Research Article: A Modular Analysis of the Auxin Signalling Network

Date Published: March 25, 2015

Publisher: Public Library of Science

Author(s): Etienne Farcot, Cyril Lavedrine, Teva Vernoux, Roeland M.H. Merks.

http://doi.org/10.1371/journal.pone.0122231

Abstract

Auxin is essential for plant development from embryogenesis onwards. Auxin acts in large part through regulation of transcription. The proteins acting in the signalling pathway regulating transcription downstream of auxin have been identified as well as the interactions between these proteins, thus identifying the topology of this network implicating 54 Auxin Response Factor (ARF) and Aux/IAA (IAA) transcriptional regulators. Here, we study the auxin signalling pathway by means of mathematical modeling at the single cell level. We proceed analytically, by considering the role played by five functional modules into which the auxin pathway can be decomposed: the sequestration of ARF by IAA, the transcriptional repression by IAA, the dimer formation amongst ARFs and IAAs, the feedback loop on IAA and the auxin induced degradation of IAA proteins. Focusing on these modules allows assessing their function within the dynamics of auxin signalling. One key outcome of this analysis is that there are both specific and overlapping functions between all the major modules of the signaling pathway. This suggests a combinatorial function of the modules in optimizing the speed and amplitude of auxin-induced transcription. Our work allows identifying potential functions for homo- and hetero-dimerization of transcriptional regulators, with ARF:IAA, IAA:IAA and ARF:ARF dimerization respectively controlling the amplitude, speed and sensitivity of the response and a synergistic effect of the interaction of IAA with transcriptional repressors on these characteristics of the signaling pathway. Finally, we also suggest experiments which might allow disentangling the structure of the auxin signaling pathway and analysing further its function in plants.

Partial Text

Auxin is a key signal for most of organogenesis and patterning processes occurring during plant development, in both shoot and root. The nature and intensity of the cellular response to this signal is known to be regulated at many levels, among which are the biosynthesis and polar transport of auxin that control the spatio-temporal distribution of the signal, but also the cellular sensitivity to the auxin signal [1]. It is still unclear how these different layers of control are integrated and allow for regulating auxin responses during plant development. In particular, the contribution of the topology of the pathway to the cellular sensitivity to auxin is still largely unknown.

Through a modelling approach, we have been able to analyze the contribution to the response dynamics of most of the topological features of the ARF/IAA signalling pathway controlling transcription in response the plant hormone auxin, thus providing key insights into the regulatory potential of this signalling pathway crucial to plant development.

Instead of defining each individual variable, we adopt the following nomenclature:
I and A respectively denote the concentration of IAA and ARF proteins.DXY generically denote the concentration of an X:Y dimer.R denotes the concentration of IAA mRNA.G, GA, GAA and GAI respectively denote the probability of the promoter being free, bound to an ARF protein or bound to an ARF:ARF or ARF:IAA dimer.We use x to denote the concentration of auxin. Note that because of our simplifying assumptions regarding auxin perception, x is more accurately interpreted as a combined rate including the level of auxin and its receptors, but will often be referred to as “auxin level” in the following for simplicity.

 

Source:

http://doi.org/10.1371/journal.pone.0122231