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Expanding functional repertoires of fungal peroxisomes: contribution to growth and survival processes.

Maruyama J, Kitamoto K - Front Physiol (2013)

Bottom Line: Peroxisomes were also recently found to play a vital role in the biosynthesis of biotin, which is an essential cofactor for various carboxylation and decarboxylation reactions.In plants, the BioF protein contains a conserved PTS1 motif and is also localized in peroxisomes.These findings indicate that the involvement of peroxisomes in biotin biosynthesis is evolutionarily conserved between fungi and plants, and that peroxisomes play a key role in fungal growth.

View Article: PubMed Central - PubMed

Affiliation: Department of Biotechnology, The University of Tokyo Tokyo, Japan.

ABSTRACT
It has long been regarded that the primary function of fungal peroxisomes is limited to the β-oxidation of fatty acids, as mutants lacking peroxisomal function fail to grow in minimal medium containing fatty acids as the sole carbon source. However, studies in filamentous fungi have revealed that peroxisomes have diverse functional repertoires. This review describes the essential roles of peroxisomes in the growth and survival processes of filamentous fungi. One such survival mechanism involves the Woronin body, a Pezizomycotina-specific organelle that plugs the septal pore upon hyphal lysis to prevent excessive cytoplasmic loss. A number of reports have demonstrated that Woronin bodies are derived from peroxisomes. Specifically, the Woronin body protein Hex1 is targeted to peroxisomes by peroxisomal targeting sequence 1 (PTS1) and forms a self-assembled structure that buds from peroxisomes to form the Woronin body. Peroxisomal deficiency reduces the ability of filamentous fungi to prevent excessive cytoplasmic loss upon hyphal lysis, indicating that peroxisomes contribute to the survival of these multicellular organisms. Peroxisomes were also recently found to play a vital role in the biosynthesis of biotin, which is an essential cofactor for various carboxylation and decarboxylation reactions. In biotin-prototrophic fungi, peroxisome-deficient mutants exhibit growth defects when grown on glucose as a carbon source due to biotin auxotrophy. The biotin biosynthetic enzyme BioF (7-keto-8-aminopelargonic acid synthase) contains a PTS1 motif that is required for both peroxisomal targeting and biotin biosynthesis. In plants, the BioF protein contains a conserved PTS1 motif and is also localized in peroxisomes. These findings indicate that the involvement of peroxisomes in biotin biosynthesis is evolutionarily conserved between fungi and plants, and that peroxisomes play a key role in fungal growth.

No MeSH data available.


Related in: MedlinePlus

Differentiation of the Woronin body from peroxisomes. (A) Fluorescence microscopic analysis of wild-type and Δpex11 strains of A. oryzae expressing EGFP-PTS1 and mDsRed-AoHex1 fusion proteins for visualization of peroxisomes and the major Woronin body protein, respectively (Escaño et al., 2009). Asterisks denote septa and arrows indicate Woronin bodies (red) independent of peroxisomes (green). Arrowheads represent assembly of Hex1 attached to the matrix side of the peroxisome. Bars: 5 μm. (B) Schematic model of Woronin body differentiation from peroxisomes.
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Figure 3: Differentiation of the Woronin body from peroxisomes. (A) Fluorescence microscopic analysis of wild-type and Δpex11 strains of A. oryzae expressing EGFP-PTS1 and mDsRed-AoHex1 fusion proteins for visualization of peroxisomes and the major Woronin body protein, respectively (Escaño et al., 2009). Asterisks denote septa and arrows indicate Woronin bodies (red) independent of peroxisomes (green). Arrowheads represent assembly of Hex1 attached to the matrix side of the peroxisome. Bars: 5 μm. (B) Schematic model of Woronin body differentiation from peroxisomes.

