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Photosynthetica

, Volume 56, Issue 1, pp 427–432 | Cite as

Susceptibility of an ascorbate-deficient mutant of Arabidopsis to high-light stress

  • L.-D. Zeng
  • M. Li
  • W. S. Chow
  • C.-L. Peng
Article

Abstract

Ascorbate is an important antioxidant involved in both enzymatic and nonenzymatic reactions in plant cells. To reveal the function of ascorbate associated with defense against photo-oxidative damage, responses of the ascorbate-deficient mutant vtc2-1 of Arabidopsis thaliana to high-light stress were investigated. After high-light treatment at 1,600 μmol(photon) m–2 s–1 for 8 h, the vtc2-1 mutant exhibited visible photo-oxidative damage. The total ascorbate content was lower, whereas accumulation of H2O2 was higher in the vtc2-1 mutant than that in the wild type. The chlorophyll (Chl) content and PSII Chl fluorescence parameters, such as maximal quantum yield of PSII photochemistry, yield, and electron transport rate, in vtc2-1 mutant decreased more than that in the wild type, whereas the nonphotochemical quenching coefficient increased more in the wild type than that in vtc2-1 mutant. Therefore, the vtc2-1 mutant was more sensitive to high-light stress than the wild type. Accumulation of reactive oxygen species was mainly responsible for the damage of PSII in the vtc2-1 mutant under high light. The results indicate that ascorbate plays a critical role in maintaining normal photosynthetic function in plants under high-light stress.

Additional key words

Arabidopsis thaliana ascorbic acid high-light stress chlorophyll fluorescence reactive oxygen species 

Abbreviations

APX

ascorbate peroxidase

AsA

ascorbic acid

AsA-GSH cycle

ascorbate–glutathione cycle

CAT

catalase

Chl

chlorophyll

DAB

diaminobenzidine

ETR

electron transport rate

F0

minimal fluorescence yield of the dark-adapted state

Fm

maximal fluorescence yield of the dark-adapted state

Fm

maximal fluorescence yield of the light-adapted state

Fs

steady-state fluorescence yield

Fv

variable fluorescence

Fv/Fm

maximal quantum yield of PSII photochemistry

NPQ

nonphotochemical quenching

ORF

open reading frame

qN

nonphotochemical quenching coefficient

qP

photochemical quenching coefficient

RH

relative humidity

ROS

reactive oxygen species

SOD

superoxide dismutase

TCA

trichloroacetic acid

ФPSII

effective quantum yield of PSII photochemistry.

