Arabidopsis Class II Formins AtFH13 and AtFH14 Can Form Heterodimers but Exhibit Distinct Patterns of Cellular Localization

Kollárová, Eva; Forero, Anežka Baquero; Stillerová, Lenka; Přerostová, Sylva; Cvrčková, Fatima

doi:10.3390/ijms21010348

Cited by 14 publications

(17 citation statements)

References 57 publications

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“…4,42 The PTEN-like domain of class II formins has also been shown to mediate formin-microtubule interactions. 44 Sharing domain organizations does not necessarily indicate relatedness, as the formin family is thought to have undergone gene duplication, divergence, and domain shuffling throughout its history. 40,43,45 We therefore wanted to determine how chytrid formins fit into this complex family history.…”

Section: Ll Open Accessmentioning

confidence: 99%

The actin networks of chytrid fungi reveal evolutionary loss of cytoskeletal complexity in the fungal kingdom

et al. 2021

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The actin networks of chytrid fungi reveal evolutionary loss of cytoskeletal complexity in the fungal kingdom Highlights d Chytrid fungi diverged before the radiation of Dikarya (multicellular fungi and yeast) d Chytrids have actin genes and structures typical of both Dikarya and animal cells d The regulation of chytrid actin structures resembles that of animal/dikaryotic cells d Presence of a BNI1/BNR1 type formin correlates with the presence of actin cables

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Section: Ll Open Accessmentioning

confidence: 99%

The actin networks of chytrid fungi reveal evolutionary loss of cytoskeletal complexity in the fungal kingdom

et al. 2021

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“…Arabidopsis, for example, has 10 Class II formins, 4 of which have N-terminal PTEN-like domains that localize these formins to membranes (Deeks et al 2002;Cvrcková et al 2004;Grunt et al 2008;Breitsprecher and Goode 2013). The PTEN-like domain of class II formins has also been shown to mediate formin-microtubule interactions (Kollárová et al 2020). Despite having similar domain organization, our phylogenetic analysis of FH2 domains (see below) suggests that these chytrid formins are not related to Class II plant formins and may represent a secondary gain of a PTEN/PTEN-like domain (Pruyne 2017).…”

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confidence: 99%

The actin networks of chytrid fungi reveal evolutionary loss of cytoskeletal complexity in the fungal kingdom

Prostak

Robinson

Titus

et al. 2020

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Cells from across the eukaryotic tree use actin polymers and a number of conserved regulators for a wide variety of functions including endocytosis, cytokinesis, and cell migration. Despite this conservation, the actin cytoskeleton has undergone significant evolution and diversification, highlighted by the differences in the actin cytoskeletal networks of mammalian cells and yeast. Chytrid fungi diverged before the emergence of the Dikarya (multicellular fungi and yeast), and therefore provide a unique opportunity to study the evolution of the actin cytoskeleton. Chytrids have two life stages: zoospore cells that can swim with a flagellum, and sessile sporangial cells that, like multicellular fungi, are encased in a chitinous cell wall. Here we show that zoospores of the amphibian-killing chytrid Batrachochytrium dendrobatidis (Bd) build dynamic actin structures that resemble those of animal cells, including pseudopods, an actin cortex, and filopodia-like actin spikes. In contrast, Bd sporangia assemble actin patches similar to those of yeast, as well as perinuclear actin shells. Our identification of actin cytoskeletal elements in the genomes of five species of chytrid fungi indicate that these actin structures are controlled by both fungalspecific components as well as actin regulators and myosin motors found in animals but not other fungal lineages. The use of specific small molecule inhibitors indicate that nearly all of Bd's actin structures are dynamic and use distinct nucleators: while pseudopods and actin patches are Arp2/3-dependent, the actin cortex appears formin-dependent, and actin spikes require both nucleators. The presence of animal-and yeast-like actin cytoskeletal components in the genome combined with the intermediate actin phenotypes in Bd suggests that the simplicity of the yeast cytoskeleton may be due to evolutionary loss. evolutionary Rosetta Stone with which we can map the simplified actin features of yeast to those of animals.Bd, like other chytrids, has two developmental stages: motile "zoospore" cells that lack a cellwall and swim with a flagellum, and non-motile sporangia that grow and produce new zoospores ( Fig. 1b; (Berger et al. 2005;Longcore et al. 1999). We recently showed that zoospores can also crawl across surfaces using actin-filled, Arp2/3-dependent pseudopods (Fritz-Laylin, Lord, et al. 2017). Other than these pseudopods, actin's role in any developmental stage of Bd has not been studied. To fill this knowledge gap, we identified homologs of key actin regulatory proteins and myosin motors in multiple species of chytrids and related fungi. We also identified new actin structures in zoospores and sporangia, and tested the requirements of Arp2/3 and formin family proteins for their assembly. We find that both the regulatory networks and actin structures of Bd are intermediate in complexity between animals and Dikarya, suggesting that the streamlined actin networks of common model fungi are a result of secondary evolutionary loss of actin network components. RESULTS Bd has dev...

