., Durnford D.G.: The chlorophyll-carotenoid proteins of oxygenic photosynthesis. - Annu. Rev. Plant Phys. 47: 685-714, 1996. Go to original source...
    29. Guo Y.P., Guo D.P., Zhou H.F. et al.: Photoinhibition and xanthophyll cycle activity in bayberry (Myrica rubra) leaves induced by high irradiance. - Photosynthetica 44: 439-446, 2006a. Go to original source...
    30. Guo Y.P., Zhou H.F., Zhang L.C.: Photosynthetic characteristics and protective mechanisms against photooxidation during high temperature stress in two citrus species. - Sci. Hortic.-Amsterdam 108: 260-267, 2006b.
    31. Guo Y., Zhou Z., Yuan Y., Yue T.: Survey of patulin in apple juice concentrates in Shaanxi (China) and its dietary intake. - Food Control 34: 570-573, 2013. Go to original source...
    32. Halliwell B., Foyer C.H.: Properties and physiological function of a glutathione reductase purified from spinach leaves by affinity chromatography. - Planta 139: 9-17, 1978. Go to original source...
    33. Heber U., Neimanis S., Dietz K.J.: Fractional control of photosynthesis by the QB-protein, the cytochrome-f cytochrome-B6 complex and other components of the photosynthetic apparatus. - Planta 173: 267-274, 1988 Go to original source...
    34. Henriques F.S.: Leaf chlorophyll fluorescence: background and fundamentals for plant biologists. - Bot. Rev. 75: 249-270, 2009. Go to original source...
    35. Hunter J.J., Morgan J.I.W., Merigan W.H. et al.: The susceptibility of the retina to photochemical damage from visible light. - Prog. Retin. Eye Res. 31: 28-42, 2012. Go to original source...
    36. Jacksona J.E., Palmera J.W.: Effects of shade on the growth and cropping of apple trees. II. Effects on components of yield. - J. Hortic. Sci. 52: 253-266, 1977. Go to original source...
    37. Jung S.Y., Kim J.S., Cho K.Y. et al.: Antioxidant responses of cucumber (Cucumis sativus) to photoinhibition and oxidative stress induced by norflurazon under high and low PPFDs. - Plant Sci. 153: 145-154, 2000. Go to original source...
    38. Kalaji H.M., Govindjee, Bosa K. et al.: Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. - Environ. Exp. Bot. 73: 64-72, 2011. Go to original source...
    39. Kayihan C., Eyidogan F., Afsar N. et al.: Cu/Zn superoxide dismutase activity and respective gene expression during cold acclimation and freezing stress in barley cultivars. - Biol. Plantarum 56: 693-698, 2012. Go to original source...
    40. Kim S.J., Yu D.J., Kim T.C., Lee H.J.: Growth and photosynthetic characteristics of blueberry (Vacciniun corymbosum cv. Bluecrop) under various shade levels. - Sci. Hortic.-Amsterdam 129: 486-492, 2011.
    41. Lei T.T., Nilsen E.T., Semones W.: Light environment under Rhododendron maximum thickets and estimated carbon gain of regenerating forest tree seed. - Plant Ecol. 184: 143-156, 2006. Go to original source...
    42. Liu B., Li M., Cheng L. et al.: Influence of rootstock on anti-oxidant system in leaves and roots of young apple trees in response to drought stress. - Plant Growth Regul. 67: 247-256, 2012. Go to original source...
    43. Lloyd J., Wong S.C., Styles J.M. et al.: Measuring and modelling whole-tree gas exchange. - Aust. J. Plant Physiol. 22: 987-1000, 1995. Go to original source...
    44. López-Marín J., Gálvez A., González A. et al.: Effect of shade on yield, quality and photosynthesis related parameters of sweet pepper plants. - Acta Hortic. 956: 545-552, 2012. Go to original source...
    45. Masabni J., Sun Y.P., Niu G.H., del Valle P.: Shade effect on growth and productivity of tomato and chili pepper. HortTechnology 26: 344-350, 2016. Go to original source...
    46. Mittler R., Vanderauwera S., Gollery M., van Breusegem F.: Reactive oxygen gene network of plants. - Trends Plant Sci. 9: 490-498, 2004. Go to original source...
    47. Miyata K., Noguchi K., Terashima I.: Cost and benefit of the repair of photodamaged photosystem II in spinach leaves: roles of acclimation to growth light. - Photosynth. Res. 113: 165-180, 2012. Go to original source...
