E. Kondorosi, J.M. Vinardell, E. Fedorova, A. Cebolla, F. Roudier, S. Tarayre, G. Horvath,
K. Fulop, D. Vaubert, A. Kondorosi
Institut des Sciences du Vegetal, CNRS UPR 2355, 91198 Gif sur Yvette, France 1. Introduction
Plant organ development is a constant interplay between cell cycle and differentiation programs. Various stages of nodule development are controlled by differential regulation of the cell cycle. As a first step, the rhizobial Nod factors activate the cell cycle in the nodulation sensitive root zone. In Medicago sativa roots the GO-arrested cortical cells dedifferentiate and reenter the cell cycle in front of the protoxylem poles. These cells undergo the Gl/S transition, however, the cell cycle is completed by cell division only in the inner cortex. Maintenance of mitotic activity and recruitment of the neighbouring cells lead to extensive but localized cell proliferation and formation of the nodule primordium.
As a second step, the nodule primordium differentiates. In the case of Medicago, an autonomous meristem is established in the apical region whereas submeristematic cells develop to various nodule cell types. Cell differentiation necessitates an irreversible cell cycle exit that is coordinated by the expression of unique genes to specify tissue identity. Terminal differentiation can occur by complete loss of cell cycle activity as it is in the peripheral nodule tissues. In contrast, the cell cycle remains partially active in the central region. This might be necessary for the differentiation of symbiotic nitrogen-fixing nodule cells which do not divide but replicate their genome. This form of the cell cycle, allowing genome duplication without mitosis is referred to as endoreduplication or endocycles. In contrast to the mitotic cycle, the endocycle consists of the DNA synthesis (S-phase) and a gap period, and inhibition of mitosis is due to the inactivation of the cyclin-dependent kinase (CDK)-mitotic cyclin complexes.
In M. sativa and M. truncatula nodules, the diploid cells remain uninfected and genome duplication seems to be a prerequisite for Rhizobium infection. Repeated rounds of endocycles result in the formation of cells from 8°C to 32°C nuclear DNA content (Truchet et al. 1978; Cebolla et al. 1999). The increased genome size and nuclear volume is accompanied by gradual and proportional enlargement of the cell size. This nodule zone (zone II) is characterized also by the expression of many early nodulins and cell cycle genes. The signals and the mechanisms which coordinate cell cycle and tissue-specific events remain unknown. Rhizobium infection or Nod factors are amongst the most likely candidates, however, many of these early events occur also in spontaneous nodules of M. sativa in the absence of rhizobia and Nod factors. This suggests the involvement of developmental signals in the coordination of cell cycle and nodule-specific events. One may speculate that the cell proliferation is limited and the size of the nodule primordium might be sensed in the plant. As a differentiation checkpoint, it could trigger further differentiation events during nodule development.
When rhizobia, as part of the symbiosomes, are released from the infection threads into the cytoplasm, they differentiate simultaneously with the host cell. Curiously, their development shares some common features with that of the host cells. During their maturation in nodule zone II, they grow and lose progressively their ability to divide. Measurement of DNA content indicated from 4-to 8-fold more DNA content in the bacteroids (for example in pea and M. sativa nodules) than in the free-living bacteria (Bisseling et al. 1977). Although this work was not followed up and the results were not confirmed with the recent techniques, the parallelism between bacteroid and host cell development might lead to the postulation of a common developmental switch/signal for both the prokaryote and eukaryote cell types.
Endoreduplication in plants is extremely widespread and genetically programmed. Multiplication of the genome is proposed to increase metabolic activity, rRNA synthesis and transcriptional activity. Moreover, the cell size for a given cell type is generally proportional to the amount of nuclear DNA, therefore endoreduplication constitutes an effective strategy for cell growth as well (Kondorosi et al. 2000). In Medicago, the highest ploidy levels were measured in the nodules. Below we give a short overview on studies focused on the better understanding of the regulation and mechanism of endocycles and on the significance of endoreduplication cycles in nitrogen-fixing nodule development.
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