How peroxisomes partition between cells. A story of yeast, mammals and filamentous fungi

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Eukaryotic cells are subcompartmentalized into discrete, membrane-enclosed organelles. These organelles must be preserved in cells over many generations to maintain the selective advantages afforded by compartmentalization. Cells use complex molecular mechanisms of organelle inheritance to achieve high accuracy in the sharing of organelles between daughter cells. Here we focus on how a multi-copy organelle, the peroxisome, is partitioned in yeast, mammalian cells, and filamentous fungi, which differ in their mode of cell division. Cells achieve equidistribution of their peroxisomes through organelle transport and retention processes that act coordinately, although the strategies employed vary considerably by organism. Nevertheless, we propose that mechanisms common across species apply to the partitioning of all membrane-enclosed organelles.

Introduction

The cell is the self-propagating unit of all living organisms. Eukaryotic cells are equipped with a set of membrane-enclosed compartments called organelles that are each specialized for distinct biochemical functions. To maintain the benefits of compartmentalization, cells must transmit their organelles to future generations through a process termed organelle inheritance. While certain aspects of cell division, such as DNA replication and segregation, have long been recognized to occur with a high level of precision, organelle inheritance has traditionally been thought of as being random, with each daughter cell just needing to receive some ‘seed’ material to expand the organelle compartment [1]. However, numerous factors involved in the inheritance of different organelles have been identified in recent years [2], making it increasingly apparent that cells stringently regulate the inheritance of their organelles. Here we discuss strategies for organelle inheritance used by cells that divide asymmetrically, by median fission, and by hyphal growth (Figure 1). We focus on a multi-copy organelle, the peroxisome, but discuss other organelles to illustrate regulatory mechanisms specific for their inheritance.

Section snippets

Why study peroxisome inheritance?

Peroxisomes are ubiquitous, single-membrane-delimited organelles involved in a variety of cellular processes, including notably the β-oxidation of fatty acids and the metabolism of reactive oxygen species. The existence of congenital peroxisome biogenesis disorders [3] has prompted intensive research into the molecular biology of the organelle. As yeast peroxisome assembly mutants are conditionally viable, the core biogenic machinery of peroxisomes has been identified in yeast and shown to be

Peroxisome partitioning in budding yeast

Cells of baker's yeast, Saccharomyces cerevisiae, undergo a repetitive pattern of growth and division termed budding in which they produce a bud that is initially very small. Yeast actively partition organelles between mother cell and bud to achieve an equidistribution of organelles at cytokinesis. Vectorial delivery of some organelles to the bud is balanced by retention of the remaining organelles in the mother cell. Attributes like these make budding yeast an attractive model with which to

Peroxisome partitioning in mammalian cells

Animal cells share cargo transport between the microtubule and actin cytoskeletons [37, 38]. Microtubules that extend from the centrosome in the perinuclear region to the plasma membrane allow for bi-directional, long-distance transport of cargo using kinesin and dynein motors. Actin comprises a network of short, randomly oriented filaments at the cell periphery, which suggests that myosins move cargo over short distances. A widely studied example of organelle dynamics in animal cells is the

Peroxisome partitioning in filamentous fungi

Filamentous fungi grow via elongation of hyphae at their tips to form straight primary hyphae that branch to form secondary hyphae. Cytoplasmic streaming toward the apical tip is likely caused by internal osmotic gradients established by differential ion transport along the hyphae [63]. Hyphae are subdivided into individual cells by incomplete septa that permit the passage of cytoplasm and organelles. Filamentous fungi are thus multicellular organisms with mechanisms of cell-to-cell

Conclusion

At first glance it might appear that different organisms use different strategies for peroxisome inheritance. However, principles of peroxisome partitioning common to all organisms are beginning to emerge. Therefore, although each type of organelle uses a set of inheritance factors that is unique to it, a set of ‘golden rules’ nevertheless appears to govern the partitioning of all organelle populations. First, peroxisomes travel along cytoskeletal tracks by attaching themselves to molecular

Competing interest

The authors declare that they have no competing financial or personal interests.

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

Acknowledgements

This work was supported by a Foundation Grant from the Canadian Institutes of Health Research to RAR. We apologize for not citing valuable contributions due to space constraints.

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