The Nucleus-encoded Trans-acting Factor MCA1 Plays a Critical Role in the Regulation of Cytochrome F Synthesis in Chlamydomonas Chloroplasts

Overview

Journal Plant Cell

Publisher Oxford University Press

Specialties Biology
Cell Biology

Date 2011 Jan 11

PMID 21216944

Citations 37

Authors

Alix Boulouis

Cecile Raynaud

Sandrine Bujaldon

Aude Aznar

Francis-Andre Wollman

Yves Choquet

Affiliations

Soon will be listed here.

Abstract

Organelle gene expression is characterized by nucleus-encoded trans-acting factors that control posttranscriptional steps in a gene-specific manner. As a typical example, in Chlamydomonas reinhardtii, expression of the chloroplast petA gene encoding cytochrome f, a major subunit of the cytochrome b(6)f complex, depends on MCA1 and TCA1, required for the accumulation and translation of the petA mRNA. Here, we show that these two proteins associate in high molecular mass complexes that also contain the petA mRNA. We demonstrate that MCA1 is degraded upon interaction with unassembled cytochrome f that transiently accumulates during the biogenesis of the cytochrome b(6)f complex. Strikingly, this interaction relies on the very same residues that form the repressor motif involved in the Control by Epistasy of cytochrome f Synthesis (CES), a negative feedback mechanism that downregulates cytochrome f synthesis when its assembly within the cytochrome b(6)f complex is compromised. Based on these new findings, we present a revised picture for the CES regulation of petA mRNA translation that involves proteolysis of the translation enhancer MCA1, triggered by its interaction with unassembled cytochrome f.

Citing Articles

Systematic identification and characterization of genes in the regulation and biogenesis of photosynthetic machinery.

Kafri M, Patena W, Martin L, Wang L, Gomer G, Ergun S Cell. 2023; 186(25):5638-5655.e25.

PMID: 38065083 PMC: 10760936. DOI: 10.1016/j.cell.2023.11.007.

Applications of Synthetic Pentatricopeptide Repeat Proteins.

Kwok van der Giezen F, Honkanen S, Colas des Francs-Small C, Bond C, Small I Plant Cell Physiol. 2023; 65(4):503-515.

PMID: 38035801 PMC: 11094755. DOI: 10.1093/pcp/pcad150.

Plant organellar RNA maturation.

Small I, Melonek J, Bohne A, Nickelsen J, Schmitz-Linneweber C Plant Cell. 2023; 35(6):1727-1751.

PMID: 36807982 PMC: 10226603. DOI: 10.1093/plcell/koad049.

The thylakoid membrane protein NTA1 is an assembly factor of the cytochrome bf complex essential for chloroplast development in Arabidopsis.

Li N, Wong W, Feng L, Wang C, Wong K, Zhang N Plant Commun. 2022; 4(1):100509.

PMID: 36560880 PMC: 9860185. DOI: 10.1016/j.xplc.2022.100509.

Pas de Trois: An Overview of Penta-, Tetra-, and Octo-Tricopeptide Repeat Proteins From and Their Role in Chloroplast Gene Expression.

Macedo-Osorio K, Martinez-Antonio A, Badillo-Corona J Front Plant Sci. 2021; 12:775366.

PMID: 34868174 PMC: 8635915. DOI: 10.3389/fpls.2021.775366.

References

Kuras R, Buschlen S, Wollman F . Maturation of pre-apocytochrome f in vivo. A site-directed mutagenesis study in Chlamydomonas reinhardtii. J Biol Chem. 1995; 270(46):27797-803. DOI: 10.1074/jbc.270.46.27797. View

Zerges W, Rochaix J . Low density membranes are associated with RNA-binding proteins and thylakoids in the chloroplast of Chlamydomonas reinhardtii. J Cell Biol. 1998; 140(1):101-10. PMC: 2132599. DOI: 10.1083/jcb.140.1.101. View

Auchincloss A, Zerges W, Perron K, Girard-Bascou J, Rochaix J . Characterization of Tbc2, a nucleus-encoded factor specifically required for translation of the chloroplast psbC mRNA in Chlamydomonas reinhardtii. J Cell Biol. 2002; 157(6):953-62. PMC: 2174033. DOI: 10.1083/jcb.200201060. View

Xu F, Morin C, Mitchell G, Ackerley C, Robinson B . The role of the LRPPRC (leucine-rich pentatricopeptide repeat cassette) gene in cytochrome oxidase assembly: mutation causes lowered levels of COX (cytochrome c oxidase) I and COX III mRNA. Biochem J. 2004; 382(Pt 1):331-6. PMC: 1133946. DOI: 10.1042/BJ20040469. View

