An mTRAN-mRNA interaction mediates mitochondrial translation initiation in plants

Author:

Tran Huy Cuong1ORCID,Schmitt Vivian1ORCID,Lama Sbatie1ORCID,Wang Chuande2ORCID,Launay-Avon Alexandra34ORCID,Bernfur Katja5ORCID,Sultan Kristin6ORCID,Khan Kasim1ORCID,Brunaud Véronique34ORCID,Liehrmann Arnaud347ORCID,Castandet Benoît34ORCID,Levander Fredrik68ORCID,Rasmusson Allan G.1ORCID,Mireau Hakim2ORCID,Delannoy Etienne34ORCID,Van Aken Olivier1ORCID

Affiliation:

1. Department of Biology, Lund University, Lund, Sweden.

2. Université Paris-Saclay, INRAE, AgroParisTech, Institut Jean-Pierre Bourgin (IJPB), 78000 Versailles, France.

3. Université Paris-Saclay, CNRS, INRAE, Université d’Évry, Institute of Plant Sciences Paris-Saclay (IPS2), 91405 Orsay, France.

4. Université Paris Cité, CNRS, INRAE, Institute of Plant Sciences Paris-Saclay (IPS2), 91405, Orsay, France.

5. Department of Chemistry, Lund University, Lund, Sweden.

6. Department of Immunotechnology, Lund University, Lund, Sweden.

7. Université Paris-Saclay, CNRS, Université d’Évry, Laboratoire de Mathématiques et Modélisation d’Évry, 91037 Évry-Courcouronnes, France.

8. National Bioinformatics Infrastructure Sweden, Science for Life Laboratory, Lund University, Lund, Sweden.

Abstract

Plant mitochondria represent the largest group of respiring organelles on the planet. Plant mitochondrial messenger RNAs (mRNAs) lack Shine-Dalgarno-like ribosome-binding sites, so it is unknown how plant mitoribosomes recognize mRNA. We show that “mitochondrial translation factors” mTRAN1 and mTRAN2 are land plant–specific proteins, required for normal mitochondrial respiration chain biogenesis. Our studies suggest that mTRANs are noncanonical pentatricopeptide repeat (PPR)–like RNA binding proteins of the mitoribosomal “small” subunit. We identified conserved Adenosine (A)/Uridine (U)-rich motifs in the 5′ regions of plant mitochondrial mRNAs. mTRAN1 binds this motif, suggesting that it is a mitoribosome homing factor to identify mRNAs. We demonstrate that mTRANs are likely required for translation of all plant mitochondrial mRNAs. Plant mitochondrial translation initiation thus appears to use a protein-mRNA interaction that is divergent from bacteria or mammalian mitochondria.

Publisher

American Association for the Advancement of Science (AAAS)

Subject

Multidisciplinary

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