journal article
Feb 01, 2002
Chlorophyll Biosynthesis. Expression of a SecondChl IGene of Magnesium Chelatase in Arabidopsis Supports Only Limited Chlorophyll Synthesis
Abstract
AbstractMagnesium (Mg) chelatase is a heterotrimeric enzyme complex that catalyzes a key regulatory and enzymatic reaction in chlorophyll biosynthesis, the insertion of Mg2+ into protoporphyrin IX. Studies of the enzyme complex reconstituted in vitro have shown that all three of its subunits, CHL I, CHL D, and CHL H, are required for enzymatic activity. However, a new T-DNA knockout mutant of the chlorina locus, ch42-3 (Chl I), in Arabidopsis is still able to accumulate some chlorophyll despite the absence of Chl I mRNA and protein. In barley (Hordeum vulgare), CHL I is encoded by a single gene. We have identified an open reading frame that apparently encodes a second Chl Igene, Chl I2. Chl I1 and Chl I2 mRNA accumulate to similar levels in wild type, yet CHL I2 protein is not detectable in wild type or ch42-3, although the protein is translated and stromally processed as shown by in vivo pulse labeling and in vitro chloroplast imports. It is surprising that CHL D accumulates to wild-type levels in ch42-3, which is in contrast to reports that CHL D is unstable in CHL I-deficient backgrounds of barley. Our results show that limited Mg chelatase activity and CHL D accumulation can occur without detectable CHL I, despite its obligate requirement in vitro and its proposed chaperone-like stabilization and activation of CHL D. Thus, the unusual post-translational regulation of the CHL I2 protein provides an opportunity to study the different steps involved in stabilization and activation of the heterotrimeric Mg chelatase in vivo.
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References
40
[1]
Barkan "Approaches to investigating nuclear genes that function in chloroplast biogenesis in land plants." Method Enzymol (1998) 10.1016/s0076-6879(98)97006-9
[2]
Bremer "An ordinal classification for the families of flowering plants." Ann Missouri Bot Gard (1998) 10.2307/2992015
[3]
Bruce "In vitro import of proteins into chloroplasts." (1994) 10.1007/978-94-011-0511-8_32
[4]
Dailey "Enzymes of heme biosynthesis." J Biol Inorg Chem (1997) 10.1007/s007750050151
[5]
ChloroP, a neural network‐based method for predicting chloroplast transit peptides and their cleavage sites
Olof Emanuelsson, Henrik Nielsen, Gunnar von Heijne
Protein Science
1999
10.1110/ps.8.5.978
[6]
Fischerova "Linkage relationships of recessive chlorophyll mutations in Arabidopsis thaliana." Biol Plant (1975) 10.1007/bf02920831
[7]
Fodje "Interplay between an AAA module and an integrin I domain may regulate the function of magnesium chelatase." J Mol Biol (2001) 10.1006/jmbi.2001.4834
[8]
Forsthoefel "T-DNA insertion mutagenesis in Arabidopsis: prospects and perspectives." Aust J Plant Physiol (1992)
[9]
Gibson "Magnesium chelatase from Rhodobacter sphaeroides: initial characterization of the enzyme using purified subunits and evidence for a BCH I-BCH D complex." Biochem J (1999) 10.1042/bj3370243
[10]
Gibson "Magnesium-protoporphyrin chelatase of Rhodobacter sphaeroides: reconstitution of activity by combining the products of the BCH H, BCH I, and BCH D genes expressed in Escherichia coli." Proc Natl Acad Sci USA (1995) 10.1073/pnas.92.6.1941
[11]
Gräfe "Mg-chelatase of tobacco: the role of the subunit CHL D in the chelation step of protoporphyrin IX." Proc Natl Acad Sci USA (1999) 10.1073/pnas.96.5.1941
[12]
Hansson "Molecular basis for semidominance of missense mutations in the XANTHA-H (42-kDa) subunit of magnesium chelatase." Proc Natl Acad Sci USA (1999) 10.1073/pnas.96.4.1744
[13]
Jensen "Determinants of catalytic activity with the use of purified I, D and H subunits of the magnesium protoporphyrin IX chelatase from Synechocystis PCC6803." Biochem J (1998) 10.1042/bj3340335
[14]
Jensen "ATPase activity associated with the magnesium-protoporphyrin IX chelatase enzyme of Synechocystis PCC6803: evidence for ATP hydrolysis during Mg2+ insertion, and the MgATP-dependent interaction of the ChlI and ChlD subunits." Biochem J (1999) 10.1042/bj3390127
[15]
Jensen "Structural genes for Mg-chelatase subunits in barley: xantha-f, -g and -h." Mol Gen Genet (1996)
[16]
Kannangara "Magnesium chelatase: association with ribosomes and mutant complementation studies identify barley subunit xantha-G as a functional counterpart of Rhodobacter subunit BCH D." Mol Gen Genet (1997) 10.1007/s004380050394
[17]
Kjemtrup "Gene silencing from plant DNA carried by a gemnivirus." Plant J (1998) 10.1046/j.1365-313x.1998.00101.x
[18]
