Photosynthetica 2015, 53(3):369-377 | DOI: 10.1007/s11099-015-0129-y

Structural and functional changes in the photosynthetic apparatus of Chlamydomonas reinhardtii during nitrogen deprivation and replenishment

É. Preininger1,*, A. Kósa1, Z. S. Lőrincz1, P. Nyitrai2, J. Simon1, B. Böddi1, Á. Keresztes1, I. Gyurján1
1 Department of Plant Anatomy, Eötvös Loránd University, Budapest, Hungary
2 Department of Plant Physiology and Molecular Plant Biology, Eötvös Loránd University, Budapest, Hungary

Nitrogen is an essential factor for normal plant and algal development. As a component of nucleic acids, proteins, and chlorophyll (Chl) molecules, it has a crucial role in the organization of a functioning photosynthetic apparatus. Our aim was to study the effects of nitrogen starvation in cultures of the unicellular green alga, Chlamydomonas reinhardtii, maintained on nitrogen-free, and then on nitrogen-containing medium. During the three-week-long degreening process, considerable changes were observed in the Chl content, the ratio of Chl-protein complexes, and photosynthetic activity of the cultures as well as in the ultrastructure of single chloroplasts. The regreening process was much faster then the degradation; total greening of the cells occurred within four days. The rate of regeneration depended on the nitrogen content. At least 50% of the normal nitrogen content of Tris-Acetate-Phosphate (TAP) medium was required in the medium for the complete regreening of the cells and regeneration of chloroplasts.

Additional key words: electron microscopy; nitrogen starvation; O2 evolution; 77K fluorescence

Received: August 29, 2014; Accepted: January 22, 2015; Published: September 1, 2015  Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Preininger, É., Kósa, A., Lőrincz, Z.S., Nyitrai, P., Simon, J., Böddi, B., Keresztes, Á., & Gyurján, I. (2015). Structural and functional changes in the photosynthetic apparatus of Chlamydomonas reinhardtii during nitrogen deprivation and replenishment. Photosynthetica, 53(3), 369-377. doi: 10.1007/s11099-015-0129-y
Share...
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

