scholarly journals Localizing gene regulation reveals a staggered wood decay mechanism for the brown rot fungusPostia placenta

2016 ◽  
Vol 113 (39) ◽  
pp. 10968-10973 ◽  
Author(s):  
Jiwei Zhang ◽  
Gerald N. Presley ◽  
Kenneth E. Hammel ◽  
Jae-San Ryu ◽  
Jon R. Menke ◽  
...  
Keyword(s):  
Cell Walls ◽  
Plant Biomass ◽  
Wood Decay ◽  
Brown Rot ◽  
Glycoside Hydrolases ◽  
Ros Generation ◽  
Rna Seq ◽  
Postia Placenta ◽  
Brown Rot Fungi ◽  
Whole Transcriptome

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 inPostia 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.

Comparative Morphology of Early Stages of Brown-Rot Wood Decay

IAWA Journal ◽  
1993 ◽  
Vol 14 (2) ◽  
pp. 127-138 ◽  
Author(s):  
W. Wayne Wilcox
Keyword(s):  
Wood Decay ◽  
Brown Rot ◽  
Comparative Morphology ◽  
Diagnostic Feature ◽  
Postia Placenta ◽  
Brown Rot Fungi ◽  
Early Stages ◽  
Poria Placenta ◽  
White Fir ◽  
Early Progression

Early stages of decay by two brown-rot fungi in two woods were studied by light and scanning electron microscopy. The earliest diagnostic feature to appear was hyphae in the earlywood lumina. The earliest effect on cell walls was the loss of birefringence in the earlywood; Poria placenta (syn. Postia placenta) caused this loss at the earliest stage of decay observed, in both Douglas-fir and white fir, while Gloeophyllum trabeum caused significant weight loss before loss of birefringence was visible. Attack on the latewood progressed from the earlywood, and was different in pattern among the wood/fungus combinations. Hyphal and bore hole diameter increased throughout the early progression of decay and would be useful in evaluating the stage of decay, if the starting diameter of hyphae could be determined. Separation between cells was not observed until moderate stages of decay and, therefore, was not useful in diagnosing early stages of decay.

scholarly journals Brown Rot-Type Fungal Decomposition of Sorghum Bagasse: Variable Success and Mechanistic Implications

2018 ◽  
Vol 2018 ◽  
pp. 1-7 ◽  
Author(s):  
Gerald N. Presley ◽  
Bongani K. Ndimba ◽  
Jonathan S. Schilling
Keyword(s):  
Plant Biomass ◽  
Specific Activity ◽  
Biomass Conversion ◽  
Xylanase Activity ◽  
Brown Rot ◽  
Fomitopsis Pinicola ◽  
Postia Placenta ◽  
Brown Rot Fungi ◽  
Protein Levels ◽  
Serpula Lacrymans

Sweet sorghum is a promising crop for a warming, drying African climate, and basic information is lacking on conversion pathways for its lignocellulosic residues (bagasse). Brown rot wood-decomposer fungi use carbohydrate-selective pathways that, when assessed on sorghum, a grass substrate, can yield information relevant to both plant biomass conversion and fungal biology. In testing sorghum decomposition by brown rot fungi (Gloeophyllum trabeum,Serpula lacrymans), we found thatG. trabeumreadily degraded sorghum, removing xylan prior to removing glucan.Serpula lacrymans, conversely, caused little decomposition. Ergosterol (fungal biomarker) and protein levels were similar for both fungi, butS. lacrymansproduced nearly 4x lower polysaccharide-degrading enzyme specific activity on sorghum thanG. trabeum, perhaps a symptom of starvation. Linking this information to genome comparisons including other brown rot fungi known to have a similar issue regarding decomposing grasses(Postia placenta, Fomitopsis pinicola)suggested that a lack of CE 1 feruloyl esterases as well as low xylanase activity inS. lacrymans(3x lower than inG. trabeum) may hinderS. lacrymans,P. placenta,andF. pinicolawhen degrading grass substrates. These results indicate variability in brown rot mechanisms, which may stem from a differing ability to degrade certain lignin-carbohydrate complexes.

