When bigger is better: the role of polyploidy in organogenesis

Abstract

Defining how organ size is regulated, a process controlled not only by the number of cells but also by the size of the cells, is a frontier in developmental biology. Large cells are produced by increasing DNA content or ploidy, a developmental strategy employed throughout the plant and animal kingdoms. The widespread use of polyploidy during cell differentiation makes it important to define how this hypertrophy contributes to organogenesis. I discuss here examples from a variety of animals and plants in which polyploidy controls organ size, the size and function of specific tissues within an organ, or the differentiated properties of cells. In addition, I highlight how polyploidy functions in wound healing and tissue regeneration.

Keywords: cell cycle; development; endocycle; endomitosis; endoreduplication.

Figure 1

Cell Cycle Variants Yielding Polyploid Cells. (A) The archetypal cell cycle responsible for cell proliferation contains a G1 phase during which sufficient cell growth must occur prior to the onset of DNA replication in S phase. Another gap phase (G2) precedes mitosis and the return to G1 in the two daughter cells. (B) The endocycle involves oscillations between a gap phase and S phase and can produce either polyploid or polytene cells, distinguished by whether the replicated chromatids remain in physical association. (C) Endomitosis is distinguished by entry into mitosis but a failure to complete all aspects of mitosis. This can involve a failure of nuclear envelope breakdown but assembly of a spindle within the nucleus and segregation of sister chromatids, nuclear envelope breakdown and anaphase segregation, or completion of all of the events of mitosis, including nuclear division, but without cytokinesis.

Figure 2

Examples of Polyploid Tissues within Organs. (A) The subperineurial glia (SPG, pink) are surface glia in the Drosophila nervous system, surrounding the neuronal cell bodies (blue) and axons (yellow). Increased size of the SPG resulting from polyploidy is required to maintain the blood-brain barrier as neuronal mass increases during development. (B) The trophoblast giant cells (TGC, light blue) make a barrier between the maternal and fetal compartments of the placenta. (C) In mouse and human skin, there is a basal layer with quiescent (grey) or proliferating cells (red). Cell division (green cell) moves daughter cells towards the outer layer of the skin (top of drawing). In the suprabasal layers the keratinocytes undergo endomitosis (blue) and the endocycle (pink) to increase their ploidy and size. (D) In the sepal, the outer layer, of Arabidopsis flowers (left) there are both giant, polyploid cells (pink cells, right) and diploid cells (grey, right). The numbers but not positions of the two cell types are regulated. (E) The Drosophila rectum contains four papillae composed of polyploid cells that endocycle for two divisions then divide to produce the required number of polyploid cells in each papillae. The bottom figure represents an enlargement of the rectal papillae, with the 8C cells that underwent endocycles followed by mitotic divisions shown in green and Delta expressing cells shown in purple. (F) Megakaryocytes have a nucleus (green) with up to 128C DNA content with multiple invaginations in the nuclear envelope. The large cell size resulting from polyploidy is required for the megakaryocytes to bud off sufficient numbers of platelets (small pink circles). (G) The Drosophila ovarian follicle cells (green) endocycle to 16C (bottom left). Genomic replication is then shut off, but six genomic regions undergo repeated origin firing and gene amplification (bottom right). (H) In wound healing in the Drosophila epidermis polyploid cells that are either in a multinucleate syncytium or mononucleate cells are produced at the wound site.