Initiation and maintenance of plant stem cells in root and shoot apical meristems

Abstract

Plant stem cells are a small group of cells with a self-renewal capacity and serve as a steady supply of precursor cells to form new differentiated tissues and organs in plants. Root stem cells and shoot stem cells, which are located in the root apical meristem and in the shoot apical meristem, respectively, play a critical role in plant longitudinal growth. These stem cells in shoot and root apical meristems remain as pluripotent state throughout the lifespan of the plant and control the growth and development of plants. The molecular mechanisms of initiation and maintenance of plant stem cells have been extensively investigated. In this review, we mainly discuss how the plant phytohormones, such as auxin and cytokinin, coordinate with the key transcription factors to regulate plant stem cell initiation and maintenance in root and shoot apical meristems. In addition, we highlight the common regulatory mechanisms of both root and shoot apical meristems.

Keywords: Auxin; Cytokinin; Initiation; Maintenance; Stem cell; Transcription factors.

Fig. 1

Initiation and maintenance of plant stem cells in root and shoot apical meristems. A Initiation of root stem cells during embryogenesis. Gene regulation in the initiation of stem cells in embryonic root apical meristem at the late globular stage. Antagonism between auxin and cytokinin determines the establishment of root stem cell niche. Auxin antagonizes cytokinin output by direct transcriptional activation of ARR7 and ARR15, feedback repressors of cytokinin signaling (CK signaling). Auxin regulates embryonic root stem cell initiation through the action of the MP transcription factor and auxin-labile inhibitor IAA12. And auxin cooperates with some transcription factors OBE1/2, TAA1/2, TMO5/7, and NTT to regulate the initiation of root stem cells. B Initiation of shoot stem cells during embryogenesis. Gene regulation in the initiation of stem cells in embryonic shoot apical meristem at globular embryo stage. WOX2 is involved in the initiation of shoot stem cells through regulating PIN1-dependent auxin transport. WOX2 upregulates the HD-ZIP III transcription factors, which seem to mediate WOX2 function in the initiation of shoot stem cell through regulating cytokinin biosynthesis. Thus, WOX2 and its redundant WOX paralogs are required for the initiation of the shoot stem cell by establishing a regulatory framework that balances the cytokinin and auxin pathways. ZLL and TPL mediate the initiation of stem cells in the embryonic SAM which involves the negative regulation of auxin signaling. C Regulatory pathways control the maintenance of root stem cells. Gene regulation in the maintenance of stem cells in root apical meristem. The QC-specific transcriptional regulation of WOX5 is directly restricted by ROW1, and also regulated by CLE40-ACR4 regulatory module. WOX5 inhibits CYCD1;1, CYCD3;3, and CDF4 activity to control root stem cells. And auxin induces the expression of TPST and RGF genes, and TPST in turn sulfates the RGF peptides to induce the expression of PLT. Coordination among cytokinin and auxin maintains the size of root meristem and ensures root growth. The two hormones through a simple regulatory circuit converging on the SHY2 protein, which is activated by cytokinin and inhibited by auxin and a repressor of auxin signaling that negatively regulates the PIN. D Regulatory pathways control the maintenance of shoot stem cells. The central regulatory pathway for the maintenance of shoot stem cells includes an autoregulatory negative-feedback loop comprising stem cell-promoting transcription factor WUS and differentiation-promoting peptide CLV3. Cytokinin positively regulates the maintenance of shoot stem cell activity. A feedback module between WUS and cytokinin signaling pathway produces accurate positioning of stem cell niche. The spatial auxin–cytokinin cross talk for the shoot stem cell maintenance was determined by the negative regulation of the expression of IPT5 and ARR7/15 via the auxin signaling component ARFs, and in turn by the inhibition of YUCs expression via cytokinin-responsive factors