Cyclin-dependent kinase activity retains the shoot apical meristem cells in an undifferentiated state

Abstract

SUMMARYAs the shoot apex produces most of the cells that comprise the aerial part of the plant, perfect orchestration between cell division rates and fate specification is essential for normal organ formation and plant development. However, the inter-dependence of cell-cycle machinery and meristem-organizing genes is still poorly understood. To investigate this mechanism, we specifically inhibited the cell-cycle machinery in the shoot apex by expression of a dominant negative allele of the A-type cyclin-dependent kinase (CDK) CDKA;1 in meristematic cells. A decrease in the cell division rate within the SHOOT MERISTEMLESS domain of the shoot apex dramatically affected plant growth and development. Within the meristem, a subset of cells was driven into the differentiation pathway, as indicated by premature cell expansion and onset of endo-reduplication. Although the meristem structure and expression patterns of the meristem identity genes were maintained in most plants, the reduced CDK activity caused splitting of the meristem in some plants. This phenotype correlated with the level of expression of the dominant negative CDKA;1 allele. Therefore, we propose a threshold model in which the effect of the cell-cycle machinery on meristem organization is determined by the level of CDK activity.

eIF4A RNA Helicase Associates with Cyclin-Dependent Protein Kinase A in Proliferating Cells and Is Modulated by Phosphorylation

“…Down-regulation of CDKA activity in tobacco (Hemerly et al, 1995) and Arabidopsis (Gaamouche et al, 2010) leads to uncoupling of the two processes, whereby loss of CDKA strongly inhibits cell proliferation, but cell growth is not particularly perturbed and the resultant cells are actually larger. Taken together, these observations indicate that CDKA is not required for cell growth per se and, therefore, may not be required for protein translation.…”

“…While it is clear that key cell cycle regulators (such as the cyclin-dependent protein kinase A [CDKA]) are not necessary for cell growth per se (Dissmeyer et al, 2009;Gaamouche et al, 2010), the mechanisms coordinating growth and division remain largely obscure. Based on previous work where we found a physical association between eukaryotic initiation factor 4A (eIF4A) and CDKA (Hutchins et al, 2004), a protein required for cell size homeostasis and normal growth (Bush et al, 2015), we hypothesize that the coordination of growth and cell division may involve reversible phosphorylation of key components of the cellular machinery.…”

PhyscomitrellaCyclin-Dependent Kinase A Links Cell Cycle Reactivation to Other Cellular Changes during Reprogramming of Leaf Cells

“…The central cell cycle regulator is CDKA, whose activity is precisely regulated both spatially and temporally (Gutierrez, 2005). Previously, not only has CDKA been shown to regulate cell cycle progression, but it has also been implicated in the specification of cell fate in Arabidopsis (Hemerly et al, 2000;Gaamouche et al, 2010). However, the phenotypes that have implicated CDKA in specifying cell fate include considerably aberrant division; therefore, it is not clear whether the observed changes in cell state are under direct control by CDKA or instead reflect secondary consequences contingent on the misregulated cell cycle.…”

“…For example, in Arabidopsis thaliana, reduction of RBR expression levels in the shoot meristem caused diminished expression of CLAVATA3 and WUSCHEL regulating stem cell identity (Borghi et al, 2010). Similarly, the induction of a kinase-negative form of CDKA in the shoot meristem caused a portion of the meristem cells to expand and exhibit endoreduplication and thus resemble differentiated cells (Gaamouche et al, 2010). These results could be taken to mean that RBR and CDKA regulate both cell division and other cellular characteristics, but on the other hand, cellular characteristics could have been affected as a consequence of the altered cell division, for example, because of abnormal intercellular communication.…”

Systems Analysis of Shoot Apical Meristem Growth and Development: Integrating Hormonal and Mechanical Signaling

“…CYCD3 activity is required to sustain normal response of both division and differentiation to cytokinin (Riou-Khamlichi et al, 1999;Dewitte et al, 2007). CYCD3 activates cyclin-dependent kinase activity of CDKA (Healy et al, 2001), whose inhibition causes differentiation of SAM cells (Gaamouche et al, 2010). Unlike CDKA, CYCD3 is an unstable protein subject to rapid turnover (Planchais et al, 2004), providing a rapid response sensor to the presence of both cytokinin and Suc (Riou-Khamlichi et al, 2000).…”