The AFB1 auxin receptor controls the cytoplasmic auxin response pathway inArabidopsis thaliana

Abstract

The phytohormone auxin triggers root growth inhibition within seconds via a non-transcriptional pathway. Among members of the TIR1/AFBs auxin receptor family, AFB1 has a primary role in this rapid response. However, the unique features that confer this specific function have not been identified. Here we show that the N-terminal region of AFB1, including the F-box domain and residues that contribute to auxin binding, are essential and sufficient for its specific role in the rapid response. Substitution of the N-terminal region of AFB1 with that of TIR1 disrupts its distinct cytoplasm-enriched localization and activity in rapid root growth inhibition. Importantly, the N-terminal region of AFB1 is indispensable for auxin-triggered calcium influx which is a prerequisite for rapid root growth inhibition. Furthermore, AFB1 negatively regulates lateral root formation and transcription of auxin-induced genes, suggesting that it plays an inhibitory role in canonical auxin signaling. These results suggest that AFB1 may buffer the transcriptional auxin response while it regulates rapid changes in cell growth that contribute to root gravitropism.

Auxin coreceptor IAA17/AXR3 controls cell elongation inArabidopsis thalianaroot by modulation of auxin and gibberellin perception

“…The AFB1 auxin co-receptor and several Aux/IAA proteins localize not only to the nucleus, but also partially to the cytoplasm (Prigge et al 2020; Zhang et al 2019), and the AFB1-dependent rapid signaling occurs in the cytoplasm (Dubey et al 2023; Prigge et al 2020). We therefore tested whether AXR3-1 might function outside the nucleus and participate in the rapid auxin response.…”

“…The various sensitivity of individual processes can be explained by a wide range of auxin actions, including spatial and temporal aspects and different sensitivity of individual cells to auxin (Sauer, Robert, and Kleine-Vehn 2013). Given that various signaling pathways can exert both cooperative and opposing effects on modulation of root growth and morphology (Dubey et al 2023; Li et al 2021), it is plausible to infer that modulation of the nuclear signaling pathway could also affect other auxin cascades. Interestingly, although a rapid non-transcriptional response is required for the early events of gravitropic response (Serre et al 2021), our data indicate that the cytoplasmic auxin response pathway is not sufficient to promote gravitropic bending in combination with a disrupted nuclear auxin pathway.…”

“…Interestingly, we observed a weak but consistent effect of cytoplasm-localized AXR3-1 on growth rate. It is intriguing to speculate that the accumulation of the protein in the cytoplasm interferes with the AFB1-dependent auxin response pathway (Dubey et al 2023; Prigge et al 2020).…”

“…In the root, a mutualistic interaction of other signaling pathways was also shown. The synergistic functioning of the nuclear auxin pathway and the cytoplasmic AFB1 receptor for fast auxin responses (Dubey et al 2023; Prigge et al 2020; Serre et al 2021) is essential for the regulation of root bending. However, their antagonistic effect is involved in the formation of lateral roots (Dubey et al 2023).…”

Genetically encoded, noise-tolerant, auxin biosensors in yeast facilitate metabolic engineering and directed evolution

“…We have demonstrated how the single-fusion biosensor can be used to determine the distribution of function for a library of TIR1/AFB variants, and plan to perform comprehensive mutational scanning and directed evolution of these proteins in the future, to further refine the sequence function map of these multifaceted signaling proteins [120][121][122][123][124][125] and to engineer novel functions 126 . For mutational studies in Aux/IAAs the single-fusion ratiometric sensor, also provides a simple quantitative reporter of Aux/IAA degradation, which would prove useful in studying the numerous functional elements of these transcriptional regulators 21,[127][128][129][130][131][132] .…”