Abstract
The HY1 locus of Arabidopsis is necessary for phytochrome chromophore biosynthesis and is defined by mutants that show a long hypocotyl phenotype when grown in the light. We describe here the molecular cloning of the HY1 gene by using chromosome walking and mutant complementation. The product of the HY1 gene shows significant similarity to animal heme oxygenases and contains a possible transit peptide for transport to plastids. Heme oxygenase activity was detected in the HY1 protein expressed in Escherichia coli. Heme oxygenase catalyzes the oxygenation of heme to biliverdin, an activity that is necessary for phytochrome chromophore biosynthesis. The predicted transit peptide is sufficient to transport the green fluorescent protein into chloroplasts. The accumulation of the HY1 protein in plastids was detected by using immunoblot analysis with an anti-HY1 antiserum. These results indicate that the Arabidopsis HY1 gene encodes a plastid heme oxygenase necessary for phytochrome chromophore biosynthesis.
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- Bevan M. Binary Agrobacterium vectors for plant transformation. Nucleic Acids Res. 1984 Nov 26;12(22):8711–8721. doi: 10.1093/nar/12.22.8711. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bowler C., Chua N. H. Emerging themes of plant signal transduction. Plant Cell. 1994 Nov;6(11):1529–1541. doi: 10.1105/tpc.6.11.1529. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brownstein B. H., Silverman G. A., Little R. D., Burke D. T., Korsmeyer S. J., Schlessinger D., Olson M. V. Isolation of single-copy human genes from a library of yeast artificial chromosome clones. Science. 1989 Jun 16;244(4910):1348–1351. doi: 10.1126/science.2544027. [DOI] [PubMed] [Google Scholar]
- Chang C., Bowman J. L., DeJohn A. W., Lander E. S., Meyerowitz E. M. Restriction fragment length polymorphism linkage map for Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1988 Sep;85(18):6856–6860. doi: 10.1073/pnas.85.18.6856. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chiu W., Niwa Y., Zeng W., Hirano T., Kobayashi H., Sheen J. Engineered GFP as a vital reporter in plants. Curr Biol. 1996 Mar 1;6(3):325–330. doi: 10.1016/s0960-9822(02)00483-9. [DOI] [PubMed] [Google Scholar]
- Chory J., Chatterjee M., Cook R. K., Elich T., Fankhauser C., Li J., Nagpal P., Neff M., Pepper A., Poole D. From seed germination to flowering, light controls plant development via the pigment phytochrome. Proc Natl Acad Sci U S A. 1996 Oct 29;93(22):12066–12071. doi: 10.1073/pnas.93.22.12066. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chory J., Peto C. A., Ashbaugh M., Saganich R., Pratt L., Ausubel F. Different Roles for Phytochrome in Etiolated and Green Plants Deduced from Characterization of Arabidopsis thaliana Mutants. Plant Cell. 1989 Sep;1(9):867–880. doi: 10.1105/tpc.1.9.867. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clack T., Mathews S., Sharrock R. A. The phytochrome apoprotein family in Arabidopsis is encoded by five genes: the sequences and expression of PHYD and PHYE. Plant Mol Biol. 1994 Jun;25(3):413–427. doi: 10.1007/BF00043870. [DOI] [PubMed] [Google Scholar]
- Cline K., Werner-Washburne M., Lubben T. H., Keegstra K. Precursors to two nuclear-encoded chloroplast proteins bind to the outer envelope membrane before being imported into chloroplasts. J Biol Chem. 1985 Mar 25;260(6):3691–3696. [PubMed] [Google Scholar]
