DNA endoreduplication and polyteny understood as evolutionary strategies

Nagl, W.

doi:10.1038/261614a0

Cited by 222 publications

(173 citation statements)

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“…It can be restricted to certain cell types or tissues but most of the differentiated cells in numerous higher plant species undergo several rounds of DNA synthesis leading to endopolyploidy (Nagl, 1975). Endopolyploidy has been described as being associated with increased gene expression (Galitski et al, 1999;Raslova et al, 2003) and increased cell growth (Lee et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

In planta quantification of endoreduplication using fluorescent in situ hybridization (FISH)

et al. 2011

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SUMMARYEndopolyploidy, i.e. amplification of the genome in the absence of mitosis, occurs in many plant species and happens along with organ and cell differentiation. Deciphering the functional roles of endopolyploidy is hampered by the fact that polyploid tissues generally comprise cells with various ploidy levels. In some fleshy fruits (amongst them tomato fruit) the ploidy levels present at the end of development range from 2C to 256C in the same tissue. To investigate the temporal and spatial distribution of endopolyploidy it is necessary to address the DNA content of individual nuclei in situ. Conventional methods such as fluorometry or densitometry can be used for some tissues displaying favorable characteristics, e.g. small cells, small nuclei, organization in a monolayer, but high levels of varying polyploidy are usually associated with large sizes of nuclei and cells, in a complex three dimensional (3-D) organization of the tissues. The conventional methods are inadequate for such tissue, becoming semi-quantitative and imprecise. We report here the development of a new method based on fluorescent in situ bacterial artificial chromosome hybridizations that allows the in situ determination of the DNA ploidy level of individual nuclei. This method relies on the counting of hybridization signals and not on intensity measurements and is expected to provide an alternative method for mapping endopolyploidy patterns in mature, 3-D organized plant tissues as illustrated by the analysis of ploidy level and cell size in pericarp from mature green tomato fruit.

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Section: Introductionmentioning

confidence: 99%

In planta quantification of endoreduplication using fluorescent in situ hybridization (FISH)

et al. 2011

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“…In contrast, during the endoreduplication cycle, no cytokinesis occurs between rounds of DNA replication, resulting in successive doublings of the DNA ploidy level. This process occurs in a wide variety of cell types in arthropods and mammals and is particularly prominent in dicotyledonous plants (1), especially in species with a small genome and a short life cycle, in which repetitive DNA replication might support growth under conditions that require rapid development (2,3).…”

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Atypical E2F activity restrains APC/C ^CCS52A2 function obligatory for endocycle onset

Lammens

Boudolf

Kheibarshekan

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

167

221

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The endocycle represents an alternative cell cycle that is activated in various developmental processes, including placental formation, Drosophila oogenesis, and leaf development. In endocycling cells, mitotic cell cycle exit is followed by successive doublings of the DNA content, resulting in polyploidy. The timing of endocycle onset is crucial for correct development, because polyploidization is linked with cessation of cell division and initiation of terminal differentiation. The anaphase-promoting complex/cyclosome (APC/C) activator genes CDH1, FZR, and CCS52 are known to promote endocycle onset in human, Drosophila, and Medicago species cells, respectively; however, the genetic pathways governing development-dependent APC/C CDH1/FZR/CCS52 activity remain unknown. We report that the atypical E2F transcription factor E2Fe/DEL1 controls the expression of the CDH1/FZR orthologous CCS52A2 gene from Arabidopsis thaliana. E2Fe/DEL1 misregulation resulted in untimely CCS52A2 transcription, affecting the timing of endocycle onset. Correspondingly, ectopic CCS52A2 expression drove cells into the endocycle prematurely. Dynamic simulation illustrated that E2Fe/DEL1 accounted for the onset of the endocycle by regulating the temporal expression of CCS52A2 during the cell cycle in a development-dependent manner. Analogously, the atypical mammalian E2F7 protein was associated with the promoter of the APC/C-activating CDH1 gene, indicating that the transcriptional control of APC/C activator genes by atypical E2Fs might be evolutionarily conserved.D uring the mitotic cell cycle, DNA that is duplicated during the S phase is divided at the M phase, so that each daughter cell produced has a genomic DNA content equal to that of its parents. In contrast, during the endoreduplication cycle, no cytokinesis occurs between rounds of DNA replication, resulting in successive doublings of the DNA ploidy level. This process occurs in a wide variety of cell types in arthropods and mammals and is particularly prominent in dicotyledonous plants (1), especially in species with a small genome and a short life cycle, in which repetitive DNA replication might support growth under conditions that require rapid development (2, 3).Mitotic cell cycle progression and endoreduplication are linked events. Premature or delayed exit from the cell division program results in an increased or decreased DNA ploidy, respectively (4-10). Therefore, the onset of endoreduplication must be controlled precisely. At the molecular level, endoreduplication is likely achieved through elimination of the components needed to progress through mitosis (11). Predominant roles in this process are played by the anaphase-promoting complex/cyclosome (APC/C) activator genes, such as CDH1, FZR, and CCS52A, which have been found to promote endocycle onset and progression in human, Drososphila melanogaster, and Medicago truncatula cells, respectively (12-17). The mechanisms controlling the transcriptional activity of these genes remain unclear, however.Over the years, it has beco...

