Comparison of the paralogous transcription factors AraR and XlnR in Aspergillus oryzae
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The paralogous transcription factors AraR and XlnR in Aspergillus regulate genes that are involved in degradation of cellulose and hemicellulose and catabolism of pentose. AraR and XlnR target the same genes for pentose catabolism but target different genes encoding enzymes for polysaccharide degradation. To uncover the relationship between these paralogous transcription factors, we examined their contribution to regulation of the PCP genes and compared their preferred recognition sequences. Both AraR and XlnR are involved in induction of all the pentose catabolic genes in A. oryzae except larA encoding l-arabinose reductase, which was regulated by AraR but not by XlnR. DNA-binding studies revealed that the recognition sequences of AraR and XlnR also differ only slightly; AraR prefers CGGDTAAW, while XlnR prefers CGGNTAAW. All the pentose catabolic genes possess at least one recognition site to which both AraR and XlnR can bind. Cooperative binding by the factors was not observed. Instead, they competed to bind to the shared sites. XlnR bound to the recognition sites mentioned above as a monomer, but bound to the sequence TTAGSCTAA on the xylanase promoters as a dimer. Consequently, AraR and XlnR have significantly similar, but not the same, DNA-binding properties. Such a slight difference in these paralogous transcription factors may lead to complex outputs in enzyme production depending on the concentrations of coexisting inducer molecules in the natural environment.
KeywordsAspergillus oryzae Pentose catabolism AraR XlnR
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Conflict of interest
The authors declare that they have no competing interests.
This article does not contain any studies with human participants or animals performed by any of the authors.
- Battaglia E, Hansen SF, Leendertse A, Madrid S, Mulder H, Nikolaev I, de Vries RP (2011a) Regulation of pentose utilisation by AraR, but not XlnR, differs in Aspergillus nidulans and Aspergillus niger. Appl Microbiol Biotech 91:387–397. https://doi.org/10.1007/s00253-011-3242-2 CrossRefGoogle Scholar
- Battaglia E, Klaubauf S, Vallet J, Ribot C, Lebrun MH, de Vries RP (2013) Xlr1 is involved in the transcriptional control of the pentose catabolic pathway, but not hemi-cellulolytic enzymes in Magnaporthe oryzae. Fungal Genet Biol 57:76–84. https://doi.org/10.1016/j.fgb.2013.06.005 CrossRefPubMedGoogle Scholar
- de Vries RP, Benoit I, Doehlemann G, Kobayashi T, Magnuson JK, Panisko EA, Baker SE, Lebrun MH (2011) Post-genomic approaches to understanding interactions between fungi and their environment. IMA Fungus 2:81–86. https://doi.org/10.5598/imafungus.2011.02.01.11 CrossRefPubMedPubMedCentralGoogle Scholar
- de Souza WR, Maitan-Alfenas GP, de Gouvêa PF, Brown NA, Savoldi M, Battaglia E, Goldman MH, de Vries RP, Goldman GH (2013) The influence of Aspergillus niger transcription factors AraR and XlnR in the gene expression during growth in d-xylose, l-arabinose and steam-exploded sugarcane bagasse. Fungal Genet Biol 60:29–45. https://doi.org/10.1016/j.fgb.2013.07.007 CrossRefPubMedGoogle Scholar
- Hasper AA, Visser J, de Graaff LH (2000) The Aspergillus niger transcriptional activator XlnR, which is involved in the degradation of the polysaccharides xylan and cellulose, also regulates d-xylose reductase gene expression. Mol Microbiol 36:193–200. https://doi.org/10.1046/j.1365-2958.2000.01843.x CrossRefPubMedGoogle Scholar
- Kaneda J, Sasaki K, Gomi K, Shintani T (2011) Heterologous expression of Aspergillus oryzae xylose reductase and xylitol dehydrogenase genes facilitated xylose utilization in the yeast Saccharomyces cerevisiae. Biosci Biotechnol Biochem 75:168–170. https://doi.org/10.1271/bbb.100639 CrossRefPubMedGoogle Scholar
- Klaubauf S, Narang HM, Post H, Zhou M, Brunner K, Mach-Aigner AR, Mach RL, Heck AJ, Altelaar AF, de Vries RP (2014) Similar is not the same: differences in the function of the (hemi-)cellulolytic regulator XlnR (Xlr1/Xyr1) in filamentous fungi. Fungal Genet Biol 72:73–81. https://doi.org/10.1016/j.fgb.2014.07.007 CrossRefPubMedGoogle Scholar
- Kowalczyk JE, Benoit I, de Vries RP (2014) Regulation of plant biomass utilization in Aspergillus. Adv Appl Microbiol 88:31–56. https://doi.org/10.1016/B978-0-12-800260-5.00002-4 CrossRefPubMedGoogle Scholar
- Kowalczyk JE, Gruben BS, Battaglia E, Wiebenga A, Majoor E, de Vries RP (2015) Genetic interaction of Aspergillus nidulans galR, xlnR and araR in regulating d-galactose and l-arabinose release and catabolism gene expression. PloS One 10:e0143200. https://doi.org/10.1371/journal.pone.0143200 CrossRefPubMedPubMedCentralGoogle Scholar
- Li N, Kunitake E, Aoyama M, Ogawa M, Kanamaru K, Kimura M, Koyama Y, Kobayashi T (2016) McmA-dependent and -independent regulatory systems governing expression of ClrB-regulated cellulase and hemicellulase genes in Aspergillus nidulans. Mol Microbiol 102:810–826. https://doi.org/10.1111/mmi.13493 CrossRefPubMedGoogle Scholar
- Marui J, Kitamoto N, Kato M, Kobayashi T, Tsukagoshi N (2002a) Transcriptional activator, AoXlnR, mediates cellulose-inductive expression of the xylanolytic and cellulolytic genes in Aspergillus oryzae. FEBS Lett 528:279–282. https://doi.org/10.1016/S0014-5793(02)03328-8 CrossRefPubMedGoogle Scholar
- Marui J, Tanaka A, Mimura S, de Graaff LH, Visser J, Kitamoto N, Kato M, Kobayashi T, Tsukagoshi N (2002b) A transcriptional activator, AoXlnR, controls the expression of genes encoding xylanolytic enzymes in Aspergillus oryzae. Fungal Genet Biol 35:157–169. https://doi.org/10.1006/fgbi.2001.1321 CrossRefPubMedGoogle Scholar
- Noguchi Y, Tanaka H, Kanamaru K, Kato M, Kobayashi T (2011) Xylose triggers reversible phosphorylation of XlnR, the fungal transcriptional activator of xylanolytic and cellulolytic genes in Aspergillus oryzae. Biosci Biotechnol Biochem 75:953–959. https://doi.org/10.1271/bbb.100923 CrossRefPubMedGoogle Scholar