Photosynthetica 2018, 56(4):1081-1092 | DOI: 10.1007/s11099-018-0807-7

Effects of GeO2 on chlorophyll fluorescence and antioxidant enzymes in apple leaves under strong light

Z. B. Wang1, Y. F. Wang1, J. J. Zhao1, L. Ma1, Y. J. Wang1, X. Zhang1, Y. T. Nie1, Y. P. Guo1,2,*, L. X. Mei1, Z. Y. Zhao1,3
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
3 Shaanxi Engineering Research Center for Apple, Yangling, Shaanxi, China

In this study, we chose apple leaf as plant material and studied effects of GeO2 on operation of photosynthetic apparatus and antioxidant enzyme activities under strong light. When exogenous GeO2 concentration was below 5.0 mg L-1, maximum photochemical quantum yield of PSII and actual quantum yield of PSII photochemistry increased significantly compared with the control under irradiances of 800 and 1,600 μmol(photon) m-2 s-1. Photosynthetic electron transport chain capacity between QA-QB, QA-PSI acceptor, and QB-PSI acceptor showed a trend of rising up with 1.0, 2.0, and 5.0 mg(GeO2) L-1 and declining with 10.0 mg(GeO2) L-1. On the other hand, dissipated energy via both ΔpH and xanthophyll cycle decreased remarkably compared with the control when GeO2 concentration was below 5.0 mg L-1. Our results suggested that low concentrations of GeO2 could alleviate photoinhibition and 5.0 mg(GeO2) L-1 was the most effective. In addition, we found, owing to exogenous GeO2 treatment, that the main form of this element in apple leaves was organic germanium, which means chemical conversion of germanium happened. The organic germanium might be helpful to allay photoinhibition due to its function of scavenging free radicals and lowering accumulation of reactive oxygen species, which was proven by higher antioxidant enzyme activities.

Keywords: chlorophyll fluorescence; irradiance; photodamage; photosynthetic electron transport chain

Received: April 6, 2016; Accepted: June 19, 2017; Prepublished online: December 1, 2018; Published: November 1, 2018Show citation

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Wang, Z.B., Wang, Y.F., Zhao, J.J., Ma, L., Wang, Y.J., Zhang, X., ... Zhao, Z.Y. (2018). Effects of GeO2 on chlorophyll fluorescence and antioxidant enzymes in apple leaves under strong light. Photosynthetica56(4), 1081-1092. doi: 10.1007/s11099-018-0807-7.
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References

