A newly discovered function of peroxisomes: Involvement in biotin biosynthesis

Plant Signaling and Behavior

Volumn 7, Issue 12, 2012, Pages 1589-1593

  Maruyama, Jun Ichi ^a   Yamaoka, Shohei ^c   Matsuo, Ichiro ^d   Tsutsumi, Nobuhiro ^b   Kitamoto, Katsuhiko ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d GUNMA UNIVERSITY   (Japan)

Author keywords

Biotin; Embryo development; Fungi; Mitochondria; Peroxisome

Indexed keywords

BIOTIN;

BIOSYNTHESIS; FUNGUS; METABOLISM; MITOCHONDRION; PEROXISOME;

BIOTIN; FUNGI; MITOCHONDRIA; PEROXISOMES;

EID: 84871253265     PISSN: 15592316     EISSN: 15592324     Source Type: Journal    
DOI: 10.4161/psb.22405     Document Type: Article

References (50)

1. Mano S, Nishimura M. Plant peroxisomes. Vitam Horm 2005; 72:111-54; PMID:16492470; http://dx.doi.org/10.1016/S0083-6729(05)72004-5.
2. Nishimura M, Hayashi M, Kato A, Yamaguchi K, Mano S. Functional transformation of microbodies in higher plant cells. Cell Struct Funct 1996; 21:387-93; PMID:9118245; http://dx.doi.org/10.1247/csf.21.387.
3. Reumann S, Weber AP. Plant peroxisomes respire in the light: some gaps of the photorespiratory C2 cycle have become filled-others remain. Biochim Biophys Acta 2006; 1763:1496-510.
4. Weber H. Fatty acid-derived signals in plants. Trends Plant Sci 2002; 7:217-24; PMID:11992827; http://dx.doi.org/10.1016/S1360-1385(02)02250-1.
5. Woodward AW, Bartel B. Auxin: regulation, action, and interaction. Ann Bot 2005; 95:707-35; PMID:15749753; http://dx.doi.org/10.1093/aob/mci083.
6. Hu J, Aguirre M, Peto C, Alonso J, Ecker J, Chory J. A role for peroxisomes in photomorphogenesis and development of Arabidopsis. Science 2002; 297:405-9; PMID:12130786; http://dx.doi.org/10.1126/science.1073633.
7. Schumann U, Wanner G, Veenhuis M, Schmid M, Gietl C. AthPEX10, a nuclear gene essential for peroxisome and storage organelle formation during Arabidopsis embryogenesis. Proc Natl Acad Sci U S A 2003; 100:9626-31; PMID:12883010; http://dx.doi.org/10.1073/pnas.1633697100.
8. Sparkes IA, Brandizzi F, Slocombe SP, El-Shami M, Hawes C, Baker A. An Arabidopsis pex10 null mutant is embryo lethal, implicating peroxisomes in an essential role during plant embryogenesis. Plant Physiol 2003; 133:1809-19; PMID:14576288; http://dx.doi.org/10.1104/pp.103.031252.
9. Tzafrir I, Pena-Muralla R, Dickerman A, Berg M, Rogers R, Hutchens S, et al. Identification of genes required for embryo development in Arabidopsis. Plant Physiol 2004; 135:1206-20; PMID:15266054; http://dx.doi.org/10.1104/pp.104.045179.
10. Fan J, Quan S, Orth T, Awai C, Chory J, Hu J. The Arabidopsis PEX12 gene is required for peroxisome biogenesis and is essential for development. Plant Physiol 2005; 139:231-9; PMID:16113209; http://dx.doi.org/10.1104/pp.105.066811.
11. Nito K, Hayashi M, Nishimura M. Direct interaction and determination of binding domains among peroxisomal import factors in Arabidopsis thaliana. Plant Cell Physiol 2002; 43:355-66; PMID:11978862; http://dx.doi.org/10.1093/pcp/pcf057.