- Cornejo J., Beale S. I. Algal heme oxygenase from Cyanidium caldarium. Partial purification and fractionation into three required protein components. J Biol Chem. 1988 Aug 25;263(24):11915–11921. [PubMed] [Google Scholar]
- Cornejo J., Beale S. I., Terry M. J., Lagarias J. C. Phytochrome assembly. The structure and biological activity of 2(R),3(E)-phytochromobilin derived from phycobiliproteins. J Biol Chem. 1992 Jul 25;267(21):14790–14798. [PubMed] [Google Scholar]
- Elich T. D., Lagarias J. C. Formation of a photoreversible phycocyanobilin-apophytochrome adduct in vitro. J Biol Chem. 1989 Aug 5;264(22):12902–12908. [PubMed] [Google Scholar]
- Gavel Y., von Heijne G. A conserved cleavage-site motif in chloroplast transit peptides. FEBS Lett. 1990 Feb 26;261(2):455–458. doi: 10.1016/0014-5793(90)80614-o. [DOI] [PubMed] [Google Scholar]
- Grill E., Somerville C. Construction and characterization of a yeast artificial chromosome library of Arabidopsis which is suitable for chromosome walking. Mol Gen Genet. 1991 May;226(3):484–490. doi: 10.1007/BF00260662. [DOI] [PubMed] [Google Scholar]
- Ito-Maki M., Ishikawa K., Matera K. M., Sato M., Ikeda-Saito M., Yoshida T. Demonstration that histidine 25, but not 132, is the axial heme ligand in rat heme oxygenase-1. Arch Biochem Biophys. 1995 Feb 20;317(1):253–258. doi: 10.1006/abbi.1995.1160. [DOI] [PubMed] [Google Scholar]
- Konieczny A., Ausubel F. M. A procedure for mapping Arabidopsis mutations using co-dominant ecotype-specific PCR-based markers. Plant J. 1993 Aug;4(2):403–410. doi: 10.1046/j.1365-313x.1993.04020403.x. [DOI] [PubMed] [Google Scholar]
- Lagarias J. C., Lagarias D. M. Self-assembly of synthetic phytochrome holoprotein in vitro. Proc Natl Acad Sci U S A. 1989 Aug;86(15):5778–5780. doi: 10.1073/pnas.86.15.5778. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lassner M. W., Lardizabal K., Metz J. G. A jojoba beta-Ketoacyl-CoA synthase cDNA complements the canola fatty acid elongation mutation in transgenic plants. Plant Cell. 1996 Feb;8(2):281–292. doi: 10.1105/tpc.8.2.281. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lincoln B. C., Mayer A., Bonkovsky H. L. Microassay of heme oxygenase by high-performance liquid chromatography: application to assay of needle biopsies of human liver. Anal Biochem. 1988 May 1;170(2):485–490. doi: 10.1016/0003-2697(88)90662-8. [DOI] [PubMed] [Google Scholar]
- Ma H., Yanofsky M. F., Meyerowitz E. M. Molecular cloning and characterization of GPA1, a G protein alpha subunit gene from Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1990 May;87(10):3821–3825. doi: 10.1073/pnas.87.10.3821. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Matera K. M., Zhou H., Migita C. T., Hobert S. E., Ishikawa K., Katakura K., Maeshima H., Yoshida T., Ikeda-Saito M. Histidine-132 does not stabilize a distal water ligand and is not an important residue for the enzyme activity in heme oxygenase-1. Biochemistry. 1997 Apr 22;36(16):4909–4915. doi: 10.1021/bi962321m. [DOI] [PubMed] [Google Scholar]
- Nagatani A., Reed J. W., Chory J. Isolation and Initial Characterization of Arabidopsis Mutants That Are Deficient in Phytochrome A. Plant Physiol. 1993 May;102(1):269–277. doi: 10.1104/pp.102.1.269. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nam H. G., Giraudat J., Den Boer B., Moonan F., Loos WDB., Hauge B. M., Goodman H. M. Restriction Fragment Length Polymorphism Linkage Map of Arabidopsis thaliana. Plant Cell. 1989 Jul;1(7):699–705. doi: 10.1105/tpc.1.7.699. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ochman H., Gerber A. S., Hartl D. L. Genetic applications of an inverse polymerase chain reaction. Genetics. 1988 Nov;120(3):621–623. doi: 10.1093/genetics/120.3.621. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Oelmüller R., Kendrick R. E. Blue light is required for survival of the tomato phytochrome-deficient aurea mutant and the expression of four nuclear genes coding for plastidic proteins. Plant Mol Biol. 1991 Feb;16(2):293–299. doi: 10.1007/BF00020560. [DOI] [PubMed] [Google Scholar]