Mentions: A relationship between peroxisomes and the Woronin body is suggested from the fact that Hex1 contains peroxisomal targeting signal sequence 1 (PTS1) at the C-terminus (Jedd and Chua, 2000). Time-lapse imaging demonstrated that Woronin bodies bud from peroxisomes in N. crassa (Tey et al., 2005) and that Woronin body biogenesis requires the presence of peroxins that mediate peroxisomal protein import (Ramos-Pamplona and Naqvi, 2006; Managadze et al., 2007; Liu et al., 2008). The peripheral membrane peroxisomal protein Pex11 is implicated in peroxisomal proliferation and division (Erdmann and Blobel, 1995; Marshall et al., 1995), and in the absence of Pex11, filamentous fungi only contain few enlarged peroxisomes (Figure 3A, EGFP-PTS1) (Hynes et al., 2008; Escaño et al., 2009; Opaliński et al., 2012). It was also demonstrated that ability of Pex11-deficient strain of A. oryzae to prevent the excessive loss of cytoplasm is reduced by ~30% compared to wild type (Escaño et al., 2009), indicating that Pex11 is involved in Woronin body function. Under fluorescence microscopy, Woronin bodies are typically observed as small dots independent of peroxisomes (Figure 3A, mDsRed-AoHex1). In the absence of Pex11, however, the Woronin body protein Hex1 forms a structure that attaches to the matrix side of the peroxisomal membrane, but the mature Woronin body fails to differentiate from peroxisomes (Figure 3A) (Escaño et al., 2009). The Pezizomycotina-specific protein WSC (Woronin body sorting complex) recruits the Hex1 assembly to the matrix side of the peroxisomal membrane and facilitates the budding of the Woronin body (Liu et al., 2008). It has been suggested that Pex11 elongates the peroxisomal membrane to facilitate the division of peroxisomes by dynamin-related proteins (Koch et al., 2003, 2004; Schrader, 2006). Heterologous expression of Hex1 in the yeast Saccharomyces cerevisiae suggested that dynamin-related proteins participate in the budding of Woronin bodies from peroxisomes (Würtz et al., 2008). ApsB, a component of the microtubule-organizing center (MTOC), has been shown to interact with Hex1 and to localize to peroxisomes via peroxisomal targeting signal sequence 2 (PTS2) (Zekert et al., 2010). Hex1 physically associates with the essential matrix import peroxin Pex26 and promotes the enrichment of Pex26 in the membranes of differentiated peroxisomes (Liu et al., 2011). After Woronin bodies differentiate from peroxisomes, evidence suggests that the Pezizomycotina-specific protein Leashin (LAH) tethers the Woronin bodies to the vicinity of the septum (Ng et al., 2009). A schematic model of Woronin body differentiation from peroxisomes is presented in Figure 3B. Although a number of proteins functionally/spatially related to the Woronin body have been identified (Engh et al., 2007; Fleissner and Glass, 2007; Kim et al., 2009; Maruyama et al., 2010; Lai et al., 2012; Yu et al., 2012), the molecular mechanism for Woronin body biogenesis remains to be completely resolved.


Expanding functional repertoires of fungal peroxisomes: contribution to growth and survival processes.

Maruyama J, Kitamoto K - Front Physiol (2013)