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“…While cell division is dependent on mitotic cell cycle, cell expansion and cell differentiation are often coupled with a modified cell cycle called endoreduplication. 1 Endoreduplication enables a cell to increase its ploidy by replicating its genome without subsequent chromosomal and cellular division. This endocycle, widespread in eukaryotes but especially common in plants, may provide individual cells with the gene-expression capacity to reach larger sizes.…”

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FZR2/CCS52A1mediated endoreduplication in Arabidopsis development

Larson‐Rabin

Masson

et al. 2009

Plant Signaling & Behavior

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Plant organogenesis generally involves three basic processes: cell division, cell expansion and cell differentiation. Endoreduplication, a process of genome replication without intervening mitosis, often occurs during cell expansion and cell differentiation. The switch from the mitotic cell cycle to the endocycle, however, is still poorly understood in plants. We have recently demonstrated that FIZZY-RELATED2 (FZR2) is a factor controlling endoreduplication in Arabidopsis. fzr2 mutants lacked gross morphological defects but showed a general decrease of endoploidy level in trichomes and other leaf cells, while expression of FZR2 under constitutive or tissue specific promoters induced extra or ectopic endoreduplication in all tissues examined. We also showed that decrease of leaf cell size in fzr2 mutants could be compensated by increased cell proliferation. In this addendum, we discuss additional phenotypes of FZR2 misexpression, including apparent mosaic leaf sectors in which local cell overexpansion due to 35S::FZR2 appears to be compensated by reduced cell expansion in neighboring tissues.Plants begin vegetative development as single zygotes and reach final sizes million-fold bigger, with complex tissues and cell types. During development, plants undergo three basic processes: cell division, cell expansion and cell differentiation. While cell division is dependent on mitotic cell cycle, cell expansion and cell differentiation are often coupled with a modified cell cycle called endoreduplication. 1 Endoreduplication enables a cell to increase its ploidy by replicating its genome without subsequent chromosomal and cellular division. This endocycle, widespread in eukaryotes but especially common in plants, may provide individual cells with the gene-expression capacity to reach larger sizes. 2 In the well-studied dicotyledon model Arabidopsis thaliana, endoreduplication occurs in most of the differentiated cell types, such as trichoblasts and trichomes, or cells with very high metabolic activity, such as the endosperm. 3 The switch from mitotic cycles to endocycles requires cells to start another round of DNA replication without intervening mitosis. Therefore, a cell must induce re-entry into S-phase after G 1 -phase while inhibiting M-phase. The regulatory mechanisms mediating the G 1 to S transition in endocycles share components of the mitotic pathways, 4 with the CDK/CYCLIN B complex influencing DNA replication. 5 Much evidence in yeast, fly and plants has pointed to the involvement of a WD-40 protein, Fizzy-Related/Ccs52, in triggering the switch to endoreduplication by controlling the degradation of Cyclin B. 6,7 Using reverse genetics in Arabidopsis, we investigated FIZZY-RELATED2 loss-of-function mutants. 8 fzr2 plants showed reduced endoreduplication and cell size in both pavement cells and trichomes. 8 When FZR2 was misexpressed with the CMV 35S promoter, transgenic plants showed a range of phenotypes such as retarded growth, supernumerary trichome branches and distorted roots, with ectopic endoreduplica...

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DNA endoreduplication and polyteny understood as evolutionary strategies

Cited by 222 publications

References 13 publications

In planta quantification of endoreduplication using fluorescent in situ hybridization (FISH)

In planta quantification of endoreduplication using fluorescent in situ hybridization (FISH)

Atypical E2F activity restrains APC/C ^CCS52A2 function obligatory for endocycle onset

FZR2/CCS52A1mediated endoreduplication in Arabidopsis development

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DNA endoreduplication and polyteny understood as evolutionary strategies

Cited by 222 publications

References 13 publications

In planta quantification of endoreduplication using fluorescent in situ hybridization (FISH)

In planta quantification of endoreduplication using fluorescent in situ hybridization (FISH)

Atypical E2F activity restrains APC/C CCS52A2 function obligatory for endocycle onset

FZR2/CCS52A1mediated endoreduplication in Arabidopsis development

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Atypical E2F activity restrains APC/C ^CCS52A2 function obligatory for endocycle onset