    48. Moskova I., Todorova D., Alexieva V. et al.: Effect of exogenous hydrogen peroxide on enzymatic and nonenzymatic antioxidants in leaves of young pea plants treated with paraquat. - Plant Growth Regul. 57: 193-202, 2009. Go to original source...
    49. Nakano Y., Asada K.: Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. - Plant Cell Physiol. 22: 867-880, 1981.
    50. Murata N., Allakherdviev 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.
    51. Murata N., Takahashi S., Nishiyama Y., Allakherdviev S.I.: Photoinhibition of photosystem II under environmental stress. -BBA-Bioenergetics 1767: 414-421, 2007. Go to original source...
    52. Pires M.V., Almeida A.A.F., Figueiredo A.L. et al.: Photosynthetic characteristics of ornamental passion flowers grown under different light intensities. - Photosynthetica 49: 593-602, 2011. Go to original source...
    53. Sáez P.L., Bravo L.A., Latsague M.I. et al.: Light energy management in micropropagated plants of Castanea sativa, effects of photoinhibition. - Plant Sci. 201:12-24, 2013. Go to original source...
    54. Sakuraba Y., Yokono M., Akimoto S. et al.: Deregulated chlorophyll b synthesis reduces the energy transfer rate between photosynthetic pigments and induces photodamage in Arabidopsis thaliana. - Plant Cell Physiol. 51: 1055-1065, 2010. Go to original source...
    55. Satoh S., Ikeuchi M., Mimuro M., Tanaka A.: Chlorophyll b expressed in cyanobacteria functions as a light harvesting antenna in photosystem I through flexibility of the proteins. - J. Biol. Chem. 276: 4293-4297, 2001. Go to original source...
    56. Snelgar W.P., Hopkirk G.: Effect of overhead shading on yield and fruit quality of kiwifruit (Actinidia deliciosa). - J. Hortic. Sci. 63: 731-742, 1988. Go to original source...
    57. Song Y., Miao Y., Song C.P.: Behind the scenes: the roles of reactive oxygen species in guard cells. - New Phytol. 201: 1121-1140, 2014. Go to original source...
    58. Sridharamurthy M., Kovach A., Zhao Y. et al.: H2O2 inhibits ABA-signaling protein phosphatase HAB1. - PLoS ONE: doi: 10.1371/journal.pone.0113643, 2014. Go to original source...
    59. Takahashi S., Murata N.: How do environmental stresses accelerate photoinhibition? - Trends Plant Sci. 13: 178-182, 2008. Go to original source...
    60. Takahashi S., Murata N.: Glycerate-3-phosphate, produced by CO2 fixation in the Calvin cycle, is critical for the synthesis of the D1 protein of photosystem II. - BBA-Bioenergetics 1757: 198-205, 2006. Go to original source...
    61. Takahashi S., Milward S.E., Yamori W. et al.: The solar action spectrum of photosystem II damage. - Plant Physiol. 153: 988-993, 2010. Go to original source...
    62. Thordal-Christensen H., Zhang Z., Wei Y., Collinge D.B.: Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction. - Plant J. 11: 1187-1194, 1997. Go to original source...
    63. Wang S., Liang D., Li C. et al.: Influence of drought stress on the cellular ultrastructure and antioxidant system in leaves of drought-tolerant and drought-sensitive apple rootstocks. - Plant Physiol. Bioch. 51: 81-89, 2012. Go to original source...
    64. Yan N., Wang X.Q., Xu X.F. et al.: Plant growth and photo-synthetic performance of Zizania latifolia are altered by endophytic Ustilago esculenta infection. - Physiol. Mol. Plant Pathol. 83: 75-83, 2013. Go to original source...
    65. Zai X.M., Zhu S.N., Qin P. et al.: Effect of Glomus mosseae on chlorophyll content, chlorophyll fluorescence parameters, and chloroplast ultrastructure of beach plum (Prunus maritima) under NaCl stress. - Photosynthetica 50: 323-328, 2012. Go to original source...
    66. Zhang S.B., Hu H., Xu K. et al.: Flexible and reversible responses to different irradiance levels during photosynthetic acclimation of Cypripedium guttatum. - J. Plant Physiol. 164: 611-620, 2007. Go to original source...

    Return to the content