WUSCHEL acts as an auxin response rheostat to maintain apical stem cells in Arabidopsis

Yanfei Ma,Klaus Brackmann,Anna Medzihradszky,Jan U Lohmann,Thomas Greb,Carlos S Galván-Ampudia,Andrej Miotk,Gözde Utan,Christophe Gaillochet,Joachim Forner,Olga Ermakova,Zoran Šutiković,Christian Wenzl,Teva Vernoux

doi:10.1038/s41467-019-13074-9

Abstract

To maintain the balance between long-term stem cell self-renewal and differentiation, dynamic signals need to be translated into spatially precise and temporally stable gene expression states. In the apical plant stem cell system, local accumulation of the small, highly mobile phytohormone auxin triggers differentiation while at the same time, pluripotent stem cells are maintained throughout the entire life-cycle. We find that stem cells are resistant to auxin mediated differentiation, but require low levels of signaling for their maintenance. We demonstrate that the WUSCHEL transcription factor confers this behavior by rheostatically controlling the auxin signaling and response pathway. Finally, we show that WUSCHEL acts via regulation of histone acetylation at target loci, including those with functions in the auxin pathway. Our results reveal an important mechanism that allows cells to differentially translate a potent and highly dynamic developmental signal into stable cell behavior with high spatial precision and temporal robustness.

Highlights

To maintain the balance between long-term stem cell self-renewal and differentiation, dynamic signals need to be translated into spatially precise and temporally stable gene expression states
We found that auxin is present and sensed fairly uniformly across the shoot apical meristem (SAM) including the central stem cell domain, with local minima only detected at young primordia and developing organ boundaries (Fig. 1a, b and refs. 17,18)
Computational analysis of the DR5v2 and pCLV3 signals revealed that the auxin response minimum invariantly coincided with the center of the stem cell domain (Fig. 1c–f)

Summary

Introduction

To maintain the balance between long-term stem cell self-renewal and differentiation, dynamic signals need to be translated into spatially precise and temporally stable gene expression states. In the apical plant stem cell system, local accumulation of the small, highly mobile phytohormone auxin triggers differentiation while at the same time, pluripotent stem cells are maintained throughout the entire life-cycle. We demonstrate that the WUSCHEL transcription factor confers this behavior by rheostatically controlling the auxin signaling and response pathway. The shoot apical meristem (SAM) is a highly dynamic and continuously active stem cell system responsible for the generation of all above ground tissues of plants. The stem cells are located in the central zone and are maintained by a feedback loop consisting of the stem cell promoting WUSCHEL (WUS) homeodomain transcription factor and the restrictive CLAVATA (CLV) pathway[1,2]. We demonstrate that WUSCHEL acts via regulation of histone acetylation at target loci, including those with functions in the auxin pathway

Methods

Results

Conclusion