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References

  1. Adams W.I., Demmig-Adams B., Verhoeven A. et al.: Photoinhibition during winter stress: Involvement of sustained xanthophyll cycle-dependent energy dissipation.–Funct. Plant Biol. 22: 261–276, 1995.Google Scholar
  2. Agius F., González-Lamothe R., Caballero J.L. et al.: Engineering increased vitamin C levels in plants by overexpression of a D-galacturonic acid reductase.–Nat. Biotechnol. 21: 177–181, 2003.CrossRefPubMedGoogle Scholar
  3. Alscher R.G., Donahue J.L., Cramer C.L.: Reactive oxygen species and antioxidants: Relationships in green cells.–Physiol. Plantarum 100: 224–233, 1997.CrossRefGoogle Scholar
  4. Asada K.: Production and scavenging of reactive oxygen species in chloroplasts and their functions.–Plant Physiol. 141: 391–396, 2006.CrossRefPubMedPubMedCentralGoogle Scholar
  5. Conklin P., Barth C.: Ascorbic acid, a familiar small molecule intertwined in the response of plants to ozone, pathogens, and the onset of senescence.–Plant Cell Environ. 27: 959–970, 2004.CrossRefGoogle Scholar
  6. Conklin P.L., Saracco S.A., Norris S.R. et al.: Identification of ascorbic acid-deficient Arabidopsis thaliana mutants.–Genetics 154: 847–856, 2000.PubMedPubMedCentralGoogle Scholar
  7. Conti E., Izaurralde E.: Nonsense-mediated mRNA decay: Molecular insights and mechanistic variations across species.–Curr. Opin. Cell Biol. 17: 316–325, 2005.CrossRefPubMedGoogle Scholar
  8. Ding Z.S., Zhou B.Y., Sun X.F. et al.: High light tolerance is enhanced by overexpressed PEPC in rice under drought stress.–Acta Agron. Sin. 38: 285–292, 2012.CrossRefGoogle Scholar
  9. Dowdle J., Ishikawa T., Gatzek S. et al.: Two genes in Arabidopsis thaliana encoding GDP-L-galactose phosphorylase are required for ascorbate biosynthesis and seedling viability.–Plant J. 52: 673–689, 2007.CrossRefPubMedGoogle Scholar
  10. Endo M., Nakamura S., Araki T. et al.: Phytochrome b in the mesophyll delays flowering by suppressing flowering locusT expression in Arabidopsis vascular bundles.–Plant Cell 17: 1941–1952, 2005.CrossRefPubMedPubMedCentralGoogle Scholar
  11. Finkel T., Holbrook N.J.: Oxidants, oxidative stress and the biology of ageing.–Nature 408: 239–247, 2000.CrossRefPubMedGoogle Scholar
  12. Gallie D.R.: Increasing vitamin C content in plant foods to improve their nutritional value–successes and challenges.–Nutrients 5: 3424–3446, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  13. Gao Q., Zhang L.: Ultraviolet-B-induced oxidative stress and antioxidant defense system responses in ascorbate-deficient VTC1 mutants of arabidopsis thaliana.–J. Plant Physiol. 165: 138–148, 2008.CrossRefPubMedGoogle Scholar
  14. Genty B., Briantais J.-M., Baker N.R.: The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence.–Biochim. Biophy. Acta 990: 87–92, 1989.CrossRefGoogle Scholar
  15. Gillespie K.M., Ainsworth E.A.: Measurement of reduced, oxidized and total ascorbate content in plants.–Nat. Protoc. 2: 871–874, 2007.CrossRefPubMedGoogle Scholar
  16. Huang J.L., Wang S.H., Zhang Z.X.: [Effect of external asa on the photoinhibition of ginger leaves in vitro.]–Acta Bot. Boreali-Occ. Sin. 10: 2041–2046, 2008. [In Chinese]Google Scholar
  17. Ishikawa T., Dowdle J., Smirnoff N.: Progress in manipulating ascorbic acid biosynthesis and accumulation in plants.–Physiol. Plantarum 126: 343–355. 2006.CrossRefGoogle Scholar
  18. Ishikawa T., Shigeoka S.: Recent advances in ascorbate biosynthesis and the physiological significance of ascorbate peroxidase in photosynthesizing organisms.–Biosci. Biotech. Bioch. 72: 1143–1154, 2008.CrossRefGoogle Scholar
  19. Jander G., Norris S.R., Rounsley S.D. et al.: Arabidopsis mapbased cloning in the post-genome era.–Plant Physiol. 129: 440–450, 2002.CrossRefPubMedPubMedCentralGoogle Scholar
  20. Kotchoni S.O., Larrimore K.E., Mukherjee M. et al.: Alterations in the endogenous ascorbic acid content affect flowering time in Arabidopsis.–Plant Physiol. 149: 803–815, 20CrossRefPubMedPubMedCentralGoogle Scholar
  21. Laing W.A., Wright M.A., Cooney J. et al.: The missing step of the l-galactose pathway of ascorbate biosynthesis in plants, an l-galactose guanyltransferase, increases leaf ascorbate content.–P. Natl. Acad. Sci. USA 104: 9534–9539, 2007.CrossRefGoogle Scholar
