Gene-Specific Translation Regulation Mediated by the Hormone-Signaling Molecule EIN2

• Published in: Cell 2015-10, Vol.163 (3), p.684-697
• Main Authors: Merchante, Catharina, Brumos, Javier, Yun, Jeonga, Hu, Qiwen, Spencer, Kristina R., Enríquez, Paul, Binder, Brad M., Heber, Steffen, Stepanova, Anna N., Alonso, Jose M.
• Format: Article
• Language: English
• Subjects: 3' Untranslated Regions; Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Ethylenes - metabolism; F-Box Proteins - genetics; Gene Expression Regulation, Plant; Nuclear Proteins - metabolism; Protein Biosynthesis; Receptors, Cell Surface - metabolism; Ribosomes - metabolism; RNA, Messenger - metabolism; Signal Transduction; Transcription Factors - metabolism
• ISSN: 0092-8674; 1097-4172
• DOI: 10.1016/j.cell.2015.09.036

The central role of translation in modulating gene activity has long been recognized, yet the systematic exploration of quantitative changes in translation at a genome-wide scale in response to a specific stimulus has only recently become technically feasible. Using the well-characterized signaling pathway of the phytohormone ethylene and plant-optimized genome-wide ribosome footprinting, we have uncovered a molecular mechanism linking this hormone’s perception to the activation of a gene-specific translational control mechanism. Characterization of one of the targets of this translation regulatory machinery, the ethylene signaling component EBF2, indicates that the signaling molecule EIN2 and the nonsense-mediated decay proteins UPFs play a central role in this ethylene-induced translational response. Furthermore, the 3′UTR of EBF2 is sufficient to confer translational regulation and required for the proper activation of ethylene responses. These findings represent a mechanistic paradigm of gene-specific regulation of translation in response to a key growth regulator. [Display omitted] •Ribosome footprinting uncovers a role of translation in the ethylene response•The EBF2 3′UTR is sufficient to confer translational control•Regulation of EBF2 translation is required for proper ethylene responses•EBF2 translation control depends on functional EIN2 and UPFs, but not EIN3/EIL1 Ribosome footprinting unveils gene-specific regulation of translation by the hormone ethylene involving the 3′UTR of the transcript of a known negative regulator, as well as a key ethylene signaling protein and the components of the nonsense-mediated decay machinery.