Characterization of the Genes Encoding Phycoerythrin in the Red Alga Rhodella Violacea: Evidence for a Splitting of the RpeB Gene by an Intron

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1992 Oct 15

PMID 1409666

Citations 8

Authors

C Bernard

J C Thomas

D Mazel

A Mousseau

A M Castets

N Tandeau de Marsac

J P Dubacq

Affiliations

Soon will be listed here.

Abstract

The phycobilisome of the eukaryotic unicellular red alga Rhodella violacea presents in some respects an organization that is intermediate between those of the homologous counterparts found in cyanobacteria (the putative chloroplast progenitor) and more advanced, pluricellular red algae. This suggests evolutionary relationships that we investigated at the genome level. The present work describes the sequences of two rhodophytan phycobilisome genes, rpeA and rpeB. These chloroplast genes encode the alpha and beta subunits of phycoerythrin, the major component of the light-harvesting antennae and one of the most abundant cellular proteins in these algae. The amino acid sequences deduced from both rpeA and rpeB present strong homologies with those previously reported for phycoerythrin subunits of cyanobacteria, rhodophyta, and cryptomonads. The main difference with the corresponding cyanobacterial genes was the unexpected occurrence of an intervening sequence that split rpeB into two exons. This intervening sequence presents characteristics of group II introns but lacks several structural domains. Transcriptional analyses showed that the two rpe genes are cotranscribed and that the major RNA species detected corresponds to a mature mRNA lacking the intron. As the phycobiliproteins form a group of closely related polypeptides in cyanobacteria and rhodophyta, the molecular events affecting the corresponding genes, such as the rpeB intron, may be a clue to elucidate some aspects of the molecular processes involved in the evolution of plastid genes.

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References

Ofarrell P . High resolution two-dimensional electrophoresis of proteins. J Biol Chem. 1975; 250(10):4007-21. PMC: 2874754. View

Morschel E, Wehrmeyer W, Koller K . Biliprotein assembly in the disc-shaped phycobilisomes of Rhodella violacea. Electron microscopical and biochemical analysis of B-phycoerythrin and B-phycoerythrin--C-phycocyanin aggregates. Eur J Cell Biol. 1980; 21(3):319-27. View

Xu M, Kathe S, Nierzwicki-Bauer S, Shub D . Bacterial origin of a chloroplast intron: conserved self-splicing group I introns in cyanobacteria. Science. 1990; 250(4987):1566-70. DOI: 10.1126/science.2125747. View

van der Veen R, Arnberg A, Van Der Horst G, Bonen L, Tabak H, Grivell L . Excised group II introns in yeast mitochondria are lariats and can be formed by self-splicing in vitro. Cell. 1986; 44(2):225-34. DOI: 10.1016/0092-8674(86)90756-7. View

Brawerman G . Determinants of messenger RNA stability. Cell. 1987; 48(1):5-6. DOI: 10.1016/0092-8674(87)90346-1. View

Sidler W, Kumpf B, Suter F, Klotz A, Glazer A, Zuber H . The complete amino-acid sequence of the alpha and beta subunits of B-phycoerythrin from the rhodophytan alga Porphyridium cruentum. Biol Chem Hoppe Seyler. 1989; 370(2):115-24. DOI: 10.1515/bchm3.1989.370.1.115. View

Turner S, Burger-Wiersma T, Giovannoni S, Mur L, Pace N . The relationship of a prochlorophyte Prochlorothrix hollandica to green chloroplasts. Nature. 1989; 337(6205):380-2. DOI: 10.1038/337380a0. View

Schmelzer C, Schweyen R . Self-splicing of group II introns in vitro: mapping of the branch point and mutational inhibition of lariat formation. Cell. 1986; 46(4):557-65. DOI: 10.1016/0092-8674(86)90881-0. View

Laemmli U . Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970; 227(5259):680-5. DOI: 10.1038/227680a0. View

10.

Egelhoff T, Grossman A . Cytoplasmic and chloroplast synthesis of phycobilisome polypeptides. Proc Natl Acad Sci U S A. 1983; 80(11):3339-43. PMC: 394038. DOI: 10.1073/pnas.80.11.3339. View

11.

Goldschmidt-Clermont M, Choquet Y, Girard-Bascou J, Michel F, Schirmer-Rahire M, Rochaix J . A small chloroplast RNA may be required for trans-splicing in Chlamydomonas reinhardtii. Cell. 1991; 65(1):135-43. DOI: 10.1016/0092-8674(91)90415-u. View

12.

Wilbanks S, de Lorimier R, Glazer A . Phycoerythrins of marine unicellular cyanobacteria. III. Sequence of a class II phycoerythrin. J Biol Chem. 1991; 266(15):9535-9. View

13.

Reith M, Douglas S . Localization of beta-phycoerythrin to the thylakoid lumen of Cryptomonas phi does not involve a signal peptide. Plant Mol Biol. 1990; 15(4):585-92. DOI: 10.1007/BF00017833. View

14.

Anderson L, Grossman A . Structure and light-regulated expression of phycoerythrin genes in wild-type and phycobilisome assembly mutants of Synechocystis sp. strain PCC 6701. J Bacteriol. 1990; 172(3):1297-305. PMC: 208598. DOI: 10.1128/jb.172.3.1297-1305.1990. View

15.

Kuhsel M, Strickland R, Palmer J . An ancient group I intron shared by eubacteria and chloroplasts. Science. 1990; 250(4987):1570-3. DOI: 10.1126/science.2125748. View

16.

Mazel D, Guglielmi G, Houmard J, Sidler W, Bryant D, de Marsac N . Green light induces transcription of the phycoerythrin operon in the cyanobacterium Calothrix 7601. Nucleic Acids Res. 1986; 14(21):8279-90. PMC: 311859. DOI: 10.1093/nar/14.21.8279. View

17.

Glazer A . Light guides. Directional energy transfer in a photosynthetic antenna. J Biol Chem. 1989; 264(1):1-4. View

18.

Damerval T, Castets A, Guglielmi G, Houmard J, de Marsac N . Occurrence and distribution of gas vesicle genes among cyanobacteria. J Bacteriol. 1989; 171(3):1445-52. PMC: 209765. DOI: 10.1128/jb.171.3.1445-1452.1989. View

19.

Michel F, Umesono K, Ozeki H . Comparative and functional anatomy of group II catalytic introns--a review. Gene. 1989; 82(1):5-30. DOI: 10.1016/0378-1119(89)90026-7. View

20.

Choquet Y, Goldschmidt-Clermont M, Girard-Bascou J, Kuck U, Bennoun P, Rochaix J . Mutant phenotypes support a trans-splicing mechanism for the expression of the tripartite psaA gene in the C. reinhardtii chloroplast. Cell. 1988; 52(6):903-13. DOI: 10.1016/0092-8674(88)90432-1. View