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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

Phylogenetic relationship and peroxisomal localization of plant BioF proteins. (A) Phylogenetic analysis of plant BioF proteins (Maruyama et al., 2012). The amino acid residues of C-terminal peroxisomal targeting signals (PTS1) are indicated by open boxes. The full-length amino acid sequences of the plant BioF proteins were aligned using the method described in Figure 5. The Genbank accession numbers for the sequences used in the analysis are as follows: Arabidopsis thaliana, NP_974731.1; Arabidopsis lyrata, XP_002871105.1; Oryza sativa-1, BAD87813.1; Oryza sativa-2, NP_001065381.1; Hordeum vulgare, BAK03504.1; Brachypodium distachyon, XP_003574335.1; Sorgham bicolor, XP_002467492.1; Zea mays-1, ACG35792.1; Zea mays-2, ACG35881.1; Selaginella moellendorffii-1, XP_002969752.1; Selaginella moellendorffii-2, XP_002981364.1; Physcomitrella patens, XP_001769874.1; Picea sitchensis, ABR18106.1; Vinis vinifera, XP_002268950.1; Medicago truncatula, XP_003598166.1; Glycine max-1, XP_003527547.1; and Glycine max-2, XP_003522881.1. The amino acid sequence of the BioF protein of Marchantia polymorpha was confirmed by PCR amplification and cDNA sequencing based on information obtained from the Marchantia expression sequence tag database (Maruyama et al., 2012). (B) Peroxisomal localization of plant BioF protein. Note that BioF (EGFP-BioF-PTS1) co-localizes with the peroxisomes (PTS2-mRFP1), but disperses in the absence of PTS1 (EGFP-BioF-ΔPTS1) (Tanabe et al., 2011). Bars: 5 μm.
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Figure 7: Phylogenetic relationship and peroxisomal localization of plant BioF proteins. (A) Phylogenetic analysis of plant BioF proteins (Maruyama et al., 2012). The amino acid residues of C-terminal peroxisomal targeting signals (PTS1) are indicated by open boxes. The full-length amino acid sequences of the plant BioF proteins were aligned using the method described in Figure 5. The Genbank accession numbers for the sequences used in the analysis are as follows: Arabidopsis thaliana, NP_974731.1; Arabidopsis lyrata, XP_002871105.1; Oryza sativa-1, BAD87813.1; Oryza sativa-2, NP_001065381.1; Hordeum vulgare, BAK03504.1; Brachypodium distachyon, XP_003574335.1; Sorgham bicolor, XP_002467492.1; Zea mays-1, ACG35792.1; Zea mays-2, ACG35881.1; Selaginella moellendorffii-1, XP_002969752.1; Selaginella moellendorffii-2, XP_002981364.1; Physcomitrella patens, XP_001769874.1; Picea sitchensis, ABR18106.1; Vinis vinifera, XP_002268950.1; Medicago truncatula, XP_003598166.1; Glycine max-1, XP_003527547.1; and Glycine max-2, XP_003522881.1. The amino acid sequence of the BioF protein of Marchantia polymorpha was confirmed by PCR amplification and cDNA sequencing based on information obtained from the Marchantia expression sequence tag database (Maruyama et al., 2012). (B) Peroxisomal localization of plant BioF protein. Note that BioF (EGFP-BioF-PTS1) co-localizes with the peroxisomes (PTS2-mRFP1), but disperses in the absence of PTS1 (EGFP-BioF-ΔPTS1) (Tanabe et al., 2011). Bars: 5 μm.

Mentions: As described above, plant BioF protein functions as a KAPA synthase and was shown to be cytosolic by GFP fusion at the C-terminus (Pinon et al., 2005). Phylogenetic analysis revealed that BioF proteins from various plant species possess PTS1 at the C-terminus (Figure 7A) (Tanabe et al., 2011; Maruyama et al., 2012), suggesting that the peroxisomal localization of BioF proteins is conserved throughout the plant kingdom. An N-terminal GFP-BioF fusion protein co-localizes with peroxisomes, and deletion of PTS1 causes cytosolic localization, suggesting that BioF is localized to peroxisomes via the PTS1 sequence (Figure 7B) (Tanabe et al., 2011).