12. Hayashi M, Yagi M, Nito K, Kamada T, Nishimura M. Differential contribution of two peroxisomal protein receptors to the maintenance of peroxisomal functions in Arabidopsis. J Biol Chem 2005; 280:14829-35; PMID:15637057; http://dx.doi.org/10.1074/jbc.M411005200.
13. Woodward AW, Bartel B. The Arabidopsis peroxisomal targeting signal type 2 receptor PEX7 is necessary for peroxisome function and dependent on PEX5. Mol Biol Cell 2005; 16:573-83; PMID:15548601; http://dx.doi.org/10.1091/mbc.E04-05-0422.
14. Khan BR, Zolman BK. pex5 Mutants that differentially disrupt PTS1 and PTS2 peroxisomal matrix protein import in Arabidopsis. Plant Physiol 2010; 154:1602-15; PMID:20974890; http://dx.doi.org/10.1104/pp.110.162479.
15. Mano S, Nakamori C, Nito K, Kondo M, Nishimura M. The Arabidopsis pex12 and pex13 mutants are defective in both PTS1-and PTS2-dependent protein transport to peroxisomes. Plant J 2006; 47:604-18; PMID:16813573; http://dx.doi.org/10.1111/j.1365-313X.2006.02809.x.
16. Helm M, Lück C, Prestele J, Hierl G, Huesgen PF, Fröhlich T, et al. Dual specificities of the glyoxysomal/peroxisomal processing protease Deg15 in higher plants. Proc Natl Acad Sci U S A 2007; 104:11501-6; PMID:17592111; http://dx.doi.org/10.1073/pnas.0704733104.
17. Schuhmann H, Huesgen PF, Gietl C, Adamska I. The DEG15 serine protease cleaves peroxisomal targeting signal 2-containing proteins in Arabidopsis. Plant Physiol 2008; 148:1847-56; PMID:18952862; http://dx.doi.org/10.1104/pp.108.125377.
18. Lingard MJ, Bartel B. Arabidopsis LON2 is necessary for peroxisomal function and sustained matrix protein import. Plant Physiol 2009; 151:1354-65; PMID:19748917; http://dx.doi.org/10.1104/pp.109.142505.
19. Ratzel SE, Lingard MJ, Woodward AW, Bartel B. Reducing PEX13 expression ameliorates physiological defects of late-acting peroxin mutants. Traffic 2011; 12:121-34; PMID:20969679; http://dx.doi.org/10.1111/j.1600-0854.2010.01136.x.
20. Hu J, Baker A, Bartel B, Linka N, Mullen RT, Reumann S, et al. Plant peroxisomes: biogenesis and function. Plant Cell 2012; 24:2279-303; PMID:22669882; http://dx.doi.org/10.1105/tpc.112.096586.
21. Zolman BK, Monroe-Augustus M, Silva ID, Bartel B. Identification and functional characterization of Arabidopsis PEROXIN4 and the interacting protein PEROXIN22. Plant Cell 2005; 17:3422-35; PMID:16272432; http://dx.doi.org/10.1105/tpc.105.035691.
22. Nito K, Kamigaki A, Kondo M, Hayashi M, Nishimura M. Functional classification of Arabidopsis peroxisome biogenesis factors proposed from analyses of knockdown mutants. Plant Cell Physiol 2007; 48:763-74; PMID:17478547; http://dx.doi.org/10.1093/pcp/pcm053.
23. Goto S, Mano S, Nakamori C, Nishimura M. Arabidopsis ABERRANT PEROXISOME MORPHOLOGY9 is a peroxin that recruits the PEX1-PEX6 complex to peroxisomes. Plant Cell 2011; 23:1573-87; PMID:21487094; http://dx.doi.org/10.1105/tpc.110.080770.
24. Zolman BK, Bartel B. An Arabidopsis indole-3-butyric acid-response mutant defective in PEROXIN6, an apparent ATPase implicated in peroxisomal function. Proc Natl Acad Sci U S A 2004; 101:1786-91; PMID:14745029; http://dx.doi.org/10.1073/pnas.0304368101.
