Transcriptional regulation has long been recognized as a vital process in the plant’s responses to the environment and in the execution of developmental programs. In contrast, very little is known about the selective translation of specific mRNAs and its regulation. The development of the ribosome footprinting technology (also known as Ribo-seq) has opened the door to genome-scale high-resolution analyses of translation across various species, genotypes, and conditions. We employed Ribo-seq to access the role of translational regulation in the response of plants to hormone ethylene. Our studies revealed that ethylene not only triggers a transcriptional cascade, but also elicits activation of a novel gene-specific translation-regulation mechanism, in which the signaling molecule EIN2 and the nonsense-mediated decay proteins UPFs play a central role. Characterization of the translational module in the ethylene response indicates that EIN2 can bind to the 3’UTR of the EBF2 mRNA, represses EBF2 translation in a UPF-dependent manner, and targets EBF2 transcripts to the cytoplasmic P-bodies. EBF2 encodes a negative regulator of ethylene signaling and has long been known to be induced by ethylene at the transcriptional level. Our studies suggest that although in the presence of ethylene EBF2 transcripts are indeed actively produced, they are targeted to P-bodies for storage without being translated. Once ethylene is withdrawn and EIN2 is degraded, the UPF-mediated translational repression is relieved, the accumulated EBF2 transcripts are released from the P-bodies and become massively translated to produce the EBF2 protein and shut down further ethylene signaling. These findings represent a new mechanistic paradigm of gene-specific translational regulation and shed fresh light on the molecular mechanisms behind the ability of plants to quickly reset to normal growth as soon as the stress hormone ethylene is removed. The apparent conservation of this mechanism across species not only underscores the critical role of gene-specific regulation of translation in the response to this key growth regulator, but also provides new means to selectively manipulate gene expression in agriculturally relevant ethylene-controlled processes such as fruit ripening, senescence, organ abscission, or pathogen response.
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