Differentiation of the Woronin body from peroxisomes. (A) Fluorescence microscopic analysis of wild-type and Δpex11 strains of A. oryzae expressing EGFP-PTS1 and mDsRed-AoHex1 fusion proteins for visualization of peroxisomes and the major Woronin body protein, respectively (Escaño et al., 2009). Asterisks denote septa and arrows indicate Woronin bodies (red) independent of peroxisomes (green). Arrowheads represent assembly of Hex1 attached to the matrix side of the peroxisome. Bars: 5 μm. (B) Schematic model of Woronin body differentiation from peroxisomes.
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
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Figure 3: Differentiation of the Woronin body from peroxisomes. (A) Fluorescence microscopic analysis of wild-type and Δpex11 strains of A. oryzae expressing EGFP-PTS1 and mDsRed-AoHex1 fusion proteins for visualization of peroxisomes and the major Woronin body protein, respectively (Escaño et al., 2009). Asterisks denote septa and arrows indicate Woronin bodies (red) independent of peroxisomes (green). Arrowheads represent assembly of Hex1 attached to the matrix side of the peroxisome. Bars: 5 μm. (B) Schematic model of Woronin body differentiation from peroxisomes.
Mentions: A relationship between peroxisomes and the Woronin body is suggested from the fact that Hex1 contains peroxisomal targeting signal sequence 1 (PTS1) at the C-terminus (Jedd and Chua, 2000). Time-lapse imaging demonstrated that Woronin bodies bud from peroxisomes in N. crassa (Tey et al., 2005) and that Woronin body biogenesis requires the presence of peroxins that mediate peroxisomal protein import (Ramos-Pamplona and Naqvi, 2006; Managadze et al., 2007; Liu et al., 2008). The peripheral membrane peroxisomal protein Pex11 is implicated in peroxisomal proliferation and division (Erdmann and Blobel, 1995; Marshall et al., 1995), and in the absence of Pex11, filamentous fungi only contain few enlarged peroxisomes (Figure 3A, EGFP-PTS1) (Hynes et al., 2008; Escaño et al., 2009; Opaliński et al., 2012). It was also demonstrated that ability of Pex11-deficient strain of A. oryzae to prevent the excessive loss of cytoplasm is reduced by ~30% compared to wild type (Escaño et al., 2009), indicating that Pex11 is involved in Woronin body function. Under fluorescence microscopy, Woronin bodies are typically observed as small dots independent of peroxisomes (Figure 3A, mDsRed-AoHex1). In the absence of Pex11, however, the Woronin body protein Hex1 forms a structure that attaches to the matrix side of the peroxisomal membrane, but the mature Woronin body fails to differentiate from peroxisomes (Figure 3A) (Escaño et al., 2009). The Pezizomycotina-specific protein WSC (Woronin body sorting complex) recruits the Hex1 assembly to the matrix side of the peroxisomal membrane and facilitates the budding of the Woronin body (Liu et al., 2008). It has been suggested that Pex11 elongates the peroxisomal membrane to facilitate the division of peroxisomes by dynamin-related proteins (Koch et al., 2003, 2004; Schrader, 2006). Heterologous expression of Hex1 in the yeast Saccharomyces cerevisiae suggested that dynamin-related proteins participate in the budding of Woronin bodies from peroxisomes (Würtz et al., 2008). ApsB, a component of the microtubule-organizing center (MTOC), has been shown to interact with Hex1 and to localize to peroxisomes via peroxisomal targeting signal sequence 2 (PTS2) (Zekert et al., 2010). Hex1 physically associates with the essential matrix import peroxin Pex26 and promotes the enrichment of Pex26 in the membranes of differentiated peroxisomes (Liu et al., 2011). After Woronin bodies differentiate from peroxisomes, evidence suggests that the Pezizomycotina-specific protein Leashin (LAH) tethers the Woronin bodies to the vicinity of the septum (Ng et al., 2009). A schematic model of Woronin body differentiation from peroxisomes is presented in Figure 3B. Although a number of proteins functionally/spatially related to the Woronin body have been identified (Engh et al., 2007; Fleissner and Glass, 2007; Kim et al., 2009; Maruyama et al., 2010; Lai et al., 2012; Yu et al., 2012), the molecular mechanism for Woronin body biogenesis remains to be completely resolved.

Bottom Line: Peroxisomes were also recently found to play a vital role in the biosynthesis of biotin, which is an essential cofactor for various carboxylation and decarboxylation reactions.In plants, the BioF protein contains a conserved PTS1 motif and is also localized in peroxisomes.These findings indicate that the involvement of peroxisomes in biotin biosynthesis is evolutionarily conserved between fungi and plants, and that peroxisomes play a key role in fungal growth.

View Article: PubMed Central - PubMed

Affiliation: Department of Biotechnology, The University of Tokyo Tokyo, Japan.

ABSTRACT
It has long been regarded that the primary function of fungal peroxisomes is limited to the β-oxidation of fatty acids, as mutants lacking peroxisomal function fail to grow in minimal medium containing fatty acids as the sole carbon source. However, studies in filamentous fungi have revealed that peroxisomes have diverse functional repertoires. This review describes the essential roles of peroxisomes in the growth and survival processes of filamentous fungi. One such survival mechanism involves the Woronin body, a Pezizomycotina-specific organelle that plugs the septal pore upon hyphal lysis to prevent excessive cytoplasmic loss. A number of reports have demonstrated that Woronin bodies are derived from peroxisomes. Specifically, the Woronin body protein Hex1 is targeted to peroxisomes by peroxisomal targeting sequence 1 (PTS1) and forms a self-assembled structure that buds from peroxisomes to form the Woronin body. Peroxisomal deficiency reduces the ability of filamentous fungi to prevent excessive cytoplasmic loss upon hyphal lysis, indicating that peroxisomes contribute to the survival of these multicellular organisms. Peroxisomes were also recently found to play a vital role in the biosynthesis of biotin, which is an essential cofactor for various carboxylation and decarboxylation reactions. In biotin-prototrophic fungi, peroxisome-deficient mutants exhibit growth defects when grown on glucose as a carbon source due to biotin auxotrophy. The biotin biosynthetic enzyme BioF (7-keto-8-aminopelargonic acid synthase) contains a PTS1 motif that is required for both peroxisomal targeting and biotin biosynthesis. In plants, the BioF protein contains a conserved PTS1 motif and is also localized in peroxisomes. These findings indicate that the involvement of peroxisomes in biotin biosynthesis is evolutionarily conserved between fungi and plants, and that peroxisomes play a key role in fungal growth.

No MeSH data available.


Related in: MedlinePlus