Multi-transcriptomics identifies targets of the endoribonuclease DNE1 and highlights its coordination with decapping

Author:

Pouclet Aude1ORCID,Pflieger David1ORCID,Merret Rémy2ORCID,Carpentier Marie-Christine2ORCID,Schiaffini Marlene1ORCID,Zuber Hélène1ORCID,Gagliardi Dominique1ORCID,Garcia Damien1ORCID

Affiliation:

1. Institut de biologie moléculaire des plantes, CNRS, Université de Strasbourg , 67000 Strasbourg , France

2. Laboratoire Génome et Développement des Plantes, Université de Perpignan via Domitia, CNRS, UMR5096 , 66000 Perpignan , France

Abstract

Abstract Decapping is a crucial step in mRNA degradation in eucaryotes and requires the formation of a holoenzyme complex between the decapping enzyme DECAPPING 2 (DCP2) and the decapping enhancer DCP1. In Arabidopsis (Arabidopsis thaliana), DCP1-ASSOCIATED NYN ENDORIBONUCLEASE 1 (DNE1) is a direct protein partner of DCP1. The function of both DNE1 and decapping is necessary to maintain phyllotaxis, the regularity of organ emergence in the apex. In this study, we combined in vivo mRNA editing, RNA degradome sequencing, transcriptomics, and small RNA-omics to identify targets of DNE1 and study how DNE1 and DCP2 cooperate in controlling mRNA fate. Our data reveal that DNE1 mainly contacts and cleaves mRNAs in the coding sequence and has sequence cleavage preferences. DNE1 targets are also degraded through decapping, and both RNA degradation pathways influence the production of mRNA-derived small interfering RNAs. Finally, we detected mRNA features enriched in DNE1 targets including RNA G-quadruplexes and translated upstream open reading frames. Combining these four complementary high-throughput sequencing strategies greatly expands the range of DNE1 targets and allowed us to build a conceptual framework describing the influence of DNE1 and decapping on mRNA fate. These data will be crucial to unveil the specificity of DNE1 action and understand its importance for developmental patterning.

Funder

University of Strasbourg

IdEx Unistra

Publisher

Oxford University Press (OUP)

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