Dancing genomes: fungal nuclear positioning

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.

Figure 1. Microtubules and nuclear movement

In Saccharomyces cerevisiae, all microtubules (MTs) originate from the spindle pole body. Kinetochore MTs are required for chromosome segregation, and interpolar MTs are required for nuclear pole separation. Astral MTs interact with the cell cortex and septin ring at the bud neck to orientate the mitotic spindle across the mother–daughter cell junction.

Figure 2. Mitotic dynamics in Candida albicans

a,b | In wild-type yeast (part a) and pseudohyphal (part b) cells, the nuclei are aligned by the mitotic spindle (spindle pole bodies are in yellow, kinetochore microtubules are in green and interpolar microtubules are in black) and divide across the mother–bud neck. c | In yeast cells lacking the dynein heavy chain, the nuclei divide in the mother cell and a checkpoint delays cell cycle progression until the nucleus enters the daughter cell. d | In pseudohyphal cells lacking dynein, nuclei migrate into the daughter cell and divide there. There is no checkpoint to ensure that the mother nucleus returns to the mother cell. In this schematic, the details of microtubule attachment to chromosomes and of inter-microtubule interactions are not shown.

Figure 3. Overview of dikaryon formation

a | Hyphae of many types of filamentous fungi can fuse regardless of mating type. b | If fusion occurs between mates with compatible mating loci (blue and pink nuclei), rapid nuclear migration and exchange between the two parental mycelia is initiated. It is unknown how microtubules (MTs) and MT-based motors are regulated during this process, but there is no migration if noncompatible mates fuse. c | The nuclei migrate until they reach the distal tip of a hypha and then pair with a nucleus from the other parent. In some cells, a specialized polarized cell structure forms, called a clamp, crozier or hook cell (depending on the species). Some dikaryons form without a clamp. The clamp cell is a side projection of the hypha, and one nucleus migrates up into this projection while the opposite mating-type nucleus remains in the hypha. Both nuclei divide synchronously. Owing to the placement of the septa and the subsequent fusion of the clamp cell back to the main hypha, one daughter nucleus from each mitosis ends up in each cell of the hyphal tube. d | This intricate process produces a dikaryotic hypha: it is compartmentalized such that two parental nuclei share the same cytosol. The dikaryon state can persist for extended periods and there can be exchange of genetic material between nuclei.