Two-Step Regulation of a Meristematic Cell Population Acting in Shoot Branching in Arabidopsis.

Bihai Shi,Tengfei Xu,Gregory P Copenhaver,Marcus G Heisler,Jin Wang,Ying Wang,Cui Zhang,Klaus Theres,Carolyn Ohno,Robert Sablowski,Yan Xu,Caihuan Tian,Yuling Jiao,Quan Wang

doi:10.1371/journal.pgen.1006168

Abstract

Shoot branching requires the establishment of new meristems harboring stem cells; this phenomenon raises questions about the precise regulation of meristematic fate. In seed plants, these new meristems initiate in leaf axils to enable lateral shoot branching. Using live-cell imaging of leaf axil cells, we show that the initiation of axillary meristems requires a meristematic cell population continuously expressing the meristem marker SHOOT MERISTEMLESS (STM). The maintenance of STM expression depends on the leaf axil auxin minimum. Ectopic expression of STM is insufficient to activate axillary buds formation from plants that have lost leaf axil STM expressing cells. This suggests that some cells undergo irreversible commitment to a developmental fate. In more mature leaves, REVOLUTA (REV) directly up-regulates STM expression in leaf axil meristematic cells, but not in differentiated cells, to establish axillary meristems. Cell type-specific binding of REV to the STM region correlates with epigenetic modifications. Our data favor a threshold model for axillary meristem initiation, in which low levels of STM maintain meristematic competence and high levels of STM lead to meristem initiation.

Highlights

In plants, many somatic cells can regenerate into complete plants; many plant cells are considered totipotent, unlike most somatic cells in animals [1]
Branches arise from axillary meristems (AMs), which form in the crook between the leaf and the stem
Our results show that initiation of branching meristems in the shoot requires a meristematic cell population embedded in differentiated cells

Summary

Introduction

Many somatic cells can regenerate into complete plants; many plant cells are considered totipotent, unlike most somatic cells in animals [1]. During AM initiation, a morphologically detectable bump forms in the leaf axil and develops into a bud [9,10,11]. The ‘detached meristem’ model proposes that a few pluripotent cells detach from the primary shoot apical meristem (SAM) and associate with the leaf axil as the leaf differentiates from the SAM [10, 12]. Histological analysis shows that leaf axil cells likely remain undifferentiated, providing support for the detached meristem theory [12, 13]. Analysis of the Arabidopsis thaliana phabulosa-1d mutant led to the alternative ‘de novo induction’ model [14], in which an AM initiates from differentiated leaf cells. A major difference between these models is whether AM initiation requires a meristematic cell lineage [10, 15, 16]

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