Plants need to constantly surveil their surroundings to adapt to environmental fluctuations, which they achieve primarily through transcriptional reprogramming. Thus, plants are excellent models for identifying novel transcriptional regulatory mechanisms. In this study, we characterize the regulation mediated by long non-coding transcription that initiates on the complementary strand in the 5' end of coding genes (convergent antisense transcription, CASt). In Arabidopsis, CASt is associated with stress-responsive genes that are highly expressed. Our analysis shows that CASt depends on a specific gene architecture that is evolutionarily conserved in higher plants. CASt is present in genes with an extended first intron and over-represented in genes encoding functional transporters in Arabidopsis, such as the AMINO ACID PERMEASE (AAP) transporter family. Experimental evidence points to a role for CASt in priming their host genes for stress responsiveness in evolutionary divergent plant species. Furthermore, we were able to predict stress responsiveness in rice AAP genes based on the presence of a long first intron and CASt. Collectively, we show an evolutionary strategy and regulatory mechanism specific to plants for enhancing stress responsiveness through modification of gene architecture and antisense transcription.
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