Editors' ChoicePlant biology

Auxin signaling without Aux/IAAs

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Sci. Signal.  15 Nov 2016:
Vol. 9, Issue 454, pp. ec268
DOI: 10.1126/scisignal.aal3883

The hormone auxin controls plant development at all stages and in most, if not all, tissues. The best characterized pathway for auxin-mediated regulation of gene expression is through inhibition of an E3 ubiquitin ligase, which binds to auxin and related chemicals, to alleviate repression of the PB1 domain–containing members of the ARF family of transcriptions factors. ETTIN (ETT, also known as ARF3) lacks a PB1 domain and thus cannot be regulated in the same manner as other ARFs because ETT does not interact with the repressive partner proteins Aux/IAAs. ETT functions in many of the developmental processes that are regulated by auxin, such as the female reproductive organ, lateral root formation, and establishment of leaf polarity. Simonini et al. found that ETT and INDEHISCENT (IND), encoding another transcription factor, were expressed in the same region of the developing gynoecium (a part of the female reproductive organ). IND, along with another transcription factor SPATULA (SPT), regulate auxin polarity by inhibiting expression of the gene encoding PINOID (PID), a kinase controlling auxin transport, a process important in the developing gynoecium. The PID gene contained two auxin response elements (AuxREs), and chromatin immunoprecipitation experiments and yeast one-hybrid assays showed that ETT interacted with these sequences in a manner dependent on the conserved AuxRE motif. Plants with the ett-3 mutation had an expanded region of PID expression in the developing gynoecium, and this was further expanded in ett-3, ind-2 double mutants, indicating that ETT and IND may function together to repress PID expression. Four different interaction assays indicated that ETT and IND directly interacted, and a region specific to ETTIN, not present in other ARFs, was necessary and sufficient for the interaction. Unlike the E3 ligase component that binds to natural auxin (indole 3-acetic acid, IAA) and synthetic analogs, only IAA disrupted the interaction between ETT and IND. A screen for point mutants of IND or targeted mutation of cysteines in ETT identified residues critical for the IAA-dependent regulation of the ETT-IND interaction. Expression of the INDD30G mutant that bound to ETT in the presence and absence of IAA resulted in abnormal female reproductive organ development, but this mutant rescued the indehiscent phenotype (inability of a fruit or seed pod to open), suggesting that the role of IND in the gynoecium, but not the fruit, depended on IAA and ETT. Because ETT is involved in the development of several tissues in which IND is not, the authors screened for other transcription factor partners for ETT and identified five additional potential interacting partners in addition to IND and two others that were previously reported. Yeast two-hybrid analysis of these transcription factors revealed that IAA disrupted the interaction between ETT and each of them. Indeed, expression of the ETT2C-S mutant that is not regulated by IAA resulted in abnormal development of lateral roots, primary branch fusion and ovule development, processes that are controlled by one or more of the transcription factors identified as IAA-regulated partners of ETT. Thus, ETT appears to serve as the auxin-regulated partner in various transcription factor complexes, providing evidence for a second auxin signaling mechanism.

S. Simonini, J. Deb, L. Moubayidin, P. Stephenson, M. Valluru, A. Freire-Rios, K. Sorefan, D. Weijers, J. Friml, L. Østergaard, A noncanonical auxin-sensing mechanism is required for organ morphogenesis in Arabidopsis. Genes Dev. 30, 2286–2296 (2016). [Abstract]

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