  1. Adams J.H., Thomas D.: Germanium and germanium compounds.-In: Kirk-Othmer (ed.): Encyclopedia of Chemical Technology. Pp. 540-555. Wiley, New York 1994.
  2. 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...
  3. Balarinová K., Barták M., Hazdrová J. et al.: Changes in photosynthesis, pigment composition and glutathione contents in two Antarctic lichens during a light stress and recovery.-Photosynthetica 52: 538-547, 2014. Go to original source...
  4. Bilger W., Björkman O.: Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence and photosynthesis in leaves of Hedera canariensis.-Photosynth. Res. 25: 173-185, 1990. Go to original source...
  5. Chen C., Li H., Zhang D. et al.: The role of anthocyanin in photoprotection and its relationship with the xanthophyll cycle and the antioxidant system in apple peel depends on the light conditions.-Physiol. Plantarum 149: 354-366, 2013. Go to original source...
  6. Cheong Y.H., Kim S.U., Seo D.C. et al.: Effect of inorganic and organic germanium treatments on the growth of lettuce (Lactuca sativa).-J. Korean Soc. Appl. Bi. 52: 389-396, 2009. Go to original source...
  7. Díaz-Vivancos P., Clemente-Moreno M.J., Rubio M. et al.: Alteration in the chloroplastic metabolism leads to ROS accumulation in pea plants in response to plum pox virus.-J. Exp. Bot. 59: 2147-2160, 2008 Go to original source...
  8. Diao M., Ma L., Wang J.W.: Selenium promotes the growth and photosynthesis of tomato seedlings under salt stress by enhancing chloroplast antioxidant defense system.-J. Plant Growth Regul. 33: 671-682, 2014. Go to original source...
  9. Garg N., Manchanda G.: ROS generation in plants: boon or bane?-Plant Biosyst. 143: 81-96, 2009. Go to original source...
  10. 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...
  11. Gill S.S., Tuteja N.: Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants.-Plant Physiol. Bioch. 48: 909-930, 2010. Go to original source...
  12. Goodman S.: Therapeutic effects of organic germanium.-Med. Hypotheses 26: 207-215, 1988. Go to original source...
  13. Halperin S.J., Barzilay A., Carson M. et al.: Germanium accumulation and toxicity in barley.-J. Plant Nutr. 18: 1417-1426, 1995. Go to original source...
  14. Han M.J., Kim S.U., Seo D.C. et al.: Uptake properties of germanium to vegetable plants and its effect on seed germination and on early stage growth.-Korean J. Environ. Agric. 26: 217-222, 2007. Go to original source...
  15. Hasanuzzaman M., Fujita M.: Selenium pretreatment upregulates the antioxidant defense and methylglyoxal detoxification system and confers enhanced tolerance to drought stress in rapeseed seedlings.-Biol. Trace Elem. Res. 143: 1758-1776, 2011. Go to original source...
  16. Henriques F.S.: Leaf chlorophyll fluorescence: background and fundamentals for plant biologists.-Bot. Rev. 75: 249-270, 2009. Go to original source...
  17. Jahns P., Holzwarth A.R.: The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II.-Biochim. Biophys. Acta 1817: 182-193, 2012.
  18. Kaplan B.J., Parish W.W., Andrus G.M. et al.: Germane facts about germanium sesquioxide: I. Chemistry and anticancer properties.-J. Altern. Complem. Med. 10: 337-344, 2004. Go to original source...
  19. Kitajima M., Butler W.L.: Quenching of chlorophyll fluorescence and primary photochemistry in chloroplasts by dibromothymoquinone.-Biochim. Biophys. Acta 376: 105-115, 1975. Go to original source...
  20. Kramer D.M., Johnson G., Kiirats O., Edwards G.E.: New fluxparameters for the determination of QA redox state and excitation fluxes.-Photosynth. Res. 79: 209-218, 2004. Go to original source...
  21. Lazár D.: The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light.-Funct. Plant Biol. 33: 9-30, 2006. Go to original source...
  22. Lichtenthaler H.K.: Chlorophylls and carotenoids: pigments of photosynthetic biomembranes.-Methods Enzymol. 148: 350-382, 1987. Go to original source...
  23. Li L., Zhou Z., Liang J., Lv R.: In vivo evaluation of the highirradiance effects on PSII activity in photosynthetic stems of Hexinia polydichotoma.-Photosynthetica 53: 621-624, 2015. Go to original source...
  24. Lim J.S., Seo D.C., Park W.Y. et al.: Effects of soil texture on germanium uptake and growth in rice plant by soil application with germanium.-Korean J. Environ. Agric. 27: 245-252, 2008. Go to original source...
  25. Liu Y., Hou L.Y., Li Q.M. et al.: The effects of exogenous antioxidant germanium (Ge) on seed germination and growth of Lycium ruthenicum Murr subjected to NaCl stress.-Environ. Technol. 37: 909-919, 2016. Go to original source...
