As it is widely occurring in angiosperms, the endoreduplication process is likely to have been selected during evolution to the benefit of plant and organ development. According to the different types of situation encountered in various plant species, in relation to plant-, organ- or cell physiology, several functional roles – not exclusive to each other – were reported to explain tentatively the relevance of endoreduplication.
Endoreduplication might contribute to the adaptation to adverse environmental factors, allowing the maintenance of growth under stress conditions. The extended amplification of nuclear DNA may provide a means to protect the genome from DNA-damaging conditions such as UV damage or prevent uneven chromosome segregation during mitosis. For instance, exposure to UV-B induces endoreduplication in epidermal cells surrounding trichomes in cucumber cotyledons (Yamasaki et al., 2010
), and the UV-B-insensitive 4
) in arabidopsis stimulates endoreduplication during hypocotyl growth and leaf development (Hase et al., 2006
). In addition, it was found that endoreduplication may confer an increased tolerance to UV-B exposure, since tetraploid arabidopsis was hyper-resistant to UV-B compared with diploid arabidopsis (Hase et al., 2006
). Endoreduplication is also involved in the adaptation to high salt concentration (Ceccarelli et al., 2006
), to water deficit (Cookson et al., 2006
) and low temperatures (Barow, 2006
), thus suggesting that an increase in DNA content can be of advantage to cope with an adverse environment.
Endoreduplication often occurs during the differentiation of cells that are highly specialized in their morphology and its blockage by mutation results in developmental abnormalities (Kondorosi et al., 2000
; Edgar and Orr-Weaver, 2001
). In arabidopsis, the influence of endoreduplication on cell growth was best characterized in epidermal cells of mature leaves (Melaragno et al., 1993
), during hypocotyl development in which the ploidy levels vary according to light conditions (Gendreau et al., 1997
), and in leaf single-celled trichomes according to a genetically regulated process (Hulskamp et al., 1999
; Larkin et al., 2007
). The growth of trichomes was shown indeed to be dependent on the succession of endocycles. The formation of a two-branched trichome cell requires three rounds of endocycle, leading to a 16C DNA ploidy level, and a supplementary endocycle may eventually occur to give rise to the formation of a third branch and 32C DNA content.
A new and original role for endoreduplication has been recently reported in arabidopsis trichomes. Bramsiepe et al. (2010)
demonstrated very elegantly that endoreduplication is an important determinant for cell fate, as they managed to change trichome fate into an epidermal pavement cell fate even in already advanced stages of trichome differentiation by compromising endoreduplication. Conversely they could restore the trichome fate in a patterning mutant by promoting endoreduplication.
As illustrated for trichomes, endoreduplication often occurs during the differentiation of cells that are highly specialized in their morphology. The influence of endoreduplication on the differentiation of metabolically specialized cells was also reported. For instance the highly polyploid endosperm cells of maize kernels accumulate large amounts of starch and storage proteins (Kowles et al., 1990
; Sabelli and Larkins, 2009
). During the formation of nitrogen-fixing root nodules in legumes as a response to interaction with the symbiotic bacterium Sinorhizobium meliloti
, the symbiotic nodule cells hosting the rhizobia and programmed to fix nitrogen develop into very large and highly endoreduplicated cells during their differentiation process (Cebolla et al., 1999
; Vinardell et al., 2003
; González-Sama et al., 2006
). Interestingly this endoreduplication-associated differentiation is tightly linked to an important transcriptional activity that is remarkably specific to the nodule (Mergaert et al., 2003
). As far as tomato fruit is concerned, only descriptive analyses for transcriptional and metabolic profiling in cells from various tomato fruit tissues were provided (Lemaire-Chamley et al., 2005
; Schauer et al., 2006
; Mounet et al., 2009
; Steinhauser et al., 2010
), without any direct link with the extent of endoreduplication.
Since a correlation can be found between endoreduplication and cell differentiation-specific metabolism, it is commonly stated that endoreduplication may contribute to modulate transcriptional activity by increasing the availability of DNA templates for gene expression as the gene copy number is obviously multiplied, and therefore may contribute to modulate subsequent translational and metabolic activities. Although this is true for animal cells (Hu and Cross, 2010
) or yeasts (Galitski et al., 1999
), the physiological role of endoreduplication in stimulating transcriptional activity has never been convincingly demonstrated or disproven in plant cells. For example, altering the DNA ploidy levels has no clear impact on the expression level of some endosperm-specific genes in maize (Leiva-Neto et al., 2004
), thus making endoreduplication in maize endosperm a more likely mechanism to provide a store of nitrogen and nucleotides during embryogenesis and/or germination.
The most unanimously accepted functional role of endoreduplication relates to cell- and organ-size determination, since endoreduplication and cell size in many different plant species, organs and cell types are naturally and intimately positively correlated (Joubès and Chevalier, 2000
; Sugimoto-Shirasu and Roberts, 2003
; Kondorosi and Kondorosi, 2004
). As a result of successive rounds of DNA synthesis during endoreduplication, nuclei become hypertrophied which in turn influences the final size of a cell which therefore adjusts its cytoplasmic volume with respect to the nuclear DNA content (according to the ‘karyoplasmic ratio’ theory; Sugimoto-Shirasu and Roberts, 2003
). Therefore endoreduplication is a likely driver for cell expansion. Such a positive correlation between cell size and ploidy level in developing tomato fruit tissue was indeed demonstrated (Cheniclet et al., 2005
). However, the ability to form large cells is not fully restricted to endoreduplicating cells. For instance, amongst the various species of fleshy fruits, cell sizes of approx. 200 µm, 220 µm and 350 µm in diameter can be observed in kiwi, persimmon and grape, respectively, while endoreduplication never occurs in these three species. These cell sizes are quite comparable to the sizes measured for the largest cells present in fruits which undergo high numbers of endocycle rounds (diameters of >200 µm in cucumber, 450 µm in melon, 600–1000 µm in tomato; Bourdon et al., 2010
). Conversely smaller cell diameters can be associated to endoreduplicating cells of strawberry (50 µm), cherry (65 µm) or peach (120 µm). Nevertheless it appears as a rule of thumb that the largest cells are always present in fruits which undergo the highest number of endocycles, which suggests that polyploidy via endoreduplication might be necessary for plant cells to reach very large sizes.
Cheniclet et al. (2005)
reported that the level of endoreduplication is tightly correlated with final fruit size in tomato, and therefore endoreduplication could participate in modulating the rate of organ growth and/or cell expansion.
In a recent analysis (Bourdon et al. 2010
), it was reported that endoreduplication always occurs in fleshy fruits which develop rapidly (in <13 weeks) comprising three to eight rounds of endocycle, in particular in the Solanaceae and Cucurbitaceae species analysed so far. With the exception of some Rosaceae species (apricot, peach and plum), endoreduplication does not occur in most of the species where fruit development lasts for a very long period of time (over 14 weeks; Fig. ). It was thus concluded that endoreduplication does indeed influence the fruit growth rate, most probably at the level of the cell expansion rate.
Occurrence of endoreduplication in fleshy fruits. The maximal number of endocycles determined in fully ripened fleshy fruits was plotted against the duration of fruit growth until ripening.