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Plant Physiol, February 2002, Vol. 128, pp. 463-471
Oxygen Deficiency Responsive Gene Expression in
Chlamydomonas reinhardtii through a Copper-Sensing Signal
Transduction Pathway1
Jeanette M.
Quinn,
Mats
Eriksson,2
Jeffrey L.
Moseley, and
Sabeeha
Merchant*
Department of Chemistry and Biochemistry (J.M.Q., M.E., J.L.M.,
S.M.) and Molecular Biology Institute (J.M., S.M.), University of
California, Los Angeles, California 90095-1569
Chlamydomonas reinhardtii activates
Cpx1, Cyc6, and Crd1,
encoding, respectively, coproporphyrinogen oxidase, cytochrome
c6,and a novel di-iron enzyme when
transferred to oxygen-deficientgrowth conditions. This response is
physiologically relevant becauseC. reinhardtii
experiences these growth conditions routinely,and furthermore, one of
the target genes, Crd1, is functionallyrequired for
normal growth under oxygen-depleted conditions. Thesame genes are
activated also in response to copper-deficiencythrough copper-response
elements that function as target sitesfor a transcriptional activator.
The core of the copper-responseelement, GTAC, is required also for the
hypoxic response, as isa trans-acting locus, CRR1.
Mercuric ions, which antagonize thecopper-deficiency response, also
antagonize the oxygen-deficiencyresponse of these target genes. Taken
together, these observationssuggest that the oxygen- and
copper-deficiency responses sharesignal transduction components.
Nevertheless, whereas the copper-responseelement is sufficient for the
nutritional copper response, theoxygen-deficiency response requires,
in addition, a second cis-element,indicating that the response to
oxygen depletion is not identicalto the nutritional copper response.
The distinction between thetwo responses is also supported by
comparative analysis of theresponse of the target genes,
Cyc6, Cpx1, and Crd1, to
copperversus oxygen deficiency. A Crr1-independent pathway for
Hyd1expression in oxygen-depleted C.
reinhardtii demonstrates theexistence of multiple
oxygen/redox-responsive circuits in thismodelorganism.
Differential Expression of the Chlamydomonas [FeFe]-Hydrogenase-Encoding HYDA1 Gene Is Regulated by the COPPER RESPONSE REGULATOR1.
M. Pape, C. Lambertz, T. Happe, and A. Hemschemeier (2012)
Plant Physiology
159, 1700-1712
|Abstract »|Full Text »|PDF »
Cytosolic Ni(II) Sensor in Cyanobacterium: NICKEL DETECTION FOLLOWS NICKEL AFFINITY ACROSS FOUR FAMILIES OF METAL SENSORS.
A. W. Foster, C. J. Patterson, R. Pernil, C. R. Hess, and N. J. Robinson (2012)
J. Biol. Chem.
287, 12142-12151
|Abstract »|Full Text »|PDF »
Systems Biology Approach in Chlamydomonas Reveals Connections between Copper Nutrition and Multiple Metabolic Steps.
M. Castruita, D. Casero, S. J. Karpowicz, J. Kropat, A. Vieler, S. I. Hsieh, W. Yan, S. Cokus, J. A. Loo, C. Benning, et al. (2011)
PLANT CELL
23, 1273-1292
|Abstract »|Full Text »|PDF »
The CRR1 Nutritional Copper Sensor in Chlamydomonas Contains Two Distinct Metal-Responsive Domains.
F. Sommer, J. Kropat, D. Malasarn, N. E. Grossoehme, X. Chen, D. P. Giedroc, and S. S. Merchant (2010)
PLANT CELL
22, 4098-4113
|Abstract »|Full Text »|PDF »
Anaerobic Expression of the Ferredoxin-Encoding FDX5 Gene of Chlamydomonas reinhardtii Is Regulated by the Crr1 Transcription Factor.
C. Lambertz, A. Hemschemeier, and T. Happe (2010)
Eukaryot. Cell
9, 1747-1754
|Abstract »|Full Text »|PDF »
Characterizing the Anaerobic Response of Chlamydomonas reinhardtii by Quantitative Proteomics.
M. Terashima, M. Specht, B. Naumann, and M. Hippler (2010)
Mol. Cell. Proteomics
9, 1514-1532
|Abstract »|Full Text »|PDF »
Pattern of Expression and Substrate Specificity of Chloroplast Ferredoxins from Chlamydomonas reinhardtii.
