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Functional Characterization of Aspergillus Nidulans Homologues of Saccharomyces Cerevisiae Spa2 and Bud6

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Functional Characterization of Aspergillus Nidulans Homologues of Saccharomyces Cerevisiae Spa2 and Bud6 University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Papers in Plant Pathology Plant Pathology Department June 2006 Functional Characterization of Aspergillus nidulans Homologues of Saccharomyces cerevisiae Spa2 and Bud6 Aleksandra Virag University of Nebraska-Lincoln, [email protected] Steven D. Harris University of Nebraska-Lincoln, [email protected] Follow this and additional works at: https://digitalcommons.unl.edu/plantpathpapers Part of the Plant Pathology Commons Virag, Aleksandra and Harris, Steven D., "Functional Characterization of Aspergillus nidulans Homologues of Saccharomyces cerevisiae Spa2 and Bud6" (2006). Papers in Plant Pathology. 48. https://digitalcommons.unl.edu/plantpathpapers/48 This Article is brought to you for free and open access by the Plant Pathology Department at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Papers in Plant Pathology by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. EUKARYOTIC CELL, June 2006, p. 881–895 Vol. 5, No. 6 1535-9778/06/$08.00ϩ0 doi:10.1128/EC.00036-06 Copyright © 2006, American Society for Microbiology. All Rights Reserved. Functional Characterization of Aspergillus nidulans Homologues of Saccharomyces cerevisiae Spa2 and Bud6 Aleksandra Virag and Steven D. Harris* Plant Science Initiative and Department of Plant Pathology, University of Nebraska, Lincoln, Nebraska Received 6 February 2006/Accepted 12 April 2006 The importance of polarized growth for fungi has elicited significant effort directed at better understanding underlying mechanisms of polarization, with a focus on yeast systems. At sites of tip growth, multiple protein complexes assemble and coordinate to ensure that incoming building material reaches the appropriate destination sites, and polarized growth is maintained. One of these complexes is the polarisome that consists of Spa2, Bud6, Pea2, and Bni1 in Saccharomyces cerevisiae. Filamentous hyphae differ in their development and Downloaded from life style from yeasts and likely regulate polarized growth in a different way. This is expected to reflect on the composition and presence of protein complexes that assemble at the hyphal tip. In this study we searched for polarisome homologues in the model filamentous fungus Aspergillus nidulans and characterized the S. cerevisiae Spa2 and Bud6 homologues, SpaA and BudA. Compared to the S. cerevisiae Spa2, SpaA lacks domain II but has three additional domains that are conserved within filamentous fungi. Gene replacement strains and localization studies show that SpaA functions exclusively at the hyphal tip, while BudA functions at sites of ec.asm.org septum formation and possibly at hyphal tips. We show that SpaA is not required for the assembly or maintenance of the Spitzenko¨rper. We propose that the core function of the polarisome in polarized growth is maintained but with different contributions of polarisome components to the process. at UNIV OF NEBRASKA-LINCOLN on September 18, 2007 The defining feature of filamentous fungi is the ability to branched actin filaments that form a cortical actin network form highly polarized hyphae capable of invading and explor- involved in endocytosis, and (iii) the polarisome, which con- ing new territory. The pivotal events that enable the formation trols the formation of actin cables that support the transport of of polarized hyphae are the specification and stabilization of an exocytic vesicles (61). axis of cell polarity. Despite recent progress, the molecular The polarisome was identified in S. cerevisiae as a 12S mul- mechanisms underlying these events remain poorly understood tiprotein complex that contains Spa2, Pea2, and Bud6/Aip3 in the filamentous fungi (22). With the completion of several and interacts with Bni1 (54). All polarisome components lo- fungal genome sequencing projects and the development of calize to the tips of growing buds and shmoos during polarized tools that facilitate the construction of null mutants, one ap- tip growth and the mother-bud neck during cytokinesis. Bni1 proach to addressing this problem is to characterize annotated (bud neck involved) is a formin with multiple domains that homologues of gene products known to be important for po- controls the localized assembly of actin cables (12, 48, 49) at larized growth in the yeast Saccharomyces cerevisiae. This ap- these sites. A bni1 deletion mutant is viable but has a spherical proach is based on the premise that S. cerevisiae provides a shape and a wider bud neck due to defects in polarization (42). strong paradigm for the basic mechanisms involved in the The proline-rich FH1 domain of Bni1 is responsible for bind- establishment and maintenance of hyphal polarity. ing profilin, a protein that sequesters ATP-bound G-actin and During the vegetative cycle in S. cerevisiae, the axial (i.e., thereby locally increases the concentration of actin monomer. Bud3, Bud4, and