scholarly journals A Fungal Secretome Adapted for Stress Enabled a Radical Wood Decay Mechanism

mBio ◽  
2021 ◽  
Author(s):  
Jesus Castaño ◽  
Jiwei Zhang ◽  
Mowei Zhou ◽  
Chia-Feng Tsai ◽  
Joon Yong Lee ◽  
...  
Keyword(s):  
Reactive Oxygen Species ◽  
Cell Walls ◽  
Critical Role ◽  
Wood Decay ◽  
Brown Rot ◽  
Oxygen Species ◽  
Decay Mechanism ◽  
Brown Rot Fungi ◽  
Carbon Recycling ◽  
Fungal Secretome

Brown rot fungi play a critical role in carbon recycling and are of industrial interest. These fungi typically use reactive oxygen species (ROS) to indiscriminately “loosen” wood cell walls at the outset of decay.

scholarly journals Oxidative Damage Control during Decay of Wood by Brown Rot Fungus Using Oxygen Radicals

2018 ◽  
Vol 84 (22) ◽  
Author(s):  
Jesus D. Castaño ◽  
Jiwei Zhang ◽  
Claire E. Anderson ◽  
Jonathan S. Schilling
Keyword(s):  
Reactive Oxygen Species ◽  
Cell Walls ◽  
Reactive Oxygen ◽  
Brown Rot ◽  
White Rot ◽  
Ros Generation ◽  
Oxygen Species ◽  
Content Type ◽  
Brown Rot Fungi ◽  
Brown Rot Fungus

ABSTRACTBrown rot wood-degrading fungi deploy reactive oxygen species (ROS) to loosen plant cell walls and enable selective polysaccharide extraction. These ROS, including Fenton-generated hydroxyl radicals (HO˙), react with little specificity and risk damaging hyphae and secreted enzymes. Recently, it was shown that brown rot fungi reduce this risk, in part, by differentially expressing genes involved in HO˙ generation ahead of those coding carbohydrate-active enzymes (CAZYs). However, there are notable exceptions to this pattern, and we hypothesized that brown rot fungi would require additional extracellular mechanisms to limit ROS damage. To assess this, we grewPostia placentadirectionally on wood wafers to spatially segregate early from later decay stages. Extracellular HO˙ production (avoidance) and quenching (suppression) capacities among the stages were analyzed, along with the ability of secreted CAZYs to maintain activity postoxidation (tolerance). First, we found that H2O2and Fe2+concentrations in the extracellular environment were conducive to HO˙ production in early (H2O2:Fe2+ratio 2:1) but not later (ratio 1:131) stages of decay. Second, we found that ABTS radical cation quenching (antioxidant capacity) was higher in later decay stages, coincident with higher fungal phenolic concentrations. Third, by surveying enzyme activities before/after exposure to Fenton-generated HO˙, we found that CAZYs secreted early, amid HO˙, were more tolerant of oxidative stress than those expressed later and were more tolerant than homologs in the model CAZY producerTrichoderma reesei. Collectively, this indicates thatP. placentauses avoidance, suppression, and tolerance mechanisms, extracellularly, to complement intracellular differential expression, enabling this brown rot fungus to use ROS to degrade wood.IMPORTANCEWood is one of the largest pools of carbon on Earth, and its decomposition is dominated in most systems by fungi. Wood-degrading fungi specialize in extracting sugars bound within lignin, either by removing lignin first (white rot) or by using Fenton-generated reactive oxygen species (ROS) to “loosen” wood cell walls, enabling selective sugar extraction (brown rot). Although white rot lignin-degrading pathways are well characterized, there are many uncertainties in brown rot fungal mechanisms. Our study addressed a key uncertainty in how brown rot fungi deploy ROS without damaging themselves or the enzymes they secrete. In addition to revealing differentially expressed genes to promote ROS generation only in early decay, our study revealed three spatial control mechanisms to avoid/tolerate ROS: (i) constraining Fenton reactant concentrations (H2O2, Fe2+), (ii) quenching ROS via antioxidants, and (iii) secreting ROS-tolerant enzymes. These results not only offer insight into natural decomposition pathways but also generate targets for biotechnological development.

