Auxin Response Factors promote organogenesis by chromatin-mediated repression of the pluripotency gene SHOOTMERISTEMLESS

Yuhee Chung,Lars Østergaard,Run Jin,Doris Wagner,Yang Zhu,Sara Simonini,Miin-Feng Wu,C Stewart Gillmor,Alma Armenta-Medina,Andre Kuhn

doi:10.1038/s41467-019-08861-3

Abstract

Specification of new organs from transit amplifying cells is critical for higher eukaryote development. In plants, a central stem cell pool maintained by the pluripotency factor SHOOTMERISTEMLESS (STM), is surrounded by transit amplifying cells competent to respond to auxin hormone maxima by giving rise to new organs. Auxin triggers flower initiation through Auxin Response Factor (ARF) MONOPTEROS (MP) and recruitment of chromatin remodelers to activate genes promoting floral fate. The contribution of gene repression to reproductive primordium initiation is poorly understood. Here we show that downregulation of the STM pluripotency gene promotes initiation of flowers and uncover the mechanism for STM silencing. The ARFs ETTIN (ETT) and ARF4 promote organogenesis at the reproductive shoot apex in parallel with MP via histone-deacetylation mediated transcriptional silencing of STM. ETT and ARF4 directly repress STM, while MP acts indirectly, through its target FILAMENTOUS FLOWER (FIL). Our data suggest that – as in animals- downregulation of the pluripotency program is important for organogenesis in plants.

Highlights

Specification of new organs from transit amplifying cells is critical for higher eukaryote development
We further demonstrate that the class B Auxin Response Factor (ARF) ETT and ARF4, which are expressed in incipient reproductive primordia, act in parallel with MP to downregulate STM as well as BP
We reveal that silencing of the pluripotency gene STM and BP by FIL and ETT/ARF4 is mediated by histone deacetylation

Summary

Introduction

Specification of new organs from transit amplifying cells is critical for higher eukaryote development. Auxin triggers flower initiation through Auxin Response Factor (ARF) MONOPTEROS (MP) and recruitment of chromatin remodelers to activate genes promoting floral fate. The ARFs ETTIN (ETT) and ARF4 promote organogenesis at the reproductive shoot apex in parallel with MP via histone-deacetylation mediated transcriptional silencing of STM. Increased auxin levels lead to ubiquitinmediated degradation of Aux/IAA proteins[8], releasing the corepressors and allowing MP to recruit the SWI/SNF family chromatin remodelers BRAHMA and SPLAYED (SYD)[9] In this fashion, MP directly upregulates genes important for flower development, such as those encoding the transcription factors FILAMENTOUS FLOWER (FIL) and LEAFY (LFY)[9,10]. We further demonstrate that the class B ARFs ETT and ARF4, which are expressed in incipient reproductive primordia, act in parallel with MP to downregulate STM as well as BP. We reveal that silencing of the pluripotency gene STM and BP by FIL and ETT/ARF4 is mediated by histone deacetylation

Methods

Results

Conclusion