Forging the ring: from fungal septins' divergent roles in morphology, septation and virulence to factors contributing to their assembly into higher order structures

Vargas-Muñiz, José M.; Juvvadi, Praveen R.; Steinbach, William J.

doi:10.1099/mic.0.000359

Cited by 8 publications

(5 citation statements)

References 74 publications

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“…In the rice blast fungus Magnaportha oryzae , septins are important for the invasive appressorium [ 99 ]. Septins have also been implicated in other types of specialized morphogenesis in a variety of different plant and animal pathogens [ 67 , 92 , 100 , 101 ].…”

Section: Mcc/eisosomes Affect Other Plasma Membrane Domains That Cmentioning

confidence: 99%

MCC/Eisosomes Regulate Cell Wall Synthesis and Stress Responses in Fungi

Foderaro

Douglas

Konopka

2017

JoF

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The fungal plasma membrane is critical for cell wall synthesis and other important processes including nutrient uptake, secretion, endocytosis, morphogenesis, and response to stress. To coordinate these diverse functions, the plasma membrane is organized into specialized compartments that vary in size, stability, and composition. One recently identified domain known as the Membrane Compartment of Can1 (MCC)/eisosome is distinctive in that it corresponds to a furrow-like invagination in the plasma membrane. MCC/eisosomes have been shown to be formed by the Bin/Amphiphysin/Rvs (BAR) domain proteins Lsp1 and Pil1 in a range of fungi. MCC/eisosome domains influence multiple cellular functions; but a very pronounced defect in cell wall synthesis has been observed for mutants with defects in MCC/eisosomes in some yeast species. For example, Candida albicans MCC/eisosome mutants display abnormal spatial regulation of cell wall synthesis, including large invaginations and altered chemical composition of the walls. Recent studies indicate that MCC/eisosomes affect cell wall synthesis in part by regulating the levels of the key regulatory lipid phosphatidylinositol 4,5-bisphosphate (PI4,5P2) in the plasma membrane. One general way MCC/eisosomes function is by acting as protected islands in the plasma membrane, since these domains are very stable. They also act as scaffolds to recruit >20 proteins. Genetic studies aimed at defining the function of the MCC/eisosome proteins have identified important roles in resistance to stress, such as resistance to oxidative stress mediated by the flavodoxin-like proteins Pst1, Pst2, Pst3 and Ycp4. Thus, MCC/eisosomes play multiple roles in plasma membrane organization that protect fungal cells from the environment.

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Section: Mcc/eisosomes Affect Other Plasma Membrane Domains That Cmentioning

confidence: 99%

MCC/Eisosomes Regulate Cell Wall Synthesis and Stress Responses in Fungi

Foderaro

Douglas

Konopka

2017

JoF

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“…An increasing body of work suggests that septins play important roles in fungal pathogens (Douglas et al, 2005; Bridges and Gladfelter, 2014; Khan et al, 2015; Vargas-Muniz et al, 2016). An examination of fungal septin mutants suggests that a critical septin role is defining and restricting polar outgrowths that allow the fungus to invade and explore host tissue.…”

Section: Septin-dependent Host Infection By Fungal Pathogensmentioning

confidence: 99%

Septins Focus Cellular Growth for Host Infection by Pathogenic Fungi

Momany

Talbot

2017

Front. Cell Dev. Biol.

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One of the key challenges faced by microbial pathogens is invasion of host tissue. Fungal pathogens adopt a number of distinct strategies to overcome host cell defenses, including the development of specialized infection structures, the secretion of proteins that manipulate host responses or cellular organization, and the ability to facilitate their own uptake by phagocytic mechanisms. Key to many of these adaptations is the considerable morphogenetic plasticity displayed by pathogenic species. Fungal pathogens can, for example, shift their growth habit between non-polarized spores, or yeast-like cells, and highly polarized hyphal filaments. These polarized filaments can then elaborate differentiated cells, specialized to breach host barriers. Septins play fundamental roles in the ability of diverse fungi to undergo shape changes and organize the F-actin cytoskeleton to facilitate invasive growth. As a consequence, septins are increasingly implicated in fungal pathogenesis, with many septin mutants displaying impairment in their ability to cause diseases of both plants and animals. In this mini-review, we show that a common feature of septin mutants is the emergence of extra polar outgrowths during morphological transitions, such as emergence of germ tubes from conidia or branches from hyphae. We propose that because septins detect and stabilize membrane curvature, they prevent extra polar outgrowths and thereby focus fungal invasive force, allowing substrate invasion.

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“…Yet, within any given fungal or mammalian organism (or, in metazoans, cell type), septin hetero-octamers can be assembled from alternative sets of subunits, which, it has been proposed, arose from gene duplication and divergence ( Cao et al 2009 ; Valadares et al 2017 ). Ostensibly, this diversification has allowed different combinations of subunits associated with a common core structure to generate distinct supramolecular arrangements that fulfill separate physiological functions using the same underlying scaffold ( Barral and Kinoshita 2008 ; Garcia et al 2011 , 2016 ; Vargas-Muñiz et al 2016 ; Khan et al 2018 ; Rosa et al 2020 ).…”

Section: Discussionmentioning

confidence: 99%

Reconstructed evolutionary history of the yeast septins Cdc11 and Shs1

Takagi

Cho

Duvalyan

et al. 2020

G3 Genes|Genomes|Genetics

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Septins are GTP-binding proteins conserved across metazoans. They can polymerize into extended filaments and, hence, are considered a component of the cytoskeleton. The number of individual septins varies across the tree of life—yeast (Saccharomyces cerevisiae) has seven distinct subunits, a nematode (Caenorhabditis elegans) has two, and humans have 13. However, the overall geometric unit (an apolar hetero-octameric protomer and filaments assembled there from) has been conserved. To understand septin evolutionary variation, we focused on a related pair of yeast subunits (Cdc11 and Shs1) that appear to have arisen from gene duplication within the fungal clade. Either Cdc11 or Shs1 occupies the terminal position within a hetero-octamer, yet Cdc11 is essential for septin function and cell viability, whereas Shs1 is not. To discern the molecular basis of this divergence, we utilized ancestral gene reconstruction to predict, synthesize, and experimentally examine the most recent common ancestor (“Anc.11-S”) of Cdc11 and Shs1. Anc.11-S was able to occupy the terminal position within an octamer, just like the modern subunits. Although Anc.11-S supplied many of the known functions of Cdc11, it was unable to replace the distinct function(s) of Shs1. To further evaluate the history of Shs1, additional intermediates along a proposed trajectory from Anc.11-S to yeast Shs1 were generated and tested. We demonstrate that multiple events contributed to the current properties of Shs1: (1) loss of Shs1–Shs1 self-association early after duplication, (2) co-evolution of heterotypic Cdc11–Shs1 interaction between neighboring hetero-octamers, and (3) eventual repurposing and acquisition of novel function(s) for its C-terminal extension domain. Thus, a pair of duplicated proteins, despite constraints imposed by assembly into a highly conserved multi-subunit structure, could evolve new functionality via a complex evolutionary pathway.

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Forging the ring: from fungal septins' divergent roles in morphology, septation and virulence to factors contributing to their assembly into higher order structures

Cited by 8 publications

References 74 publications

MCC/Eisosomes Regulate Cell Wall Synthesis and Stress Responses in Fungi

MCC/Eisosomes Regulate Cell Wall Synthesis and Stress Responses in Fungi

Septins Focus Cellular Growth for Host Infection by Pathogenic Fungi

Reconstructed evolutionary history of the yeast septins Cdc11 and Shs1

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