Capit. Plant Cell Wall Deconstruction

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Plant Cell Wall Deconstruction by Ascomycete Fungi

N. Louise Glass,1 Monika Schmoll,4 Jamie H.D. Cate,2, 3 and Samuel Coradetti1
1
Annu. Rev. Microbiol. 2013.67:477-498. Downloaded from www.annualreviews.org by Universidade Federal de Tocantins on 01/16/14. For personal use only.
Plant and Microbial Biology Department, 2 Molecular and Cellular Biology Department, and 3 Chemistry Department, University of California, Berkeley, California 94720; email: Lglass@berkeley.edu
4 Austrian Institute of Technology GmbH (AIT), Health and Environment, Bioresources, 3430 Tulln, Austria
Annu. Rev. Microbiol. 2013. 67:47798 First published online as a Review in Advance on June 28, 2013 The Annual Review of Microbiology is online at micro.annualreviews.org This articles doi: 10.1146/annurev-micro-092611-150044 Copyright c 2013 by Annual Reviews. All rights reserved
Keywords
Neurospora, Trichoderma, plant cell wall, cellulase, hemicellulase, polysaccharide monooxygenase
Abstract
Plant biomass degradation by fungi requires a diverse set of secreted enzymes and signicantly contributes to the global carbon cycle. Recent advances in genomic and systems-level studies have begun to reveal how lamentous ascomycete species exploit carbon sources in different habitats. These studies have laid the groundwork for unraveling new enzymatic strategies for deconstructing the plant cell wall, including the discovery of polysaccharide monooxygenases that enhance the activity of cellulases. The identication of genes encoding proteins lacking functional annotation, but that are coregulated with cellulolytic genes, suggests functions associated with plant biomass degradation remain to be elucidated. Recent research shows that signaling cascades mediating cellulolytic responses often act in a lightdependent manner and show crosstalk with other metabolic pathways. In this review, we cover plant biomass degradation, from sensing, to transmission and modulation of signals, to activation of transcription factors and gene induction, to enzyme complement and function.
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Contents
INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . CELL WALL DECONSTRUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cellulose Deconstruction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Hemicellulose Deconstruction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Pectin Deconstruction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . REGULATORY MECHANISMS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Carbon Catabolite Repression . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Chromatin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Transcription Factors Involved in Cellulose Deconstruction . . . . . . . . . . . . . . . . . . . . . . Transcription Factors Involved in Hemicellulose and Pectin Deconstruction . . . . . . Antisense Transcription . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Crosstalk Between Regulatory Pathways . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . ENVIRONMENTAL AND DEVELOPMENTAL REGULATION OF PLANT CELL WALLDEGRADING CAPACITY . . . . . . . . . . . . . . . . . . . . . . . . Light . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Heterotrimeric G-Protein Pathway . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . cAMP Pathway . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . pH . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . CONCLUSIONS . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 478 479 479 479 483 483 483 484 484 485 487 487 487 487 489 489 490 490 490
INTRODUCTION
Lignocellulosic plant matter is the most abundant natural material present on earth and is composed of four major polymeric building blocks: the polyphenol lignin and three polysaccharides, cellulose, hemicellulose, and pectin. In combination with plant cell wallassociated enzymes, structural proteins, and proteoglycans, these components form an intricately linked network that provides strength and durability to the plant cell wall (95). Photosynthesis converts approximately 100 billion metric tons of CO2 and H2 O to cellulose every year (42), which is exploited industrially as a source of fermentable sugars for the production of liquid biofuels (22, 90, 139). However, the inability to efciently convert insoluble polysaccharides, such as cellulose, to fermentable sugars poses a barrier to commercial production of biofuels (57). Filamentous fungi are among the most efcient degraders of plant biomass and are the main source of commercial enzymes used to degrade lignocellulose (64). The most commonly used organism for commercial production of cellulases is Trichoderma reesei (Hypocrea jecorina). However, recent work in the model lamentous fungus Neurospora crassa has shown that the variety of molecular, genetic, and biochemical techniques available for this organism (37) can expedite analyses of fungal deconstruction of plant biomass. In this review, we cover environmental and regulatory aspects of production of plant cell walldegrading enzymes by lamentous fungi, including recent characterization of proteins with new enzymatic functions associated with cell wall deconstruction. This review focuses on recent developments in studies of lamentous ascomycete fungi, in particular T. reesei, Aspergillus niger, and N. crassa, and concentrates on cellulose, hemicellulose, and pectin deconstruction by these organisms.