  22. Li F., Wu Q.Y., Sun Y.L. et al.: Overexpression of chloroplastic monodehydroascorbate reductase enhanced tolerance to temperature and methyl viologen-mediated oxidative stresses.–Physiol. Plantarum 139: 421–434, 2010.Google Scholar
  23. Linster C.L., Gomez T.A., Christensen K.C. et al.: Arabidopsis VTC2 encodes a GDP-l-galactose phosphorylase, the last unknown enzyme in the Smirnoff-Wheeler pathway to ascorbic acid in plants.–J. Biol. Chem. 282: 18879–18885, 2007.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Locato V., Gadaleta C., De Gara L. et al.: Production of reactive species and modulation of antioxidant network in response to heat shock: A critical balance for cell fate.–Plant Cell Environ. 31: 1606–1619, 2008.CrossRefPubMedGoogle Scholar
  25. Lorence A., Chevone B.I., Mendes P. et al.: Myo-inositol oxygenase offers a possible entry point into plant ascorbate biosynthesis.–Plant Physiol. 134: 1200–1205, 2004.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Müller-Moulé P., Conklin P.L., Niyogi K.K.: Ascorbate deficiency can limit violaxanthin de-epoxidase activity in vivo.–Plant Physiol. 128: 970–977, 2002.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Müller-Moulé P., Golan T., Niyogi K.K.: Ascorbate-deficient mutants of Arabidopsis grow in high light despite chronic photooxidative stress.–Plant Physiol. 134: 1163–1172, 2004.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Müller-Moulé P.: An expression analysis of the ascorbate biosynthesis enzyme VTC2.–Plant Mol. Biol. 68: 31–41, 2008.CrossRefPubMedGoogle Scholar
  29. Noctor G., Veljovic-Jovanovic S., Foyer C.H.: Peroxide processing in photosynthesis: Antioxidant coupling and redox signalling.–Philos. T. R. Soc. B 355: 1465–1475, 2000.CrossRefGoogle Scholar
  30. Pekker I., Tel-Or E., Mittler R.: Reactive oxygen intermediates and glutathione regulate the expression of cytosolic ascorbate peroxidase during iron-mediated oxidative stress in bean.–Plant Mol. Biol. 49: 429–438, 2002.CrossRefPubMedGoogle Scholar
  31. Pignocchi C., Foyer C.H.: Apoplastic ascorbate metabolism and its role in the regulation of cell signalling.–Curr Opin. Plant Biol. 6: 379–389, 2003.CrossRefPubMedGoogle Scholar
  32. Porra R.J., Thompson W.A., Kriedemann P.E.: Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophylls a and b extracted with four different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy.–BBABioenergetics 975: 384–394, 1989.CrossRefGoogle Scholar
  33. Romero-Puertas P.M., Rodríguez-Serrano S.M., Corpas F. et al.: Cadmium-induced subcellular accumulation of O2·and H2O2 in pea leaves.–Plant Cell Environ. 27: 1122–1134, 2004.CrossRefGoogle Scholar
  34. Smirnoff N.: Plant resistance to environmental stress.–Curr. Opin. Biotechnol. 9: 214–219, 1998.CrossRefPubMedGoogle Scholar
  35. Smirnoff N.: Ascorbic acid: Metabolism and functions of a multifacetted molecule.–Curr. Opin. Plant Biol. 3: 229–235, 2000.CrossRefPubMedGoogle Scholar
  36. Sun Y.Y., Bi J.C., Zhao Z.C. et al.: [The advancement on leaf senescence in crops.]–Crops 4: 11–19, 2013. [In Chinese].Google Scholar
  37. Wheeler G.L., Jones M.A., Smirnoff N.: The biosynthetic pathway of vitamin C in higher plants.–Nature 393: 365–369, 1998.CrossRefPubMedGoogle Scholar
  38. Wolucka B.A., van Montagu M.: GDP-mannose 3′, 5′-epimerase forms GDP-L-gulose, a putative intermediate for the de novo biosynthesis of vitamin C in plants.–J. Biol. Chem. 278: 47483–47490, 2003.CrossRefPubMedGoogle Scholar
  39. Wolucka B.A., van Montagu M.: The VTC2 cycle and the de novo biosynthesis pathways for vitamin C in plants: An opinion.–Phytochemistry 68: 2602–2613, 2007.CrossRefPubMedGoogle Scholar
  40. Xie J.Q., Li G.X., Wang X.K. et al.: [Effect of exogenous ascorbic acid on photosynthesis and growth of rice under O3 stress.]–Chin. J. Eco-Agr. 17: 1176–1181. 2009. [In Chinese]CrossRefGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2018

Authors and Affiliations

  1. 1.Guangzhou Key Laboratory of Subtropical Biodiversity and Biomonitor, Guangdong Provincial Key Laboratory of Biotechnology for Plant DevelopmentCollege of Life Science, South China Normal UniversityGuangzhouChina
  2. 2.School of Life ScienceHuizhou UniversityHuizhou City, Guangdong ProvinceChina
  3. 3.Division of Plant Science, Research School of Biology, College of Medicine, Biology and EnvironmentThe Australian National University, ActonAustralian Capital TerritoryAustralia

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