Bud10) and bipolar (Bud8, Bud9, Rax1, and The FH2 domain then catalyzes the addition of these mono- Rax2) landmark proteins direct the establishment of polarity mers to the barbed end of nascent actin filaments (38). The (6, 14, 31). They generate positional information that is rec- C-terminal Dia autoregulatory domain of Bni1 binds in an ognized by the Ras-related GTPase Bud1 and its associated intramolecular fashion to the N-terminal Rho-binding domain, regulators, Bud2 and Bud5. Activated Bud1 then triggers as- thereby inhibiting the actin-filament nucleation function of sembly of the polarity establishment machinery, in which the Bni1 (38). Autoinhibition is released upon the binding of a Rho-related GTPase Cdc42 plays a central role. In its GTP- GTP-bound Rho-GTPase with the Rho-binding domain. The bound active state, Cdc42 interacts with downstream effectors Rho-GTPases implicated in the activation of Bni1 include that include the p21-activated kinases Ste20 and Cla4 (46). In Cdc42 (11), Rho1 (30), as well as Rho3 and Rho4 (9). The less addition, activated Cdc42 recruits several protein complexes to conserved FH3 domain is proposed to be important for the polarization sites. These include the following: (i) the exocyst, localization of Bni1 (45). which is required for the localized fusion of vesicles with the plasma membrane, (ii) the Arp2/3 complex, which nucleates Spa2 (spindle pole associated) is a proposed scaffold protein that was originally identified as a protein that interacts with human anti-spindle pole autoantibodies (56). Spa2 deletion mutants form rounder cells and exhibit a significantly reduced * Corresponding author. Mailing address: Plant Science Initiative, capacity to generate pheromone-induced shmoos (15). As a University of Nebraska, N234 Beadle Center, Lincoln, NE 68588-0660. Phone: (402) 472-2938. Fax: (402) 472-3139. E-mail: sharri1@unlnotes scaffold protein, Spa2 interacts with numerous proteins, in- .unl.edu. cluding the other polarisome components (i.e., Bni1, Bud6/ 881 882 VIRAG AND HARRIS EUKARYOT.CELL TABLE 1. Strains used in this study Strain Genotype Source or reference A28 pabaA6 biA1 FGSC (accession no. A28) GR5 pyrG89 wA3 pyroA4 FGSC (accession no. A773) UI224 pyrG89 yA2 argB2 51 TN02A3 pyrG89 argB2 pyroA4 ⌬nkuA::argB 39 ASH630 pyrG89 wA3 sepA1 Lab collection AKS70 pyrG89 yA2 pabaA1 sepA::gfp::pyr-4 52 ACP115 pyrG89 wA3 pyroA4 tpmA::gfp::pyr-4 43 AHS11 pyrG89 wA3 pyroA4 tubA::gfp::pyr-4 Lab collection AAV1 pyrG89 spaA::gfp::pyr-4 wA3 pyroA4 This study AAV2 pyrG89 wA3 pyroA4 alcA(p)::gfp::budA::pyr-4 This study AAV9 pyrG89 ⌬spaA::pyr-4 wA3 pyroA4 This study AAV11 pyrG89 ⌬spaA::pyr-4 wA3 pyroA4 This study AAV12 pyrG89 yA2 spaA::gfp::argB argB2 This study AAV21 pyrG89 wA3 pyroA4 ⌬budA::pyro-A4 This study AAV64 pyrG89 wA3 argB2 pyroA4 This study Downloaded from AAV65 pyrG89 yA2 argB2 pyroA4 This study AAV85 pyrG89 ⌬spaA::pyr-4 wA3 pyroA4 tubA::gfp::pyr-4 This study AAV86 pyrG89 ⌬spaA::pyr-4 wA3 pyroA4 tpmA::gfp::pyr-4 This study AAV87 pyrG89 sepA::gfp::pyr-4 ⌬spaA::pyr-4 wA3 pyroA4 This study ec.asm.org Aip3, and Pea2), members of mitogen-activated protein kinase tants lack septa, possess abnormally wide hyphae that undergo pathways (i.e., Ste11, Ste7, Mkk1, Mkk2, and Slt2) (54, 60), abnormal apical branching, and display restricted colonial and actin-interacting proteins (i.e., Myo2, Myo1, and Pan1) growth. SepA-GFP localizes to the hyphal tip as a narrow (55). It is important to note that Spa2 and Bni1 have homo- crescent subtended by a dot and also forms a constricting ring at UNIV OF NEBRASKA-LINCOLN on September 18, 2007 logues, Sph1 (47) and Bnr1 (26), respectively, with whom they at sites of septum formation (52). The colocalization of SepA share overlapping functions. For example, the spa2⌬ sph1⌬ with actin at both hyphal tips and septation sites suggests a double deletion mutant is viable with a slightly exacerbated likely role in regulating the dynamics of actin structures (52). phenotype compared to that of either of the single deletion A structure that is present at the hyphal tip in fungi that form mutants (47), while the bni1⌬ bnr1⌬ double disruption mutant only true filaments, including A. nidulans, is the Spitzenko¨rper (3, shows a temperature-sensitive phenotype and is not viable at 24). The Spitzenko¨rper is an accumulation of vesicles and other the restrictive temperature (26). cell components that is present only at actively growing hyphal Two parallel screens, one for mutants defective in the bipo- tips. It is not clear whether the function of the Spitzenko¨rper lar pattern of bud site selection (65) and one for actin-inter- overlaps, and to what extent, with the function of the polarisome acting proteins (2), led to the identification of Bud6/Aip3 (bud in filamentous fungi (24, 61). site selection/actin-interacting protein). Besides the defect in To date, the only filamentous fungi in which Spa2 and Bud6 bipolar budding, bud6 deletion mutants have rounder vegeta- homologues have been characterized are Candida albicans and tive cells than the wild type does, a wider bud neck and bud Ashbya gossypii (8, 29, 66).
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