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“…Related to its role in amyloplast– cytoskeleton connection, this protein also participates in gravity sensing ( Song et al, 2019 ). Two typical Arabidopsis thaliana Class II formins, FH13 (At5g58160) and FH14 (At1g31810), partly co-localize with the endoplasmic reticulum and microtubules when heterologously expressed in tobacco leaf epidermis ( Kollárová et al, 2020 ), again consistent with these proteins associating with endomembranes. Thus, formin-membrane interaction is widespread and, in some cases, involves also membranes other than the plasmalemma.…”

Section: Introductionmentioning

confidence: 76%

The Arabidopsis thaliana Class II Formin FH13 Modulates Pollen Tube Growth

2021

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Formins are a large, evolutionarily conserved family of actin-nucleating proteins with additional roles in regulating microfilament, microtubule, and membrane dynamics. Angiosperm formins, expressed in both sporophytic and gametophytic tissues, can be divided into two subfamilies, Class I and Class II, each often exhibiting characteristic domain organization. Gametophytically expressed Class I formins have been documented to mediate plasma membrane-based actin assembly in pollen grains and pollen tubes, contributing to proper pollen germination and pollen tube tip growth, and a rice Class II formin, FH5/RMD, has been proposed to act as a positive regulator of pollen tube growth based on mutant phenotype and overexpression data. Here we report functional characterization of the Arabidopsis thaliana pollen-expressed typical Class II formin FH13 (At5g58160). Consistent with published transcriptome data, live-cell imaging in transgenic plants expressing fluorescent protein-tagged FH13 under the control of the FH13 promoter revealed expression in pollen and pollen tubes with non-homogeneous signal distribution in pollen tube cytoplasm, suggesting that this formin functions in the male gametophyte. Surprisingly, fh13 loss of function mutations do not affect plant fertility but result in stimulation of in vitro pollen tube growth, while tagged FH13 overexpression inhibits pollen tube elongation. Pollen tubes of mutants expressing a fluorescent actin marker exhibited possible minor alterations of actin organization. Our results thus indicate that FH13 controls or limits pollen tube growth, or, more generally, that typical Class II formins should be understood as modulators of pollen tube elongation rather than merely components of the molecular apparatus executing tip growth.

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Arabidopsis Class II Formins AtFH13 and AtFH14 Can Form Heterodimers but Exhibit Distinct Patterns of Cellular Localization

Cited by 14 publications

References 57 publications

The actin networks of chytrid fungi reveal evolutionary loss of cytoskeletal complexity in the fungal kingdom

The actin networks of chytrid fungi reveal evolutionary loss of cytoskeletal complexity in the fungal kingdom

The actin networks of chytrid fungi reveal evolutionary loss of cytoskeletal complexity in the fungal kingdom

The Arabidopsis thaliana Class II Formin FH13 Modulates Pollen Tube Growth

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