- Parks B. M., Quail P. H. Phytochrome-Deficient hy1 and hy2 Long Hypocotyl Mutants of Arabidopsis Are Defective in Phytochrome Chromophore Biosynthesis. Plant Cell. 1991 Nov;3(11):1177–1186. doi: 10.1105/tpc.3.11.1177. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Quail P. H. Phytochrome: a light-activated molecular switch that regulates plant gene expression. Annu Rev Genet. 1991;25:389–409. doi: 10.1146/annurev.ge.25.120191.002133. [DOI] [PubMed] [Google Scholar]
- Reed J. W., Nagatani A., Elich T. D., Fagan M., Chory J. Phytochrome A and Phytochrome B Have Overlapping but Distinct Functions in Arabidopsis Development. Plant Physiol. 1994 Apr;104(4):1139–1149. doi: 10.1104/pp.104.4.1139. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rhie G., Beale S. I. Biosynthesis of phycobilins. Ferredoxin-supported nadph-independent heme oxygenase and phycobilin-forming activities from Cyanidium caldarium. J Biol Chem. 1992 Aug 15;267(23):16088–16093. [PubMed] [Google Scholar]
- Rhie G., Beale S. I. Phycobilin biosynthesis: reductant requirements and product identification for heme oxygenase from Cyanidium caldarium. Arch Biochem Biophys. 1995 Jun 20;320(1):182–194. doi: 10.1006/abbi.1995.1358. [DOI] [PubMed] [Google Scholar]
- Sentenac H., Bonneaud N., Minet M., Lacroute F., Salmon J. M., Gaymard F., Grignon C. Cloning and expression in yeast of a plant potassium ion transport system. Science. 1992 May 1;256(5057):663–665. doi: 10.1126/science.1585180. [DOI] [PubMed] [Google Scholar]
- Sharrock R. A., Quail P. H. Novel phytochrome sequences in Arabidopsis thaliana: structure, evolution, and differential expression of a plant regulatory photoreceptor family. Genes Dev. 1989 Nov;3(11):1745–1757. doi: 10.1101/gad.3.11.1745. [DOI] [PubMed] [Google Scholar]
- Shinomura T., Nagatani A., Chory J., Furuya M. The Induction of Seed Germination in Arabidopsis thaliana Is Regulated Principally by Phytochrome B and Secondarily by Phytochrome A. Plant Physiol. 1994 Feb;104(2):363–371. doi: 10.1104/pp.104.2.363. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shinomura T., Nagatani A., Hanzawa H., Kubota M., Watanabe M., Furuya M. Action spectra for phytochrome A- and B-specific photoinduction of seed germination in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):8129–8133. doi: 10.1073/pnas.93.15.8129. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Skerra A. A general vector, pASK84, for cloning, bacterial production, and single-step purification of antibody Fab fragments. Gene. 1994 Apr 8;141(1):79–84. doi: 10.1016/0378-1119(94)90131-7. [DOI] [PubMed] [Google Scholar]
- Smith A. G., Santana M. A., Wallace-Cook A. D., Roper J. M., Labbe-Bois R. Isolation of a cDNA encoding chloroplast ferrochelatase from Arabidopsis thaliana by functional complementation of a yeast mutant. J Biol Chem. 1994 May 6;269(18):13405–13413. [PubMed] [Google Scholar]
- Sun J., Loehr T. M., Wilks A., Ortiz de Montellano P. R. Identification of histidine 25 as the heme ligand in human liver heme oxygenase. Biochemistry. 1994 Nov 22;33(46):13734–13740. doi: 10.1021/bi00250a026. [DOI] [PubMed] [Google Scholar]
