Chytrid rhizoid morphogenesis is adaptive and resembles hyphal development in ‘higher’ fungi

Abstract

13 E: micnli@mba.ac.uk 14 T: +44 (0)1752 426328 15 16 17 18 19 20 21 22 42 prevalence and fungal evolution. We demonstrate that the sophisticated cell biology and 43 developmental plasticity previously considered characteristic of hyphal fungi are shared 44 more widely across the Kingdom Fungi and therefore could be conserved from their most 45 recent common ancestor. 46 47 48 101 after ~2 h (Supplementary Figure 6), suggesting the presence of a currently unknown control 102 mechanism regulating rhizoid branching in chytrids. During rhizoid development, lateral 103 branching was more frequent than apical branching (Figure 1F and G), as observed in 104 5 dikaryan hyphae [20]. Fractal analysis (fractal dimension = Db) of 24 h chytrid cells revealed 105 that rhizoids approximate a 2D biological fractal (Mean Db = 1.51 ± 0.24), with rhizoids 106 relatively more fractal at the centre of the cell (Max Db = 1.69-2.19) and less fractal towards 107 the growing periphery (Min Db = 0.69-1.49) (Supplementary Figure 8). Similar patterns of 108 fractal organisation are also observed in hyphae-based mycelial colonies [21]. Together 109 these findings suggest that a form of apical dominance at the growing edge rhizoid tips may 110 suppress apical branching to maintain rhizoid network integrity as in dikaryan hyphae [22, 111 23]. 112 113 Cell wall and actin dynamics govern branching in chytrid rhizoids 114 Given the apparent hyphal-like properties of the chytrid cell, we sought a greater 115 understanding of the potential subcellular machinery underpinning rhizoid morphogenesis. 116Chemical characterisation of the R. globosum rhizoid showed that the chitin-containing cell 117 wall and actin patches were located throughout the rhizoid (Figure 2A). As the cell wall and 130 homologs [26][27][28], which is the target for caspofungin. Despite the absence of FKS1 131 homologues in chytrid genomes, quantification of glucans in R. globosum showed that they 132 157 substantially differential rhizoid development compared to cells from the exogenous carbon 158 replete conditions that we interpret to be an adaptive searching phenotype ( Figure 3A and B; 159 Supplementary Table 4; Supplementary Movie 10). Under carbon starvation, R. globosum rhizoids. (B) The spherical thallus of R. globosum is connected to the rhizoid system via an 641 mycelial colonies. Processing and fractal analysis workflow for 24 h R. globosum cells. 642 Chytrid rhizoid systems become decreasingly fractal towards the growing edge. Final column 643 images are pseudo-coloured by fractal dimension. 644 645 Supplementary Table 1 -Morphometric features of developing R. globosum rhizoids 646 associated with Figure 1 E-G. 647 648 Supplementary Table 2 -Morphometric features and statistical comparisons of 649 chemically inhibited R. globosum rhizoids, associated with Figure 2 B-C.650 25 651 Supplementary Table 3 -Morphometric features and statistical comparisons of R. 652 globosum rhizoids growing in carbon replete or deplete media, associated with Figure 653 3 A-C. 654 655 Sup...

Comparative genomics reveals the origin of fungal hyphae and multicellularity

“…These chytrid rhizoids have been considered as possible precursors of the first fungal hyphae, and critical participants of the evolution of hyphal growth. Investigation of rhizoid morphogenesis in Rhizoclosmatium globosum seems to confirm these assumptions by showing that apical and fractal-like growth mode of rhizoids are very similar to that of fungal hyphae (Laundon et al, 2019).…”

“…Capsaspora owczarzaki) , filamentous hyphae might have evolved by the gradual elongation of substrateanchoring, anucleate hypha-like outgrowths (rhizoids) of early fungal ancestors through tubular, multinucleate intermediates. These rhizoids resemble the early diverging fungal lineage Chytridiomycota (Dee et al, 2015;Harris, 2011;Laundon et al, 2019;Nagy et al, 2017;Stajich et al, 2009). In multicellular organisms the cooperation between individual cells is beneficial for the whole organism, but it can also be costly or beneficial to the cooperators.…”