The mitotic inhibitor ccs52 is required for endoreduplication and ploidy-dependent cell enlargement in plants

Abstract

Plant organs develop mostly post-embryonically from persistent or newly formed meristems. After cell division arrest, differentiation frequently involves endoreduplication and cell enlargement. Factors controlling transition from mitotic cycles to differentiation programmes have not been identified yet in plants. Here we describe ccs52, a plant homologue of APC activators involved in mitotic cyclin degradation. The ccs52 cDNA clones were isolated from Medicago sativa root nodules, which exhibit the highest degree of endopolyploidy in this plant. ccs52 represents a small multigenic family and appears to be conserved in plants. Overexpression of ccs52 in yeast triggered mitotic cyclin degradation, cell division arrest, endoreduplication and cell enlargement. In Medicago, enhanced expression of ccs52 was found in differentiating cells undergoing endoreduplication. In transgenic M.truncatula plants, overexpression of the ccs52 gene in the antisense orientation resulted in partial suppression of ccs52 expression and decreased the number of endocycles and the volume of the largest cells. Thus, the ccs52 product may switch proliferating cells to differentiation programmes which, in the case of endocycles, result in cell size increments.

How rhizobial symbionts invade plants: the Sinorhizobium–Medicago model

“…However, what makes comparative study of both these systems most interesting is that they form different types of nodules, in which the nodule structure and the differentiation programme imposed on the symbiotic bacteria are different. become polyploid owing to cycles of genomic endoreduplication without cytokinesis 14,66 . Plant cell endoreduplication is required for the formation of functional nodules, and is dependent on the degradation of mitotic cyclins by anaphase-promoting complex (APC), an E3 ubiquitin ligase 66,67 .…”

“…In developing indeterminate nodules, which we focus on here, infection threads grow through the developing meristematic zone to the underlying cell layers through which the wave of mitotic activity has already passed 65 . These layers of invasion-competent cells have exited mitosis and become polyploid owing to cycles of genomic endoreduplication without cytokinesis 14,66 . Plant cell endoreduplication is required for the formation of functional nodules, and is dependent on the degradation of mitotic cyclins by anaphase-promoting complex (APC), an E3 ubiquitin ligase 66,67 .…”

“…become polyploid owing to cycles of genomic endoreduplication without cytokinesis 14,66 . Plant cell endoreduplication is required for the formation of functional nodules, and is dependent on the degradation of mitotic cyclins by anaphase-promoting complex (APC), an E3 ubiquitin ligase 66,67 . The advantages of cellular polyploidy are a higher transcription rate and a higher metabolic rate than cells with the normal 2n DNA content 68 -characteristics that might be important for the invaded plant cells to support bacterial nitrogen fixation (discussed later).…”

An EAR-Dependent Regulatory Module Promotes Male Germ Cell Division and Sperm Fertility in Arabidopsis

“…First, the failure of daz1 daz2 germ cells to enter mitosis is not due to incomplete replication, since mutant cells reenter S-phase after skipping mitosis ( Figure 3K). Moreover, daz1 daz2 germ cells show reduced mitotic B1-type cyclin expression, and endoreduplication is known to be associated with reduced G2/M-cyclin-dependent kinase activity (Cebolla et al, 1999;Kiang et al, 2009). Second, DAZ1/DAZ2-deficient germ cells fail to enter mitosis even though DUO1 is still expressed, and, importantly, the expression of DAZ1 in duo1 mutant germ cells is able to restore mitotic division independently of gamete (C) DAZ1 repression activity in Arabidopsis protoplasts.…”

Regulating DNA Replication in Plants

“…In Arabidopsis, homologs of both Cdc20/Fzy and Cdh1/Fzr APC/C activators exist and participate in controlling the onset of endocycles by targeting various cyclins (Gutierrez 2009). The Arabidopsis homolog of Cdh1/Fzr is known as CCS52A (CELL CYCLE SWITCH 52A), and its loss of function produces a reduction in ploidy (Cebolla et al 1999;Larson-Rabin et al 2009). Interestingly, CCS52A is a target of E2FE/DEL1, one of the three atypical E2F encoded in the Arabidopsis genome (Ramirez-Parra et al 2007;Lammens et al 2008) and homolog of the human E2F7-9.…”