Illuminating the molecular mechanisms underlying shoot apical meristem homeostasis in plants

Abstract

Unlike animals, terrestrial plants are sessile and able to give rise to new organs throughout their lifetime. In the most extreme cases, they can survive for over a thousand years. With such protracted life cycles, plants have evolved sophisticated strategies to adapt to variable environments by coordinating their morphology as well as their growth, and have consequently acquired a high degree of developmental plasticity, which is supported by small groups of long-lived stem cells found in proliferative centers called meristems. Shoot apical meristems (SAMs) contain multipotent stem cells and provide a microenvironment that ensures both a self-renewable reservoir, to produce primordia and sustain growth, and a differentiating population that develops into all of the above-ground organs of land plants. The homeodomain transcription factor WUSCHEL (WUS) is expressed in the organizing center and acts as a master regulator to govern shoot stem cell homeostasis. In this review, I highlight recent advances in our understanding of the molecular mechanisms and signaling networks that underlie SAM maintenance, and discuss how plants utilize WUS to integrate intrinsic and extrinsic cues.

Keywords: CLAVATA3; WUSCHEL; environmental stress; homeostasis; shoot apical meristem.

Figure 1. Regulation of Arabidopsis shoot apical meristem homeostasis. A. Whole plant (left) and schematic representation of the shoot apical meristem (right). The SAM is composed of layers L1 (blue), L2 (green), and L3 (red). OC: organizing center. CZ: central zone. PZ: peripheral zone. LP: leaf primordium. RZ: rib zone. Dark blue and red ovals with haloes represent the gradients of CLV3 and WUS expression, respectively. The trapezoid defined by green dots covers the area of stem cells in the SAM. B, C. Transcriptional regulatory networks (B) and hormonal control system (C) through WUS and CLV3 as described in the text. D. Overview of the WUS–CLV negative feedback loop for maintenance of stem cell homeostasis. In B–D, WUS and CLV3 are highlighted by red and dark blue, respectively. Arrows depict positive regulatory relationships and bars and crosses mark negative regulatory relationships. The broken line indicates that direct molecular evidence is not yet available.