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CELL WALL DECONSTRUCTION Cellulose Deconstruction

Cellulose is the most challenging material within plant cell walls to deconstruct. It is composed of glucan chains with repeating (14) D-glucose units that form microbrils in lignocellulose within the plant cell wall. The classical scheme for fungal cellulose degradation includes (a) endo-1,4--glucanases [glycoside hydrolase 5 (GH5) family (21)] that cleave internal bonds in the cellulose chain; (b) exo-1,4--glucanases or cellobiohydrolases (GH7 and GH6) that cleave cellobiose molecules from either the reducing or nonreducing ends of a cellulose chain; and (c) -glucosidases (GH3) that hydrolyze cellobiose into two glucose molecules (133) (Figure 1). In T. reesei, Cel7A/CBH1 and Cel6A/CBH2 account for 80% of the total secreted protein under cellulose-inducing conditions; Cel7A alone represents 60% of this amount (87). In N. crassa, 65% of the secretome is made up of four proteins (CBH-1, GH6-2, GH5-1, and GH3-4) (94). Synergy between exoglucanases (Cel7A) and endoglucanases (Cel5A) has been observed during hydrolysis of bacterial cellulose (61). Similarly, although application of puried Cel7A or Cel6A to cellulose microbrils showed halting (so-called trafc jams) (59), ammonia-treated cellulose was completely degraded by the synergistic action of these two enzymes. After GH5-1, CBH-1, GH6-2, and GH3-4, the next most abundant group of proteins in the N. crassa cellulose secretome includes three GH61 proteins (94). Previously, GH61 proteins were classied as endoglucanases (62). However, recent work in N. crassa and in Thermoascus aurantiacus showed that GH61 proteins encode a novel class of copper-dependent enzymes, now called polysaccharide monooxygenases (PMOs), that catalyze the oxidative cleavage of cellulose in the presence of an external electron donor (12, 98). Although the specic catalytic mechanism is the subject of current research (58), in nature GH61 enzymes likely receive electrons from the action of cellobiose dehydrogenases (93, 125) (Figure 2). In N. crassa, deletion of a single cellobiose dehydrogenase gene reduced the total cellulase activity secreted by the fungus by nearly half, indicating that a redox-active system is a signicant part of the cellulolytic machinery (93). The number of genes encoding members of the GH61 family is quite variable among lamentous fungi. For example, members of the Sordariomycetes, such as Chaetomium globosum (Cg), Myceliophthora thermophila (Mt), Thielavia terrestris (Tt), and N. crassa (Nc), have a highly expanded PMO (GH61) family, whereas this family is reduced in T. reesei (Tr) and Aspergillus niger (An) (14, 53) (Figure 3). However, a comparative analysis of RNA-Seq data shows that the levels of expression of GH61 genes do not simply correlate with the number present in the genome (Figure 3). The relative induction of some GH61 genes on plant biomass can also vary depending on the specic feedstock (14). Because lamentous ascomycete genomes encode and express multiple PMO variants, these enzymes may have specic targets in the plant cell wall ultrastructure (Figure 2b). The secretomes of lamentous ascomycete species when exposed to cellulose remain to be fully characterized. For example, proteins similar to plant cell wall expansins, termed swollenins, have been identied (102). Swollenins contain a carbohydrate binding domain (CBM) and have been proposed to disrupt cellulose structure via nonhydrolytic mechanisms (25, 102, 138), although the biochemical action of these proteins remains to be fully elucidated (60, 136). Recently, CBM33-containing proteins have also been implicated in cellulose deconstruction (58). As substrate accessibility is one key issue in plant cell wall degradation, accessory proteins are likely to enhance the efciency of this process (40).
Hemicellulose Deconstruction
Hemicellulose is a group of heterogeneous polysaccharides, a major fraction of which are represented by xylans substituted with arabinose, glucuronic acid, or other hexose sugars (11).
www.annualreviews.org Plant Cell Wall Deconstruction 479
Cellulose
Cellobiohydrolase I (GH7) Endoglucanase (GH5.5) Cellobiohydrolase II (GH6)
Polysaccharide monooxygenase (PMO/GH61) Cellobiose dehydrogenase (CDH)
Xylan
Endo--1,4-xylanase (GH10, GH11) Acetylxylan esterase (CE1CE7)
Feruloyl esterase (CE1) -L-Arabinofuranosidase (GH3, GH10, GH43, GH51, GH54, GH62) -Glucuronidase (GH67) Lignin
Xyloglucan
Xyloglucanase (GH44, GH74)
Galactomannan
Endo--1,4-mannase (GH5.7)
-Xylosidase (GH31) -Galactosidase (GH1, GH2, GH3, GH35, GH42)
-Fucosidase (GH1, GH29, GH30, GH95) -L-Arabinofuranosidase
-Galactosidase (GH27, GH36)
Homogalacturonan
Rhamnogalacturonan-acetylesterase (CE12) Endoxylogalacturonan hydrolase (GH28) Endopolygalacturonase (GH28) Pectate lyase (PL1) Exopolygalacturonase
Rhamnogalacturonan I
-L-Arabinofuranosidase Feruloyl esterase -Glucuronidase (GH1, GH2, GH79)
Arabinanase (GH43, GH93)
Pectin methylesterase (CE8, CE12) Pectin acetylesterase (CE12)
Rhamnogalacturonase (GH28) Rhamnogalacturonan lyase (PL4, PL11) Endo--1,6-galactanase (GH5, GH30) Endo--1,4-galactanase (GH35, GH53) -galactosidase
D-glucose D-galactose D-mannose
D-glucuronic acid D-galacturonic acid D-arabinofuranose
D-xylose L-rhamnose L-fucose
Feruloyl group O-acetyl O-methyl
Enzyme activity
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a
OH RO HO OH HO OR O O HO OH H H O
1 4
OH O2+2e+2H+ PMO/CDH RO HO RO HO
HO OH O
OH HO OR HO O O H OH H2O HO OH H OR O OH H2O OH
HO
b
8.2 10.5 10.4 10.4 16.5 8.3
10.6
15.5
8.3
CBM1
Figure 2
TtGH61E
TaGH61A
NcPMO-3
Oxidation of glucan chains in cellulose by polysaccharide monooxygenase (PMO) enzymes. (a) Oxidation chemistry catalyzed by the combined activity of cellobiose dehydrogenase (CDH) and PMOs, generating cleaved glucan chains. (b) Proposed targeting of PMOs to the hydrophobic face of cellulose 1 by utilizing at binding surfaces and aromatic residues, analogous to carbohydrate binding domain 1 (CBM1) (63). The position of the N-terminal histidine in the PMO active site is also shown for Thielavia terrestris GH61 (TtGH61E) (55), as well as N-3-methylation for Thermoascus aurantiacus GH61 (TaGH61A) (98) and Neurospora crassa PMO-3 (NcPMO-3) (69). The active site copper for NcPMO-3 is shown for reference. The glucan chains are shown as black lines, with distances in angstroms between pyranose units labeled with red dotted lines. Distances between aromatic residues in angstroms are labeled with blue dotted lines. Alternative binding of each protein can be formed by moving along the glucan chain by an odd number of pyranose units, as illustrated for two PMO-3 enzymes to the right. Figure adapted from Reference 69.
