Comparative genomics reveals the origin of fungal hyphae and multicellularity

Kiss, Enikő; Hegedüs, Botond; Virágh, Máté; Varga, Torda; Merényi, Zsolt; Kószó, Tamás; Bálint, Balázs; Prasanna, Arun N.; Krizsán, Krisztina; Kocsubé, Sándor; Riquelme, Meritxell; Takeshita, Norio; Nagy, László G.

doi:10.1038/s41467-019-12085-w

Cited by 97 publications

(76 citation statements)

References 116 publications

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“…The transition to filamentous growth is regulated by evolutionarily conserved signaling pathways [17,57]. One of these is the MAPK cascade that activates the transcription factor, Tec1.…”

Section: Discussionmentioning

confidence: 99%

Mapping the architecture of regulatory variation provides insights into the evolution of complex traits

Lupo

Krieger

Jonas

et al. 2020

Preprint

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Background: Organisms evolve complex traits by recruiting existing programs to new contexts, referred as co-option. Within a species, single upstream regulators can trigger full differentiation programs. Distinguishing whether co-option of differentiation programs results from variation in single regulator, or in multiple genes, is key for understanding how complex traits evolve. As an experimentally accessible model for studying this question we turned to budding yeast, where a differentiation program (filamentous) is activated in S. cerevisiae only upon starvation, but used by the related species S. paradoxus also in rich conditions. Results: To define expression variations associated with species-specific activation of the filamentous program, we profiled the transcriptome of S. cerevisiae, S. paradoxus and their hybrid along two cell cycles at 5-minutes resolution. As expected in cases of co-option, expression of oscillating genes varies between the species in synchrony with their growth phenotypes and was dominated by upstream trans-variations. Focusing on regulators of filamentous growth, we identified gene-linked variations (cis) in multiple genes across regulatory layers, which propagated to affect expression of target genes, as well as binding specificities of downstream transcription factor. Unexpectedly, variations in regulators essential for S. cerevisiae filamentation were individually too weak to explain activation of this program in S. paradoxus. Conclusions: Our study reveals the complex architecture of regulatory variation associated with species-specific use of a differentiation program. Based on these results, we suggest a new model in which evolutionary co-option of complex traits is stabilized in a distributed manner through multiple weak-effect variations accumulating throughout the regulatory network.including size, growth pattern, and body morphology [2][3][4]. A compelling model is that complex traits do not evolve de-novo but emerge through recruitment (co-option) of existing gene expression program to new contexts. Evidence supporting co-option were presented in the context of morphological evolution, where major interspecies differences in the positioning of body appendages or wing patterns were linked to variations in cis-regulatory elements controlling the expression of major regulators, including homeobox transcription factors or developmental signaling proteins [5][6][7][8][9][10].Modulating the expression of single upstream regulators provides a genetic shortcut for the evolution of complex traits [11]. Complicating this view, however, is the fact that gene expression networks, such as these activating complex traits, are polygenic and include multiple activators and inhibitors that could act as drivers [12]. Further, due to the inter-connected nature of genetic circuits, variations in seemingly distant genes could propagate to influence the same phenotype [13]. This was exemplified recently in Drosophila, where expression variation in a Hox gene that correlated with morphological...

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“…The transition to filamentous growth is regulated by evolutionarily conserved signaling pathways [17,57]. One of these is the MAPK cascade that activates the transcription factor, Tec1.…”

Section: Discussionmentioning

confidence: 99%

Mapping the architecture of regulatory variation provides insights into the evolution of complex traits

Lupo

Krieger

Jonas

et al. 2020

Preprint

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“…All replaceable septin strains (Hs- SEPT3 , Hs- SEPT6 , Hs- SEPT9 , and Hs- SEPT10 ) showed abnormal cell morphologies ( Fig. 6A, B, S7A ), notably reminiscent of elongated pseudohyphal forms often seen in pathogenic and invasive fungal species 54–56 . The fraction of elongated cells differed across human septins, with Hs- SEPT3 producing lower proportions of elongated cells ( Fig.…”

Section: Resultsmentioning

confidence: 99%

Systematic humanization of the yeast cytoskeleton discerns functionally replaceable from divergent human genes

Garge

Laurent

Kachroo³

et al. 2019

Preprint

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“…While both rhizoids and hyphae are polar, elongated and bifurcating structures, rhizoid feeding structures are a basal condition within the true fungi (Eumycota), and the dikaryan mycelium composed of multicellular septate hyphae is highly derived (Figure 1A and B). Hyphal cell types are observed outside of the Eumycota, such as within the Oomycota, however the origin of fungal hyphae within the Eumycota was independent [13, 16] and has not been reported in their closest relatives the Holozoans (animals, choanoflagellates and their kin). Comparative genomics has indicated that hyphae originated within the Chytridiomycota-Blastocladiomycota-Zoopagomycota nodes of the fungal tree [16], and is supported by fossil Blastocladiomycota and extant Monoblepharidomycetes having hyphae [13, 17].…”

Section: Introductionmentioning

confidence: 99%

“…Hyphal cell types are observed outside of the Eumycota, such as within the Oomycota, however the origin of fungal hyphae within the Eumycota was independent [13, 16] and has not been reported in their closest relatives the Holozoans (animals, choanoflagellates and their kin). Comparative genomics has indicated that hyphae originated within the Chytridiomycota-Blastocladiomycota-Zoopagomycota nodes of the fungal tree [16], and is supported by fossil Blastocladiomycota and extant Monoblepharidomycetes having hyphae [13, 17]. However, even though rhizoids have been considered precursory to hyphae [14], comparisons between rhizoid and hyphal developmental biology have not yet been made.…”

Section: Introductionmentioning

confidence: 99%

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

Laundon

Chrismas

Wheeler

et al. 2019

Preprint

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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...

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Comparative genomics reveals the origin of fungal hyphae and multicellularity

Cited by 97 publications

References 116 publications

Mapping the architecture of regulatory variation provides insights into the evolution of complex traits

Mapping the architecture of regulatory variation provides insights into the evolution of complex traits

Systematic humanization of the yeast cytoskeleton discerns functionally replaceable from divergent human genes

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

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