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

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.

Mathematical modeling of plant cell fate transitions controlled by hormonal signals

“…This scenario results in loss of stem cells, since the defective WUS protein cannot induce production of CLV3. Experimentally such a scenario can be studied using WUS loss-of-function mutants, as it has been done in [28] or inducible RNAi [26,42,43]. The loss of stem cells observed in the simulations is in agreement with experimental data.…”

“…It is known that auxin promotes cell fate transition from the PZ to lateral organs. Auxin signaling is repressed by WUS [43] in the meristem center and modulated by HEC in the meristem periphery [9]. The proposed computational framework is ideally suited to investigate details of these interactions.…”

“…The choice of the steady state as the initial condition is supported by experiments relying on inducible changes of gene expression. The plant is grown to the inflorescence state and only then the changes in gene expression are induced using e.g., dexamethasone or ethanol [9,40,[42][43][44]. Control measurements demonstrate that in the absence of the induced changes the meristem size remains constant and is identical as in the wild type.…”

“…WUS over-expression: There exist different experimental works studying an ubiquituous increase of WUS [42,43]. Experimentally this has been accomplished using a glucocorticoidinducible form of WUS under a promoter that causes ubiquitous expression.…”

Structural basis for the complex DNA binding behavior of the plant stem cell regulator WUSCHEL

“…The HD transcription factor WUS plays key roles for plant development with at least four distinct and essential subfunctions: Firstly, regulation of stem cell identity in the shoot apical meristem (SAM), where it is required for noncell autonomous induction and maintenance of stem cell fate via stimulation of cytokinin and suppression of auxin signalling 2,4,6,17,28,39 . Secondly, regulation of floral patterning through direct regulation of differentiation genes 16 .…”