Hemicellulose provides extensive cross-linking between cellulose microbrils (117) and is the second most abundant component of the plant cell wall (117). A variety of enzymes are required for xylan degradation (34) (Figure 1), including endo--1,4 xylanases (GH10, GH11), -L-arabinofuranosidases (GH3, GH10, GH43, GH51, GH54, and GH62), -xylosidases (GH43 and GH3), acetylxylan esterases (CE1CE7), and ferulic acid esterases (CE1). As with genes encoding cellulose-degrading enzymes, the number of predicted hemicellulase genes varies among lamentous ascomycete fungi (Figure 3). For example, T. reesei shows a reduction in genes encoding GH43 enzymes, but an increase in genes encoding -glucuronidases (GH79) (53). In A. niger and T. reesei, exposure to xylose induces hemicellulase genes, as well as enzymes involved in xylose utilization (xylose reductase and D-xylulokinase), although levels above 1 mM
Figure 1 Activities of major Carbohydrate Active enZyme (CAZy) (21) classes on common glycoside linkages in the plant cell wall polysaccharides cellulose, hemicellulose (xylan, xyloglucan, galactomannan), and pectin (homogalacturonan and rhamnogalacturonan I). Note that many CAZy classes show a broad range of activities (133). The most well-characterized enzymatic activities are summarized here.
200
150
o o 150
100
o o
100
o o o
50
50
+ o + * + * * + + + + o + * * * + * G A Nc GW An + * + G Tr 0
G B Cg
G B Mt
G B Tt
CE12 CE8 PL PL4 PL3 PL1 GH93 GH105 GH88 GH78 o GH28 GH36 GH35 GH27 GH131 GH5 GH62 GH51 GH43 GH2 CE5 CE4 CE3 CE1 GH11 GH10 GH5-7 GH74 GH12 GH3 GH1 GH5-5 GH6 + GH7 * GH61 CDH
x1,000 FPKM
Genes
CAZy gene count and expression data

Figure 3 Genome Carbohydrate Active enZymes (CAZy) and expression data from lamentous ascomycete fungi. Predictions are given for Aspergillus niger (An) CBS 513.88 (5), Trichoderma reesei (Tr) (80), Chaetomium globosum (Cg) CBS 148.51 (17), Thielavia terrestris (Tt) NRRL 8126, Myceliophthora thermophila (Mt) ATCC 42464 (14), and Neurospora crassa (Nc) OR74A (46). Enzyme class predictions shown are from the CAZy (21) database except for T. reesei (53) and C. globosum (97). Classes are grouped according to their activities on major components of plant cell walls, although many classes include a broad range of activities that may act on many polymers. Total transcript abundance is shown for major CAZy classes from published fungal RNA-Seq data: N. crassa (27), A. niger (31), M. thermophila, C. globosum, and T. terrestris (14). Libraries were reprocessed from the raw sequence data with current genomic annotations and identical software and settings where possible. Processing of A. niger libraries required some customization as they were performed on the ABI SOLiD sequencing platform, whereas the others were all performed on Illumina platforms. FPKM (fragments per kilobase of transcript per million mapped reads) values as calculated by Cufinks were averaged from among biological replicates and pooled for all enzymes of each class. CAZy classes GH7, GH28, and GH61 are highlighted with symbols +, o, and , respectively. Abbreviations: B, bagasse; A, Avicel; W, wheat straw.
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have the opposite effect (4, 30, 75). In T. reesei, L-arabitol, a metabolite in the degradation cascade of L-arabinose, can also induce xylanase expression (74, 75). In contrast to A. niger and T. reesei, most genes encoding hemicellulases are not induced when N. crassa is exposed to xylose (124), but exposure to xylan induces 350 genes, including many predicted hemicellulase enzymes described above, as well as genes encoding proteins of unknown biochemical function (i.e., hypothetical proteins) (124). Strains containing deletions of genes encoding proteins identied in the secretome, including hemicellulases and hypothetical proteins, show altered protein secretion levels and enzymatic activities and are ripe for future study.
Pectin Deconstruction
Among plant cell wall polysaccharides, pectin has the highest structural and functional complexity (54, 82), with four major structural classes: homogalacturonan (HG), rhamnogalacturonan I (RG-I), xylogalacturonan (XG), and rhamnogalacturonan II (RG-II) (Figure 1). HG is composed of -1,4-linked D-galacturonic acid (D-Gal) residues and accounts for 60% of the pectin in plant cell walls (19). RG-I is the second most abundant pectin class and is composed of a unique backbone of repeating units of [D-GalA-1,2--L-Rha-1,4]n , which can be substituted at the C-4 position with either arabinan, galactan, or arabinogalactan side chains. A number of enzymes are necessary for efcient degradation of pectin (78), including polygalacturonases and rhamnogalacturonases (GH28), polysaccharide lyases (pectin and pectate lyases, PL1, PL2, and PL3), and rhamnogalacturonan lyases (PL4), as well as pectin methylesterases (CE8), pectin acetylesterases (CE12 and CE13), and rhamnogalacturonan acetylesterases (CE12). Enzymes that function on RG-I side chain substitutions include arabinanases (GH43, GH93), arabinosidases/-arabinofuranosidases (GH3, GH43, GH51, GH54, and GH62), galactanases (GH5, GH16, GH30, GH35, and GH53), - and -galactosidases (GH1, GH2, GH4, GH16, GH27, GH35, GH36, GH42, GH43, and GH53), -glucuronidases (GH1, GH2, and GH79), and feruloyl esterases (CE1). Of the 60 genes identied in the A. niger genome predicted to encode pectinolytic enzymes, the expression of 46 was detected (78); a large number of these pectin-degrading enzymes have been identied experimentally by mass spectrometry (131). Similar to predicted cellulase and hemicellulase genes, the number of genes encoding pectin-degrading enzymes is also variable in lamentous ascomycete genomes (Figure 3). For example, A. niger encodes 22 GH28 (polygalacturonase) enzymes (78, 91, 133); N. crassa and M. thermophila have only two (14, 15). However, as with the PMO/GH61 genes, the expression level of genes encoding GH28 enzymes under plant biomass conditions is very similar among different lamentous ascomycete species (14, 27, 31, 127) (Figure 3).
