Posttranslational control of ALA synthesis includes GluTR degradation by clp protease and stabilization by GluTR-binding protein

Plant Physiology

Volumn 170, Issue 4, 2016, Pages 2040-2051

  Apitz, Janina ^a   Nishimura, Kenji ^b,c   Schmied, Judith ^a   Wolf, Anja ^a   Hedtke, Boris ^a   van Wijk, Klaas J ^b   Grimm, Bernhard ^a  

^a HUMBOLDT UNIVERSITY   (Germany)

^b Department of Molecular Biology and Genetics   (United States)

^c OKAYAMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; AMINOLEVULINIC ACID; ARABIDOPSIS PROTEIN; CHAPERONE; ENDOPEPTIDASE CLP; GLUTAMYL TRNA REDUCTASE; PROTEIN BINDING; PROTOCHLOROPHYLLIDE;

ARABIDOPSIS; BIOLOGICAL MODEL; CHEMISTRY; ENZYME STABILITY; ENZYMOLOGY; FLUORESCENCE; GENE INACTIVATION; GENETIC COMPLEMENTATION; GENETICS; METABOLISM; MUTATION; PLANT LEAF; PROTEIN DEGRADATION; PROTEIN PROCESSING; TRANSGENIC PLANT;

ALDEHYDE OXIDOREDUCTASES; AMINOLEVULINIC ACID; ARABIDOPSIS; ARABIDOPSIS PROTEINS; ENDOPEPTIDASE CLP; ENZYME STABILITY; FLUORESCENCE; GENE KNOCKOUT TECHNIQUES; GENETIC COMPLEMENTATION TEST; MODELS, BIOLOGICAL; MOLECULAR CHAPERONES; MUTATION; PLANT LEAVES; PLANTS, GENETICALLY MODIFIED; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOLYSIS; PROTOCHLOROPHYLLIDE;

EID: 84962079677     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.15.01945     Document Type: Article

References (56)