25. Lingard MJ, Monroe-Augustus M, Bartel B. Peroxisome-associated matrix protein degradation in Arabidopsis. Proc Natl Acad Sci U S A 2009; 106:4561-6; PMID:19246395; http://dx.doi.org/10.1073/pnas.0811329106.
26. Erdmann R, Veenhuis M, Mertens D, Kunau WH. Isolation of peroxisome-deficient mutants of Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 1989; 86:5419-23; PMID:2568633; http://dx.doi.org/10.1073/pnas.86.14.5419.
27. Hynes MJ, Murray SL, Khew GS, Davis MA. Genetic analysis of the role of peroxisomes in the utilization of acetate and fatty acids in Aspergillus nidulans. Genetics 2008; 178:1355-69; PMID:18245820; http://dx.doi.org/10.1534/genetics.107.085795.
28. van der Klei IJ, Yurimoto H, Sakai Y, Veenhuis M. The significance of peroxisomes in methanol metabolism in methylotrophic yeast. Biochim Biophys Acta 2006; 1763:1453-62.
29. Bartoszewska M, Opaliński L, Veenhuis M, van der Klei IJ. The significance of peroxisomes in secondary metabolite biosynthesis in filamentous fungi. Biotechnol Lett 2011; 33:1921-31; PMID:21660569; http://dx.doi.org/10.1007/s10529-011-0664-y.
30. Kimura A, Takano Y, Furusawa I, Okuno T. Peroxisomal metabolic function is required for appressorium-mediated plant infection by Colletotrichum lagenarium. Plant Cell 2001; 13:1945-57; PMID:11487704.
31. Asakura M, Okuno T, Takano Y. Multiple contributions of peroxisomal metabolic function to fungal pathogenicity in Colletotrichum lagenarium. Appl Environ Microbiol 2006; 72:6345-54; PMID:16957261; http://dx.doi.org/10.1128/AEM.00988-06.
32. Bonnet C, Espagne E, Zickler D, Boisnard S, Bourdais A, Berteaux-Lecellier V. The peroxisomal import proteins PEX2, PEX5 and PEX7 are differently involved in Podospora anserina sexual cycle. Mol Microbiol 2006; 62:157-69; PMID:16987176; http://dx.doi.org/10.1111/j.1365-2958.2006.05353.x.
33. Peraza-Reyes L, Zickler D, Berteaux-Lecellier V. The peroxisome RING-finger complex is required for meiocyte formation in the fungus Podospora anserina. Traffic 2008; 9:1998-2009; PMID:18785921; http://dx.doi.org/10.1111/j.1600-0854.2008.00812.x.
34. Liu F, Ng SK, Lu Y, Low W, Lai J, Jedd G. Making two organelles from one: Woronin body biogenesis by peroxisomal protein sorting. J Cell Biol 2008; 180:325-39; PMID:18227279; http://dx.doi.org/10.1083/jcb.200705049.
35. Escaño CS, Juvvadi PR, Jin FJ, Takahashi T, Koyama Y, Yamashita S, et al. Disruption of the Aopex11-1 gene involved in peroxisome proliferation leads to impaired Woronin body formation in Aspergillus oryzae. Eukaryot Cell 2009; 8:296-305; PMID:19136573; http://dx.doi.org/10.1128/EC.00197-08.
36. Tanabe Y, Maruyama J, Yamaoka S, Yahagi D, Matsuo I, Tsutsumi N, et al. Peroxisomes are involved in biotin biosynthesis in Aspergillus and Arabidopsis. J Biol Chem 2011; 286:30455-61; PMID:21730067; http://dx.doi.org/10.1074/jbc.M111.247338.
37. Magliano P, Flipphi M, Sanglard D, Poirier Y. Characterization of the Aspergillus nidulans biotin biosynthetic gene cluster and use of the bioDA gene as a new transformation marker. Fungal Genet Biol 2011; 48:208-15; PMID:20713166; http://dx.doi.org/10.1016/j.fgb.2010.08.004.