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

Maruyama J, Kitamoto K - Front Physiol (2013)

Phylogenetic relationship and peroxisomal localization of plant BioF proteins. (A) Phylogenetic analysis of plant BioF proteins (Maruyama et al., 2012). The amino acid residues of C-terminal peroxisomal targeting signals (PTS1) are indicated by open boxes. The full-length amino acid sequences of the plant BioF proteins were aligned using the method described in Figure 5. The Genbank accession numbers for the sequences used in the analysis are as follows: Arabidopsis thaliana, NP_974731.1; Arabidopsis lyrata, XP_002871105.1; Oryza sativa-1, BAD87813.1; Oryza sativa-2, NP_001065381.1; Hordeum vulgare, BAK03504.1; Brachypodium distachyon, XP_003574335.1; Sorgham bicolor, XP_002467492.1; Zea mays-1, ACG35792.1; Zea mays-2, ACG35881.1; Selaginella moellendorffii-1, XP_002969752.1; Selaginella moellendorffii-2, XP_002981364.1; Physcomitrella patens, XP_001769874.1; Picea sitchensis, ABR18106.1; Vinis vinifera, XP_002268950.1; Medicago truncatula, XP_003598166.1; Glycine max-1, XP_003527547.1; and Glycine max-2, XP_003522881.1. The amino acid sequence of the BioF protein of Marchantia polymorpha was confirmed by PCR amplification and cDNA sequencing based on information obtained from the Marchantia expression sequence tag database (Maruyama et al., 2012). (B) Peroxisomal localization of plant BioF protein. Note that BioF (EGFP-BioF-PTS1) co-localizes with the peroxisomes (PTS2-mRFP1), but disperses in the absence of PTS1 (EGFP-BioF-ΔPTS1) (Tanabe et al., 2011). Bars: 5 μm.
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Figure 7: Phylogenetic relationship and peroxisomal localization of plant BioF proteins. (A) Phylogenetic analysis of plant BioF proteins (Maruyama et al., 2012). The amino acid residues of C-terminal peroxisomal targeting signals (PTS1) are indicated by open boxes. The full-length amino acid sequences of the plant BioF proteins were aligned using the method described in Figure 5. The Genbank accession numbers for the sequences used in the analysis are as follows: Arabidopsis thaliana, NP_974731.1; Arabidopsis lyrata, XP_002871105.1; Oryza sativa-1, BAD87813.1; Oryza sativa-2, NP_001065381.1; Hordeum vulgare, BAK03504.1; Brachypodium distachyon, XP_003574335.1; Sorgham bicolor, XP_002467492.1; Zea mays-1, ACG35792.1; Zea mays-2, ACG35881.1; Selaginella moellendorffii-1, XP_002969752.1; Selaginella moellendorffii-2, XP_002981364.1; Physcomitrella patens, XP_001769874.1; Picea sitchensis, ABR18106.1; Vinis vinifera, XP_002268950.1; Medicago truncatula, XP_003598166.1; Glycine max-1, XP_003527547.1; and Glycine max-2, XP_003522881.1. The amino acid sequence of the BioF protein of Marchantia polymorpha was confirmed by PCR amplification and cDNA sequencing based on information obtained from the Marchantia expression sequence tag database (Maruyama et al., 2012). (B) Peroxisomal localization of plant BioF protein. Note that BioF (EGFP-BioF-PTS1) co-localizes with the peroxisomes (PTS2-mRFP1), but disperses in the absence of PTS1 (EGFP-BioF-ΔPTS1) (Tanabe et al., 2011). Bars: 5 μm.
Mentions: As described above, plant BioF protein functions as a KAPA synthase and was shown to be cytosolic by GFP fusion at the C-terminus (Pinon et al., 2005). Phylogenetic analysis revealed that BioF proteins from various plant species possess PTS1 at the C-terminus (Figure 7A) (Tanabe et al., 2011; Maruyama et al., 2012), suggesting that the peroxisomal localization of BioF proteins is conserved throughout the plant kingdom. An N-terminal GFP-BioF fusion protein co-localizes with peroxisomes, and deletion of PTS1 causes cytosolic localization, suggesting that BioF is localized to peroxisomes via the PTS1 sequence (Figure 7B) (Tanabe et al., 2011).

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