    Supplementary files

    Download filephs-201503-0006_S1.pdf

    File size: 268.12 kB

    References

    1. Abe J., Kubo T., Takagi Y. et al.: The transcriptional program of synchronous gametogenesis in Chlamydomonas reinhardtii. - Curr. Genet. 46: 304-315, 2004. Go to original source...
    2. Abe J., Kubo T., Saito T. et al.: The regulatory networks of gene expression during the sexual differentiation of Chlamydomonas reinhardtii, as analyzed by mutants for gametogenesis. - Plant Cell Physiol. 46: 312-316, 2005. Go to original source...
    3. Appenroth K.J., Keresztes Á., Sárvári É. et al.: Multiple effects of chromate on Spirodela polyrhiza: Electron microscopy and biochemical investigations. - Plant Biol. 5: 315-323, 2003. Go to original source...
    4. Aseeva E., Ossenbühl F., Eichacker L.A. et al.: Complex formation of Vipp1 depends on its α-helical PspA-like domain. - J. Biol. Chem. 279: 35535-35541, 2004. Go to original source...
    5. Baszyński T., Pańczyk B., Król M. et al.: The effect of nitrogen deficiency on some aspects of photosynthesis in maize leaves. - Z. Pflanzenphysiol. 74: 200-207, 1975. Go to original source...
    6. Beardall J., Roberts S., Millhouse J.: Effects of nitrogen limitation on uptake of inorganic carbon and specific activity of ribulose-1,5-bisphosphate carboxylase/oxygenase in green microalgae. - Can. J. Bot. 69: 1146-1150, 1991. Go to original source...
    7. Beck C.F., Haring M.A.: Gametic differentiation of Chlamydomonas. - Int. Rev. Cytol. 168: 259-302, 1996. Go to original source...
    8. Bennoun P.: The present model for chlororespiration. - Photosynth. Res. 73: 273-277, 2002. Go to original source...
    9. Berges J.A., Charlebois D.O., Mauzerall D.C. et al.: Differential effects of nitrogen limitation on photosynthetic efficiency of photosystems I and II in microalgae. - Plant Physiol. 110: 689-696, 1996. Go to original source...
    10. Bouma D.: Effects of nitrogen nutrition on leaf expansion and photosynthesis of Trifolium subterraneum L. Comparison between different levels of nitrogen supply. - Ann. Bot. 34: 1131-1142, 1970. Go to original source...
    11. Coleman L.W., Rosen B.H., Schwartzbach S.D.: Preferential loss of chloroplast proteins in nitrogen deficient Euglena. - Plant Cell Physiol. 29: 1007-1014, 1988.
    12. Davies J.P., Grossman A.R.: The use of Chlamydomonas (Chlorophyta: Volvocales) as a model algal system for genome studies and the elucidation of photosynthetic processes. - J. Phycol. 34: 907-917, 1998. Go to original source...
    13. Doncheva S., Vassileva V., Ignatov G. et al.: Influence of nitrogen deficiency on photosynthesis and chloroplast ultrastructure of pepper plants. - Agr. Food Sci. Finland 10: 59-64, 2001. Go to original source...
    14. Fernandez E., Galvan A.: Inorganic nitrogen assimilation in Chlamydomonas. - J. Exp. Bot. 58: 2279-2287, 2007. Go to original source...
    15. Fernandez E., Galvan A.: Nitrate assimilation in Chlamydomonas. - Eucaryot. Cell. 7: 555-559, 2008. Go to original source...
    16. Giordano M., Kansiz M., Heraud P. et al.: Fourier transformation infrared pectroscopy as a novel tool to investigate changes in intracellular macromolecular pools in the marine microalga Chaetoceros muellerii (Bacillariophyceae). - J. Phycol. 37: 271-279, 2001. Go to original source...
    17. Goodenough U.W., Levine R.P.: Chloroplast ultrastructure in mutant strains of Chlamydomonas reinhardi lacking components of the photosynthetic apparatus. - Plant Physiol. 44: 990-1000, 1969. Go to original source...
    18. Guiaimét J.J., Pichersky E., Noodén L.D.: Mass exodus from senescing soybean chloroplasts. - Plant Cell Physiol. 40: 986-992, 1999. Go to original source...
    19. Gyurján I., Erdős G., Keresztes Á. et al.: Photosynthetic functions and structure in pigment-deficient mutants of Chlamydomonas reinhardtii. - Photosynthetica 14: 12-16, 1980.
    20. Gyurján I., Nagy A.H., Erdős G. et al.: Photosynthetic functions and thylakoid membrane polipeptide composition in lightsensitive mutants of Chlamydomonas reinhardtii. - Photosynth. Res. 3: 255-271, 1982. Go to original source...
    21. Hoober J.K., Boyd C.O., Paavola L.G.: Origin of tylakoid membranes in Chlamydomonas reinhardtii y-1 at 38°C. - Plant Physiol. 96: 1321-1328, 1991. Go to original source...
    22. James G.O., Hocart C.H., Hillier W. et al.: Fatty acid profiling of Chlamydomonas reinhardtii under nitrogen deprivation. - Bioresource Technol. 102: 3343-3351, 2011. Go to original source...
    23. Joyard J., Teyssier E., Miège C. et al.: The biochemical machinery of plastid envelope membranes. - Plant Physiol. 118: 715-723, 1998. Go to original source...
    24. Komatsu M., Waguri S., Ueno T. et al.: Impairment of starvationinduced and constitutive autophagy in Atg7-deficient mice. - J. Cell Biol. 169: 425-434, 2005. Go to original source...
    25. Kroll D., Meierhoff K., Bechtold N. et al..: VIPP1, a nuclear gene of Arabidopsis thaliana essential for thylakoid membrane formation. - P. Natl. Acad. Sci. USA 98: 4238-4242, 2001. Go to original source...
    26. Kutík J., Činčerová A., Dvořák M.: Chloroplasts ultrastructural development during the ontogeny of the second leaf of wheat under nitrogen deficiency. - Photosynthetica 28: 447-453, 1993.
    27. Lawlor D.W., Kontturi M., Young A.T.: Photosynthesis by flag leaves of wheat in relation to protein, ribulose bisphosphate carboxilase activity and nitrogen supply. - J. Exp. Bot. 40: 43-52, 1989. Go to original source...
    28. Martin N.C., Goodenough U.W.: Gametic differentiation in Chlamydomonas reinhardtii. I. Production of gametes and their fine structure. - J. Cell Biol. 67: 587-605, 1975. Go to original source...