REGULATORY MECHANISMS Carbon Catabolite Repression

Easily metabolized carbon sources such as glucose and sucrose are used preferentially over plant biomass, a phenomenon called carbon catabolite repression (CCR). CCR affects production of hydrolytic enzymes in T. reesei, Aspergillus spp., and N. crassa (7, 101, 123). Under conditions of starvation, the derepression of genes encoding cellulase, hemicellulase, and pectin-degrading enzymes results in a low expression level (27, 31, 43, 78, 83). These secreted enzymes are believed to function as scouts that, in the presence plant biomass, produce monomeric and/or small polymeric sugars that are subsequently transported into the cell via membrane-bound transporters. These
Inducer: chemical compound that initiates gene expression upon detection/uptake Ubiquitin pathway: ubiquitin-activating (E1), ubiquitinconjugating (E2), and ubiquitin-ligating (E3) enzymes act in a cascade to target proteins for degradation or to regulate their activity Carbohydrate Active enZyme (CAZyme): carbohydrate-active catalytic and carbohydrate binding enzymes that degrade, modify, or create glycosidic bonds Cellodextrins: -1,4-linked glucose polymers of varying lengths resulting from deconstruction of cellulose
sugars can function as signaling molecules that induce high expression of genes encoding enzymes required for plant biomass deconstruction. Signal transduction could occur during or via transport of sugars into the cell, or by the sugars or metabolites derived from them acting inside the cell to induce the full repertoire of a broad range of enzymes/proteins required for utilization of plant material. Some aspects of CCR in lamentous fungi are mediated by a conserved zinc-nger transcription factor (CreA/Cre1) that functions primarily as a repressor of lignocellulolytic genes (38, 101, 119). In Aspergillus spp., CreA regulates genes involved in xylose, xylan, cellulose, arabinose, proline, and ethanol utilization (reviewed in 29). In T. reesei and N. crassa, CRE1/CRE-1 regulates both xylan and cellulose utilization (73, 96, 123, 144). However, deletion of creA homologs does not induce the expression of lignocellulolytic genes in the absence of an inducer derived from plant cell wall material (such as cellobiose or xylose; see below). CreA/CRE1 regulates transcription of genes in a double-lock manner. For example, in Aspergillus spp., CreA represses transcription of xlnR, which encodes a transcription factor that regulates genes encoding enzymes involved in xylan utilization, as well as represses genes encoding the enzymes themselves (xlnA) (30, 89, 126). In addition to transcriptional repression, ubiquitination, which functions in protein turnover, assembly and function, is involved in CCR in A. nidulans and T. reesei (70). In T. reesei, the ubiquitin C-terminal hydrolase CRE2 and the E3 ubiquitin ligase LIM1 play a role in regulation of cellulase gene expression (33, 51). However, the targets of the ubiquitin pathway have not yet been identied, nor is it clear whether the ubiquitinylated factor is destined for degradation by the proteasome or if ubiquitinylation causes a signal-specic activation (137).
Chromatin
In lamentous fungi, the effects of chromatin remodeling on metabolic processes have been studied in Aspergillus spp. and Fusarium with respect to nitrogen (13) and secondary metabolism (reviewed in 45). In T. reesei, the Hap2/3/5 complex, CRE1, and an unknown GTAATA binding protein affect nucleosome positioning, thus inuencing accessibility of the TATA box for transcription initiation (140, 141). In A. nidulans, CreA function is dependent on histone acetylation status as well as on GcnE, a homolog of the Saccharomyces cerevisiae histone acetyltransferase GCN5 (47, 99), an important coactivator for positive and negative transcriptional regulation. In T. reesei, an enrichment for expression of genes related to gcn5 was correlated with increased protein production (9). In many lamentous ascomycete species, genes involved in the production of secondary metabolites are found in coregulated gene clusters (16). In A. nidulans, regulation of secondary metabolic clusters is affected by LaeA, a predicted protein methyltransferase (120). Unlike in other lamentous ascomycete fungi, in T. reesei, CAZyme-encoding genes are also frequently found in clusters with genes involved in production of secondary metabolites (80). Importantly, the homolog of laeA in T. reesei (lae1) is essential for expression of 50 CAZyme-encoding genes, including glycoside hydrolases involved in both cellulose and hemicellulose degradation (114).
Transcription Factors Involved in Cellulose Deconstruction

The action of cellulases on cellulose microbrils results in the formation of cellobiose and higher-order oligosaccharides (cellodextrins) (Figure 1). A low concentration of cellobiose induces cellulase gene expression and activity in T. reesei (132), Aspergillus spp. (26), and N. crassa (39). In N. crassa, a strain carrying deletions for the three major -glucosidase genes (thus preventing almost all conversion of cellobiose into glucose) results in the induction of cellulases in response to cellobiose (144). The induction of genes/enzymes in the triple -glucosidase mutant
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recapitulates the wild-type response to crystalline cellulose. In T. reesei, the oligosaccharide sophorose, which can be generated by the transglycosylation of cellobiose by -glucosidase enzymes, acts as a potent inducer of cellulases (118). Sophorose does not induce expression of cellulolytic genes in N. crassa or other lamentous fungi (49, 144). However, recent work in a T. reesei strain suggests that cellobiose, not sophorose, may be the natural inducing molecule (143). In addition, unlike in other lamentous fungi, lactose induces cellulase gene expression in T. reesei, although apparently via a mechanism other than on sophorose (113). In T. reesei, 220 genes predicted to encode carbohydrate-modifying enzymes are induced upon growth on lactose, sophorose, cellulose, or plant biomass (44, 53). In A. niger, 65% of mRNA-encoding CAZymes under lignocellulosic conditions are composed of ve families: GH7, GH11, GH61, GH62, and CE1 (cellobiohydrolases, xylanases, PMOs, arabinofuranosidases, and acetyl esterases, respectively) (31) (Figure 3). When N. crassa is exposed to Avicel, 212 genes are differentially upregulated (Avicel regulon) (27, 144) (Figure 3). More than 50% of the proteins encoded by these 212 genes are predicted to enter the secretory pathway (27), including 17 of 21 predicted cellulase genes and 11 of 19 predicted hemicellulase genes in the N. crassa genome (127). As in other lamentous ascomycete fungi, a large number of genes encoding hypothetical proteins are coregulated with lignocellulolytic genes in N. crassa (127). A number of these hypothetical proteins are predicted to be secreted and have in fact been identied in secretomes of fungi exposed to plant biomass (2, 127, 131). These observations suggest that many of these proteins function in some capacity for plant biomass deconstruction. In T. reesei and Aspergillus spp., the transcriptional regulator XYR1/XlnR regulates expression of hemicellulase and cellulase genes, respectively (76, 86, 121) (Figure 4). Strains carrying a deletion of xyr1 in T. reesei or an A. oryzae xlnR mutant are decient for xylanase and cellulase activity (86, 121). In T. reesei, a nonconserved transcriptional activator, ACE2 (8), and the repressor ACE1 (6) also regulate cellulase gene expression. In N. crassa and Fusarium oxysporum, the xlnR homolog is required for xylan utilization (see below) but only modulates cellulase gene expression and activity (18, 20, 124). In N. crassa, two conserved transcription factor genes [cellulose degradation regulator (clr)1 and clr-2] are required for growth specically on crystalline cellulose (27) (Figure 4). The function of clr-2 in regulating cellulase gene expression is conserved in A. nidulans (27). CLR1/CLR-2 regulate 135 genes of the 210 Avicel regulon, including cellulase and hemicellulase genes, genes encoding cellodextrin transporters, and genes likely to be involved in degrading more complex sources of lignocellulose including mannan, pectin, and arabinose. The CLR-1/CLR-2 regulon also includes 55 hypothetical proteins, whose role in cellulose deconstruction has yet to be examined. A novel transcription factor identied in A. aculeatus, ClbR, is involved in XlnR-independent cellobiose and cellulose induction of cbh1 (GH7) and cmc2 (endoglucanase) (66) (Figure 4). In T. reesei, an additional conserved transcriptional regulator, BglR, was identied that specically regulates genes encoding -glucosidase enzymes (with the exception of bgl1) (85). The role of BglR in other species during plant biomass deconstruction has not yet been examined.
