Unraveling the regulation of nitrogen assimilation in the marine diatom thalassiosira pseudonana (bacillariophyceae): Diurnal variations in transcript levels for five genes involved in nitrogen assimilation

Journal of Phycology

Volumn 45, Issue 2, 2009, Pages 413-426

  Brown, Kathryn L ^a   Twing, Katrina I ^a,b   Robertson, Deborah L ^a  

^a CLARK UNIVERSITY   (United States)

^b UNIVERSITY OF DELAWARE   (United States)

Author keywords

Diatoms; Gene expression; Glutamine synthetase; Nitrate reductase; Nitrite reductase; Nitrogen assimilation; Quantitative real time PCR

Indexed keywords

BACILLARIOPHYCEAE; BACILLARIOPHYTA; NIA; NITZSCHIA ALBA; THALASSIOSIRA PSEUDONANA;

EID: 64349114666     PISSN: 00223646     EISSN: 15298817     Source Type: Journal    
DOI: 10.1111/j.1529-8817.2009.00648.x     Document Type: Article

References (74)

1. Allen, A. E., Vardi, A. Bowler, C. 2006. An ecological and evolutionary context for integrated nitrogen metabolism and related signaling pathways in marine diatoms. Curr. Opin. Plant Biol. 9 : 264 73.
2. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. Lipman, D. J. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acid Res. 25 : 3389 402.
3. Armbrust, E. V., Berges, J. A., Bowler, C., Green, B. R., Martinez, D., Putnam, N. H., Zhou, S., et al. 2004. The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306 : 79 86.
4. Berges, J. A. 1997. Algal nitrate reductase. Eur. J. Phycol. 32 : 3 8.
5. Berges, J. A., Cochlan, W. P. Harrison, P. J. 1995. Laboratory and field responses of algal nitrate reductase to diel periodicity in irradiance, nitrate exhaustion, and the presence of ammonium. Mar. Ecol. Prog. Ser. 124 : 259 69.
6. Berges, J. A. Harrison, P. J. 1995. Nitrate reductase activity quantitatively predicts the rate of nitrate incorporation under steady state light limitation: a revised assay and characterization of the enzyme in three species of phytoplankton. Limnol. Oceanogr. 40 : 82 93.
7. Blasing, O. E., Gibon, Y., Gunther, M., Hohne, M., Morcuende, R., Osuna, D., Thimm, O., Usadel, B., Scheible, W.-R. Stitt, M. 2005. Sugars and circadian regulation make major contributions to the global regulation of diurnal gene expression in Arabidopsis. Plant Cell. 17 : 3257 81.
8. Bode, A., Botas, J. A. Fernandez, E. 1997. Nitrate storage by phytoplankton in a coastal upwelling environment. Mar. Biol. 129 : 399 406.
9. Bruland, K. W., Rue, E. L., Smith, G. J. DiTullio, G. R. 2005. Iron, macronutrients and diatom blooms in the Peru upwelling regime: brown and blue waters of Peru. Mar. Chem. 93 : 81 103.
10. Clark, D. R., Flynn, K. J. Owens, N. J. P. 2002. The large capacity for dark nitrate-assimilation in diatoms may overcome nitrate limitation of growth. J. Phycol. 155 : 101 8.
11. Colandene, J. D. Garrett, R. H. 1996. Functional dissection and site-directed mutagenesis of the structural gene for NAD(P)H-nitrite reductase in Neurospora crassa. J. Biol. Chem. 271 : 24096 104.
12. Collos, Y. 1986. Time-lag algal growth dynamics: biological constraints on primary production in aquatic environments. Mar. Ecol. Prog. Ser. 33 : 193 206.
13. Dickson, M. L. Wheeler, P. A. 1995. Ammonium uptake and regeneration rates in a coastal upwelling regime. Mar. Ecol. Prog. Ser. 121 : 239 48.
14. Dortch, Q. 1990. The interaction between ammonium and nitrate uptake in phytoplankton. Mar. Ecol. Prog. Ser. 61 : 183 201.
15. Dortch, Q., Clayton, J. R., Thoresen, S. S. Ahmed, S. I. 1984. Species differences in accumulation of nitrogen pools in phytoplankton. Mar. Biol. 81 : 237 50.
