Trends in Genetics
Volume 31, Issue 6, June 2015, Pages 307-315
Journal home page for Trends in Genetics

Review
Special Issue: Organogenesis
When bigger is better: the role of polyploidy in organogenesis

https://doi.org/10.1016/j.tig.2015.03.011Get rights and content

Highlights

  • The large cells that are necessary in plant and animal organs usually are generated by increased ploidy.

  • A large cell has multiple advantages versus a comparable mass of diploid cells.

  • Cell hypertrophy via increased ploidy can produce an envelope or control organ shape.

  • Polyploidy is linked to cell differentiation and function.

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.

Section snippets

Polyploidy: going big

Organogenesis, the formation of organs during development, involves determination and differentiation of the cell types necessary for organ function and the proper arrangement of these cell types into tissues. A second crucial but poorly understood aspect of organogenesis is the regulation of size. Not only must the overall size of the organ be controlled, but each of the tissue layers within the organ needs to be scaled to be the proper size. Tissue and organ size are dictated by the sum of

Overview of somatic polyploidy

The role of polyploidy in development is distinct from species ploidy because it involves increased DNA content in specific somatic cell types during development. This is in contrast to organisms, such as many plants, in which a polyploid genome content is transmitted through the germline, resulting in every cell in the body being polyploid. Somatic polyploidy of specific tissues within an organism is sometimes termed endopolyploidy, but here I refer to it solely as polyploidy. Somatic

Tissue envelopes or barriers composed of polyploid cells

There are several examples in which one tissue layer within an organ is composed of polyploid cells, suggesting that an increase in size of these tissues by cell proliferation may be problematic. This has been defined most clearly for the subperineurial glia (SPG) of the Drosophila nervous system (Figure 2A) [20]. These flat cells are surface glia, bounded on all their sides by septate junctions, a form of tight junction. The SPG provide the blood–brain barrier in Drosophila, and this requires

Polyploid cells controlling organ structure

In contrast to polyploid cells composing a distinct tissue layer within an organ, in some organs dispersed polyploid cells influence the structure or shape of the overall organ. Two examples are Arabidopsis sepals (the outer layers of the flower) and leaves. The sepals are composed of interspersed giant, polyploid cells and small diploid cells (Figure 2D). Although the ratio of these two cell types is regulated, the spatial distribution varies between sepals. Polyploidization of the giant cells

Polyploidization linked to the differentiation or function of specific cell types

In addition to the role of polyploid cells in affecting the morphology or function of an organ, polyploidy can be necessary for the function of some cell types. Perhaps the most dramatic example is the neurons of slugs. In Aplysia, the nuclei of the giant neurons, cells 1 mm in diameter, are 200 000C [38]. Other slugs have giant neurons that are 10 000C [39]. The neurons of the CNS ganglia also reach enormous levels of ploidy in other, but not all, gastropods ([40] for a survey). These animals

Polyploidy in wound repair and organ regeneration

The above themes emphasize the role of polyploidization during normal organogenesis in development, but it also plays a role in tissue repair and organ regeneration, as noted above for cardiomyocytes. Wound repair has been examined in the abdominal epidermis of adult Drosophila [60]. Following wounding, unexpectedly, the epidermis is repaired by the formation of polyploid mononucleate cells as well as of large syncytial cells by cell fusion, rather than via a restoration of cell number (Figure 2

Developmental regulation of polyploidy

Extensive progress has been made in defining the alterations in cell cycle parameters and regulators responsible for the endocycle and endomitosis. Several excellent recent reviews detail the control of these variant cell cycles 49, 66, 67, 68. Briefly, E2F transcription factor family members are crucial for the endocycle in plants, mammals, and Drosophila. In Drosophila, S–G oscillations result from cyclic synthesis and degradation of E2F1 [69], and this is the key driver of the endocycle. In

Concluding remarks

An intriguing set of organs implementing polyploidization as a growth strategy has been identified in plants and animals, raising a set of fascinating questions about how this adaptation arose evolutionarily and how it is mechanistically regulated (Box 1). With increasing awareness of the role of polyploidy in size control more examples of polyploid cells in organs are likely to be uncovered, and these may reveal further uses for this strategy. A current limitation in the field is the

Acknowledgments

I thank Tom DiCesare for help with the figures as well as Satyaki Rajavasireddy and Ben Williams for the photo in Figure 2D. Laura Frawley, Jared Nordman, and Boryana Petrova provided helpful comments on the manuscript. This work was supported by National Institutes of Health grant GM57960 and an American Cancer Society Research Professorship.

Glossary

Endocycle
a variant cell cycle with oscillating gap (G) and DNA synthesis (S) phases that produces mononucleate polyploid or polytene cells (Figure 1B).
Polyploid
a multiple, integral increase in the haploid genome content, defined in C values, where C is the haploid genome content. When chromosomes can be visualized, ploidy can be expressed by N values, where N is the haploid number of chromosomes. Note that for simplicity in this review ploidy levels are reported solely as C values.
Polytene

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