Shine-Dalgarno Sequences Play an Essential Role in the Translation of Plastid MRNAs in Tobacco

Overview

Journal Plant Cell

Publisher Oxford University Press

Specialties Biology
Cell Biology

Date 2017 Nov 15

PMID 29133466

Citations 25

Authors

Lars B Scharff

Miriam Ehrnthaler

Marcin Janowski

Liam H Childs

Claudia Hasse

Jurgen Gremmels

Stephanie Ruf

Reimo Zoschke

Ralph Bock

Affiliations

Soon will be listed here.

Abstract

In prokaryotic systems, the translation initiation of many, though not all, mRNAs depends on interaction between a sequence element upstream of the start codon (the Shine-Dalgarno sequence [SD]) and a complementary sequence in the 3' end of the 16S rRNA (anti-Shine-Dalgarno sequence [aSD]). Although many chloroplast mRNAs harbor putative SDs in their 5' untranslated regions and the aSD displays strong conservation, the functional relevance of SD-aSD interactions in plastid translation is unclear. Here, by generating transplastomic tobacco () mutants with point mutations in the aSD coupled with genome-wide analysis of translation by ribosome profiling, we provide a global picture of SD-dependent translation in plastids. We observed a pronounced correlation between weakened predicted SD-aSD interactions and reduced translation efficiency. However, multiple lines of evidence suggest that the strength of the SD-aSD interaction is not the only determinant of the translational output of many plastid mRNAs. Finally, the translation efficiency of mRNAs with strong secondary structures around the start codon is more dependent on the SD-aSD interaction than weakly structured mRNAs. Thus, our data reveal the importance of the aSD in plastid translation initiation, uncover chloroplast genes whose translation is influenced by SD-aSD interactions, and provide insights into determinants of translation efficiency in plastids.

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References

Chotewutmontri P, Barkan A . Dynamics of Chloroplast Translation during Chloroplast Differentiation in Maize. PLoS Genet. 2016; 12(7):e1006106. PMC: 4945096. DOI: 10.1371/journal.pgen.1006106. View

Burkhardt D, Rouskin S, Zhang Y, Li G, Weissman J, Gross C . Operon mRNAs are organized into ORF-centric structures that predict translation efficiency. Elife. 2017; 6. PMC: 5318159. DOI: 10.7554/eLife.22037. View

Kozak M . Regulation of translation via mRNA structure in prokaryotes and eukaryotes. Gene. 2005; 361:13-37. DOI: 10.1016/j.gene.2005.06.037. View

Goodman D, Church G, Kosuri S . Causes and effects of N-terminal codon bias in bacterial genes. Science. 2013; 342(6157):475-9. DOI: 10.1126/science.1241934. View

Kahlau S, Bock R . Plastid transcriptomics and translatomics of tomato fruit development and chloroplast-to-chromoplast differentiation: chromoplast gene expression largely serves the production of a single protein. Plant Cell. 2008; 20(4):856-74. PMC: 2390737. DOI: 10.1105/tpc.107.055202. View

Muhlbauer S, Lossl A, Tzekova L, Zou Z, Koop H . Functional analysis of plastid DNA replication origins in tobacco by targeted inactivation. Plant J. 2002; 32(2):175-84. DOI: 10.1046/j.1365-313x.2002.01408.x. View

Kuroda H, Suzuki H, Kusumegi T, Hirose T, Yukawa Y, Sugiura M . Translation of psbC mRNAs starts from the downstream GUG, not the upstream AUG, and requires the extended Shine-Dalgarno sequence in tobacco chloroplasts. Plant Cell Physiol. 2007; 48(9):1374-8. DOI: 10.1093/pcp/pcm097. View

Sugiura M, Hirose T, Sugita M . Evolution and mechanism of translation in chloroplasts. Annu Rev Genet. 1999; 32:437-59. DOI: 10.1146/annurev.genet.32.1.437. View

Rogalski M, Ruf S, Bock R . Tobacco plastid ribosomal protein S18 is essential for cell survival. Nucleic Acids Res. 2006; 34(16):4537-45. PMC: 1636375. DOI: 10.1093/nar/gkl634. View

10.

Ingolia N, Ghaemmaghami S, Newman J, Weissman J . Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science. 2009; 324(5924):218-23. PMC: 2746483. DOI: 10.1126/science.1168978. View

11.

Manuell A, Quispe J, Mayfield S . Structure of the chloroplast ribosome: novel domains for translation regulation. PLoS Biol. 2007; 5(8):e209. PMC: 1939882. DOI: 10.1371/journal.pbio.0050209. View

12.

Kode V, Mudd E, Iamtham S, Day A . The tobacco plastid accD gene is essential and is required for leaf development. Plant J. 2005; 44(2):237-44. DOI: 10.1111/j.1365-313X.2005.02533.x. View

13.

Jacob W, Santer M, Dahlberg A . A single base change in the Shine-Dalgarno region of 16S rRNA of Escherichia coli affects translation of many proteins. Proc Natl Acad Sci U S A. 1987; 84(14):4757-61. PMC: 305184. DOI: 10.1073/pnas.84.14.4757. View

14.

Suay L, Salvador M, Abesha E, Klein U . Specific roles of 5' RNA secondary structures in stabilizing transcripts in chloroplasts. Nucleic Acids Res. 2005; 33(15):4754-61. PMC: 1188514. DOI: 10.1093/nar/gki760. View

15.

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

16.

Kozak M . Initiation of translation in prokaryotes and eukaryotes. Gene. 1999; 234(2):187-208. DOI: 10.1016/s0378-1119(99)00210-3. View

17.

Sugiura M . Plastid mRNA translation. Methods Mol Biol. 2014; 1132:73-91. DOI: 10.1007/978-1-62703-995-6_4. View

18.

Staub J, Maliga P . Accumulation of D1 polypeptide in tobacco plastids is regulated via the untranslated region of the psbA mRNA. EMBO J. 1993; 12(2):601-6. PMC: 413243. DOI: 10.1002/j.1460-2075.1993.tb05692.x. View

19.

Pfalz J, Bayraktar O, Prikryl J, Barkan A . Site-specific binding of a PPR protein defines and stabilizes 5' and 3' mRNA termini in chloroplasts. EMBO J. 2009; 28(14):2042-52. PMC: 2718276. DOI: 10.1038/emboj.2009.121. View

20.

Plader W, Sugiura M . The Shine-Dalgarno-like sequence is a negative regulatory element for translation of tobacco chloroplast rps2 mRNA: an additional mechanism for translational control in chloroplasts. Plant J. 2003; 34(3):377-82. DOI: 10.1046/j.1365-313x.2003.01732.x. View