Defining individual size in the model filamentous fungus Neurospora crassa

Abstract

It is challenging to apply the tenets of individuality to filamentous fungi: a fungal mycelium can contain millions of genetically diverse but totipotent nuclei, each capable of founding new mycelia. Moreover, a single mycelium can potentially stretch over kilometres, and it is unlikely that its distant parts share resources or have the same fitness. Here, we directly measure how a single mycelium of the model ascomycete Neurospora crassa is patterned into reproductive units (RUs), meaning subpopulations of nuclei that propagate together as spores, and function as reproductive individuals. The density of RUs is sensitive to the geometry of growth; we detected 50-fold smaller RUs when mycelia had expanding frontiers than when they were constrained to grow in one direction only. RUs fragmented further when the mycelial network was perturbed. In mycelia with expanding frontiers, RU composition was strongly influenced by the distribution of genotypes early in development. Our results provide a concept of fungal individuality that is directly connected to reproductive potential, and therefore to theories of how fungal individuals adapt and evolve over time. Our data show that the size of reproductive individuals is a dynamic and environment-dependent property, even within apparently totally connected fungal mycelia.

Hyphal ontogeny in Neurospora crassa: a model organism for all seasons

“…The morphogenetic changes initiate when a conidium begins to grow isotropically during the first hours of hydration; soon after, the symmetry is broken, growth becomes polarized, and the resulting germ tube continues extending by apical polarized growth until it becomes a fully mature hypha. Further branching from subapical compartments generates new hyphal tips capable of fusing with each other and generating a mycelium 6, 15– 18 .…”

A Nuclei-Based Conceptual Model of (Eco)evolutionary Dynamics in Fungal Heterokaryons

“…This implies that nuclear competition extends to sporulation and can lead to decreased fitness of germlings. However, nuclei can cooperate and Ma et al (2016) show that mycelium of N. crassa is comprised of subpopulations of nuclei that reproduce together and function as “reproductive units.” The third point to consider is that the distribution of NGH across the mycelium can create phenotypic heterogeneity within mycelium where selection could then act on this heterogeneity. While some studies show that nuclear ratios are evenly distributed or homogenised across the mycelium ( Meunier et al, 2018 ; Cornell et al, 2022 ) there is evidence of uneven nuclear distribution as well ( He et al, 2021 ).…”

“…In such a situation, a subpopulation of nuclei, operating in proximity to each other (i.e., belonging to the same or neighbouring hyphae), generating a certain phenotype, is likely to be selected together. Therefore, inspired by the idea of “reproductive units” ( Ma et al, 2016 ), we propose a conceptual model of three-level fungal organisation as spatially structured populations (metapopulation) of nuclei.…”

“…Theoretical approaches, such as individual-based models (IBMs) are excellent tool to tackle and explore complex systems, gain additional understanding of how such systems evolve but also provide novel insights, which could lead to hypotheses testable in the lab. However, there are very few such studies that investigate nuclear genotype heterogeneity and nuclear dynamics and the potential effects on the evolution of filamentous fungi ( Gifford and Schoustra, 2013 ; Ma et al, 2016 ; Scott et al, 2019 ; Kokkoris et al, 2020 ).…”

Fungal spore transport by omnivorous mycophagous slug in temperate forest

“…This may be because research methodology for spore and seed dispersal has not yet been established (Murray, 1988; Otani & Shibata, 2000). Recent developments in molecular biological techniques or global positioning system devices for tracking the movement of life are expected to advance research in this area (Ashley, 2010; Danks et al, 2020; Ma et al, 2016).…”