Abstract
Basic leucine zippers (bZIPs) form a large plant transcription factor family. C and S1 bZIP groups can heterodimerize, fulfilling crucial roles in seed development and stress response. S1 sequences also harbor a unique regulatory mechanism, termed Sucrose-Induced Repression of Translation (SIRT). The conservation of both C/S1 bZIP interactions and SIRT remains poorly characterized in non-model species, leaving their evolutionary origin uncertain and limiting crop research. In this work, we explored recently published plant sequencing data to establish a detailed phylogeny of C and S1 bZIPs, investigating their intertwined role in plant evolution, and the origin of SIRT. Our analyses clarified C and S1 bZIP orthology relationships in angiosperms, and identified S1 sequences in gymnosperms. We experimentally showed that the gymnosperm orthologs are regulated by SIRT, tracing back the origin of this unique regulatory mechanism to the ancestor of seed plants. Additionally, we discovered an earlier S ortholog in the charophyte algae Klebsormidium flaccidum, together with a C ortholog. This suggests that C and S groups originated by duplication from a single algal proto-C/S ancestor. Based on our observations, we propose a model wherein the C/S1 bZIP dimer network evolved in seed plants from pre-existing C/S bZIP interactions.
Highlights
Basic leucine zippers form a large plant transcription factor family
We explored recently published plant sequencing data to establish a detailed phylogeny of C and S1 Basic leucine zippers (bZIPs), investigating their intertwined role in plant evolution, and the origin of Sucrose-Induced Repression of Translation (SIRT)
The specificity of S1 bZIP activity in low energy conditions is achieved via a unique regulatory mechanism, termed Sucrose-Induced Repression of Translation (SIRT)[22,23,24], which relies on the presence of a characteristic uORF at the 5′leader of the bZIP transcript (5′uORF)
Summary
Basic leucine zippers (bZIPs) form a large plant transcription factor family. C and S1 bZIP groups can heterodimerize, fulfilling crucial roles in seed development and stress response. S1 sequences harbor a unique regulatory mechanism, termed Sucrose-Induced Repression of Translation (SIRT) The conservation of both C/S1 bZIP interactions and SIRT remains poorly characterized in non-model species, leaving their evolutionary origin uncertain and limiting crop research. The specificity of S1 bZIP activity in low energy conditions is achieved via a unique regulatory mechanism, termed Sucrose-Induced Repression of Translation (SIRT)[22,23,24], which relies on the presence of a characteristic uORF at the 5′leader of the bZIP transcript (5′uORF). SIRT is considered a characterizing feature of these transcription factors, as no similar uORF sequences or uORF-based repression mechanism by sucrose has been observed in other bZIP groups, or more generally in other plant gene families[26]. C and S1 bZIP members interact while avoiding dimerization with other S sequences[13,27], indicating the presence of selective pressure to prevent promiscuity
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