Trade-off between plasticity and velocity in mycelial growth

Abstract

Tip-growing fungal cells maintain the cell polarity at the apical regions and elongate by de novo synthesis of cell wall. Cell polarity and growth rate affect the mycelial morphogenesis, however, it remains unclear how they act cooperatively to determine cell shape. Here we investigated their relationship by analyzing hyphal tip growth of filamentous fungi growing inside extremely narrow 1µm-width channels of microfluidic devices. Since the channels are much narrower than the diameter of hyphae, the hyphae must change its morphology when they grow through the channels. Live imaging analysis revealed that hyphae of some species continued growing through the channels, whereas hyphae of other species often ceased growing when passing through the channels or lost the cell polarity after emerging from the channels. Fluorescence live imaging analysis of the Spitzenkörper, a collection of secretory vesicles and polarity-related proteins at hyphal tips, in Neurospora crassa hyphae indicates that hyphal tip growth requires a very delicate balance of ordered exocytosis to maintain polarity in spatially confined environments. We analyzed the mycelial growth of seven fungal species from different lineages, which also include phytopathogenic fungi. This comparative cell biology showed that the growth defects in the channels were not correlated with their taxonomic classification nor with the width of hyphae, but, correlated with the hyphal elongation rate. This is the first report indicating a trade-off between plasticity and velocity in mycelial growth, and serves to understand fungal invasive growth into substrates or plant/animal cells, with direct impact on fungal biotechnology, ecology and pathogenicity.

Cell Rupture and Morphogenesis Control of the Dimorphic Yeast Candida albicans by Nanostructured Surfaces

“…Contact-dependent/mechanical response or thigmotropism has been observed in plant root tips and fungal hyphal growth. − Perturbation of these structures results in a stretching of the cell wall and/or plasma membrane, thereby activating an intercellular signaling cascade . While microscale structures have been shown to redirect the growth of fungal hyphae, this is among the first nanoscale thigmotropic response that controls a genetic process, i.e., fungal cell morphology switch.…”

Microfabrication and its use in investigating fungal biology

“…During growth in confined channels, branching was suppressed in filamentous fungi but resumed either when hyphae emerged from the end of the channel, or a side channel was encountered (Figure 2c) (Aleklett et al, 2021;Baranger et al, 2020;Fukuda et al, 2021;Hanson et al, 2006;Held et al, 2011). This was observed in both air-filled and nutrient-filled channels, suggesting that constriction is sensed by a signal such as contact or the build-up of a secreted factor/waste product, to negatively regulate branching.…”

“…Neither perfusion flow rate nor the direction of flow appears to affect the rate of fungal growth or the direction of spore germination (in 0.8 µlh −1 ). Together with the finding that perfusion of yeast does not trigger stress signaling, there is little evidence that fungi are highly sensitive to shear stress, although this remains to be explored (Baranger et al, 2020;Crane et al, 2014;Fukuda et al, 2021).…”

“…A panel of seven fungi was used to examine whether the ratio of channel width to hyphal diameter affected elongation and was not a straightforward predictor of whether a hypha could successfully grow through a constriction (Fukuda et al, 2021). Instead, it was the fungal growth rate that played a predominant role.…”

“…However, when turgor pressure, and hence growth rate, were reduced by treatment with 0.6 M KCl, N. crassa hyphae were able to maintain polarity and pass through the channel. Therefore, polarized growth is abolished when there is an overabundance of apical polarity components relative to the width of the constriction (Fukuda et al, 2021). Orthogonal collisions of the hyphal tip with an obstacle are another cause of disorganization of the polarity machinery.…”