, Volume 54, Issue 1, pp 93–100 | Cite as

Growth irradiance affects ureide accumulation and tolerance to photoinhibition in Eutrema salsugineum (Thellungiella salsuginea)

  • V. M. Malik
  • J. M. Lobo
  • C. Stewart
  • S. Irani
  • C. D. Todd
  • G. R. Gray
Original Papers


Plants are able to acclimate to their growth light environments by utilizing a number of short- and long-term mechanisms. One strategy is to prevent accumulation of excess reactive oxygen species that can lead to photoinhibition of photosynthesis. Ureides, generated from purine degradation, have been proposed as antioxidants and involved in certain abiotic stress responses. Eutrema salsugineum (Thellungiella salsuginea) is an extremophilic plant known to exhibit a high degree of tolerance to a variety of abiotic stresses that invariably generate reactive oxygen species. In the present study we have investigated the possible role of the ureide metabolic pathway during acclimation to growth irradiance and its conference of tolerance to photoinhibition in Eutrema. Ureide accumulation was greater under high light growth which also conferred tolerance to photoinhibition at low temperature as measured by the maximal quantum yield of PSII photochemistry. This may represent an adaptive plastic response contributing to the extreme tolerance exhibited by this plant. Our results would provide evidence that ureide accumulation may be involved in abiotic stress as another defence mechanism in response to oxidative stress.