Stampacchia O, Girard-Bascou J, Zanasco J, Zerges W, Bennoun P, Rochaix J . A nuclear-encoded function essential for translation of the chloroplast psaB mRNA in chlamydomonas. Plant Cell. 1997; 9(5):773-82. PMC: 156955. DOI: 10.1105/tpc.9.5.773. View

Kuchka M, Goldschmidt-Clermont M, van Dillewijn J, Rochaix J . Mutation at the Chlamydomonas nuclear NAC2 locus specifically affects stability of the chloroplast psbD transcript encoding polypeptide D2 of PS II. Cell. 1989; 58(5):869-76. DOI: 10.1016/0092-8674(89)90939-2. View

Choquet Y, Stern D, Wostrikoff K, Kuras R, Girard-Bascou J, Wollman F . Translation of cytochrome f is autoregulated through the 5' untranslated region of petA mRNA in Chlamydomonas chloroplasts. Proc Natl Acad Sci U S A. 1998; 95(8):4380-5. PMC: 22497. DOI: 10.1073/pnas.95.8.4380. View

Schwarz C, Elles I, Kortmann J, Piotrowski M, Nickelsen J . Synthesis of the D2 protein of photosystem II in Chlamydomonas is controlled by a high molecular mass complex containing the RNA stabilization factor Nac2 and the translational activator RBP40. Plant Cell. 2007; 19(11):3627-39. PMC: 2174876. DOI: 10.1105/tpc.107.051722. View

Kuras R, Wollman F, Joliot P . Conversion of cytochrome f to a soluble form in vivo in Chlamydomonas reinhardtii. Biochemistry. 1995; 34(22):7468-75. DOI: 10.1021/bi00022a021. View

10.

de Vitry C, Olive J, Drapier D, Recouvreur M, Wollman F . Posttranslational events leading to the assembly of photosystem II protein complex: a study using photosynthesis mutants from Chlamydomonas reinhardtii. J Cell Biol. 1989; 109(3):991-1006. PMC: 2115777. DOI: 10.1083/jcb.109.3.991. View

11.

Dauvillee D, Stampacchia O, Girard-Bascou J, Rochaix J . Tab2 is a novel conserved RNA binding protein required for translation of the chloroplast psaB mRNA. EMBO J. 2003; 22(23):6378-88. PMC: 291835. DOI: 10.1093/emboj/cdg591. View

12.

Barkan A, Goldschmidt-Clermont M . Participation of nuclear genes in chloroplast gene expression. Biochimie. 2000; 82(6-7):559-72. DOI: 10.1016/s0300-9084(00)00602-7. View

13.

Nickelsen J, van Dillewijn J, Rahire M, Rochaix J . Determinants for stability of the chloroplast psbD RNA are located within its short leader region in Chlamydomonas reinhardtii. EMBO J. 1994; 13(13):3182-91. PMC: 395210. DOI: 10.1002/j.1460-2075.1994.tb06617.x. View

14.

Minai L, Wostrikoff K, Wollman F, Choquet Y . Chloroplast biogenesis of photosystem II cores involves a series of assembly-controlled steps that regulate translation. Plant Cell. 2005; 18(1):159-75. PMC: 1323491. DOI: 10.1105/tpc.105.037705. View

15.

Rimbault B, Esposito D, Drapier D, Choquet Y, Stern D, Wollman F . Identification of the initiation codon for the atpB gene in Chlamydomonas chloroplasts excludes translation of a precursor form of the beta subunit of the ATP synthase. Mol Gen Genet. 2000; 264(4):486-91. DOI: 10.1007/s004380000332. View

16.

Nickelsen J, Fleischmann M, Boudreau E, Rahire M, Rochaix J . Identification of cis-acting RNA leader elements required for chloroplast psbD gene expression in Chlamydomonas. Plant Cell. 1999; 11(5):957-70. PMC: 144227. DOI: 10.1105/tpc.11.5.957. View

17.

Choquet Y, Wollman F . Translational regulations as specific traits of chloroplast gene expression. FEBS Lett. 2002; 529(1):39-42. DOI: 10.1016/s0014-5793(02)03260-x. View

18.

Boynton J, Gillham N, Harris E, Hosler J, Johnson A, Jones A . Chloroplast transformation in Chlamydomonas with high velocity microprojectiles. Science. 1988; 240(4858):1534-8. DOI: 10.1126/science.2897716. View

19.

Zerges W, Wang S, Rochaix J . Light activates binding of membrane proteins to chloroplast RNAs in Chlamydomonas reinhardtii. Plant Mol Biol. 2002; 50(3):573-85. DOI: 10.1023/a:1020246007858. View

20.

Hattori M, Sugita M . A moss pentatricopeptide repeat protein binds to the 3' end of plastid clpP pre-mRNA and assists with mRNA maturation. FEBS J. 2009; 276(20):5860-9. DOI: 10.1111/j.1742-4658.2009.07267.x. View