Patterns of Conservation and Diversification in the Fungal Polarization Network

Abstract

The combined actions of proteins in networks underlie all fundamental cellular functions. Deeper insights into the dynamics of network composition across species and their functional consequences are crucial to fully understand protein network evolution. Large-scale comparative studies with high phylogenetic resolution are now feasible through the recent rise in available genomic data sets of both model and nonmodel species. Here, we focus on the polarity network, which is universally essential for cell proliferation and studied in great detail in the model organism, Saccharomyces cerevisiae. We examine 42 proteins, directly related to cell polarization, across 298 fungal strains/species to determine the composition of the network and patterns of conservation and diversification. We observe strong protein conservation for a group of 23 core proteins: >95% of all examined strains/species possess at least 14 of these core proteins, albeit in varying compositions, and non of the individual core proteins is 100% conserved. We find high levels of variation in prevalence and sequence identity in the remaining 19 proteins, resulting in distinct lineage-specific compositions of the network in the majority of strains/species. We show that the observed diversification in network composition correlates with lineage, lifestyle, and genetic distance. Yeast, filamentous and basal unicellular fungi, form distinctive groups based on these analyses, with substantial differences to their polarization network. Our study shows that the fungal polarization network is highly dynamic, even between closely related species, and that functional conservation appears to be achieved by varying the specific components of the fungal polarization repertoire.

Fungal evolution: cellular, genomic and metabolic complexity

“…Polarized growth has been widely studied in S. cerevisiae , and a core of proteins have been identified (Arkowitz & Bassilana, ; Riquelme, ; Martin & Arkowitz, ; Diepeveen et al ., ). This core toolkit seems to be relatively well conserved across all fungal lineages, although no individual component appears to be completely essential (Diepeveen et al ., ). Within the kingdom, true hyphal growth is an evolutionary novelty of the ‘terrestrial fungi’, a monophyletic clade that includes the phyla Zoopagomycota, Mucoromycota, Glomeromycota, Ascomycota and Basidiomycota.…”

Adaptability and evolution of the cell polarization machinery in budding yeast

“…On the basis of this ancestral mechanism, Bem1 could then have evolved in a step-wise fashion. Given that Bem1 is highly conserved in fungi (Diepeveen et al, 2018), and that fission yeast polarization is based on the same mutual recruitment mechanism (Lamas et al, 2019;Martin and Arkowitz, 2014), this hypothetical evolutionary pathway would likely lie far in the past.…”

“…Another possibility is to search for species in the current tree of life which contain intermediate steps of the evolutionary trajectory, for instance species with a more ancient version of Bem1 lacking the SH3 domain, and identify the protein self-organization principles underlying polarization in these species. This is becoming a more and more realistic option, given the very large (and still expanding) number of fungal species that has been sequenced (Diepeveen et al, 2018) and the growing interest of cell and molecular biologists to work with nonmodel systems (Russell et al, 2017).…”

Minimal in vitro systems shed light on cell polarity

“…4A), where a Cdc42-based protein pattern on the cell membrane marks the site of bud emergence (Bi and Park, 2012). Cdc42 is a highly conserved membrane-bound small GTPase (Diepeveen et al, 2018) with two states: an active, GTP-bound, state, and an inactive, GDPbound, state. Switching between the two states is highly regulated and only Cdc42-GTP signaling towards the downstream processes is sufficient for bud formation.…”

“…How the functions of Bem1 are redistributed by removing the three other proteins remains to be discovered. How molecular functions are rearranged is also relevant beyond this specific experiment: comparative studies on 298 fungal strains and species showed that redistribution of functions over different proteins in the polarization network happens regularly over the fungal tree of life (Diepeveen et al, 2018), and theoretical work suggested that small changes in reaction rates or the topology of the polarization network can dramatically rearrange functions within the polarity network (Goryachev and Leda, 2017). A minimal system for pattern formation, where proteins can be selectively added and removed, might help the understanding of how molecular functions necessary for pattern formation can be redistributed during evolution.…”