Additional key words

acclimation allantoin antioxidant reactive oxygen species 



abscisic acid




allantoate amidohydrolase






fresh mass


maximal quantum yield of PSII photochemistry


high light


moderate light


reactive oxygen species


semiquantitative reverse transcriptase-polymerase chain reaction


ureidoglycolate amidohydrolase


ureidoglycine aminohydrolase


urate oxidase


xanthine dehydrogenase


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  1. Alamillo J.M., Díaz-Leal J.L., Sánchez-Moran M.A.V., Pineda M.: Molecular analysis of ureide accumulation under drought stress in Phaseolus vulgaris L. — Plant Cell Environ. 33: 1828–1837, 2010.CrossRefPubMedGoogle Scholar
  2. Aro E.-M., Virgin I., Andersson B.: Photoinhibition of photosystem II. Inactivation, protein damage and turnover. — Biochim. Biophys. Acta 1143: 113–134, 1993.CrossRefPubMedGoogle Scholar
  3. Amtmann A.: Learning from evolution: Thellungiella generates new knowledge on essential and critical components of abiotic stress tolerance in plants. — Mol. Plant 2: 3–12, 2009.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Anderson J.M.: Photoregulation of the composition, function, and structure of thylakoid membranes. — Annu. Rev. Plant Physio. 37: 93–136, 1986.CrossRefGoogle Scholar
  5. Anderson J.M., Chow W.S., Park Y-I.: The grand design of photosynthesis: Acclimation of the photosynthetic apparatus to environmental cues. — Photosynth. Res. 46: 129–139, 1995.CrossRefPubMedGoogle Scholar
  6. Anderson J.M., Osmond C.B.: Shade-sun responses: compromises between acclimation and photoinhibition. — In: Kyle D.J., Osmond C.B., Arntzen C.J. (ed.): Topics in Photosynthesis, Vol. 9. Photoinhibition. Pp. 1–38. Elsevier, Amsterdam 1987.Google Scholar
  7. Asada K., Takahashi M.: Production and scavenging of active oxygen in photosynthesis. — In: Kyle D.J., Osmond C.B., Arntzen C.J. (ed.): Topics in Photosynthesis, Vol. 9, Photoinhibition. Pp. 227–287. Elsevier, Amsterdam 1987.Google Scholar
  8. Boardman N.K.: Comparative photosynthesis of sun and shade plants. — Annu. Rev. Plant Physio. 28: 355–377, 1977.CrossRefGoogle Scholar
  9. Brychkova G., Alikulov Z., Fluhr R., Sagi M.: A critical role for ureides in dark and senescence-induced purine remobilization is unmasked in the Atxdh1 Arabidopsis mutant. — Plant J. 54: 496–509, 2008.CrossRefPubMedGoogle Scholar
  10. Castro A.H.F., Young M.C.M., de Alvarenga A.A., Alves J.D.: Influence of photoperiod on the accumulation of allantoin in comfrey plants. — R. Bras. Fisiol. Veg. 13: 49–54, 2001.Google Scholar
  11. Chalker-Scott L.: Environmental significance of anthocyanins in plant stress responses. — Photochem. Photobiol. 70: 1–9,1999.CrossRefGoogle Scholar
  12. Chytyk C.J., Hucl P.J., Gray G.R.: Leaf photosynthetic properties and biomass accumulation of selected western Canadian spring wheat cultivars. — Can. J. Plant Sci. 91: 305–314, 2011.CrossRefGoogle Scholar
  13. Coleto I., Pineda M., Rodiño A.P. et al.: Comparison of inhibition of N2 fixation and ureide accumulation under water deficit in four common bean genotypes of contrasting drought tolerance. — Ann. Bot.-London 113: 1071–1082, 2014.CrossRefGoogle Scholar
  14. Demmig-Adams B., Adams W.W. III: Photoprotection and other responses of plants to high light stress. — Annu. Rev. Plant Phys. 43: 599–626, 1992.CrossRefGoogle Scholar
  15. Foyer C.H., Noctor G.: Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. — Antioxid. Redox Sign. 11: 861–905, 2009.CrossRefGoogle Scholar
  16. 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.CrossRefGoogle Scholar
  17. Givnish T.J.: Adaptation to sun and shade: A whole-plant perspective. — Aust. J. Plant Physiol. 15: 63–92, 1988.CrossRefGoogle Scholar
  18. Gould K.S., Markham K.R., Smith R.H., Goris J.J.: Functional role of anthocyanins in the leaves of Quintinia serrata A. Cunn. — J. Exp. Bot. 51: 1107–1115, 2000.CrossRefPubMedGoogle Scholar
  19. Gray G.R., Hope B.J., Qin X.Q. et al.: The characterization of photoinhibition and recovery during cold acclimation in Arabidopsis thaliana using chlorophyll fluorescence imaging. — Physiol. Plantarum 119: 365–375, 2003.CrossRefGoogle Scholar
  20. Griffith M., Timonin M., Wong A.C. et al.: Thellungiella: An Arabidopsis-related model plant adapted to cold temperatures. — Plant Cell Environ. 30: 529–538, 2007.CrossRefPubMedGoogle Scholar