The effect of CaCl2 on growth rate, wood decay and oxalic acid accumulation in Serpula lacrymans and related brown-rot fungi

Holzforschung ◽  
2006 ◽  
Vol 60 (3) ◽  
pp. 339-345 ◽  
Author(s):  
Anne Christine Steenkjær Hastrup ◽  
Bo Jensen ◽  
Carol Clausen ◽  
Frederick Green III
Keyword(s):  
Growth Rate ◽  
Oxalic Acid ◽  
Wood Decay ◽  
Brown Rot ◽  
Malt Extract ◽  
Dry Rot ◽  
Postia Placenta ◽  
Brown Rot Fungi ◽  
Serpula Lacrymans ◽  
Block Test

AbstractThe dry rot fungus,Serpula lacrymans, is one of the most destructive copper-tolerant fungi causing timber decay in buildings in temperate regions. Calcium and oxalic acid have been shown to play important roles in the mechanism of wood decay. The effect of calcium on growth and decay was evaluated for 12 strains ofS. lacrymansand compared to five brown-rot fungi. This was done by treating copper citrate (CC)-treated Southern yellow pine (SYP) wood with a CaCl2solution and estimating the decay rate and amount of soluble oxalic acid in an ASTM soil block test. Decay byS. lacrymanswas found to be significantly inhibited by treatment with CaCl2in the presence of copper. In addition, calcium showed no effect on two strains ofS. lacrymansand oneSerpula himantioidesstrain in non-copper-treated SYP wood blocks. The growth rate ofS. lacrymanswas not affected on malt extract agar containing CaCl2. In summary, a marked decrease was observed in the decay capacity ofS. lacrymansin pine treated with CC+CaCl2. The amount of soluble oxalic acid was measured in CC-treated blocks and blocks also treated with CaCl2. Of the comparative brown-rot fungi, bothAntrodia vaillantii(TFFH 294) andPostia placenta(Mad 698) displayed notable wood decay despite CaCl2treatment, while the remaining strains were inhibited.

Cytochemical Localization of Hydrogen Peroxide Production during Wood Decay by Brown-Rot Fungi Tyromyces palustris and Coniophora puteana

Holzforschung ◽  
2002 ◽  
Vol 56 (1) ◽  
pp. 7-12 ◽  
Author(s):  
Yoon Soo Kim ◽  
Seung Gon Wi ◽  
Kwang Ho Lee ◽  
Adya P. Singh
Keyword(s):  
Hydrogen Peroxide ◽  
Cell Walls ◽  
Wood Decay ◽  
Brown Rot ◽  
Cerium Chloride ◽  
Cytochemical Localization ◽  
Coniophora Puteana ◽  
Brown Rot Fungi ◽  
Transmission Electron ◽  
Early Degradation

Summary It is not definitively known whether or not the production of extracellular hydrogen peroxide (H2O2) is a universal characteristic of brown-rot fungi. Cytochemical localization of H2O2 was tested in two brown-rot fungi, Tyromyces palustris and Coniophora puteana, by staining with cerium chloride. Transmission electron microscopy (TEM) showed the deposition of cerium perhydroxide within the fungal hyphae as well as wood cell walls affected by brown-rot fungi. TEM work indicated that extracellular H2O2 was present in brown-rot fungi and that H2O2 from brown-rot fungi diffused into the wood cell walls in the early stages of decay. The present work strongly suggests that H2O2 plays an important role in the early degradation of cellulose by brown-rot fungi. The usefulness of this technique for localizing H2O2 at high resolution with minimal nonspecific deposition is also discussed.

Variation in germination percentage of basidiospores collected successively from wood decay fungi in culture

1983 ◽  
Vol 61 (1) ◽  
pp. 171-173 ◽  
Author(s):  
E. L. Schmidt ◽  
D. W. French
Keyword(s):  
Spore Germination ◽  
White Rot Fungi ◽  
Wood Decay ◽  
Brown Rot ◽  
Germination Percentage ◽  
White Rot ◽  
Malt Extract ◽  
Decay Fungi ◽  
Brown Rot Fungi ◽  
Wood Decay Fungi

Successive collections of basidiospores, produced in culture from the same hymenial areas of four species of wood decay fungi, were tested for spore germination percentage on malt extract agar under controlled conditions. Spores from white rot fungi retained high germination levels after 5 weeks of spore production, but germination averages for brown rot fungi decreased by more than 50%. Such variation should be considered in wood pathology research using spore germination bioassay.