A. M. Terauchi, S.-F. Lu, M. Zaffagnini, S. Tappa, M. Hirasawa, J. N. Tripathy, D. B. Knaff, P. J. Farmer, S. D. Lemaire, T. Hase, et al. (2009)
J. Biol. Chem.
284, 25867-25878
|Abstract »|Full Text »|PDF »
Flexibility in Anaerobic Metabolism as Revealed in a Mutant of Chlamydomonas reinhardtii Lacking Hydrogenase Activity.
A. Dubini, F. Mus, M. Seibert, A. R. Grossman, and M. C. Posewitz (2009)
J. Biol. Chem.
284, 7201-7213
|Abstract »|Full Text »|PDF »
Two Chlamydomonas CTR Copper Transporters with a Novel Cys-Met Motif Are Localized to the Plasma Membrane and Function in Copper Assimilation.
M. D. Page, J. Kropat, P. P. Hamel, and S. S. Merchant (2009)
PLANT CELL
21, 928-943
|Abstract »|Full Text »|PDF »
Potential for hydrogen production with inducible chloroplast gene expression in Chlamydomonas.
R. Surzycki, L. Cournac, G. Peltier, and J.-D. Rochaix (2007)
PNAS
104, 17548-17553
|Abstract »|Full Text »|PDF »
Anaerobic Acclimation in Chlamydomonas reinhardtii: ANOXIC GENE EXPRESSION, HYDROGENASE INDUCTION, AND METABOLIC PATHWAYS.
F. Mus, A. Dubini, M. Seibert, M. C. Posewitz, and A. R. Grossman (2007)
J. Biol. Chem.
282, 25475-25486
|Abstract »|Full Text »|PDF »
Global Regulation of Photosynthesis and Respiration by FnrL: THE FIRST TWO TARGETS IN THE TETRAPYRROLE PATHWAY.
S. Ouchane, M. Picaud, P. Therizols, F. Reiss-Husson, and C. Astier (2007)
J. Biol. Chem.
282, 7690-7699
|Abstract »|Full Text »|PDF »
A regulator of nutritional copper signaling in Chlamydomonas is an SBP domain protein that recognizes the GTAC core of copper response element.
J. Kropat, S. Tottey, R. P. Birkenbihl, N. Depege, P. Huijser, and S. Merchant (2005)
PNAS
102, 18730-18735
|Abstract »|Full Text »|PDF »
Sensing and Signalling in Response to Oxygen Deprivation in Plants and Other Organisms.
Genetic Dissection of Nutritional Copper Signaling in Chlamydomonas Distinguishes Regulatory and Target Genes.
M. Eriksson, J. L. Moseley, S. Tottey, J. A. del Campo, J. Quinn, Y. Kim, and S. Merchant (2004)
Genetics
168, 795-807
|Abstract »|Full Text »|PDF »
Aerobic and Anaerobic Mg-Protoporphyrin Monomethyl Ester Cyclases in Purple Bacteria: A STRATEGY ADOPTED TO BYPASS THE REPRESSIVE OXYGEN CONTROL SYSTEM.
S. Ouchane, A.-S. Steunou, M. Picaud, and C. Astier (2004)
J. Biol. Chem.
279, 6385-6394
|Abstract »|Full Text »|PDF »
Hypobaric Biology: Arabidopsis Gene Expression at Low Atmospheric Pressure.
A.-L. Paul, A. C. Schuerger, M. P. Popp, J. T. Richards, M. S. Manak, and R. J. Ferl (2004)
Plant Physiology
134, 215-223
|Abstract »|Full Text »|PDF »
Copper Response Element and Crr1-Dependent Ni2+-Responsive Promoter for Induced, Reversible Gene Expression in Chlamydomonas reinhardtii.
Reciprocal Expression of Two Candidate Di-Iron Enzymes Affecting Photosystem I and Light-Harvesting Complex Accumulation.
J. L. Moseley, M. D. Page, N. P. Alder, M. Eriksson, J. Quinn, F. Soto, S. M. Theg, M. Hippler, and S. Merchant (2002)
PLANT CELL
14, 673-688
|Abstract »|Full Text »|PDF »