1. Apel W, Schulze WX, Bock R (2010) Identification of protein stability determinants in chloroplasts. Plant J 63: 636-650
2. Apitz J, Schmied J, Lehmann MJ, Hedtke B, Grimm B (2014) GluTR2 complements a hema1 mutant lacking glutamyl-tRNA reductase 1, but is differently regulated at the post-translational level. Plant Cell Physiol 55: 645-657
3. Avissar YJ, Ormerod JG, Beale SI (1989) Distribution of deltaaminolevulinic acid biosynthetic pathways among phototrophic bacterial groups. Arch Microbiol 151: 513-519
4. Bachmair A, Finley D, Varshavsky A (1986) In vivo half-life of a protein is a function of its amino-terminal residue. Science 234: 179-186
5. Beale SI, Castelfranco PA (1973) 14 C incorporation from exogenous compounds into-aminolevulinic acid by greening cucumber cotyledons. Biochem Biophys Res Commun 52: 143-149
6. Cornah JE, Terry MJ, Smith AG (2003) Green or red: what stops the traffic in the tetrapyrrole pathway? Trends Plant Sci 8: 224-230
7. Czarnecki O, Hedtke B, Melzer M, Rothbart M, Richter A, Schröter Y, Pfannschmidt T, Grimm B (2011) An Arabidopsis GluTR binding protein mediates spatial separation of 5-aminolevulinic acid synthesis in chloroplasts. Plant Cell 23: 4476-4491
8. Duggan J, Gassman M (1974) Induction of porphyrin synthesis in etiolated bean leaves by chelators of iron. Plant Physiol 53: 206-215
9. Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP and related tools. Nat Protoc 2: 953-971
10. Goslings D, Meskauskiene R, Kim C, Lee KP, Nater M, Apel K (2004) Concurrent interactions of heme and FLU with Glu tRNA reductase (HEMA1), the target of metabolic feedback inhibition of tetrapyrrole biosynthesis, in dark-and light-grown Arabidopsis plants. Plant J 40: 957-967
11. Grimm B, Bull A, Welinder KG, Gough SP, Kannangara CG (1989) Purification and partial amino acid sequence of the glutamate 1-semialdehyde aminotransferase of barley and synechococcus. Carlsberg Res Commun 54: 67-79
12. Hedtke B, Alawady A, Chen S, Börnke F, Grimm B (2007) HEMA RNAi silencing reveals a control mechanism of ALA biosynthesis on Mg chelatase and Fe chelatase. Plant Mol Biol 64: 733-742
13. Ilag LL, Kumar AM, Söll D (1994) Light regulation of chlorophyll biosynthesis at the level of 5-aminolevulinate formation in Arabidopsis. Plant Cell 6: 265-275
14. Joyard J, Ferro M, Masselon C, Seigneurin-Berny D, Salvi D, Garin J, Rolland N (2009) Chloroplast proteomics and the compartmentation of plastidial isoprenoid biosynthetic pathways. Mol Plant 2: 1154-1180
15. Kauss D, Bischof S, Steiner S, Apel K, Meskauskiene R (2012) FLU, a negative feedback regulator of tetrapyrrole biosynthesis, is physically linked to the final steps of the Mg(++)-branch of this pathway. FEBS Lett 586: 211-216
16. Koski VM, Smith JH (1948) The isolation and spectral absorption properties of protochlorophyll from etiolated barley seedlings. J Am Chem Soc 70: 3558-3562
17. Kumar AM, Csankovszki G, Söll D (1996) A second and differentially expressed glutamyl-tRNA reductase gene from Arabidopsis thaliana. Plant Mol Biol 30: 419-426
18. Kumar MA, Chaturvedi S, Söll D (1999) Selective inhibition of HEMA gene expression by photooxidation in Arabidopsis thaliana. Phytochemistry 51: 847-851
19. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic bio-membranes. Methods Enzymol 148: 350-382
20. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408
21. Matsumoto F, Obayashi T, Sasaki-Sekimoto Y, Ohta H, Takamiya K, Masuda T (2004) Gene expression profiling of the tetrapyrrole metabolic pathway in Arabidopsis with a mini-array system. Plant Physiol 135: 2379-2391
22. Mauzerall D, Granick S (1956) The occurrence and determination of delta-aminolevulinic acid and porphobilinogen in urine. J Biol Chem 219: 435-446
23. McCormac AC, Fischer A, Kumar AM, Söll D, Terry MJ (2001) Regulation of HEMA1 expression by phytochrome and a plastid signal during deetiolation in Arabidopsis thaliana. Plant J 25: 549-561
24. Meskauskiene R, Nater M, Goslings D, Kessler F, op den Camp R, Apel K (2001) FLU: a negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 98: 12826-12831
25. Mogk A, Schmidt R, Bukau B (2007) The N-end rule pathway for regulated proteolysis: prokaryotic and eukaryotic strategies. Trends Cell Biol 17: 165-172
26. Montgomery BL, Yeh KC, Crepeau MW, Lagarias JC (1999) Modification of distinct aspects of photomorphogenesis via targeted expression of mammalian biliverdin reductase in transgenic Arabidopsis plants. Plant Physiol 121: 629-639
27. Moser J, Schubert WD, Beier V, Bringemeier I, Jahn D, Heinz DW (2001) V-shaped structure of glutamyl-tRNA reductase, the first enzyme of tRNA-dependent tetrapyrrole biosynthesis. EMBO J 20: 6583-6590
28. Nagai S, Koide M, Takahashi S, Kikuta A, Aono M, Sasaki-Sekimoto Y, Ohta H, Takamiya K, Masuda T (2007) Induction of isoforms of tetrapyrrole biosynthetic enzymes, AtHEMA2 and AtFC1, under stress conditions and their physiological functions in Arabidopsis. Plant Physiol 144: 1039-1051
29. Nakagawara E, Sakuraba Y, Yamasato A, Tanaka R, Tanaka A (2007) Clp protease controls chlorophyll b synthesis by regulating the level of chlorophyllide a oxygenase. Plant J 49: 800-809