16. Duarte, C. M. 1990. Time lags in algal growth: generality, causes and consequences. J. Plankton Res. 12 : 873 83.
17. Dugdale, R. C., Wilkerson, F. P. Morel, A. 1990. Realization of new production in coastal upwelling areas: a means to compare relative performance. Limnol. Oceanogr. 35 : 822 9.
18. Emanuelsson, O., Nielsen, H., Brunak, S. von Heijne, G. 2000. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J. Mol. Biol. 300 : 1005 16.
19. Emanuelsson, O., Nielsen, H. von Heijne, G. 1999. ChloroP, a neural network-based method for predicting chloroplast transit peptides and their cleavage sites. Protein Sci. 8 : 978 84.
20. Foyer, C. H., Parry, M. Noctor, G. 2003. Markers and signals associated with nitrogen assimilation in higher plants. J. Exp. Bot. 54 : 585 93.
21. Gao, Y. 1997. Nitrate assimilation: biochemical and environmental control. Ph.D. dissertation, Dept. of Biological Sciences, University of Southern California, Los Angeles, 200 pp.
22. Garg, R. P., Vargo, C. J., Cui, X. Kurtz, D. M. 1996. A [2Fe-2S] protein encoded by an open reading frame upstream of the Escherichia coli bacterioferritin gene. Biochemistry 35 : 6297 301.
23. Giordano, M., Chen, Y.-B., Koblizek, M. Falkowski, P. G. 2005. Regulation of nitrate reductase in Chlamydomonas reinhardtii by the redox state of the plastoquinone pool. Eur. J. Phycol. 40 : 345 52.
24. Gruber, A., Vugrinec, S., Hempel, F., Gould, S. B., Maier, U.-G. Kroth, P. G. 2007. Protein targeting into complex diatom plastids: functional characterisation of a specific targeting motif. Plant Mol. Biol. 64 : 519 30.
25. Guillard, R. 1975. Culture of phytoplankton for feeding marine invertebrates. In Smith, W. Chanley, M. [Eds.] Culture of Marine Invertebrate Animals. Plenum Press, New York, pp. 29 60.
26. Guillard, R. Ryther, J. H. 1962. Studies of marine planktonic diatoms I. Cyclotella nana Hustedt and Detonula confervacea Cleve. Can. J. Microbiol. 8 : 229 39.
27. 3/4-) in seawater. Aquac. Res. 34 : 1201 4.
28. Hildebrand, M. 2005. Cloning and functional characterization of ammonium transporters from the marine diatom Cylindrotheca fusiformis (Bacillariophyceae). J. Phycol. 41 : 105 13.
29. Hildenbrand, M. Dahlin, K. 2000. Nitrate transporter genes from the diatom Cylindrotheca fusiformis (Bacillariophyceae): mRNA levels controlled by nitrogen and during the cell cycle. J. Phycol. 36 : 702 13.
30. Hodges, M. 2002. Enzyme redundancy and the importance of 2-oxoglutarate in plant ammonium assimilation. J. Exp. Bot. 53 : 905 16.
31. Huppe, H. C. Turpin, D. H. 1994. Integration of carbon and nitrogen metabolism in plant and algal cells. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45 : 557 607.
32. Jochem, F. J., Smith, G. J., Gao, Y., Zimmerman, R. C., Cabello-Pasini, A., Kohrs, D. G. Alberte, R. S. 2000. Cytometric quantification of nitrate reductase by immunolabeling in the marine diatom Skeletonema costatum. Cytometry 3 : 173 8.
33. Jones, M. N. 1984. Nitrate reduction by shaking with cadmium: alternative to cadmium columns. Water Res. 18 : 643 6.
34. Kilian, O. Kroth, P. G. 2005. Identification and characterization of a new conserved motif within the presequence of proteins targeted into complex diatom plastids. Plant J. 41 : 175 83.
35. Krishnamurthy, N., Brown, D., Kirshner, D. Sjölander, K. 2006. PhyloFacts: an online structural phylogenomic encyclopedia for protein functional and structural classification. Genome Biol. 7 : R83.