- Suzuki T., Sato M., Ishikawa K., Yoshida T. Nucleotide sequence of cDNA for porcine heme oxygenase and its expression in Escherichia coli. Biochem Int. 1992 Dec;28(5):887–893. [PubMed] [Google Scholar]
- Takahashi S., Wang J., Rousseau D. L., Ishikawa K., Yoshida T., Host J. R., Ikeda-Saito M. Heme-heme oxygenase complex. Structure of the catalytic site and its implication for oxygen activation. J Biol Chem. 1994 Jan 14;269(2):1010–1014. [PubMed] [Google Scholar]
- Takahashi S., Wang J., Rousseau D. L., Ishikawa K., Yoshida T., Takeuchi N., Ikeda-Saito M. Heme-heme oxygenase complex: structure and properties of the catalytic site from resonance Raman scattering. Biochemistry. 1994 May 10;33(18):5531–5538. doi: 10.1021/bi00184a023. [DOI] [PubMed] [Google Scholar]
- Terry M. J., Kendrick R. E. The aurea and yellow-green-2 mutants of tomato are deficient in phytochrome chromophore synthesis. J Biol Chem. 1996 Aug 30;271(35):21681–21686. doi: 10.1074/jbc.271.35.21681. [DOI] [PubMed] [Google Scholar]
- Terry M. J., Lagarias J. C. Holophytochrome assembly. Coupled assay for phytochromobilin synthase in organello. J Biol Chem. 1991 Nov 25;266(33):22215–22221. [PubMed] [Google Scholar]
- Terry M. J., McDowell M. T., Lagarias J. C. (3Z)- and (3E)-phytochromobilin are intermediates in the biosynthesis of the phytochrome chromophore. J Biol Chem. 1995 May 12;270(19):11111–11118. doi: 10.1074/jbc.270.19.11111. [DOI] [PubMed] [Google Scholar]
- Terry M. J., Wahleithner J. A., Lagarias J. C. Biosynthesis of the plant photoreceptor phytochrome. Arch Biochem Biophys. 1993 Oct;306(1):1–15. doi: 10.1006/abbi.1993.1473. [DOI] [PubMed] [Google Scholar]
- Troxler R. F., Brown A. S., Brown S. B. Bile pigment synthesis in plants. Mechanism of 18O incorporation into phycocyanobilin in the unicellular rhodophyte. Cyanidium caldarium. J Biol Chem. 1979 May 10;254(9):3411–3418. [PubMed] [Google Scholar]
- Valvekens D., Van Montagu M., Van Lijsebettens M. Agrobacterium tumefaciens-mediated transformation of Arabidopsis thaliana root explants by using kanamycin selection. Proc Natl Acad Sci U S A. 1988 Aug;85(15):5536–5540. doi: 10.1073/pnas.85.15.5536. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ward E. R., Jen G. C. Isolation of single-copy-sequence clones from a yeast artificial chromosome library of randomly-sheared Arabidopsis thaliana DNA. Plant Mol Biol. 1990 Apr;14(4):561–568. doi: 10.1007/BF00027501. [DOI] [PubMed] [Google Scholar]
- Weller J. L., Terry M. J., Rameau C., Reid J. B., Kendrick R. E. The Phytochrome-Deficient pcd1 Mutant of Pea Is Unable to Convert Heme to Biliverdin IX[alpha]. Plant Cell. 1996 Jan;8(1):55–67. doi: 10.1105/tpc.8.1.55. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yoshida T., Biro P., Cohen T., Müller R. M., Shibahara S. Human heme oxygenase cDNA and induction of its mRNA by hemin. Eur J Biochem. 1988 Feb 1;171(3):457–461. doi: 10.1111/j.1432-1033.1988.tb13811.x. [DOI] [PubMed] [Google Scholar]
- Yoshida T., Ishikawa K., Sato M. Degradation of heme by a soluble peptide of heme oxygenase obtained from rat liver microsomes by mild trypsinization. Eur J Biochem. 1991 Aug 1;199(3):729–733. doi: 10.1111/j.1432-1033.1991.tb16177.x. [DOI] [PubMed] [Google Scholar]
- von Heijne G., Steppuhn J., Herrmann R. G. Domain structure of mitochondrial and chloroplast targeting peptides. Eur J Biochem. 1989 Apr 1;180(3):535–545. doi: 10.1111/j.1432-1033.1989.tb14679.x. [DOI] [PubMed] [Google Scholar]