Transglycosylation: the transfer of a sugar residue from one glycoside to another Avicel: proprietary name for microcrystalline cellulose Regulon: gene set regulated directly or indirectly by a transcription factor; most often determined by expression differences in wild-type versus transcription factor mutant strain
Transcription Factors Involved in Hemicellulose and Pectin Deconstruction

Loss-of-function mutants in xlnR in A. niger exhibit strongly reduced xylanolytic activities (134), and 10 genes involved in the degradation of xylan and cellulose are regulated by XlnR, including cellobiohydrolase genes (cbhA and cbhB) (49), endoglucanase genes (eglA and eglB), xylanase genes (xlnB, xlnC, and xlnD), and xylose metabolism genes (xyrA; xylose reductase) (56). Similarly, in T. reesei, XYR1 regulates cellulase, hemicellulase, and xylose metabolism genes (121) (Figure 4).
Neurospora
ACE1 ? BglR ? gh54-1 gh3-7 gh43-2 xr ---gh35-2 ce5-2 gh11-2 gh10-1 gh5-7 gh67-1 ce1-1 cdt-2 gh11-1 cdh-1 gh61-2 cbh-1
Trichoderma
Clr1 Clr2 ? ? abf1 bxl1 ---xyl1 xyn1 bga1 axe1 xyn2 xyn3 man1 grl1 ---46819 ------egl4 cbh1 cbh2 ---eg2 ---bgl1 bgl2 cel1b cel3b ---cel3c cel3d
Aspergillus
ACE1 ? BglR ? abfB xlnD xynD xyrA ---lacA ------xlnC man5a aguA axeA 8347 xlnB 7230 gh61a cbhA cbhB cbhD cbhC eglA ---eglC ---bgl4 10375 ------bglK bglH
XLR-1
ClrA ClrB XlnR
ACE1 Xyr1 ACE1
CLR-1
CLR-2
cbh-2 gh5-1 ------gh3-4 gh1-1 gh3-3 gh3-6 ------Complex substrates BglR
ClbR
Cellulose
Xylan
Repression Modulation
XLR-1 ClbR
Strict dependence Partial dependence
Sophorose
Cellobiose
Xylose
No induction
Figure 4 Transcriptional regulation of genes encoding plant cell walldegrading enzymes. Model of induction of major fungal hydrolytic enzymes by soluble inducers in Neurospora crassa (27, 124, 144), Trichoderma reesei (8, 85), and Aspergillus species (A. niger, A. nidulans, and A. aculeatus) (27, 31, 66). Horizontally aligned genes are likely orthologs listed by gene names as given in the Broad Institute database (N. crassa; http://www.broadinstitute.org/annotation/genome/neurospora/MultiHome.html), Uniprot (T. reesei; http://www.uniprot.org), or AspGD (Aspergillus spp.; http://www.aspgd.org). For T. reesei and Aspergillus genes lacking a common name, Joint Genome Institute protein IDs (T. reesei; http://genome.jgi-psf.org/Trire2/Trire2.home.html) or AspGD (A. nidulans) gene names are given. Arrows passing through a regulator represent a strict requirement for a functional copy of that regulator for specic induction. Nodes intersecting an inductive pathway indicate a modulation of specic induction. Lack of an indicated relationship does not necessarily imply a reported negative result, as systematic public datasets are few, particularly for regulatory mutant strains.
In contrast to Aspergillus spp. and T. reesei, xlnR homologs in N. crassa (xlr-1) and Fusarium spp. (xlnR) are only required for xylan/xylose utilization (18, 20, 124) (Figure 4). In N. crassa, only 30 genes are induced by exposure to xylose, most of which are involved in xylose utilization, whereas the expression of 245 genes under hemicellulose conditions is dependent on xlr-1 (124). Microarray analysis of A. oryzae showed that AoXlnR regulates 75 genes during growth on beechwood xylan (86). Of these, 19 genes were conserved between the A. oryzae XlnR and N. crassa XLR-1 regulons, including genes encoding conserved metabolic enzymes involved in xylose metabolism, hemicellulase genes (arabinofuranosidase, endoxylanase, and -xylosidase), and transporters (124). However, in N. crassa, the gene set induced by exposure to xylan versus the gene set dependent upon XLR-1 does not completely overlap, indicating that unknown transcription factors regulate additional genes involved in hemicellulose deconstruction.
