Peroxisomes in Filamentous Fungi

Leonardo Peraza-Reyes; Eric Espagne; Sylvie Arnaise; Véronique Berteaux-Lecellier*

doi:10.1128/9781555816636.ch15

Chapter 15 : Peroxisomes in Filamentous Fungi

Authors: Leonardo Peraza-Reyes¹, Eric Espagne², Sylvie Arnaise³, Véronique Berteaux-Lecellier*⁴

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Affiliations: 1: Institut de Génétique et Microbiologie, UMR8621, Université Paris-Sud, F-9140 Orsay France; Institut de Génétique et Microbiologie, UMR8621, CNRS, F-91405 Orsay, France; 2: Institut de Génétique et Microbiologie, UMR8621, Université Paris-Sud, F-9140 Orsay France; Institut de Génétique et Microbiologie, UMR8621, CNRS, F-91405 Orsay, France; 3: Institut de Génétique et Microbiologie, UMR8621, Université Paris-Sud, F-9140 Orsay France; Institut de Génétique et Microbiologie, UMR8621, CNRS, F-91405 Orsay, France; 4: Institut de Génétique et Microbiologie, UMR8621, Université Paris-Sud, F-9140 Orsay France; Institut de Génétique et Microbiologie, UMR8621, CNRS, F-91405 Orsay, France

Content Type: Monograph

Publication Year: 2010

Category: Microbial Genetics and Molecular Biology; Fungi and Fungal Pathogenesis

Book DOI: 10.1128/9781555816636

Chapter DOI: 10.1128/9781555816636.ch15

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Abstract:

This chapter presents an overview summarizing the current knowledge of the function of peroxisomes in filamentous fungi. Peroxisome formation among diverse eukaryotic organisms shares a common basic biogenetic process mediated by a number of conserved proteins known as peroxins. At the start of photosynthesis, peroxisome metabolism plays an important role in photorespiration, and peroxisomes have thus been described as "leaf peroxisomes". The chapter mentions the main metabolic peroxisomal functions of fungi, with emphasis on those that are particular to, and have been characterized more fully in, filamentous fungi. Plants, yeasts, and filamentous fungi display a wide spectrum of peroxisomal activities, mainly due to the existence of peroxisome-specific function. In addition to the fruiting-body constitution, peroxisomes also participate in differentiation processes taking place in the fertile portion (centrum) of these structures. P. anserina strains lacking the peroxisome-targeting signal (PTS) receptors peroxisomal matrix 5 (PEX5) and PEX7 exhibit abnormal formation of asci, resulting in ascospores with uneven numbers of nuclei or spores with no nuclei. The second centrum developmental event in which peroxisomes are involved in P. anserina is the transition from the prekaryogamy mitotic phase to the karyogamy and meiotic phase. In spite of the progress made in understanding peroxisome function in fungi, a detailed picture of how peroxisomes affect several other metabolic and developmental processes remains elusive. Further innovative approaches are required to fully understand the function of this organelle in fungi.

Citation: Peraza-Reyes L, Espagne E, Arnaise S, Berteaux-Lecellier* V. 2010. Peroxisomes in Filamentous Fungi, p 191-206. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch15

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Peroxisomes in Filamentous Fungi

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/content/10.1128/9781555816636.ch15.ch15fig01

FIGURE 1

Schematic representation of the putative peroxisome matrix protein import pathway in filamentous fungi. The recognition of the peroxisomal matrix proteins by Pex5 and Pex7 receptors occurs in the cytosol (Pex5 and Pex7 recognize PTS1 and PTS2, respectively); the cargo-receptor complexes then dock at the peroxisomal membrane (where both import pathways converge) and are then translocated. These last processes require the importomer, which is composed of two subcomplexes linked by Pex8: the docking complex (formed by Pex14, Pex13, and Pex14/17) and the RING finger complex (formed by Pex2, Pex10, and Pex12). After cargo release in the peroxisomal matrix, Pex5 receptors are either monoubiquitinated (by Pex4) or polyubiquitinated (by Ubc4). The release of the Pex5 ubiquitinated form requires Pex1 and Pex6, AAA-type ATPases anchored in the peroxisomal membrane by Pex26. When polyubiquitinated, Pex5 receptors are then degraded by the proteasome; when monoubiquitinated, they are recycled back to engage in another round of import. The asterisk in “Pex22*” denotes that in filamentous fungus genomes a Pex22-like protein is usually present rather than a true Pex22 ortholog (see also Table 1 ).

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FIGURE 1

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FIGURE 2

Woronin bodies. The WB is a specialized peroxisome of filamentous fungi that function in sealing the septal pores that communicate hyphal compartments. (A) P. anserina WBs delimiting apical cells of paraphysae are indicated by arrows; note the recently formed WBs at the tip of the cell (arrowheads). (B) Corresponding DAPI (4’,6-diamidino-2-phenylindole)-stained micrograph. Arrows indicate the positions of the septal pores. (C) In fungi like N. crassa, the WB structural lattice is reflected by the hexagonal shape that WBs adopt. In the image, two WBs (arrows) before plugging a septal pore are shown (note that the septal pore is not in the same plane as WBs and is not visible here). P. anserina WBs were stained by anti-hex1 antibody, a kind gift from G. Jedd. The transmission electron micrograph in panel C was done by Jorge Sepulveda and L. Peraza-Reyes, courtesy of Wilhelm Hansberg’s laboratory (UNAM, Mexico). Scale bars, 5 μm (panels A and B) and 500 nm (panel C).

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FIGURE 2

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FIGURE 3

Peroxisome dynamics in filamentous fungi. Peroxisomes are highly dynamic organelles in filamentous fungi. They are typically round (A), but their number, form, and distribution can vary according to specific metabolical mycelial demands (A to C); during the formation of differentiated cells, such as during ascus development (panel D: observe the accumulation of peroxisomes at the growing apex of an ascus); between different cell types (panel E: compare the peroxisome shape in paraphysae [asexual cells present in fruiting bodies], shown by an arrow, and in asci, shown by arrowheads); and during spore formation (panel F: note the high peroxi-some number resulting from the intense peroxisome proliferation occurring during ascospore formation). Images show peroxisomes of P. anserina. Peroxisomes were stained by the GFP-SKL reporter system ( Ruprich-Robert et al., 2002 ); images were done in collaboration with D. Zickler. Scale bars, 5 μm.

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FIGURE 3

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Tables

Peroxisomes in Filamentous Fungi

/content/10.1128/9781555816636.ch15.ch15tab01

TABLE 1

Predicted peroxins of P. anserinaa

TABLE 1

Predicted peroxins of P. anserinaa