36. Kroth, P. G., Chiovitti, A., Gruber, A., Martin-Jezequel, V., Mock, T., Parker, M. S., Stanley, M. S., et al. 2008. A model for carbohydrate metabolism in the diatom Phaeodactylum tricornutum deduced from comparative whole genome analysis. PLoS ONE 3 : e1426.
37. Kudela, R. M., Cochlan, W. P. Dugdale, R. C. 1997. Carbon and nitrogen uptake response to light by phytoplankton during an upwelling event. J. Plankton Res. 19 : 609 30.
38. Kudela, R. M. Dugdale, R. C. 2000. Nutrient regulation of phytoplankton productivity in Monterey Bay, California. Deep-Sea Res. Part II. 47 : 1023 53.
39. Lam, H.-M., Coschigano, K. T., Oliveira, I. C., Melo-Oliveira, R. Coruzzi, G. M. 1996. The molecular-genetics of nitrogen assimilation into amino acids in higher plants. Annu. Rev. Plant Physiol. Mol. Biol. 47 : 569 93.
40. Lancien, M., Gadal, P. Hodges, M. 2000. Enzyme redundancy and the importance of 2-oxoglutarate in higher plant ammonium assimilation. Plant Physiol. 123 : 817 24.
41. Lea, P. J. 1993. Nitrogen metabolism. In Lea, P. J. Leegood, R. C. [Eds.] Plant Biochemistry and Molecular Biology. John Wiley and Sons, New York, pp. 312.
42. Lehman, A., O'Rouke, N., Hatcher, L. Stepanski, E. J. 2005. JMP for Basic Univariate and Multivariate Statistics: A Step-by-Step Guide. SAS Institute Inc., Cary, North Carolina, 481 pp.
43. Lillo, C., Meyer, C. Ruoff, P. 2001. The nitrate reductase circadian system. The central clock dogma contra multiple oscillatory feedback loops. Plant Physiol. 125 : 1554 7.
44. -ΔΔCt method. Methods 25 : 402 8.
45. Lomas, M. W. Glibert, P. M. 1999a. Temperature regulation of nitrate uptake: a novel hypothesis about nitrate uptake and reduction in cool-water diatoms. Limnol. Oceanogr. 44 : 556 72.
46. - uptake and assimilation: comparison of diatoms and dinoflagellates at several growth temperatures. Mar. Biol. 133 : 541 51.
47. Luu-The, V., Paquet, N., Calvo, E. Cumps, J. 2005. Improved real-time RT-PCR method for high-throughput measurements using second derivative calculation and double correction. BioTechniques 38 : 297 3.
48. Marchler-Baue, A., Anderson, J., Derbyshire, M., DeWeese-Scott, C., Gonzales, N., Gwadz, M., Hao, L. et al. 2007. CDD: a conserved domain database for interactive domain family analysis. Nucleic Acids Res. 35 : D237 40.
49. Milligan, A. J. Harrison, P. J. 2000. Effects on non-steady-state iron limitation on nitrogen assimilatory enzymes in the marine diatom Thalassiosira weissflogii (Bacillariophyceae). J. Phycol. 36 : 78 86.
50. - and nitrogen isotope fractionation by marine phytoplankton. J. Phycol. 40 : 505 16.
51. Nielsen, H., Engelbrecht, J., Brunak, S. von Heijne, G. 1997. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10 : 1 6.
52. Olmo-Mira, M. F., Cabello, P., Pino, C., Martinez-Luque, M., Richardson, D. J., Castillo, F., Roldan, M. D. Moreno-Vivian, C. 2006. Expression and characterization of the assimilatory NADH-nitrite reductase from the phototrophic bacterium Rhodobacter capsulatus E1F1. Arch. Microbiol. 186 : 339 44.
53. Palenchar, P., Kouranov, A., Lejay, L. Coruzzi, G. 2004. Genome-wide patterns of carbon and nitrogen regulation of gene expression validate the combined carbon and nitrogen (CN)-signaling hypothesis in plants. Genome Biol. 5 : R91.
54. Parker, M. S. Armbrust, E. V. 2005. Synergistic effects of light, temperature and nitrogen source on transcription of genes for carbon and nitrogen metabolism in the centric diatom Thalassiosira pseudonana (Bacillariophyceae). J. Phycol. 41 : 1142 53.