38. Magliano P, Flipphi M, Arpat BA, Delessert S, Poirier Y. Contributions of the peroxisome and β-oxidation cycle to biotin synthesis in fungi. J Biol Chem 2011; 286:42133-40; PMID:21998305; http://dx.doi.org/10.1074/jbc.M111.279687.
39. Schneider T, Dinkins R, Robinson K, Shellhammer J, Meinke DW. An embryo-lethal mutant of Arabidopsis thaliana is a biotin auxotroph. Dev Biol 1989; 131:161-7; PMID:2909401; http://dx.doi.org/10.1016/S0012-1606(89)80047-8.
40. Patton DA, Schetter AL, Franzmann LH, Nelson K, Ward ER, Meinke DW. An embryo-defective mutant of arabidopsis disrupted in the final step of biotin synthesis. Plant Physiol 1998; 116:935-46; PMID:9501126; http://dx.doi.org/10.1104/pp.116.3.935.
41. Shellhammer J, Meinke DW. Arrested embryos from the bio1 auxotroph of Arabidopsis contain reduced levels of biotin. Plant Physiol 1990; 93:1162-7; PMID:16667573; http://dx.doi.org/10.1104/pp.93.3.1162.
42. Patton DA, Volrath S, Ward ER. Complementation of an Arabidopsis thaliana biotin auxotroph with an Escherichia coli biotin biosynthetic gene. Mol Gen Genet 1996; 251:261-6; PMID:8676868; http://dx.doi.org/10.1007/BF02172516.
43. Muralla R, Chen E, Sweeney C, Gray JA, Dickerman A, Nikolau BJ, et al. A bifunctional locus (BIO3-BIO1) required for biotin biosynthesis in Arabidopsis. Plant Physiol 2008; 146:60-73; PMID:17993549; http://dx.doi.org/10.1104/pp.107.107409.
44. Cobessi D, Dumas R, Pautre V, Meinguet C, Ferrer JL, Alban C. Biochemical and structural characterization of the Arabidopsis bifunctional enzyme dethiobiotin synthetase-diaminopelargonic acid aminotransferase: evidence for substrate channeling in biotin synthesis. Plant Cell 2012; 24:1608-25; PMID:22547782; http://dx.doi.org/10.1105/tpc.112.097675.
45. Arnal N, Alban C, Quadrado M, Grandjean O, Mireau H. The Arabidopsis Bio2 protein requires mitochondrial targeting for activity. Plant Mol Biol 2006; 62:471-9; PMID:16897469; http://dx.doi.org/10.1007/s11103-006-9034-x.
46. Patton DA, Johnson M, Ward ER. Biotin synthase from Arabidopsis thaliana. cDNA isolation and characterization of gene expression. Plant Physiol 1996; 112:371-8; PMID:8819333; http://dx.doi.org/10.1104/pp.112.1.371.
47. Weaver LM, Yu F, Wurtele ES, Nikolau BJ. Characterization of the cDNA and gene coding for the biotin synthase of Arabidopsis thaliana. Plant Physiol 1996; 110:1021-8; PMID:8819873; http://dx.doi.org/10.1104/pp.110.3.1021.
48. Baldet P, Alban C, Douce R. Biotin synthesis in higher plants: purification of bioB gene product equivalent from Arabidopsis thaliana overexpressed in Escherichia coli and its subcellular localization in pea leaf cells. FEBS Lett 1997; 419:206-10; PMID:9428635; http://dx.doi.org/10.1016/S0014-5793(97)01458-0.
49. Picciocchi A, Douce R, Alban C. Biochemical characterization of the Arabidopsis biotin synthase reaction. The importance of mitochondria in biotin synthesis. Plant Physiol 2001; 127:1224-33; PMID:11706201; http://dx.doi.org/10.1104/pp.010346.
50. Pinon V, Ravanel S, Douce R, Alban C. Biotin synthesis in plants. The first committed step of the pathway is catalyzed by a cytosolic 7-keto-8-aminopelargonic acid synthase. Plant Physiol 2005; 139:1666-76; PMID:16299174; http://dx.doi.org/10.1104/pp.105.070144.