Physiological Significance of Network Organization in Fungi

Abstract

bThe evolution of multicellularity has occurred in diverse lineages and in multiple ways among eukaryotic species. For plants and fungi, multicellular forms are derived from ancestors that failed to separate following cell division, thus retaining cytoplasmic continuity between the daughter cells. In networked organisms, such as filamentous fungi, cytoplasmic continuity facilitates the long-distance transport of resources without the elaboration of a separate vascular system. Nutrient translocation in fungi is essential for nutrient cycling in ecosystems, mycorrhizal symbioses, virulence, and substrate utilization. It has been proposed that an interconnected mycelial network influences resource translocation, but the theory has not been empirically tested. Here we show, by using mutants that disrupt network formation in Neurospora crassa (⌬so mutant, no fusion; ⌬Prm-1 mutant, ϳ50% fusion), that the translocation of labeled nutrients is adversely affected in homogeneous environments and is even more severely impacted in heterogeneous environments. We also show that the ability to share resources and genetic exchange between colonies (via hyphal fusion) is very limited in mature colonies, in contrast to in young colonies and germlings that readily share nutrients and genetic resources. The differences in genetic/resource sharing between young and mature colonies were associated with variations in colony architecture (hyphal differentiation/diameters, branching patterns, and angles). Thus, the ability to share resources and genetic material between colonies is developmentally regulated and is a function of the age of a colony. This study highlights the necessity of hyphal fusion for efficient nutrient translocation within an N. crassa colony but also shows that established N. crassa colonies do not share resources in a significant manner.T he transition from unicellular to multicellular organisms has occurred on multiple occasions in diverse lineages over considerable evolutionary time (28,38,68). While an initial adaptive advantage may have accrued simply from being larger, multicellular organisms subsequently developed increased differentiation and specialization, leading to a more efficient division of labor (8). Multicellularity may have arisen by either the aggregation of individual cells to form a colony or by the failure of daughter cells to separate following division. Comparisons of unicellular animals and their multicellular relatives support the view that multicellularity is associated with expansion of the genetic families involved in cell adhesion, cell-cell signaling, and cell differentiation (63). In contrast, multicellular plants and fungi are derived from ancestors that failed to separate following cell division, providing an opportunity to retain cytoplasmic continuity between daughter cells (75). Thus, plant cells are linked by tissue-specific patterns of plasmodesmata (41, 47), while fungi are either coenocytic or have perforated septa that allow intercompartmental exchange (40).In ascomycete an...

Nuclear dynamics in a fungal chimera

“…In real N. crassa colonies, hyphae exhibit a hierarchy of diameters, with the leading hyphae that feed the most tips having the largest diameters, primary branches having smaller diameters, and secondary branches even smaller diameters (for a 5-mmsized colony, ref. 24 gives the respective hyphal diameters to be 12 μm, 8 μm, and 6 μm). As a result, nuclear division is more likely to occur in leading hyphae, where the probability of sibling nuclei being separated is larger.…”

Fungal Morphogenesis

“…At the margins of the colony, individual hyphae show an avoidance response, whereas in the colony interior, hyphal fusion (anastomosis) permits the exchange of nutrients and perhaps growth signals (Rayner 1996;Simonin et al 2012). An important concept that underlies mycelium formation is apical dominance, which refers to the suppression of secondary polarity axes in the vicinity of an actively extending hyphal tip (Rayner 1991).…”

Early Colony Establishment in Neurospora crassa Requires a MAP Kinase Regulatory Network

“…Cell fusion between genetically identical cells can be mediated by cells that have differentiated, but in some cases, also between cells in an identical developmental state, for example, cell fusion between germinating asexual spores (conidia) of filamentous fungi (Pandey et al 2004;Roca et al 2005a;Read et al 2010). In filamentous fungi, these fusions are integral to the formation of an interconnected hyphal network, which mediates genetic mixing and the sharing of resources (Simonin et al 2012;Roper et al 2013). How this process is initiated and maintained and what proteins are involved are still mostly unknown.…”