30. Nishimura K, Apitz J, Friso G, Kim J, Ponnala L, Grimm B, van Wijk KJ (2015) Discovery of a unique Clp component, ClpF, in chloroplasts: a proposed binary ClpF-ClpS1 adaptor complex functions in substrate recognition and delivery. Plant Cell 27: 2677-2691
31. Nishimura K, Asakura Y, Friso G, Kim J, Oh SH, Rutschow H, Ponnala L, van Wijk KJ (2013) ClpS1 is a conserved substrate selector for the chloroplast Clp protease system in Arabidopsis. Plant Cell 25: 2276-2301
32. Nishimura K, van Wijk KJ (2015) Organization, function and substrates of the essential Clp protease system in plastids. Biochim Biophys Acta 1847: 915-930
33. op den Camp RG, Przybyla D, Ochsenbein C, Laloi C, Kim C, Danon A, Wagner D, Hideg E, Göbel C, Feussner I, et al (2003) Rapid induction of distinct stress responses after the release of singlet oxygen in Arabidopsis. Plant Cell 15: 2320-2332
34. Papenbrock J, Mock HP, Kruse E, Grimm B (1999) Expression studies in tetrapyrrole biosynthesis: inverse maxima of magnesium chelatase and ferrochelatase activity during cyclic photoperiods. Planta 208: 264-273
35. Papenbrock J, Mock HP, Tanaka R, Kruse E, Grimm B (2000a) Role of magnesium chelatase activity in the early steps of the tetrapyrrole biosynthetic pathway. Plant Physiol 122: 1161-1169
36. Papenbrock J, Pfündel E, Mock HP, Grimm B (2000b) Decreased and increased expression of the subunit CHL I diminishes Mg chelatase activity and reduces chlorophyll synthesis in transgenic tobacco plants. Plant J 22: 155-164
37. Pontoppidan B, Kannangara CG (1994) Purification and partial characterisation of barley glutamyl-tRNA(Glu) reductase, the enzyme that directs glutamate to chlorophyll biosynthesis. Eur J Biochem 225: 529-537
38. Rebeiz CA, Montazer-Zouhoor A, Mayasich JM, Tripathy BC, Wu SM, Rebeiz CC, Friedmann HC (1988) Photodynamic herbicides. Recent developments and molecular basis of selectivity. Crit Rev Plant Sci 6: 385-436
39. Rowland E, Kim J, Bhuiyan NH, van Wijk KJ (2015) The Arabidopsis chloroplast stromal N-terminome: complexities of amino-terminal protein maturation and stability. Plant Physiol 169: 1881-1896
40. Rudella A, Friso G, Alonso JM, Ecker JR, van Wijk KJ (2006) Downregulation of ClpR2 leads to reduced accumulation of the ClpPRS protease complex and defects in chloroplast biogenesis in Arabidopsis. Plant Cell 18: 1704-1721
41. Sakuraba Y, Tanaka R, Yamasato A, Tanaka A (2009) Determination of a chloroplast degron in the regulatory domain of chlorophyllide a oxygenase. J Biol Chem 284: 36689-36699
42. Sambrook J, Russell DW (2001) Molecular Cloning: A Laboratory Manual, Ed 3. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
43. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108
44. Sjögren LL, MacDonald TM, Sutinen S, Clarke AK (2004) Inactivation of the clpC1 gene encoding a chloroplast Hsp100 molecular chaperone causes growth retardation, leaf chlorosis, lower photosynthetic activity, and a specific reduction in photosystem content. Plant Physiol 136: 4114-4126
45. Stenbaek A, Jensen PE (2010) Redox regulation of chlorophyll biosynthesis. Phytochemistry 71: 853-859
46. Tanaka R, Tanaka A (2007) Tetrapyrrole biosynthesis in higher plants. Annu Rev Plant Biol 58: 321-346
47. Tapken W, Kim J, Nishimura K, van Wijk KJ, Pilon M (2015) The Clp protease system is required for copper ion-dependent turnover of the PAA2/ HMA8 copper transporter in chloroplasts. New Phytol 205: 511-517
48. Ujwal ML, McCormac AC, Goulding A, Kumar AM, Söll D, Terry MJ (2002) Divergent regulation of the HEMA gene family encoding glutamyltRNA reductase in Arabidopsis thaliana: expression of HEMA2 is regulated by sugars, but is independent of light and plastid signalling. Plant Mol Biol 50: 83-91
49. Varshavsky A (1996) The N-end rule: functions, mysteries, uses. Proc Natl Acad Sci USA 93: 12142-12149
50. Vothknecht UC, Kannangara CG, von Wettstein D (1996) Expression of catalytically active barley glutamyl tRNAGlu reductase in Escherichia coli as a fusion protein with glutathione S-transferase. Proc Natl Acad Sci USA 93: 9287-9291
51. Vothknecht UC, Kannangara CG, von Wettstein D (1998) Barley glutamyl tRNAGlu reductase: mutations affecting haem inhibition and enzyme activity. Phytochemistry 47: 513-519
52. Walter M, Chaban C, Schütze K, Batistic O, Weckermann K, Näke C, Blazevic D, Grefen C, Schumacher K, Oecking C, et al (2004) Visualization of protein interactions in living plant cells using bimolecular fluorescence complementation. Plant J 40: 428-438
53. Wang KH, Roman-Hernandez G, Grant RA, Sauer RT, Baker TA (2008) The molecular basis of N-end rule recognition. Mol Cell 32: 406-414
54. Wang L, Wilson S, Elliott T (1999) A mutant HemA protein with positive charge close to the N terminus is stabilized against heme-regulated proteolysis in Salmonella typhimurium. J Bacteriol 181: 6033-6041
55. Zhang M, Zhang F, Fang Y, Chen X, Chen Y, Zhang W, Dai HE, Lin R, Liu L (2015) The non-canonical tetratricopeptide repeat (TPR) domain of Fluorescent (FLU) mediates complex formation with glutamyl-tRNA reductase. J Biol Chem 290: 17559-17565
56. Zhao A, Fang Y, Chen X, Zhao S, Dong W, Lin Y, Gong W, Liu L (2014) Crystal structure of Arabidopsis glutamyl-tRNA reductase in complex with its stimulator protein. Proc Natl Acad Sci USA 111: 6630-6635