A Molecular Framework for the Control of Adventitious Rooting by TIR1/AFB2-Aux/IAA-Dependent Auxin Signaling in Arabidopsis

Abstract

In Arabidopsis thaliana, canonical auxin-dependent gene regulation is mediated by 23 transcription factors from the AUXIN RESPONSE FACTOR (ARF) family that interact with auxin/indole acetic acid repressors (Aux/IAAs), which themselves form co-receptor complexes with one of six TRANSPORT INHIBITOR1/ AUXIN-SIGNALLING F-BOX (TIR1/AFB) proteins. Different combinations of co-receptors drive specific sensing outputs, allowing auxin to control a myriad of processes. ARF6 and ARF8 are positive regulators of adventitious root initiation upstream of jasmonate, but the exact auxin co-receptor complexes controlling the transcriptional activity of these proteins has remained unknown. Here, using loss-of-function mutants we show that three Aux/IAA genes, IAA6, IAA9, and IAA17, act additively in the control of adventitious root (AR) initiation. These three IAA proteins interact with ARF6 and/or ARF8 and likely repress their activity in AR development. We show that TIR1 and AFB2 are positive regulators of AR formation and TIR1 plays a dual role in the control of jasmonic acid (JA) biosynthesis and conjugation, as several JA biosynthesis genes are up-regulated in the tir1-1 mutant. These results lead us to propose that in the presence of auxin, TIR1 and AFB2 form specific sensing complexes with IAA6, IAA9, and/or IAA17 to modulate JA homeostasis and control AR initiation.

Integration of Jasmonic Acid and Ethylene Into Auxin Signaling in Root Development

“…JA participates in the regulation of root growth, seedling development, flower development, root regeneration, seed development, seed germination, tuber formation and senescence (Wasternack and Hause, 2013;Ye et al, 2019;Zhang G. et al, 2019). JA regulates root growth in many aspects, including inhibition of primary root (Chen et al, 2011), promoting lateral roots formation (Cai et al, 2014), negatively regulating adventitious roots (Gutierrez et al, 2012;Lakehal et al, 2019), and inducing root regeneration (Ye et al, 2019;Zhang G. et al, 2019). Most of these processes are achieved via cross-talking with auxin.…”

Small Auxin Up RNAs influence the distribution of indole-3-acetic acid and play a potential role in increasing seed size in Euryale ferox Salisb.

“…Further, these roles of IAA have been demonstrated in many genetic studies on the regulation of IAA through control of the metabolism of IAA, changes of IAA distribution pattern and on plant responses to IAA signaling [14,15]. Furthermore, up to present, a large number of IAA-related genes have been documented.…”

Understanding of Adventitious Root Formation: What Can We Learn From Comparative Genetics?

“…ARF17, a target of microRNA160 (miR160), is a negative regulator of AR formation, while ARF6 and ARF8, targets of miR167, are positive regulators of adventitious rooting, which function in a complex regulatory loop at both transcriptional and posttranscriptional level ( Gutierrez et al, 2009 ). In the presence of high auxin levels, two F-box proteins from the TRANSPORT INHIBITOR1/AUXIN-SIGNALING F-BOX PROTEIN (TIR1/AFB) family, TIR1 and AFB2, promote 26S proteasome-mediated degradation of the auxin/indole-3-acetic acid (Aux/IAA) corepressors IAA6, IAA9 and IAA17, which in turn allows the transcriptional activity of ARF6 and ARF8 in the presence of auxin ( Lakehal et al, 2019 ). As a result, ARF6 and ARF8 upregulate GRETCHEN HAGEN3.3 ( GH3.3 ), GH3.5 , and GH3.6 expression, which encode the acyl-acid-amido synthetases involved in the negative regulation of active JA levels that inhibit AR formation in the hypocotyl ( Gutierrez et al, 2012 ; Figure 2C ).…”