Abstract
The small signaling molecule auxin controls numerous developmental processes in land plants, acting mostly by regulating gene expression. Auxin response proteins are represented by large families of diverse functions, but neither their origin nor their evolution is understood. Here, we use a deep phylogenomics approach to reconstruct both the origin and the evolutionary trajectory of all nuclear auxin response protein families. We found that, while all subdomains are ancient, a complete auxin response mechanism is limited to land plants. Functional phylogenomics predicts defined steps in the evolution of response system properties, and comparative transcriptomics across six ancient lineages revealed how these innovations shaped a sophisticated response mechanism. Genetic analysis in a basal land plant revealed unexpected contributions of ancient non-canonical proteins in auxin response as well as auxin-unrelated function of core transcription factors. Our study provides a functional evolutionary framework for understanding diverse functions of the auxin signal.
Highlights
Auxins are a group of structurally related chemical compounds that control a multitude of growth and developmental processes in plants
Most of the hormone-contacting residues (11 out of 12) are different from both TIR1/AFB and CORONATINE INSENSITIVE 1 (COI1) (Figure 3C and Supplementary file 2). These results suggest that the charophyte TIR1/AFB/COI1 precursor may not act as an auxin or jasmonic acid (JA) receptor, and we conclude that dedicated receptors for auxin and JA were established only in land plants
All subdomains of dedicated auxin-response proteins were recovered in transcriptomes from red algae and chlorophytes, but the multidomain protein appears only in the charophyte and land plant lineage
Summary
Auxins are a group of structurally related chemical compounds that control a multitude of growth and developmental processes in plants. While auxins have been shown to trigger rapid cellular events such as membrane hyperpolarization (Bates and Goldsmith, 1983; Etherton, 1970), calcium influx (Monshausen et al, 2011; Schenck et al, 2010), and changes in endocytosis (Paciorek et al, 2005; Robert et al, 2010), its activity in controlling growth and development appear to be mainly mediated by changes in gene expression via a nuclear auxin pathway (NAP) Perturbation of this gene regulatory pathway interferes with most, if not all, developmental responses (Weijers and Wagner, 2016).
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