Abstract
Auxin is a major developmental regulator in plants and the acquisition of a transcriptional response to auxin likely contributed to developmental innovations at the time of water-to-land transition. Auxin Response Factors (ARFs) Transcription Factors (TFs) that mediate auxin-dependent transcriptional changes are divided into A, B and C evolutive classes in land plants. The origin and nature of the first ARF proteins in algae is still debated. Here, we identify the most ‘ancient’ ARF homologue to date in the early divergent charophyte algae Chlorokybus atmophyticus, CaARF. Structural modelling combined with biochemical studies showed that CaARF already shares many features with modern ARFs: it is capable of oligomerization, interacts with the TOPLESS co-repressor and specifically binds Auxin Response Elements as dimer. In addition, CaARF possesses a DNA-binding specificity that differs from class A and B ARFs and that was maintained in class C ARF along plants evolution. Phylogenetic evidence together with CaARF biochemical properties indicate that the different classes of ARFs likely arose from an ancestral proto-ARF protein with class C-like features. The foundation of auxin signalling would have thus happened from a pre-existing hormone-independent transcriptional regulation together with the emergence of a functional hormone perception complex.
Highlights
Charophytes diverged from chlorophyte algae more than a billion years ago (y.a.) and led to land plants emergence around 450 million y.a. [1,2,3,4,5]
This transition initiated around 1 billion years ago from a Charophyte algae lineage that acquired features allowing it to adapt to the very different terrestrial conditions. Land plants coordinate their development with external stimuli through signalling mechanisms triggered by plant hormones
Evolution of these molecules and their signalling pathways likely played an important role in the aquatic to terrestrial move. In this manuscript we study the origin of auxin signalling, a plant hormone implicated in all plant developmental steps
Summary
Charophytes diverged from chlorophyte algae more than a billion years ago (y.a.) and led to land plants emergence around 450 million y.a. [1,2,3,4,5]. Given the importance of the phytohormone auxin in plant development, the acquisition of its signalling pathway allowing for auxin-dependent changes in transcription is thought to have been a milestone in the water-to-land transition [1]. In land plants, this signalling pathway, called the Nuclear Auxin Pathway (NAP), relies on three main protein families: TIR1/ AFB (Transport Inhibitor Response 1/Auxin Signalling F-box) co-receptors, Aux/IAA transcriptional repressors (Auxin/Indole-3-Acetic Acid Protein) and ARF (Auxin Response Factors) Transcription Factors (TFs) [12,13]. ARFs bind double AuxREs (Auxin Response Elements) sites arranged in three possible orientations: Direct Repeat (DR), Everted Repeat (ER) and Inverted Repeat (IR) (S2 Fig) [1,17,18,19]
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