Identification of Two Differentially Regulated Isoforms of Protochlorophyllide Oxidoreductase (POR) from Tobacco Revealed a Wide Variety of Light- and Development-dependent Regulations of POR Gene Expression Among Angiosperms

Overview

Journal Photosynth Res

Publisher Springer

Date 2005 Oct 18

PMID 16228554

Citations 11

Authors

Tatsuru Masuda

Naoki Fusada

Toshihiko Shiraishi

Hirofumi Kuroda

Koichiro Awai

Hiroshi Shimada

Hiroyuki Ohta

Ken-Ichiro Takamiya

Affiliations

Soon will be listed here.

Abstract

NADPH-protochlorophyllide oxidoreductase (POR) catalyzes the light-dependent reduction of protochlorophyllide a in the chlorophyll biosynthetic pathway. Here, we identified two distinct POR cDNAs from tobacco. Both POR isoforms are encoded by a respective single copy gene in tobacco genome. The overall deduced amino acid sequences of two tobacco cDNAs, designated here POR1 and POR2, displayed significant identities ( approximately 75%), but showed different patterns of light and developmental regulation. In contrast to the previously isolated POR isoforms of Arabidopsis thaliana and barley, the expression of both tobacco POR isoforms were not negatively regulated by light and persisted in matured green tissues. Furthermore, the expression of both genes appeared to be regulated by a diurnal regulation. These results show a wide variety of light- and development-dependent regulations of POR gene expression among angiosperms. Furthermore, phylogenetic analysis including tobacco revealed that POR gene family is differentially represented by angiosperms, most of which is probably caused by independent gene duplication in individual plant. Present results imply a modification of the previous concept that chlorophyll biosynthesis and chloroplast differentiation in angiosperms are ubiquitously controlled by unique functions of two POR isoforms.

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References

Fusada N, Masuda T, Kuroda H, Shiraishi T, Shimada H, Ohta H . NADPH-protochlorophyllide oxidoreductase in cucumber is encoded by a single gene and its expression is transcriptionally enhanced by illumination. Photosynth Res. 2005; 64(2-3):147-54. DOI: 10.1023/A:1006418608647. View

Scheumann V, Klement H, Helfrich M, Oster U, Schoch S, Rudiger W . Protochlorophyllide b does not occur in barley etioplasts. FEBS Lett. 1999; 445(2-3):445-8. DOI: 10.1016/s0014-5793(99)00169-6. View

Reinbothe S, Mache R, Reinbothe C . A second, substrate-dependent site of protein import into chloroplasts. Proc Natl Acad Sci U S A. 2000; 97(17):9795-800. PMC: 16944. DOI: 10.1073/pnas.160242597. View

Saitou N, Nei M . The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987; 4(4):406-25. DOI: 10.1093/oxfordjournals.molbev.a040454. View

Oliver R, Griffiths W . Covalent labelling of the NADPH: protochlorophyllide oxidoreductase from etioplast membranes with [3H]N-phenylmaleimide. Biochem J. 1981; 195(1):93-101. PMC: 1162858. DOI: 10.1042/bj1950093. View

Spano A, He Z, Michel H, Hunt D, Timko M . Molecular cloning, nuclear gene structure, and developmental expression of NADPH: protochlorophyllide oxidoreductase in pea (Pisum sativum L.). Plant Mol Biol. 1992; 18(5):967-72. DOI: 10.1007/BF00019210. View

Wermuth B, Bohren K, Heinemann G, VON WARTBURG J, GABBAY K . Human carbonyl reductase. Nucleotide sequence analysis of a cDNA and amino acid sequence of the encoded protein. J Biol Chem. 1988; 263(31):16185-8. View

ARONSSON H, Sohrt K, Soll J . NADPH:Protochlorophyllide oxidoreductase uses the general import route into chloroplasts. Biol Chem. 2001; 381(12):1263-7. DOI: 10.1515/BC.2000.155. View

WILKS H, Timko M . A light-dependent complementation system for analysis of NADPH:protochlorophyllide oxidoreductase: identification and mutagenesis of two conserved residues that are essential for enzyme activity. Proc Natl Acad Sci U S A. 1995; 92(3):724-8. PMC: 42692. DOI: 10.1073/pnas.92.3.724. View

10.

Murray M, Thompson W . Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 1980; 8(19):4321-5. PMC: 324241. DOI: 10.1093/nar/8.19.4321. View

11.

Kuroda H, Masuda T, Fusada N, Ohta H, Takamiya K . Expression of NADPH-Protochlorophyllide oxidoreductase gene in fully green leaves of cucumber. Plant Cell Physiol. 2000; 41(2):226-9. DOI: 10.1093/pcp/41.2.226. View

12.

Griffiths W . Reconstitution of chlorophyllide formation by isolated etioplast membranes. Biochem J. 1978; 174(3):681-92. PMC: 1185970. DOI: 10.1042/bj1740681. View

13.

Holtorf H, Reinbothe S, Reinbothe C, Bereza B, Apel K . Two routes of chlorophyllide synthesis that are differentially regulated by light in barley (Hordeum vulgare L.). Proc Natl Acad Sci U S A. 1995; 92(8):3254-8. PMC: 42144. DOI: 10.1073/pnas.92.8.3254. View

14.

Reinbothe S, Runge S, Reinbothe C, van Cleve B, Apel K . Substrate-dependent transport of the NADPH:protochlorophyllide oxidoreductase into isolated plastids. Plant Cell. 1995; 7(2):161-72. PMC: 160772. DOI: 10.1105/tpc.7.2.161. View

15.

Apel K, Santel H, Redlinger T, Falk H . The protochlorophyllide holochrome of barley (Hordeum vulgare L.). Isolation and characterization of the NADPH:protochlorophyllide oxidoreductase. Eur J Biochem. 1980; 111(1):251-8. DOI: 10.1111/j.1432-1033.1980.tb06100.x. View

16.

Su Q, Frick G, Armstrong G, Apel K . POR C of Arabidopsis thaliana: a third light- and NADPH-dependent protochlorophyllide oxidoreductase that is differentially regulated by light. Plant Mol Biol. 2002; 47(6):805-13. DOI: 10.1023/a:1013699721301. View

17.

Apel K . The protochlorophyllide holochrome of barley (Hordeum vulgare L.). Phytochrome-induced decrease of translatable mRNA coding for the NADPH: protochlorophyllide oxidoreductase. Eur J Biochem. 1981; 120(1):89-93. DOI: 10.1111/j.1432-1033.1981.tb05673.x. View

18.

Runge S, Sperling U, Frick G, Apel K, Armstrong G . Distinct roles for light-dependent NADPH:protochlorophyllide oxidoreductases (POR) A and B during greening in higher plants. Plant J. 1996; 9(4):513-23. DOI: 10.1046/j.1365-313x.1996.09040513.x. View

19.

Armstrong G, Apel K, Rudiger W . Does a light-harvesting protochlorophyllide a/b-binding protein complex exist?. Trends Plant Sci. 2000; 5(1):40-4. DOI: 10.1016/s1360-1385(99)01513-7. View

20.

Kuroda H, Masuda T, Ohta H, Shioi Y, Takamiya K . Light-enhanced gene expression of NADPH-protochlorophyllide oxidoreductase in cucumber. Biochem Biophys Res Commun. 1995; 210(2):310-6. DOI: 10.1006/bbrc.1995.1662. View