  21. Guevara D.R., Champigny M.J., Tattersall A. et al.: Transcriptomic and metabolomic analysis of Yukon Thellungiella plants grown in cabinets and their natural habitat show phenotypic plasticity. — BMC Plant Biol. 12: 175, 2012.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Havaux M., Kloppstech K.: The protective functions of carotenoid and flavonoid pigments against excess visible radiation at chilling temperature investigated in Arabidopsis npq and tt mutants. — Planta 213: 953–966, 2001.CrossRefGoogle Scholar
  23. Hesberg C., Hänsch R., Mendel R.R., Bittner F.: Tandem orientation of duplicated xanthine dehydrogenase genes from Arabidopsis thaliana: differential gene expression and enzyme activities. — J. Biol. Chem. 279: 13547–13554, 2004.CrossRefPubMedGoogle Scholar
  24. Inan G., Zhang Q., Li P.H. et al.: Salt cress. A halophyte and cryophyte Arabidopsis relative model system and its applicability to molecular genetic analyses of growth and development of extremophiles. — Plant Physiol. 135: 1718–1737, 2004.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Järvi S., Suorsa M., Aro E.-M.: Photosystem II repair in plant chloroplasts - regulation, assisting proteins and shared components with photosystem II biogenesis. — Biochim. Biophys. Acta 1847: 900–909, 2015.CrossRefPubMedGoogle Scholar
  26. Kansal R., Kuhar K., Verma I. et al.: Improved and convenient method of RNA isolation from polyphenols and polysaccharide rich plant tissues. — Indian J. Exp. Biol. 47: 842–845, 2008.Google Scholar
  27. Kant S., Bi Y.M., Weretilnyk E. et al.: The Arabidopsis halophytic relative Thellungiella halophila tolerates nitrogenlimiting conditions by maintaining growth, nitrogen uptake, and assimilation. — Plant Physiol. 147: 1168–1180, 2008.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Karuppanapandian T., Moon J.C., Kim C. et al.: Reactive oxygen species in plants: their generation, signal transduction, and scavenging mechanisms. — Aust. J. Crop Sci. 5: 709–725, 2011.Google Scholar
  29. Kazachkova Y., Batushansky A., Cisneros A. et al.: Growth platform-dependent and -independent phenotypic and metabolic responses of Arabidopsis thaliana and its halophytic relative, Eutrema salsugineum, to salt stress. — Plant Physiol. 162: 1583–1598, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  30. King C.A., Purcell L.C.: Inhibition of N2 fixation in soybean is associated with elevated ureides and amino acids. — Plant Physiol. 137: 1389–1396, 2005.CrossRefPubMedPubMedCentralGoogle Scholar
  31. Koch M.A., German D.A.: Taxonomy and systematics are key to biological information: Arabidopsis, Eutrema (Thellungiella), Noccaea and Schrenkiella (Brassicaceae) as examples. — Front. Plant Sci. 4: 267, 2013.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Kono M., Terashima I.: Long-term and short-term responses of the photosynthetic electron transport to fluctuating light. — J. Photoch. Photobio. B 137: 89–99, 2014.CrossRefGoogle Scholar
  33. Lichtenthaler H.K., Wellburn A.R.: Determination of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. — Biochem. Soc. Trans. 11: 591–592,1983.CrossRefGoogle Scholar
  34. 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.CrossRefPubMedGoogle Scholar
  35. Nakashima K., Yamaguchi-Shinozaki K., Shinozaki K.: The transcriptional regulatory network in the drought response and its crosstalk in abiotic stress responses including drought, cold and heat. — Front. Plant Sci. 5: 170, 2014.CrossRefPubMedPubMedCentralGoogle Scholar
  36. Neill S.O., Gould K.S.: Anthocyanins in leaves: light attenuators or antioxidants? — Funct. Plant Biol. 30: 865–873, 2003.CrossRefGoogle Scholar
  37. Oliver M.J., Guo L., Alexander D.C. et al: A sister group contrast using untargeted global metabolomic analysis delineates the biochemical regulation underlying desiccation tolerance in Sporobolus stapfianus. — Plant Cell 23: 1231–1248, 2011.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Powles S.B.: Photoinhibition of photosynthesis induced by visible light. — Annu. Rev. Plant Physio. 35: 15–44, 1984.CrossRefGoogle Scholar
  39. Reinbothe H., Mothes K.: Urea, ureides, and guanidines in plants. — Annu. Rev. Plant Phys. 13: 129–150, 1962.CrossRefGoogle Scholar
  40. Sagi M., Omarov R.T., Lips S.H.: The Mo-hydroxylases xanthine dehydrogenase and aldehyde oxidase in ryegrass as affected by nitrogen and salinity. — Plant Sci. 135: 125–135, 1998.CrossRefGoogle Scholar
  41. Sambrook J., Russell D.W.: Molecular Cloning: A Laboratory Manual. 3rd Edition. Pp. 2100. Cold Spring Harbor Laboratory Press, New York 2001.Google Scholar
  42. Schneider C.A., Rasband W.S., Eliceiri K.W.: NIH Image to ImageJ: 25 years of image analysis. — Nat. Methods 9: 671–675, 2012.CrossRefPubMedGoogle Scholar
