Bimodal regulation of ICR1 levels generates self-organizing auxin distribution Journal Article


Author(s): Hazak, Ora; Obolski, Uri; Prat, Tomas; Friml, Jiřĺ; Hadany, Lilach; Yalovsky, Shaul
Article Title: Bimodal regulation of ICR1 levels generates self-organizing auxin distribution
Affiliation IST Austria
Abstract: Auxin polar transport, local maxima, and gradients have become an importantmodel system for studying self-organization. Auxin distribution is regulated by auxin-dependent positive feedback loops that are not well-understood at the molecular level. Previously, we showed the involvement of the RHO of Plants (ROP) effector INTERACTOR of CONSTITUTIVELY active ROP 1 (ICR1) in regulation of auxin transport and that ICR1 levels are posttranscriptionally repressed at the site of maximum auxin accumulation at the root tip. Here, we show that bimodal regulation of ICR1 levels by auxin is essential for regulating formation of auxin local maxima and gradients. ICR1 levels increase concomitant with increase in auxin response in lateral root primordia, cotyledon tips, and provascular tissues. However, in the embryo hypophysis and root meristem, when auxin exceeds critical levels, ICR1 is rapidly destabilized by an SCF(TIR1/AFB) [SKP, Cullin, F-box (transport inhibitor response 1/auxin signaling F-box protein)]-dependent auxin signaling mechanism. Furthermore, ectopic expression of ICR1 in the embryo hypophysis resulted in reduction of auxin accumulation and concomitant root growth arrest. ICR1 disappeared during root regeneration and lateral root initiation concomitantly with the formation of a local auxin maximum in response to external auxin treatments and transiently after gravitropic stimulation. Destabilization of ICR1 was impaired after inhibition of auxin transport and signaling, proteasome function, and protein synthesis. A mathematical model based on these findings shows that an in vivo-like auxin distribution, rootward auxin flux, and shootward reflux can be simulated without assuming preexisting tissue polarity. Our experimental results and mathematical modeling indicate that regulation of auxin distribution is tightly associated with auxin-dependent ICR1 levels.
Keywords: Pattern formation; Auxin; Root development; ROP GTPases; Transport
Journal Title: PNAS
Volume: 111
Issue 50
ISSN: 1091-6490
Publisher: National Academy of Sciences  
Date Published: 2014-12-16
Start Page: E5471
End Page: E5479
Sponsor: This research was supported by Israel Science Foundation Grants 1568/13 (to L.H.), 1244/11 (to S.Y.), and 1125/13 (to S.Y.) and US–Israel Binational Science Foundation Grant BSF 2009309 (to S.Y.).
URL:
DOI: 10.1073/pnas.1413918111
Notes: We thank K. Hayashi for sharing published materials, the Manna Center for Plant Biology at Tel Aviv University for support, and S. McCormick for critical reading of the manuscript.
Open access: yes (repository)