Altered Cell Cycle Distribution, Hyperplasia, and Inhibited Differentiation in Arabidopsis Caused by the D-Type Cyclin CYCD3

Abstract

CYCD3;1 expression in Arabidopsis is associated with proliferating tissues such as meristems and developing leaves but not with differentiated tissues. Constitutive overexpression of CYCD3;1 increases CYCD3;1-associated kinase activity and reduces the proportion of cells in the G1-phase of the cell cycle. Moreover, CYCD3;1 overexpression leads to striking alterations in development. Leaf architecture in overexpressing plants is altered radically, with a failure to develop distinct spongy and palisade mesophyll layers. Associated with this, we observe hyperproliferation of leaf cells; in particular, the epidermis consists of large numbers of small, incompletely differentiated polygonal cells. Endoreduplication, a marker for differentiated cells that have exited from the mitotic cell cycle, is inhibited strongly in CYCD3;1 -overexpressing plants. Transcript analysis reveals an activation of putative compensatory mechanisms upon CYCD3;1 overexpression or subsequent cell cycle activation. These results demonstrate that cell cycle exit in the G1-phase is required for normal cellular differentiation processes during plant development and suggest a critical role for CYCD3 in the switch from cell proliferation to the final stages of differentiation.

The Arabidopsis Auxin-Inducible Gene ARGOS Controls Lateral Organ Size

“…For example, expression of a dominant-negative Arabidopsis CDKA in transgenic tobacco results in almost normal-sized leaves with fewer but larger cells (Hemerly et al, 1995). In Arabidopsis, overexpression of CycD3;1 , a G1 cyclin gene, does not increase organ size but leads to a disturbed organogenesis, with numerous small, incompletely differentiated cells (Riou-Khamlichi et al, 1999;Dewitte et al, 2003). Similar data were obtained from overexpression of E2Fa and DPa, two transcriptional factors that play a role in activating cell division genes.…”

“…CycD3;1 expression suggested that CycD3;1 acts downstream of ANT to determine leaf cell number (Dewitte et al, 2003). Most importantly, the prolonged expression of ANT is observed in fully expanded 35S-ARGOS leaves, and the loss of function of ANT blocked organ enlargement in 35S-ARGOS plants.…”

Cytokinin-Deficient Transgenic Arabidopsis Plants Show Multiple Developmental Alterations Indicating Opposite Functions of Cytokinins in the Regulation of Shoot and Root Meristem Activity

“…In these plants, cell cycle progression was limited and the uncoupling of cell growth from cell division resulted in an increase of the final cell size (De Veylder et al, 2001). By contrast, constitutive overexpression of the D-type cyclin CYCD3 (Dewitte et al, 2003) and the cell cycle-regulating transcription factors E2Fa and DPa (De Veylder et al, 2002) was shown to cause the hyperproliferation of smaller and incompletely differentiated leaf cells. These comparisons indicate that the altered leaf phenotype of AtCKX transgenic plants could be achieved through the regulation of cell cycle genes.…”

Grasses Like Mammals? Redundancy and Compensatory Regulation within the Retinoblastoma Protein Family

“…11 It has been shown that sucrose and hormone concentrations in tissue culture medium are perceived by CycD3;1/CDK in Arabidopsis, which are upregulated. 12 In tobacco cell culture, upregulation of CycD3;1 stimulates cell proliferation by the direct inhibition of RBR. 13 Thus, evidence from two readily transformable dicot species with a single RBR gene suggests that inactivation of RBR through phosphorylation by CycD/CDK may be sufficient to relieve the RBR cell cycle block.…”