Koncz "Isolation of a gene encoding a novel chloroplast protein by T-DNA tagging in Arabidopsis thaliana." EMBO J (1990) 10.1002/j.1460-2075.1990.tb08248.x
[19]
Kropat "Chlorophyll precursors are signals of chloroplast origin involved in light induction of nuclear heat-shock genes." Proc Natl Acad Sci USA (1997) 10.1073/pnas.94.25.14168
[20]
Kropat "Chloroplast signalling in the light induction of nuclear HSP70 genes requires the accumulation of chlorophyll precursors and their accessibility to cytoplasm/nucleus." Plant J (2000) 10.1046/j.1365-313x.2000.00898.x
[21]
Kruse "Isolation and characterization of tobacco (Nicotiana tabacum) cDNA clones encoding proteins involved in magnesium chelation into protoporphyrin IX." Plant Mol Biol (1997) 10.1023/a:1005913315905
[22]
Neuwald "AAA(+): a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes." Genome Res (1999) 10.1101/gr.9.1.27
[23]
Norris "Genetic dissection of carotenoid synthesis in Arabidopsis defines plastoquinones as an essential component of phytoene desaturation." Plant Cell (1995)
[24]
Papenbrock "Mg-chelatase of tobacco: identification of a Chl D cDNA sequence encoding a third subunit, analysis of the interaction of the three subunits with the yeast two-hybrid system, and reconstitution of the enzyme activity by co-expression of recombinant CHL D, CHL H and CHL I." Plant J (1997) 10.1046/j.1365-313x.1997.12050981.x
[25]
Papenbrock "Role of magnesium chelatase activity in the early steps of the tetrapyrrole biosynthetic pathway." Plant Physiol (2000) 10.1104/pp.122.4.1161
[26]
Papenbrock "Decreased and increased expression of the subunit CHL I diminishes Mg chelatase activity and reduces chlorophyll synthesis in transgenic tobacco plants." Plant J (2000) 10.1046/j.1365-313x.2000.00724.x
[27]
Petersen "Distribution of ATPase and ATP-to-ADP phosphate exchange activities in magnesium chelatase subunits of Chlorobium vibrioforme and Synechocystis PCC6803." Arch Microbiol (1999) 10.1007/s002030050692
[28]
Petersen "Identification of the Xan-g gene and expression of the Mg-chelatase encoding genes Xan-f, -g and -h in mutant and wild type barley (Hordeum vulgare L.)." Hereditas (1999) 10.1111/j.1601-5223.1999.00165.x
[29]
Pogson "Arabidopsis carotenoid mutants demonstrate that lutein is not essential for photosynthesis in higher plants." Plant Cell (1996)
[30]
Pogson "Differential expression of two 1-aminocyclopropane-1-carboxylic acid oxidase genes in broccoli after harvest." Plant Physiol (1995) 10.1104/pp.108.2.651
[31]
Pogson "Altered xanthophyll compositions adversely affect chlorophyll accumulation and nonphotochemical quenching in Arabidopsis mutants." Proc Natl Acad Sci USA (1998) 10.1073/pnas.95.22.13324
[32]
Reinbothe "Two NADPH:protochlorophyllide oxidoreductases in barley: evidence for the selective disappearance of PORA during the light-induced greening of etiolated seedlings." Plant Cell (1995) 10.2307/3870200
[33]
Rensink "The transit sequence of ferredoxin contains different domains for translocation across the outer and inner membrane of the chloroplast envelope." J Biol Chem (2000) 10.1074/jbc.275.14.10265
[34]
Runge "Distinct roles for light-dependent NADPH:protochlorophyllide oxidoreductases (POR) A and B during greening in higher plants." Plant J (1996) 10.1046/j.1365-313x.1996.09040513.x
[35]
Sambrook (1989)
[36]
DNA sequencing with chain-terminating inhibitors
F. Sanger, S. Nicklen, A. R. Coulson
Proceedings of the National Academy of Sciences
1977
10.1073/pnas.74.12.5463
[37]
Waegemann "Characterization and isolation of the chloroplast protein import machinery." Methods Cell Biol (1995) 10.1016/s0091-679x(08)61035-3
[38]
Walker "Mechanism and regulation of Mg-chelatase." Biochem J (1997) 10.1042/bj3270321
[39]
Willows "Heterologous expression of the Rhodobacter capsulatus BCH I, -D, and -H genes that encode magnesium chelatase subunits and characterization of the reconstituted enzyme." J Biol Chem (1998) 10.1074/jbc.273.51.34206
[40]
Willows "Three separate proteins constitute the magnesium chelatase of Rhodobacter sphaeroides." Eur J Biochem (1996) 10.1111/j.1432-1033.1996.00438.x
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References
Details
- Published
- Feb 01, 2002
- Vol/Issue
- 128(2)
- Pages
- 770-779
- License
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Authors
Cite This Article
Heather M. Rissler, Eva Collakova, Dean DellaPenna, et al. (2002). Chlorophyll Biosynthesis. Expression of a SecondChl IGene of Magnesium Chelatase in Arabidopsis Supports Only Limited Chlorophyll Synthesis. Plant Physiology, 128(2), 770-779. https://doi.org/10.1104/pp.010625
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