Photosynthetica 2016, 54(1):93-100 | DOI: 10.1007/s11099-015-0164-8

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

V. M. Malik1,3, J. M. Lobo1,3, C. Stewart2, S. Irani2, C. D. Todd2, G. R. Gray1,3,*
1 Department of Plant Sciences, University of Saskatchewan, Saskatoon, Canada
2 Department of Biology, University of Saskatchewan, Saskatoon, Canada
3 Department of Biochemistry, University of Saskatchewan, Saskatoon, Canada

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.

Keywords: acclimation; allantoin; antioxidant; reactive oxygen species

Received: March 12, 2015; Accepted: June 22, 2015; Published: March 1, 2016Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Malik, V.M., Lobo, J.M., Stewart, C., Irani, S., Todd, C.D., & Gray, G.R. (2016). Growth irradiance affects ureide accumulation and tolerance to photoinhibition in Eutrema salsugineum (Thellungiella salsuginea). Photosynthetica, 54(1), 93-100. doi: 10.1007/s11099-015-0164-8.
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. 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.
    2. Aro E.-M., Virgin I., Andersson B.: Photoinhibition of photosystem II. Inactivation, protein damage and turnover. - Biochim. Biophys. Acta 1143: 113-134, 1993. Go to original source...
    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. Go to original source...
    4. Anderson J.M.: Photoregulation of the composition, function, and structure of thylakoid membranes. - Annu. Rev. Plant Physio. 37: 93-136, 1986. Go to original source...
    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. Go to original source...
    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.
    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.
    8. Boardman N.K.: Comparative photosynthesis of sun and shade plants. - Annu. Rev. Plant Physio. 28: 355-377, 1977. Go to original source...
    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. Go to original source...
    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. Go to original source...
    11. Chalker-Scott L.: Environmental significance of anthocyanins in plant stress responses. - Photochem. Photobiol. 70: 1-9,1999. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    15. Foyer C.H., Noctor G.: Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. - Antioxid. Redox Sign. 11: 861-905, 2009. Go to original source...
    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. Go to original source...
    17. Givnish T.J.: Adaptation to sun and shade: A whole-plant perspective. - Aust. J. Plant Physiol. 15: 63-92, 1988. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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.
    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.
    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. Go to original source...
    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.
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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.
    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. Go to original source...
    36. Neill S.O., Gould K.S.: Anthocyanins in leaves: light attenuators or antioxidants? - Funct. Plant Biol. 30: 865-873, 2003. Go to original source...
    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. Go to original source...
    38. Powles S.B.: Photoinhibition of photosynthesis induced by visible light. - Annu. Rev. Plant Physio. 35: 15-44, 1984. Go to original source...
    39. Reinbothe H., Mothes K.: Urea, ureides, and guanidines in plants. - Annu. Rev. Plant Phys. 13: 129-150, 1962. Go to original source...
    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. Go to original source...
    41. Sambrook J., Russell D.W.: Molecular Cloning: A Laboratory Manual. 3rd Edition. Pp. 2100. Cold Spring Harbor Laboratory Press, New York 2001.
    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. Go to original source...
    43. Schubert K.R.: Products of biological nitrogen fixation in higher plants: synthesis, transport, and metabolism. - Annu. Rev. Plant Physio. 37: 539-574, 1986. Go to original source...
    44. Serraj R., Sinclair T.R., Purcell L.C.: Symbiotic N2 fixation response to drought. - J. Exp. Bot. 50: 143-155, 1999. Go to original source...
    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. Go to original source...
    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.
    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. Go to original source...
    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. Go to original source...
    49. Takahashi S., Badger M.R.: Photoprotection in plants: a new light on photosystem II damage. - Trends Plant Sci. 16: 53-60, 2011. Go to original source...
    50. Takahashi S., Murata N.: How do environmental stresses accelerate photoinhibition? - Trends Plant Sci. 13: 178-182, 2008. Go to original source...
    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. Go to original source...
    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. Go to original source...
    53. Vogels G.D., Van Der Drift C.: Differential analyses of glyoxylate derivatives. - Anal. Biochem. 33: 143-157, 1970. Go to original source...
    54. Walters R.G.: Towards an understanding of photosynthetic acclimation. - J. Exp. Bot. 56: 435-447, 2005.
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    58. Werner A.K., Witte C.P.: The biochemistry of nitrogen mobilization: purine ring catabolism. - Trends Plant Sci. 16: 381-387, 2011. Go to original source...
    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. Go to original source...
    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. Go to original source...
    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. Go to original source...
    62. Zrenner R., Stitt M., Sonnewald U., Boldt R.: Pyrimidine and purine biosynthesis and degradation in plants. - Annu. Rev. Plant Biol. 57: 805-836, 2006 Go to original source...

    Return to the content