Centering the Organizing Center in the Arabidopsis thaliana Shoot Apical Meristem by a Combination of Cytokinin Signaling and Self-Organization

PLoS One. 2016 Feb 12;11(2):e0147830. doi: 10.1371/journal.pone.0147830. eCollection 2016.

Abstract

Plants have the ability to continously generate new organs by maintaining populations of stem cells throught their lives. The shoot apical meristem (SAM) provides a stable environment for the maintenance of stem cells. All cells inside the SAM divide, yet boundaries and patterns are maintained. Experimental evidence indicates that patterning is independent of cell lineage, thus a dynamic self-regulatory mechanism is required. A pivotal role in the organization of the SAM is played by the WUSCHEL gene (WUS). An important question in this regard is that how WUS expression is positioned in the SAM via a cell-lineage independent signaling mechanism. In this study we demonstrate via mathematical modeling that a combination of an inhibitor of the Cytokinin (CK) receptor, Arabidopsis histidine kinase 4 (AHK4) and two morphogens originating from the top cell layer, can plausibly account for the cell lineage-independent centering of WUS expression within SAM. Furthermore, our laser ablation and microsurgical experiments support the hypothesis that patterning in SAM occurs at the level of CK reception and signaling. The model suggests that the interplay between CK signaling, WUS/CLV feedback loop and boundary signals can account for positioning of the WUS expression, and provides directions for further experimental investigation.

MeSH terms

  • Arabidopsis / cytology
  • Arabidopsis / genetics*
  • Arabidopsis / growth & development
  • Arabidopsis / metabolism
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / metabolism
  • Cytokinins / metabolism*
  • Feedback, Physiological
  • Gene Expression Regulation, Plant*
  • Homeodomain Proteins / genetics*
  • Homeodomain Proteins / metabolism
  • Meristem / cytology
  • Meristem / genetics*
  • Meristem / growth & development
  • Meristem / metabolism
  • Models, Statistical
  • Organogenesis, Plant / genetics
  • Plant Cells / metabolism
  • Protein Kinases / genetics*
  • Protein Kinases / metabolism
  • Protein Serine-Threonine Kinases
  • Receptor Protein-Tyrosine Kinases / genetics
  • Receptor Protein-Tyrosine Kinases / metabolism
  • Receptors, Cell Surface / genetics*
  • Receptors, Cell Surface / metabolism
  • Signal Transduction
  • Stem Cells / cytology
  • Stem Cells / metabolism

Substances

  • Arabidopsis Proteins
  • Cytokinins
  • Homeodomain Proteins
  • Receptors, Cell Surface
  • WUSCHEL protein, Arabidopsis
  • Protein Kinases
  • Receptor Protein-Tyrosine Kinases
  • CLV1 protein, Arabidopsis
  • Protein Serine-Threonine Kinases
  • WOL protein, Arabidopsis

Grants and funding

The authors have no support or funding to report.