18.9 Ploidy and genomic variation

18.9 Ploidy and genomic variation

A characteristic feature of fungi is the presence of large number of nuclei in a common cytoplasm. Even in fungi with septate hyphae the septa are perforated to some degree, so the mycelium is essentially coenocytic (although the fact that neighbouring hyphal cells can show very different differentiation states on the two sides of what appear to be open septal pores, as shown in Fig. 12.13 (Section 12.6), suggests that hyphal compartments can be physiologically distinct). Nuclei in filamentous fungi are highly dynamic in terms of both physical movement and pattern of distribution in the mycelium. The nuclei in a mycelium may cooperate or compete with each other and may even combat each other. It has even been proposed that at least some nuclei in filamentous fungi are redundant in a genetic sense and serve instead as a stockpile of carbohydrate, nitrogen and phosphorus (in the form of their DNA) which is accessed by regulated autophagy.

As far as the primary genetic function of nuclei is concerned, the fungal mycelium is commonly heterokaryotic. Heterokaryosis refers to the presence of two or more genetically distinct nuclei within the same hypha. It is uncommon in all other organisms, but heterokaryosis, along with most of the other features mentioned in the previous paragraph, is a hallmark of kingdom Fungi (Roberts & Gladfelter, 2016; Strom & Bushley, 2016). We deal with most aspects of the biology of heterokaryons in Chapters 5 & 7 and will not repeat it here, but we do have a few additional points to make.

Hyphal fusion between different fungal individuals is limited by vegetative compatibility barriers (Section 7.5). However, these compatibility barriers are not absolute, and exchange of nuclei between hyphae of different species is now believed to enhance fungal diversification. Such an event produces a fungal chimera, which is an organism that contains cells or tissues from two or more different species, and this can enhance diversification at the species level by allowing horizontal gene transfer between mycelia that are too distantly related to hybridise sexually (Roper et al., 2013).

Polyploidy, featuring past and recent whole-genome duplications, is a major evolutionary process in eukaryotes, particularly in plants and, but to a less extent, in animals; and it also occurs in fungi. Many fungi undergo ploidy changes during adaptation to adverse or new environments. Some fungi exist as stable haploid, diploid, or polyploid (triploid, tetraploid) hyphae, while others change ploidy under some conditions and revert to the original ploidy level under other conditions. Aneuploidy (an abnormal chromosome number) is sometimes observed in fungi exposed to new or stressful environments and because of previous ploidy change. The ability of an organism to replicate and segregate its genome with high fidelity is vital to its survival and to produce future generations. Errors in replication or segregation can lead to a change in ploidy or chromosome number.

Ploidy can increase through mating, endoreduplication, which is replication of the nuclear genome in the absence of mitosis, or failure of cytokinesis after replication. Evidently, some fungi have evolved the ability to tolerate large genome size changes and generate vast genomic heterogeneity without using the meiotic reduction division; indeed, the evolutionary history of Saccharomyces species has been shaped by past and recent whole genome duplication events (Albertin & Marullo, 2012; Todd et al., 2017).

We have already mentioned that species of Armillaria are unusual in having diploid tissues in the (mushroom) fruit body though this is produced by a dikaryotic mycelium (Section 5.7), and we have discussed the parasexual cycle (Section 7.8). The parasexual cycle is the sequence: diploidisation, mitotic recombination, and haploidisation through nondisjunction (improper transport of chromosomes to the poles of the division spindle during mitosis) resulting in random chromosome loss over several divisions, so the diploid is reduced to a haploid state through a series of aneuploid intermediates (Stukenbrock & Croll, 2014).

The phrase ‘the Tree of Life’ is often used to describe the evolutionary history of living things. Purposefully, the phrase creates the mental image of evolution represented as a structure like a tree: the main stem is ‘rooted’ at the (one and only) origin of life on Earth: the stem’s branches depict the major clades of evolving organisms, the secondary branches depict the orders and families that make up those clades, and the tips of the final, finest, branches bear the leaves of the tree, which represent the elemental species of organisms.

The older I get, and the more molecular genetics I read, the more I distrust that mental image of a tree of life; and the more I feel that a better mental image is of the currents in an ocean. Of flows which are sufficiently distinct to have a direction of their own, but with occasional maelstroms of mixing vortexes where different currents interact. All this being driven in organismal evolution by the insertional and transpositional genetic elements that make up the genomes of the drifting leaves. Not so much Richard Dawkins’ selfish gene (view Richard Dawkins at the Royal Institution on YouTube: https://www.youtube.com/watch?v=j9p2F2oa0_k), but more a case of the ambitious gene.

Updated July, 2018