A noncanonical auxin-sensing mechanism is required for organ morphogenesis in Arabidopsis

Abstract

Tissue patterning in multicellular organisms is the output of precise spatio-temporal regulation of gene expression coupled with changes in hormone dynamics. In plants, the hormone auxin regulates growth and development at every stage of a plant's life cycle. Auxin signaling occurs through binding of the auxin molecule to a TIR1/AFB F-box ubiquitin ligase, allowing interaction with Aux/IAA transcriptional repressor proteins. These are subsequently ubiquitinated and degraded via the 26S proteasome, leading to derepression of auxin response factors (ARFs). How auxin is able to elicit such a diverse range of developmental responses through a single signaling module has not yet been resolved. Here we present an alternative auxin-sensing mechanism in which the ARF ARF3/ETTIN controls gene expression through interactions with process-specific transcription factors. This noncanonical hormone-sensing mechanism exhibits strong preference for the naturally occurring auxin indole 3-acetic acid (IAA) and is important for coordinating growth and patterning in diverse developmental contexts such as gynoecium morphogenesis, lateral root emergence, ovule development, and primary branch formation. Disrupting this IAA-sensing ability induces morphological aberrations with consequences for plant fitness. Therefore, our findings introduce a novel transcription factor-based mechanism of hormone perception in plants.

Auxin-Induced Modulation of ETTIN Activity Orchestrates Gene Expression in Arabidopsis

“…As a first approach, we combined chromatin immunoprecipitation coupled with deep sequencing (ChIP-seq) of a pETT:ETT-GFP line (in ett-3; Simonini et al, 2016) normalized against a wild-type background (Supplemental Data Set 1) with transcriptome analysis (RNA-seq) of the ett-3 loss-of-function mutant versus the wild type (Supplemental Data Set 2). To explain the rationale of the analyses described in this work, Figure 1C graphically summarizes the experimental strategy adopted and the different data set subgroups that emerged from the comparison between the main data sets.…”

“…Whole-inflorescence tissues, excluding mature flowers and developing siliques, were collected for both ChIP-seq and RNA-seq analyses. Given the material considered and the known ETT expression pattern in the Arabidopsis shoot (Sessions et al, 1997;Nemhauser et al, 2000;Simonini et al, 2016), this study was (A) and (B) Scanning electron microscopy images of wild-type (A) and ett-3 (B) gynoecium apices. Tissues are false-colored: green, valves; pink, style; red, valve margin; orange, replum; blue, stigma.…”

“…In agreement with its lack of a PB1 domain, ETT was recently shown to mediate auxin signaling via an alternative Aux/IAAindependent pathway (Simonini et al, 2016). This signaling mechanism involves auxin (specifically IAA) modulating the interaction between ETT and its protein partners, thereby facilitating spatial and temporal changes in transcriptional responses during organ morphogenesis (Simonini et al, 2016).…”

“…ARF3/ETTIN (ETT) is a master regulator of development and morphogenesis of the female reproductive structure, the gynoecium (Sessions et al, 1997;Nemhauser et al, 2000;Simonini et al, 2016). A wild-type gynoecium ( Figure 1A) is patterned into highly distinct tissues with specific function and identity: The basal ovary is divided into two symmetrical valves that are separated by the medial region where replum and valve margins will form.…”

“…This signaling mechanism involves auxin (specifically IAA) modulating the interaction between ETT and its protein partners, thereby facilitating spatial and temporal changes in transcriptional responses during organ morphogenesis (Simonini et al, 2016).…”