Localizing gene regulation reveals a staggered wood decay mechanism for the brown rot fungus Postia placenta.
Wood-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.
Department of Bioproducts and Biosystems Engineering, University of Minnesota, Saint Paul, MN 55108;
Jiwei
J
Zhang
Department of Bioproducts and Biosystems Engineering, University of Minnesota, Saint Paul, MN 55108;
Gerald N
GN
Presley
Institute for Microbial and Biochemical Technology, US Forest Products Laboratory, Madison, WI 53726; Department of Bacteriology, University of Wisconsin, Madison, WI 53706;
Kenneth E
0000-0002-2935-5847
KE
Hammel
Eco-Friendliness Research Department, Gyeongsangnam-do Agricultural Research and Extension Services, Jinju 660-360, Republic of Korea;
Jae-San
JS
Ryu
Department of Plant Biology, University of Minnesota, Saint Paul, MN 55108;
Jon R
JR
Menke
Department of Plant Pathology, University of Minnesota, Saint Paul, MN 55108;
Melania
M
Figueroa
Chemical and Biological Sciences Divisions, Pacific Northwest National Laboratory, Richland, WA 99354.
Dehong
0000-0002-3974-2963
D
Hu
Chemical and Biological Sciences Divisions, Pacific Northwest National Laboratory, Richland, WA 99354.
Galya
G
Orr
Department of Bioproducts and Biosystems Engineering, University of Minnesota, Saint Paul, MN 55108; schillin@umn.edu.
Jonathan S
JS
Schilling
D016000:Cluster Analysis; D055453:Coriolaceae / Q000201:enzymology / Q000235:genetics* / Q000254:growth & development; D015966:Gene Expression Regulation, Fungal; D005800:Genes, Fungal; D008031:Lignin; D025282:Mycelium / Q000502:physiology; D010084:Oxidation-Reduction; D014158:Transcription, Genetic; D014934:Wood / Q000382:microbiology*
C036909:lignocellulose; D008031:Lignin
bioconversion; biodegradation; cellulase; decomposition; lignocellulose