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In A. niger, a number of genes encoding enzymes involved in pectin utilization, including polygalacturonase ( pgaD), a rhamnogalacturonan lyase (rglA), and several genes encoding rhamnogalacturonan side-chain-degrading enzymes (abnA, abnC, abfB, faeB, and lacE) (78), are derepressed under starvation conditions. The induction of additional pectinolytic genes is likely responsive to a number of different metabolites, such as galacturonic acid, rhamnose, arabinose, galactose, xylose, and ferulic acid (28, 79). Unlike cellulose and hemicellose degradation in lamentous ascomycete fungi, specic transcription factors required for the induction of pectinolytic enzymes have not yet been identied, suggesting that induction of these genes is regulated by a multifactorial system (28).
Per, Arnt, and Sim (PAS) domain: protein domain found in proteins that function as sensory modules for light, redox, or oxygen tension
Antisense Transcription
Regulation of gene expression by natural antisense transcription is a well-known phenomenon in fungi (50, 84, 88). In A. niger, 2% of RNA-Seq reads correlate with antisense transcripts, and a marked antisense-sense switch between growth on glucose and growth on wheat straw was observed for many of them. The switch in the antisense/sense ratio was abolished in a creA strain, suggesting that CreA directly or indirectly regulates the antisense/sense ratio under different carbon conditions (31).
Crosstalk Between Regulatory Pathways

In A. nidulans, cellulase gene expression is affected by AreA, the global nitrogen transcriptional regulator (71). In N. crassa, genes encoding proteins involved in amino acid metabolism are within the Avicel and CLR-1/CLR-2 regulons (27) as well as the WC-1/WC-2/VVD photoreceptor regulatory network (see below) (108). These observations suggest regulatory crosstalk between nitrogen, amino acid, and carbon metabolism during plant biomass utilization by lamentous fungi. Sulfur compounds including cysteine, methionine, and S-adenosylmethionine also affect plant biomass utilization by lamentous fungi. For example, in T. reesei, the expression of a E3 ubiquitin ligase (lim1), which is an ortholog of a negative regulator of sulfur utilization in N. crassa (scon-2) and S. cerevisiae (MET30), is induced when T. reesei is under sulfur limitation or exposed to cellulaseinducing conditions (51); LIM1 binds to the promoter of the cellobiohydrolase gene cbh2.
ENVIRONMENTAL AND DEVELOPMENTAL REGULATION OF PLANT CELL WALLDEGRADING CAPACITY Light

Filamentous fungi rapidly and efciently react to even minute amounts of light (10, 105), which can affect developmental processes, morphology, and metabolic pathways (103, 130). At the molecular level these responses are due mainly to homologs of the N. crassa blue-light photoreceptors, which consist of a complex of PAS (Per, Arnt, and Sim) domain proteins called white collar-1 (WC-1) and white collar-2 (WC-2) (White Collar Complex, WCC). The WCC regulates a broad array of genes via a hierarchical network (116) and is regulated by phosphorylation and protein turnover as well as by the third photoreceptor, Vivid (VVD). VVD functions in photoadaptation (for a review, see 104). Homologs of wc-1 and wc-2 are highly conserved in lamentous ascomycetes, although some species, such as Aspergillus spp., do not possess orthologs of VVD. In T. reesei, a genome-wide transcriptome study revealed a considerable number of glycoside hydrolases to be differentially expressed in light versus dark conditions (128). In N. crassa, WC-1, WC-2, and VVD as well as their homologs in T. reesei (BLR1, BLR2, and ENV1, respectively)
Light g
Nutrients
pH
Trichoderma reesei
BLR2 BLR1
GNB1
GNG1 gna3 GNA3 gna1
PhLP1
ENV1 GNA1
Light responsiveness of gene expression
PDE
cAMP
ACY1
PKAC1 LL xyr1 cbh1 cbh2 DD P
Expression of plant cell walldegrading enzymes

Figure 5 Environmental regulation of enzymes/genes involved in plant cell wall deconstruction. Regulatory interactions of signaling components are shown as identied in Trichoderma reesei. X indicates the yet unidentied regulator of xyr1 transcription, which is the putative target of PKAC1. Arrows indicate positive inuence on transcript abundance, whereas plungers indicate negative inuence on transcript abundance. Dashed arrows and plungers indicate hypothesized effects. Abbreviations: LL, constant light; DD, constant darkness.
positively regulate cellulase gene transcription (23, 106, 108) (Figure 5). The positive transcriptional regulation is paralleled by a negative effect on total cellulolytic activity produced by the respective mutants, suggesting a role for posttranslational mechanisms during light-regulated cellulase production (52, 108, 110). In N. crassa, the WCC binds to the promoter region of clr-1 (116), which encodes a transcription factor required for cellulose utilization (see above; 27). In T. reesei, strains containing mutations in components of other signal transduction pathways, such as heterotrimeric G proteins (genes encoding G-protein or subunit or the class I phosducin-like protein, PhLP1), show a large increase in the number of light-regulated genes (129). Similarly, the cAMP pathway also affects light-modulated cellulase gene expression in T. reesei (111).
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Heterotrimeric G-Protein Pathway

Fungi have signaling cascades for reception and transmission of information on the chemical composition of the substrates in the environment. The heterotrimeric guanine-nucleotidebinding protein (G-protein , , and subunits) pathway comprises transmembrane receptors as well as regulatory proteins [regulators of G-protein signaling (RGS) proteins or phosducinlike proteins] (68). Output pathways include the cAMP pathway and mitogen-activated protein kinase (MAPK) pathways (Figure 5). A role for G-protein signaling in cellulase gene expression was rst described in the chestnut tree pathogen, Cryphonectria parasitica; lack of the G-protein subunit CPG-1 abolished cellulase induction (135). In T. reesei, two G-protein subunits, GNA1 and GNA3, regulate cellulase gene expression in a light-dependent manner but do not enable inducer-independent cellulase production. Constitutive activation of GNA3 positively inuences cellulase gene expression in light, whereas deletion of gna1 causes strongly increased cellulase gene expression in darkness but abolishes this process in light (107, 112). Mutants carrying a deletion of the G-protein (GNB1) or (GNG1) subunits or of PhLP1 of T. reesei, predicted to act as a cochaperone for G-protein and folding, show decreased cellulase gene transcription but increased production of cellulolytic enzymes (129). In A. niger, the expression of a homolog of a PTH11-type G-protein-coupled receptor upon exposure to cellulosic material suggests the involvement of G-protein signaling in cellulase gene regulation (31). Because G-protein subunits and G-protein-coupled receptors of fungi do not respond to light, the light-dependent effect must be introduced by a different pathway. For T. reesei, the light regulatory protein ENVOY (VVD) was shown to negatively regulate transcription of gna3 and to positively contribute to feedback regulation of gna1 transcription (Figure 5). PhLP1 is connected with ENVOY, which constitutes a node between light response and heterotrimeric G-protein signaling (107, 128).