  43. Schubert K.R.: Products of biological nitrogen fixation in higher plants: synthesis, transport, and metabolism. — Annu. Rev. Plant Physio. 37: 539–574, 1986.CrossRefGoogle Scholar
  44. Serraj R., Sinclair T.R., Purcell L.C.: Symbiotic N2 fixation response to drought. — J. Exp. Bot. 50: 143–155, 1999.Google Scholar
  45. Stasolla C., Katahira R., Thorpe T.A., Ashihara H.: Purine and pyrimidine nucleotide metabolism in higher plants. — J. Plant Physiol. 160: 1271–1295, 2003.CrossRefPubMedGoogle Scholar
  46. Stepien P., Johnson G.N.: Contrasting responses of photosynthesis to salt stress in the glycophyte Arabidopsis and halophyte Thellungiella: Role of the plastid terminal oxidase as an alternative electron sink. — Plant Physiol. 149: 1154–1165, 2009.CrossRefPubMedPubMedCentralGoogle Scholar
  47. Sui N., Han G.: Salt-induced photoinhibition of PSII is alleviated in halophyte Thellungiella halophila by increases of unsaturated fatty acids in membrane lipids. — Acta Physiol. Plant. 36: 983–992, 2014.CrossRefGoogle Scholar
  48. Suzuki N., Koussevitzky S., Mittler R., Miller G.: ROS and redox signalling in the response of plants to abiotic stress. — Plant Cell Environ. 35: 259–270, 2012.CrossRefPubMedGoogle Scholar
  49. Takahashi S., Badger M.R.: Photoprotection in plants: a new light on photosystem II damage. — Trends Plant Sci. 16: 53–60, 2011.CrossRefPubMedGoogle Scholar
  50. Takahashi S., Murata N.: How do environmental stresses accelerate photoinhibition? — Trends Plant Sci. 13: 178–182, 2008.CrossRefPubMedGoogle Scholar
  51. Todd C.D., Tipton P.A., Blevins D.G. et al.: Update on ureide degradation in legumes. — J. Exp. Bot. 57: 5–12, 2006.CrossRefPubMedGoogle Scholar
  52. Ventura Y., Wuddineh W.A., Myrzabayeva M. et al.: Effect of seawater concentration on the productivity and nutritional value of annual Salicornia and perennial Sarcocornia halophytes as leafy vegetable crops. — Sci. Hortic.-Amsterdam 128: 189–196, 2011.CrossRefGoogle Scholar
  53. Vogels G.D., Van Der Drift C.: Differential analyses of glyoxylate derivatives. — Anal. Biochem. 33: 143–157, 1970.CrossRefPubMedGoogle Scholar
  54. Walters R.G.: Towards an understanding of photosynthetic acclimation. — J. Exp. Bot. 56: 435–447, 2005.CrossRefPubMedGoogle Scholar
  55. Wang P., Kong C.H, Sun B., Xu X.H.: Distribution and function of allantoin (5-ureidohydantoin) in rice grains. — J. Agric. Food Chem. 60: 2793–2798, 2012.CrossRefPubMedGoogle Scholar
  56. Watanabe S., Matsumoto M., Hakomori Y. et al.: The purine metabolite allantoin enhances abiotic stress tolerance through synergistic activation of abscisic acid metabolism. — Plant Cell Environ. 37: 1022–1036, 2014.CrossRefPubMedGoogle Scholar
  57. Watanabe S., Nakagawa A., Izumi S. et al.: RNA interferencemediated suppression of xanthine dehydrogenase reveals the role of purine metabolism in drought tolerance in Arabidopsis. — FEBS Lett. 584: 1181–1186, 2010.CrossRefPubMedGoogle Scholar
  58. Werner A.K., Witte C.P.: The biochemistry of nitrogen mobilization: purine ring catabolism. — Trends Plant Sci. 16: 381–387, 2011.CrossRefPubMedGoogle Scholar
  59. Wong C.E., Li Y., Labbe A. et al.: Transcriptional profiling implicates novel interactions between abiotic stress and hormonal responses in Thellungiella, a close relative of Arabidopsis. — Plant Physiol. 140: 1437–1450, 2006.CrossRefPubMedPubMedCentralGoogle Scholar
  60. Ye J., Coulouris G., Zaretskaya I. et al.: Primer-BLAST: A tool to design target-specific primers for polymerase chain reaction. — BMC Bioinformatics 13: 134, 2012.CrossRefPubMedPubMedCentralGoogle Scholar
  61. Yobi A., Wone B.W., Xu W. et al.: Metabolomic profiling in Selaginella lepidophylla at various hydration states provides new insights into the mechanistic basis of desiccation tolerance. — Mol. Plant 6: 369–385, 2013.CrossRefPubMedGoogle Scholar
  62. Zrenner R., Stitt M., Sonnewald U., Boldt R.: Pyrimidine and purine biosynthesis and degradation in plants. — Annu. Rev. Plant Biol. 57: 805–836, 2006CrossRefPubMedGoogle Scholar

Copyright information

© The Institute of Experimental Botany 2016

Authors and Affiliations

  • V. M. Malik
    • 1
    • 3
  • J. M. Lobo
    • 1
    • 3
  • C. Stewart
    • 2
  • S. Irani
    • 2
  • C. D. Todd
    • 2
  • G. R. Gray
    • 1
    • 3
  1. 1.Department of Plant SciencesUniversity of SaskatchewanSaskatoonCanada
  2. 2.Department of BiologyUniversity of SaskatchewanSaskatoonCanada
  3. 3.Department of BiochemistryUniversity of SaskatchewanSaskatoonCanada

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