    29. Mayer F., Czygan F.C.: [Ultarstructural changes in the green algae Ankistrodesmus braunii and Chlorella fusca var. rubescens under conditions of nitrogen deficiency.] - Planta 86: 175-185, 1969. [In German] Go to original source...
    30. McLean R.J.: Ultrastructure of Spongiochloris typica during senescence. - J. Phycol. 4: 277-283, 1968. Go to original source...
    31. Morgan-Kiss R., Ivanov A.G., Williams J. et al.: Differential thermal effects on the energy distribution between photosystem II and photosystem I in thylakoid membranes of a psychrophilic and a mesophilic alga. - Biochim. Biophys. Acta 1561: 251-265, 2002. Go to original source...
    32. Nyitrai P., Mayer M., Óvári M. et al.: Involvement of the phosphoinositide signaling pathway in the anti-senescence effect of low-concentration stressors on detached barley leaves. - Plant Biol. 9: 420-426, 2007. Go to original source...
    33. Onodera J., Ohsumi Y.: Autophagy is required for maintenance of amino acid levels and protein synthesis under nitrogen starvation. - J. Biol. Chem. 280: 31582-31586, 2005. Go to original source...
    34. Ossenbühl F., Göhre V., Meurer J. et al.: Efficient assembly of photosystem II in Chlamydomonas reinhardtii requires Alb3.1p, a homolog of Arabidopsis ALBINO3. - Plant Cell. 16: 1790-1800, 2004. Go to original source...
    35. Ördög V., Stirk W.A., Bálint P. et al: Changes in lipid, protein and pigment concentrations in nitrogen-stressed Chlorella minutissima cultures. - J. Appl. Phycol. 24: 907-914, 2012. Go to original source...
    36. Plumley F.G., Schmidt G.W.: Nitrogen-dependent regulation of photosynthetic gene expression. - P. Natl. Acad. Sci. USA 86: 2678-2682, 1989. Go to original source...
    37. Porra R.J., Thomson W.A., Kriedemann P.E.: Determination of accurate extinction coefficients and simultaneous equations for assaying chlorophyll a and b extracted with different solvents: verification of the concentration of chlorophyll standards by atomic absorption spectroscopy. - BBA-Bioenergetics 975: 384-394, 1989. Go to original source...
    38. Pyliotis N.A., Goodchild D.J., Grimme LH.: The regreening of nitrogen-deficient Chlorella fusca II. Structural changes during synchronous regreening. - Arch. Microbiol. 103: 259-270, 1975. Go to original source...
    39. Sager R., Granick S.: Nutritional studies with Chlamydomonas reinhardtii. - Ann. N.Y. Acad. Sci. 56: 831-838, 1953. Go to original source...
    40. Sayed O.H.: Analysis of photosynthetic responses and adaptation to nitrogen starvation in Chlorella using in vivo chlorophyll fluorescence. - Photosynthetica 35: 611-619, 1998. Go to original source...
    41. Scott N.S., Possingham J.V.: Changes in chloroplast DNA levels during growth of spinach leaves. - J. Exp. Bot. 34: 1756-1767, 1983. Go to original source...
    42. Semenenko V.E., Vladimirova M.G., Orleanskaya O.B. et al.: [Physiological characteristics of Chlorella sp. K at high extremal temperatures. II. Changes in biosyntheses, ultrastructure and activity of photosynthetic apparatus during uncoupling of cellular functions by extreme temperature.] - Fiziol. Rast. 16: 210-220, 1969. [In Russian]
    43. Shtaida N., Khozin-Goldberg I., Solovchenko A. et al.: Downregulation of a putative plastid PDC E1α subunit impairs photosynthetic activity and triacylglycerol accumulation in nitrogen-starved photoautotrophic Chlamydomonas reinhardtii. - J. Exp. Bot. 65: 6563-6576, 2014. Go to original source...
    44. Sinetova M.P., Markelova A.G., Los D.A.: The effect on nitrogen starvation on the ultrastructure and pigment composition of chloroplasts in the acidothermophylic microalga Galdieria sulphuraria. - Russ. J. Plant Physiol. 53: 153-162, 2006. Go to original source...
    45. Verhoeven A.S., Demmig-Adams B., Adams W.W.: Enhanced employment of the xanthophyll cycle and thermal energy dissipation in spinach exposed to hight light and N stress. - Plant Physiol. 113: 817-824, 1997. Go to original source...
    46. Wang Z.T., Ullrich N., Joo S. et al.: Algal lipid bodies: Stress induction, purification and biochemical characterization in wild-type and starchless Chlamydomonas reinhardtii. - Eukaryot. Cell 8: 1856-1868, 2009. Go to original source...
    47. Wase N., Black P.N., Stanley B.A., DiRusso C.C.: Integrated quantitative analysis of nitrogen stress response in Chlamydomonas reinhardtii using metabolite and protein profiling. - J. Proteome Res. 13: 1373-1396, 2014. Go to original source...
    48. Wei L., Derrien B., Gautier A. et al.: Nitric oxide-triggered remodeling of chloroplast bioenergetics and thylakoid proteins upon nitrogen starvation in Chlamydomonas reinhardtii. - Plant Cell 26: 353-372, 2014. Go to original source...
    49. Work V.H., Radakovits R., Jinkerson RE. et al.: Increased lipid accumulation in the Chlamydomonas reinhardtii sta7-10 starchless isoamylase mutant and increased carbohydrate synthesis in complemented strains. - Eukaryot. Cell 9: 1251-1261, 2010. Go to original source...
    50. Young E.B., Beardall J.: Photosynthetic function in Dunaliella tertiolecta (Chlorophyta) during a nitrogen starvation and recovery cycle. - J. Phycol. 39: 897-905, 2003. Go to original source...
    51. Yu S., Zhao Q., Miao X., Shi J.: Enhancement of lipid production in low-starch mutants Chlamydomonas reinhardtii by adaptive laboratory evolution. - Biores. Technol. 147: 499-507, 2013. Go to original source...
    52. Zhao D., Reddy K.R., Kakani V.G. et al.: Nitrogen deficiency effects on plant growth, leaf photosynthesis, and hyperspectral reflectance properties of sorgum. - Eur. J. Agro. 22: 391-403, 2005. Go to original source...

    Return to the content