cAMP Pathway
The secondary messenger cAMP regulates a variety of processes in fungi and is produced in response to extracellular stimuli. Cellular cAMP levels are adjusted by a balance of biosynthesis (by adenylate cyclase) and degradation (by phosphodiesterases). The primary target of this pathway is cAMP-dependent protein kinase A (PKA), which mediates the effects of cAMP by phosphorylation of regulator proteins (36). A regulatory inuence of the cAMP pathway on plant cell wall degradation in Trichoderma, Penicillium, and Aspergillus spp. has been described (35, 41). Low amounts of cAMP stimulate cellulase activity, whereas high levels of cAMP repress cellulase formation. Similar to other regulatory pathways, cAMP does not induce cellulases in the absence of an inducer derived from plant cell wall material (35, 115). In N. crassa, constitutive activation of PKA by removal of the regulatory subunit (mcb) results in a mutant that shows apolar growth and increased secretion of cellulases (67). For T. reesei, PKA and adenylate cyclase (ACY1) are involved in the regulation of cellulase gene expression, with an unknown regulator of xyr1 as the likely target (111). cAMP levels are strongly decreased in mutants lacking ENV1, and their growth phenotype in light is alleviated by the addition of a phosphodiesterase inhibitor. Consequently, ENV1 is likely to affect the cAMP pathway and hence cellulase gene expression at least in part by dampening phosphodiesterase activity (128) (Figure 5). In T. reesei, a RAS GTPase (trRas2) was reported to be involved in cAMP signaling and modulation of cellulase gene expression and to affect regulation of XYR1 in a cAMP-independent manner (142).
www.annualreviews.org Plant Cell Wall Deconstruction
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pH
Arrestin: protein that regulates activity of G-protein-coupled receptors after their phosphorylation; also binds to other receptors and signaling proteins Peptide pheromone: small peptides acting as messengers for the presence of a potential mating partner; important for sexual development
The pH response in lamentous fungi is mediated by the conserved transcription factor PacC (reviewed in 32, 92), which functions as an activator of genes expressed in alkaline conditions and as a repressor under acidic conditions. The pH response is mediated by the G-proteincoupled receptor PalH and the arrestin PalF, possibly connecting to cellulase regulation via G-protein subunits (see above). PacC inuences expression of xylanases (72), an arabinofuranosidase (48), and endopolygalacturonases (100, 122). In N. crassa, deletion of pacC causes a growth defect on cellulose (27). In T. reesei, the expression optima of cellulolytic enzymes vary with pH and the maximum efciency of cellulose degradation occurs at pH 5.0 (3). In general, different fungi have different pH optima for efcient production of cellulolytic enzymes, and gene regulation in response to pH appears to be aimed at a delicate balance between substrate degradation, uptake of the resulting sugar, metabolic activity, and enzyme activity (39, 77, 118, 132).
Development
If the environmental conditions, especially nutritional conditions, in the habitat of a fungus deteriorate, asexual and sexual development are meant to secure the survival of the species (1). In T. reesei, expression of genes encoding plant cell walldegrading enzymes is associated with the onset of conidiation (81) and asexual spores of T. reesei have cellulases associated with the fungal cell wall (65). In T. reesei, transcription of genes involved in plant cell wall degradation was correlated with sexual development (24). In particular, a peptide pheromone gene, hpp1, was differentially expressed between a strain producing a high level of cellulases versus one defective in cellulase production (109). In N. crassa, mutants lacking the pheromone gene ppg-1 show lower cellulase activity than a wild-type strain (108), suggesting a connection between sexual development and plant cell wall deconstruction may be widespread among lamentous ascomycete fungi.
CONCLUSIONS
The coordinated induction of plant cell walldegrading enzymes is responsive to detection of a variety of individual components of plant biomass; the identity of signaling compounds and the mechanism by which transcriptional induction occurs is not clear. In addition to regulation of gene expression by transcription factors, recent studies highlight novel perspectives for research toward improvement of enzyme production and secretion in lamentous fungi including chromatin regulation and natural antisense transcription. Comparative genomic and transcriptional analyses of the plant cell wall degradation repertoire of lamentous fungi have revealed both conserved and divergent components, presumably reecting the different ecological niches of these organisms in nature. Future studies combining comparative transcriptional and proteomic analyses should yield new fundamental insights into how different fungi grow on plant biomass. The wealth of yet uncharacterized genes, which are coregulated with plant cell wall degrading enzymes or signicantly regulated and expressed under inducing conditions, are likely to reveal novel accessory proteins. The characterization of these novel factors will enable the elucidation of associated biochemical mechanisms that could increase the efciency of plant cell wall degradation and may expedite development of tailor-made enzyme cocktails for particular feedstocks.
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SUMMARY POINTS 1. Induction of plant cell walldegrading enzymes occurs after sensing or uptake of lowmolecular-weight compounds resulting from deconstruction of cellulose, hemicellulose, and pectin. 2. Despite conservation of some transcription factors responsible for the regulation of plant cell walldegrading enzymes, the mechanisms and components of the genomic inventory for this process are diverse in different fungi. 3. Hydrolytic enzymes are not only induced in response to the presence of plant cell wall material, but are also regulated by CCR, chromatin remodeling, and natural antisense transcripts.