55. Parsons, T. R., Maita, Y. Lalli, C. M. 1984. A Manual of Chemical and Biological Methods for Seawater Analysis. Pergamon Press, New York, 173 pp.
56. Poulsen, N., Chesley, P. M. Kröger, N. 2006. Molecular genetic manipulation of the diatom Thalassiosira pseudonana (Bacillariophyceae). J. Phycol. 42 : 1059 65.
57. Poulsen, N. Kroger, N. 2005. A new molecular tool for transgenic diatoms. Control of mRNA and protein biosynthesis by an inducible promoter-terminator cassette. FEBS J. 272 : 7413 23.
58. Roberts, K., Granum, E., Leegood, R. C. Raven, J. A. 2007. C3 and C4 pathways of photosynthetic carbon assimilation in marine diatoms are under genetic, not environmental, control. Plant Physiol. 145 : 230 45.
59. Robertson, D. L. Alberte, R. S. 1996. Isolation and characterization of glutamine synthetase from the marine diatom Skeletonema costatum. Plant Physiol. 111 : 1169 75.
60. Robertson, D. L., Smith, G. J. Alberte, R. S. 1999. Characterization of a cDNA encoding glutamine synthetase from the marine diatom Skeletonema costatum (Bacillariophyceae). J. Phycol. 35 : 786 97.
61. Sambrook, J. Russell, D. 2001. Molecular Cloning: A Laboratory Manual. 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 999 pp.
62. Scheible, W.-R., Morcuende, R., Czechowski, T., Fritz, C., Osuna, D., Palacios-Rojas, N., Schindelasch, D., Thimm, O., Udvardi, M. K. Stitt, M. 2004. Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol. 136 : 2483 99.
63. Smith, G. J., Zimmerman, R. C. Alberte, R. S. 1992. Molecular and physiological responses of diatoms to variable levels of irradiance and nitrogen availability: growth of Skeletonema costatum in simulated upwelling conditions. Limnol. Oceanogr. 37 : 989 1007.
64. Stitt, M. 1999. Nitrate regulation of metabolism and growth. Curr. Opin. Plant Biol. 2 : 178 86.
65. Stitt, M., Muller, C., Matt, P., Gibon, Y., Carillo, P., Morcuende, R., Scheible, W.-R. Krapp, A. 2002. Steps towards an integrated view of nitrogen metabolism. J. Exp. Bot. 53 : 959 70.
66. Swamy, U., Wang, M., Tripathy, J. N., Kim, S.-K., Hirasawa, M., Knaff, D. B. Allen, J. P. 2005. Structure of spinach nitrite reductase: implications for multi-electron reactions by the iron-sulfur:siroheme cofactor. Biochemistry 44 : 16054 63.
67. Takabayashi, M., Wilkerson, F. P. Robertson, D. L. 2004. Response of glutamine synthetase gene transcription and enzyme activity to external nitrogen sources in the diatom Skeletonema costatum (Bacillariophyceae). J. Phycol. 41 : 84 94.
68. Thompson, J. D., Higgins, D. G. Gibson, T. J. 1994. Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acid Res. 22 : 4673 80.
69. Turpin, D. H. 1991. Effects of inorganic N availability on algal photosynthesis and carbon metabolism. J. Phycol. 27 : 14 20.
70. Vergara, J. J., Berges, J. A. Falkowski, P. G. 1998. Diel periodicity of nitrate reductase activity and protein levels in the marine diatom Thalassiorsira weissflogii (Bacillariophyceae). J. Phycol. 34 : 952 61.
71. Wang, R., Guegler, K., LaBrie, S. T. Crawford, N. M. 2000. Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate. Plant Cell. 12 : 1491 510.
72. Wilkerson, F. P., Dugdale, R. C., Kudela, R. M. Chavez, F. P. 2000. Biomass and productivity in Monterey Bay, California: contribution of the large phytoplankton. Deep-Sea Res. Part II. 47 : 1003 22.
73. Wray, J. L. 1993. Molecular biology, genetics and regulation of nitrite reductase in higher plants. Physiol. Plant. 89 : 607 12.
74. 13N. J. Phycol. 24 : 588 91.