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WOX5–IAA17 Feedback Circuit-Mediated Cellular Auxin Response Is Crucial for the Patterning of Root Stem Cell Niches in Arabidopsis

Tian, Huiyu, Wabnik, Krzysztof, Niu, Tiantian, Li, Hanbing, Yu, Qianqian, Pollmann, Stephan, Vanneste, Steffen, Govaerts, Willy, Rolčík, Jakub, Geisler, Markus, Friml, Jiří, Ding, Zhaojun
Molecular plant 2014 v.7 no.2 pp. 277-289
Arabidopsis, biosynthesis, computer simulation, genes, indole acetic acid, models, root meristems, root systems, stem cells, transcription (genetics), transcription factors
In plants, the patterning of stem cell-enriched meristems requires a graded auxin response maximum that emerges from the concerted action of polar auxin transport, auxin biosynthesis, auxin metabolism, and cellular auxin response machinery. However, mechanisms underlying this auxin response maximum-mediated root stem cell maintenance are not fully understood. Here, we present unexpected evidence that WUSCHEL-RELATED HOMEOBOX 5 (WOX5) transcription factor modulates expression of auxin biosynthetic genes in the quiescent center (QC) of the root and thus provides a robust mechanism for the maintenance of auxin response maximum in the root tip. This WOX5 action is balanced through the activity of indole-3-acetic acid 17 (IAA17) auxin response repressor. Our combined genetic, cell biology, and computational modeling studies revealed a previously uncharacterized feedback loop linking WOX5-mediated auxin production to IAA17-dependent repression of auxin responses. This WOX5–IAA17 feedback circuit further assures the maintenance of auxin response maximum in the root tip and thereby contributes to the maintenance of distal stem cell (DSC) populations. Our experimental studies and in silico computer simulations both demonstrate that the WOX5–IAA17 feedback circuit is essential for the maintenance of auxin gradient in the root tip and the auxin-mediated root DSC differentiation.The stem cell niche in the root meristem plays a critical role during the development of plant root systems. The polar cell-to-cell transport generates the distribution maximum of the phytohormone auxin that plays a critical role during growth and patterning of roots. Recently, the transcription factor WOX5 (WUSCHEL-RELATED HOMEOBOX 5) was identified as a master regulator of root stem cell niche patterning. Here, we demonstrate that WOX5 coordinates local auxin production and thus controls spatial restriction and maintenance of the auxin maximum in the quiescent center (QC) of the root. In turn, this root-associated auxin maximum feeds back on WOX5 expression via IAA17-dependent regulation of auxin responses. Both our experimental studies and in silico computer modeling simulations suggest that the feedback circuit between WOX5 activity and auxin signaling maximum is at the heart of auxin-mediated root patterning.