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.
Highlights
Precise orchestration of organ patterning and polarity establishment during plant growth depends on close integration of environmental, hormonal, and cellular responses
A screening for random point mutations introduced in the IND ORF resulted in the isolation of an aspartate-toglycine substitution at position 30 (D30G) (Fig. 5A), which caused the ETT–IND interaction to become indole 3-acetic acid (IAA)-insensitive (Fig. 5B). Expressing this INDD30G variant under the IND promoter in the strong ind-2 mutant background led to a striking overproliferation of stigmatic tissue accompanied by reduced pollen tube density and decreased fertility, which was not seen when ind-2 was transformed with a wild-type pIND:: IND construct or in the untransformed ind-2 mutant (Fig. 5C–E; Supplemental Fig. 6A–F). These results strongly suggest that the IAA sensitivity of the ETT– IND complex is important for proper gynoecium development and plant reproduction
ETT belongs to the auxin response factors (ARFs) family and has been associated previously with auxin-related processes during gynoecium development (Nemhauser et al 2000); given that ETT lacks the PB1 domain, it seems unlikely that ETT would function via the canonical auxin signaling pathway
Summary
Precise orchestration of organ patterning and polarity establishment during plant growth depends on close integration of environmental, hormonal, and cellular responses. Canonical auxin signaling occurs through binding of the auxin molecule to F-box proteins of the TIR1/AFB class, which forms part of the SCFTIR1/AFB complex (Dharmasiri et al 2005; Kepinski and Leyser 2005). This allows interaction with the transcriptional repressor proteins of the Aux/IAA family, which, in the absence of auxin, repress auxin response factor (ARF) proteins, preventing them from regulating their targets. In addition to its role in the gynoecium, ETT functions during lateral root (LR) formation and ovule integument development, in the establishment of leaf polarity, and in the stem–pedicel fusion process PID is a serine–threonine kinase that mediates polar auxin transport and is fundamental for proper symmetry establishment (Benjamins et al 2001; Friml et al 2004; Moubayidin and Østergaard 2014)
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