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Localizing gene regulation reveals a staggered wood decay mechanism for the brown rot fungus Postia placentaAuthor(s): Jiwei Zhang; Gerald N. Presley; Kenneth E. Hammel; Jae-San Ryu; Jon R. Menke; Melania Figueroa; Dehong Hu; Galya Orr; Jonathan S. Schilling
Source: Proceedings of the National Academy of Sciences. 113(39): 10968-10973.
Publication Series: Scientific Journal (JRNL)
Station: Forest Products Laboratory
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DescriptionWood-degrading brown rot fungi are essential recyclers of plant biomass in forest ecosystems. Their efficient cellulolytic systems, which have potential biotechnological applications, apparently depend on a combination of two mechanisms: lignocellulose oxidation (LOX) by reactive oxygen species (ROS) and polysaccharide hydrolysis by a limited set of glycoside hydrolases (GHs). Given that ROS are strongly oxidizing and nonselective, these two steps are likely segregated. A common hypothesis has been that brown rot fungi use a concentration gradient of chelated metal ions to confine ROS generation inside wood cell walls before enzymes can infiltrate. We examined an alternative: that LOX components involved in ROS production are differentially expressed by brown rot fungi ahead of GH components. We used spatial mapping to resolve a temporal sequence in Postia placenta, sectioning thin wood wafers colonized directionally. Among sections, we measured gene expression by whole-transcriptome shotgun sequencing (RNA-seq) and assayed relevant enzyme activities. We found a marked pattern of LOX up-regulation in a narrow (5-mm, 48-h) zone at the hyphal front, which included many genes likely involved in ROS generation. Up-regulation of GH5 endoglucanases and many other GHs clearly occurred later, behind the hyphal front, with the notable exceptions of two likely expansins and a GH28 pectinase. Our results support a staggered mechanism for brown rot that is controlled by differential expression rather than microenvironmental gradients. This mechanism likely results in an oxidative pretreatment of lignocellulose, possibly facilitated by expansin- and pectinase-assisted cell wall swelling, before cellulases and hemicellulases are deployed for polysaccharide depolymerization.
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CitationZhang, Jiwei; Presley, Gerald N.; Hammel, Kenneth E.; Ryu, Jae-San; Menke, Jon R.; Figueroa, Melania; Hu, Dehong; Orr, Galya; Schilling, Jonathan S. 2016. Localizing gene regulation reveals a staggered wood decay mechanism for the brown rot fungus Postia placenta. Proceedings of the National Academy of Sciences. 113(39): 10968-10973.
KeywordsBiodegradation, bioconversion, decomposition, lignocellulose, cellulase
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