scholarly journals Laccase and Its Role in Production of Extracellular Reactive Oxygen Species during Wood Decay by the Brown Rot Basidiomycete Postia placenta

2010 ◽  
Vol 76 (7) ◽  
pp. 2091-2097 ◽  
Author(s):  
Dongsheng Wei ◽  
Carl J. Houtman ◽  
Alexander N. Kapich ◽  
Christopher G. Hunt ◽  
Daniel Cullen ◽  
...  
Keyword(s):  
Reactive Oxygen Species ◽  
Protein Identification ◽  
Reactive Oxygen ◽  
Wood Decay ◽  
Brown Rot ◽  
Order Rate Constant ◽  
Spectrometric Analysis ◽  
Alternative Mechanism ◽  
Oxygen Species ◽  
Postia Placenta

ABSTRACT Brown rot basidiomycetes initiate wood decay by producing extracellular reactive oxygen species that depolymerize the structural polysaccharides of lignocellulose. Secreted fungal hydroquinones are considered one contributor because they have been shown to reduce Fe3+, thus generating perhydroxyl radicals and Fe2+, which subsequently react further to produce biodegradative hydroxyl radicals. However, many brown rot fungi also secrete high levels of oxalate, which chelates Fe3+ tightly, making it unreactive with hydroquinones. For hydroquinone-driven hydroxyl radical production to contribute in this environment, an alternative mechanism to oxidize hydroquinones is required. We show here that aspen wood undergoing decay by the oxalate producer Postia placenta contained both 2,5-dimethoxyhydroquinone and laccase activity. Mass spectrometric analysis of proteins extracted from the wood identified a putative laccase (Joint Genome Institute P. placenta protein identification number 111314), and heterologous expression of the corresponding gene confirmed this assignment. Ultrafiltration experiments with liquid pressed from the biodegrading wood showed that a high-molecular-weight component was required for it to oxidize 2,5-dimethoxyhydroquinone rapidly and that this component was replaceable by P. placenta laccase. The purified laccase oxidized 2,5-dimethoxyhydroquinone with a second-order rate constant near 104 M−1 s−1, and measurements of the H2O2 produced indicated that approximately one perhydroxyl radical was generated per hydroquinone supplied. Using these values and a previously developed computer model, we estimate that the quantity of reactive oxygen species produced by P. placenta laccase in wood is large enough that it likely contributes to incipient decay.

scholarly journals Comparative Transcriptome and Secretome Analysis of Wood Decay Fungi Postia placenta and Phanerochaete chrysosporium

2010 ◽  
Vol 76 (11) ◽  
pp. 3599-3610 ◽  
Author(s):  
Amber Vanden Wymelenberg ◽  
Jill Gaskell ◽  
Michael Mozuch ◽  
Grzegorz Sabat ◽  
John Ralph ◽  
...  
Keyword(s):  
Phanerochaete Chrysosporium ◽  
Cellulose Degradation ◽  
Expression Patterns ◽  
Wood Decay ◽  
Brown Rot ◽  
White Rot ◽  
Glycosyl Hydrolases ◽  
Decay Fungi ◽  
Postia Placenta ◽  
Wood Decay Fungi

ABSTRACT Cellulose degradation by brown rot fungi, such as Postia placenta, is poorly understood relative to the phylogenetically related white rot basidiomycete, Phanerochaete chrysosporium. To elucidate the number, structure, and regulation of genes involved in lignocellulosic cell wall attack, secretome and transcriptome analyses were performed on both wood decay fungi cultured for 5 days in media containing ball-milled aspen or glucose as the sole carbon source. Using liquid chromatography-tandem mass spectrometry (LC-MS/MS), a total of 67 and 79 proteins were identified in the extracellular fluids of P. placenta and P. chrysosporium cultures, respectively. Viewed together with transcript profiles, P. chrysosporium employs an array of extracellular glycosyl hydrolases to simultaneously attack cellulose and hemicelluloses. In contrast, under these same conditions, P. placenta secretes an array of hemicellulases but few potential cellulases. The two species display distinct expression patterns for oxidoreductase-encoding genes. In P. placenta, these patterns are consistent with an extracellular Fenton system and include the upregulation of genes involved in iron acquisition, in the synthesis of low-molecular-weight quinones, and possibly in redox cycling reactions.

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