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  • Review Article
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Dancing genomes: fungal nuclear positioning

Nature Reviews Microbiology volume 7, pages 875–886 (2009)Cite this article

Key Points

  • In fungi, nuclei move in a microtubule- and microtubule motor-dependent manner and can traverse long or short distances depending on the shape and size of the cell.

  • Nuclei undergo closed, open or partially open mitosis and use motor proteins such as dynein to pull and push on cytoplasmic microtubules that slide along the cell cortex to segregate nuclei.

  • Most filamentous fungi have multinucleate hyphae and their cell division is not spatially or temporally coordinated with nuclear division. Dynein plays an important role in maintaining the appropriate spacing between the distinct nuclei.

  • Karyogamy requires interactions between overlapping spindle microtubules emanating from the two merging nuclei.

  • One consequence of the multinucleate state in fungi may be higher levels of, and tolerance of, aneuploidy. Aneuploidy can occur in yeast through a failure of cytokinesis, as well as by non-disjunction, endoreplication or mating between non-haploid strains. Aneuplody can confer fitness advantages or disadvantages.

  • Basidiomycetes such as mushrooms are dikaryotic for much of their life cycle. Mating between compatible partners triggers rapid migration and mixing of the nuclei. To form the dikaryon, nuclei from the two parents pair and then segregate into the same cell, so that nuclei are positioned based on their genotype. How nuclear genotype is recognized at the molecular level is not well understood.

  • Nuclear movements have functions outside of chromosome segregation. For example, chromatin organization changes with the direction of nuclear migration in Neurospora crassa, mechanical removal of the nuclear envelope is mediated by dynein in the open mitoses of Ustilago maydis, autophagy is induced by nuclear movements during plant infection by Magnaporthe grisea and DNA repair or meiotic recombination are coupled with nuclear oscillations in S. cerevisiae and S. pombe, respectively.

  • Finally, nuclei may divide and migrate in a manner that preserves the original template strand in the growing hyphal tip, and this preservation mechanism may be conserved in mammalian cells.

Abstract

The many different mechanisms that fungi use to transmit and share genetic material are mediated by a broad range of chromosome and nuclear dynamics. The mechanics underlying nuclear migration are well integrated into detailed models, in which the forces supplied by plus- and minus-end-directed microtubule motors position and move the nucleus in a cell. Although we know much about how cells move nuclei, we know much less about why the cell invests in so many different nuclear 'dances'. Here, we briefly survey the available models for the mechanics of nuclear migration in fungi and then focus on examples of how fungal cells use these nuclear dances — the movement of intact nuclei in and between cells — to control the integrity, ploidy and assortment of specific genomes or individual chromosomes.

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Figure 1: Microtubules and nuclear movement.
Figure 2: Mitotic dynamics in Candida albicans.
Figure 3: Overview of dikaryon formation.

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Acknowledgements

We thank K. Finley for discussions and critical reading of the manuscript and S. Forsberg for information regarding Schizosaccharomyces pombe. J.B. is supported by the US National Institutes of Health (R01AI0624273, R01AI075096 and R01 DE14666). A.S.G. is supported by the National Science Foundation (MCB-0719126) and is the recipient of a Basil O'Connor award from the March of Dimes.

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Authors and Affiliations

  1. Department of Biological Sciences, Gillman Hall, Dartmouth College, Hanover, 03755, New Hampshire, USA

    Amy Gladfelter

  2. Department of Genetics, Cellular and Developmental Biology and Department of Microbiology, University of Minnesota, 6-160 Jackson Hall, 321 Church St. SE, Minneapolis, 55455, Minnesota, USA

    Judith Berman

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  1. Amy Gladfelter
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Correspondence to Judith Berman.

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Glossary

Dikaryon

A hyphal cell in which two compatible nuclei are maintained without karyogamy (nuclear fusion). Ascomycete dikaryons can produce crozier cells, whereas basidiomycete dikaryons can produce clamp connections for the formation of the dikaryotic state.

Aneuploid

A cell with an abnormal number of chromosomes; for example, in a diploid organism, the lack of one copy of a chromosome (monosomy) or the presence of an extra copy of a chromosome (triploidy).

Microtubule-organizing centre

(MTOC). A structure that nucleates and often retains a connection to microtubules. MTOCs at the centrosome (or centriole or spindle pole body) organize the mitotic (and meiotic) spindle apparatus.

Spindle pole body

In yeast cells, the microtubule-organizing centre that functions like a centrosome and is usually associated with the nuclear membrane for part or all of the cell cycle.

Dynein

A minus-end-directed microtubule motor protein that transports cellular cargo along microtubules. In fungi, dynein is a key motor protein that is responsible for nuclear movement through interactions with astral microtubules.

Cytoduction

The production of a cell with a mixed cytoplasm but only one of the two parental nuclei. In Saccharomyces cerevisiae, cytoduction is accomplished by mating cells with defects in nuclear fusion (karyogamy).

Supernumerary chromosomes

Small extra chromosomes that are generally dispensable for normal cell functions but that, in some cases, are required for pathogenicity and thus are 'conditionally dispensable'.

Dicentric

A chromosome that has two functional centromeres. When they are tethered to opposite poles of the mitotic spindle the chromosome will break during mitosis.

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Gladfelter, A., Berman, J. Dancing genomes: fungal nuclear positioning. Nat Rev Microbiol 7, 875–886 (2009). https://doi.org/10.1038/nrmicro2249

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