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Title: The ERECTA receptor kinase regulates Arabidopsis shoot apical meristem size, phyllotaxy and floral meristem identity

Author
item MANDEL, TALI - Hebrew University
item MOREAU, FANNY - Center For Research On Plant Macromolecules
item KUTSHER, YAARIT - Hebrew University
item Fletcher, Jennifer
item CARLES, CRISTEL - Center For Research On Plant Macromolecules
item ESHED WILLIAMS, LEOR - Hebrew University

Submitted to: Development
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/8/2013
Publication Date: 2/15/2014
Citation: Mandel, T., Moreau, F., Kutsher, Y., Fletcher, J.C., Carles, C.C., Eshed Williams, L. 2014. The ERECTA receptor kinase regulates Arabidopsis shoot apical meristem size, phyllotaxy and floral meristem identity. Development. 141:830-841.

Interpretive Summary: In plants, the shoot apical meristem contains a reservoir of stem cells that develop into leaves, stems, and flowers containing sepal, petal, stamen and carpel organs. Our previous studies have identified a signaling module consisting of the CLAVATA3 (CLV3) peptide and the WUSCHEL (WUS) gene expression regulator that plays a key role in controlling shoot stem cell activity, but additional factors that contribute to shoot stem cell maintenance during plant development remain to be characterized. Here we have shown that a cell signaling factor called ERECTA (ER) is a negative regulator of WUS gene expression that functions separately from the CLV3 peptide. We demonstrated that ER and a small RNA-mediated pathway act together to restrict the size of the shoot stem cell reservoir and confer a spiral leaf arrangement. We also showed that ER-mediated regulation of stem cell-promoting gene expression prevents a premature developmental switch in reproductive shoot apical meristem cells from a flower fate to a carpel fate. Our research shows that several distinct pathways function to correctly maintain shoot stem cell activity, providing multiple targets for manipulation to improve key agronomic traits such as fruit or grain yield.

Technical Abstract: In plants, the shoot apical meristem (SAM) serves as a reservoir of pluripotent stem cells from which all above ground organs originate. To sustain proper growth, the SAM must maintain homeostasis between the self-renewal of pluripotent stem cells and cell recruitment for lateral organ formation. At the core of the network that regulates this homeostasis in Arabidopsis are the WUSCHEL (WUS) transcription factor specifying stem cell fate and the CLAVATA (CLV) ligand-receptor system limiting WUS expression. In this study, we identified the ERECTA (ER) pathway as a second receptor kinase signaling pathway that regulates WUS expression, and therefore shoot apical and floral meristem size, independently of the CLV pathway. We demonstrate that reduction in class III HD-ZIP and ER function together leads to a significant increase in WUS expression, resulting in extremely enlarged shoot meristems and a switch from spiral to whorled vegetative phyllotaxy. We further show that strong upregulation of WUS in the inflorescence meristem leads to ectopic expression of the AGAMOUS homeotic gene to a level that switches cell fate from floral meristem founder cell to carpel founder cell, suggesting an indirect role for ER in regulating floral meristem identity. This work illustrates the delicate balance between stem cell specification and differentiation in the meristem and shows that a shift in this balance leads to abnormal phyllotaxy and to altered reproductive cell fate.