  26. Matsumoto H., Syo S., Takahashi E.: Translocation and some forms of germanium in rice plants.-Soil Sci. Plant Nutr. 21: 273-279, 1975. Go to original source...
  27. McMahon M., Regan F., Hughes H.: The determination of total germanium in real food samples including Chinese herbal remedies using graphite furnace atomic absorption spectroscopy.-Food Chem. 97: 411-417, 2006. Go to original source...
  28. Meyer S., Saccardy-Adji K., Rizza F., Genty B.: Inhibition of photosynthesis by Colletotrichum lindemuthianum in bean leaves determined by chlorophyll fluorescence imaging.-Plant Cell Environ. 24: 947-955, 2001. Go to original source...
  29. Munakata T., Agai S., Kuwano K. et al.: Induction of interferon production by natural killer cells by organogermanium compound Ge-132.-J. Interferon Res. 7: 69-76, 1987. Go to original source...
  30. Nakano Y., Asada K.: Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts.-Plant Cell Physiol. 22: 867-880, 1981.
  31. Nickel R.S., Cunningham B.A.: Improved peroxidase assay method using leuco 2,3,6-trichloroindophenol and application to comparative measurements of peroxidase catalysis.-Anal. Physiol. 172: 385-390, 1969.
  32. Rao K.V.M., Sresty T.V.S.: Antioxidant parameters in the seedlings of pigeon pea (Cajanus cajan L. Millspaugh) in response to Zn and Ni stresses.-Plant Sci. 157: 113-128, 2000.
  33. Rosenberg E.: Germanium: environmental occurrence, importance and speciation.-Rev. Environ. Sci. Bio. 8: 29-57, 2009. Go to original source...
  34. Schansker G., Tóth S.Z., Strasser R.J.: Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP.-Biochim. Biophys. Acta 1706: 250-261, 2005. Go to original source...
  35. Schreiber U., Schliwa U., Bilger W.: Continuous recording of photochemical and non-photochemical chlorophyll fluorescence quenching with a new type of modulation fluorometer.-Photosynth. Res. 10: 51-62, 1986. Go to original source...
  36. Seo D.C., Cheon Y.S., Park S.K. et al.: [Applications of different types of germanium compounds on rice plant growth and its Ge uptake.]-Korean J. Soil Sci. Fertil. 43: 166-173, 2010. [In Korean]
  37. Sparks J.P., Chandra S., Derry L.A. et al.: Subcellular localization of silicon and germanium in grass root and leaf tissues by SIMS: evidence for differential and active transport.-Biogeochemistry 104: 237-249, 2011. Go to original source...
  38. Stepien P., Klobus G.: Antioxidant defense in the leaves of C3 and C4 plants under salinity stress.-Physiol. Plantarum 125: 31-40, 2005. Go to original source...
  39. Stirbet A., Govindjee: On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: Basics and applications of the OJIP fluorescence transient.-J. Photoch. Photobio. B 104: 236-257, 2011. Go to original source...
  40. Strasser R.J.A., Srivastava A., Tsimilli-Michael M.: The fluorescence transient as a tool to characterize and screen photosynthetic samples.-In: Yunus M., Pathre U., Mohanty P. (ed.): Probing Photosynthesis: Mechanisms, Regulation and Adaptation. Pp. 445-483. Taylor and Francis, London 2000.
  41. Takahashi S., Murata N.: How do environmental stresses accelerate photoinhibition?-Trends Plant Sci. 13: 178-182, 2008. Go to original source...
  42. Tang Z., Shi Y., Zhou J.P. et al.: Effects of an organogermanium compound on antioxidant function of vMDV-infected chickens.-Chinese J. Vet. Sci. 17: 173-176, 1997. [In Chinese]
  43. Tarakhovskaya E.R., Kang E.J., Kim K.Y., Garbary D.J.: Effect of GeO2 on embryo development and photosynthesis in Fucus vesiculosus (Phaeophyceae).-Algae 27: 125-134, 2012. Go to original source...
  44. Yang M.K., Kim Y.G.: Protective role of germanium-132 against paraquat-indrced oxidative stress in the livers of senescence -accelerated mice.-J. Toxicol. Environ. Health A 58: 289-297, 1999.
  45. Wang Z.X., Chen L., Ai J. et al.: Photosynthesis and activity of photosystem II in response to drought stress in Amur Grape (Vitis amurensis Rupr.).-Photosynthetica 50: 189-196, 2012. Go to original source...
  46. Yu K.W., Murthy H.N., Jeong C.S. et al.: Organic germanium stimulated the growth of ginseng dventitious roots and ginsenoside production.-Process. Biochem. 40: 2959-2961, 2005. Go to original source...
  47. 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...
  48. Zhang J.X., Kirkham M.B.: Antioxidant responses to drought in sunflower and sorghum seedlings.-New Phytol. 132: 361-373, 1996. Go to original source...
  49. Zhang M., Tang S.U., Huang X. et al.: Selenium uptake, dynamic changes in selenium content and its influence on photosynthesis and chlorophyll fluorescence in rice (Oryza sativa L.).-Environ. Exp. Bot. 107: 39-45, 2014. Go to original source...