4. Nutrient-signaling pathways are interrelated with the light response pathway, which causes plant cell walldegrading enzymes to be regulated differentially in light versus darkness, although the presence of an inducer is still required. 5. The number of genes encoding CAZymes varies in fungi and appears to reect their preferred habitat. Nevertheless, the extent of expression of these genes does not necessarily correlate with their abundance in the genome. 6. Oxidative cleavage of cellulose by polysaccharide monooxygenases and cellobiose dehydrogenases has emerged as an important contribution to plant cell wall degradation.
FUTURE ISSUES 1. As more fungal genomes are sequenced and as transcriptome, proteome, and metabolome datasets become available, the next step is to identify conserved pathways and functions specically dedicated to plant cell wall deconstruction. 2. Biochemical and structural characterization of proteins of unknown function that are secreted with plant cell walldegrading enzymes should be determined. 3. The environmental and nutrient-sensing signaling pathways should be integrated with regulation of genes encoding plant cell walldegrading enzymes by substrate-specic transcription factors. 4. Crosstalk between polysaccharide metabolism and other metabolic pathways as well as their relevance for plant cell wall degradation should be determined. 5. Oxidative degradation of cellulose must be evaluated for its impact on the fungal cell and the signal transduction pathways responsible for the regulation of plant cell wall degradation.
DISCLOSURE STATEMENT
Dr. Glass and Dr. Cate have led patent applications related to some of the pathways covered in this review. Published patent applications include Methods and Compositions for Improving Sugar Transport, Mixed Sugar Fermentation, and Production of Biofuels (WO2011011796).
ACKNOWLEDGMENTS
We thank Dr. Johan Philipp Benz for comments on the manuscript. LITERATURE CITED
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Annual Review of Microbiology Volume 67, 2013
Contents
Fifty Years Fused to Lac Jonathan Beckwith p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
3 Cap-Independent Translation Enhancers of Plant Viruses Anne E. Simon and W. Allen Miller p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 21 Acyl-Homoserine Lactone Quorum Sensing: From Evolution to Application Martin Schuster, D. Joseph Sexton, Stephen P. Diggle, and E. Peter Greenberg p p p p p p p p p 43 Mechanisms of Acid Resistance in Escherichia coli Usheer Kanjee and Walid A. Houry p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 65 The Biology of the PmrA/PmrB Two-Component System: The Major Regulator of Lipopolysaccharide Modications H. Deborah Chen and Eduardo A. Groisman p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 83 Transcription Regulation at the Core: Similarities Among Bacterial, Archaeal, and Eukaryotic RNA Polymerases Kimberly B. Decker and Deborah M. Hinton p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 113 Bacterial Responses to Reactive Chlorine Species Michael J. Gray, Wei-Yun Wholey, and Ursula Jakob p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 141 It Takes a Village: Ecological and Fitness Impacts of Multipartite Mutualism Elizabeth A. Hussa and Heidi Goodrich-Blair p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 161 Electrophysiology of Bacteria Anne H. Delcour p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 179 Microbial Contributions to Phosphorus Cycling in Eutrophic Lakes and Wastewater Katherine D. McMahon and Emily K. Read p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 199 Structure and Operation of Bacterial Tripartite Pumps Philip Hinchliffe, Martyn F. Symmons, Colin Hughes, and Vassilis Koronakis p p p p p p p p p 221 Plasmodium Nesting: Remaking the Erythrocyte from the Inside Out Justin A. Boddey and Alan F. Cowman p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 243
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The Algal Past and Parasite Present of the Apicoplast Giel G. van Dooren and Boris Striepen p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 271 Hypoxia and Gene Expression in Eukaryotic Microbes Geraldine Butler p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 291 Wall Teichoic Acids of Gram-Positive Bacteria Stephanie Brown, John P. Santa Maria Jr., and Suzanne Walker p p p p p p p p p p p p p p p p p p p p p p 313 Archaeal Biolms: The Great Unexplored Alvaro Orell, Sabrina Fr ols, and Sonja-Verena Albers p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 337 An Inquiry into the Molecular Basis of HSV Latency and Reactivation Bernard Roizman and Richard J. Whitley p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 355
Molecular Bacteria-Fungi Interactions: Effects on Environment, Food, and Medicine Kirstin Scherlach, Katharina Graupner, and Christian Hertweck p p p p p p p p p p p p p p p p p p p p p p p 375 Fusarium Pathogenomics Li-Jun Ma, David M. Geiser, Robert H. Proctor, Alejandro P. Rooney, Kerry ODonnell, Frances Trail, Donald M. Gardiner, John M. Manners, and Kemal Kazan p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 399 Biological Consequences and Advantages of Asymmetric Bacterial Growth David T. Kysela, Pamela J.B. Brown, Kerwyn Casey Huang, and Yves V. Brun p p p p p p p 417 Archaea in Biogeochemical Cycles Pierre Offre, Anja Spang, and Christa Schleper p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 437 Experimental Approaches for Dening Functional Roles of Microbes in the Human Gut Gautam Dantas, Morten O.A. Sommer, Patrick H. Degnan, and Andrew L. Goodman p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 459 Plant Cell Wall Deconstruction by Ascomycete Fungi N. Louise Glass, Monika Schmoll, Jamie H.D. Cate, and Samuel Coradetti p p p p p p p p p p p p 477 Cnidarian-Microbe Interactions and the Origin of Innate Immunity in Metazoans Thomas C.G. Bosch p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 499 On the Biological Success of Viruses Brian R. Wasik and Paul E. Turner p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 519 Prions and the Potential Transmissibility of Protein Misfolding Diseases Allison Kraus, Bradley R. Groveman, and Byron Caughey p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 543
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The Wonderful World of Archaeal Viruses David Prangishvili p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 565 Tip Growth in Filamentous Fungi: A Road Trip to the Apex Meritxell Riquelme p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 587 A Paradigm for Endosymbiotic Life: Cell Differentiation of Rhizobium Bacteria Provoked by Host Plant Factors Eva Kondorosi, Peter Mergaert, and Attila Kereszt p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 611 Neutrophils Versus Staphylococcus aureus: A Biological Tug of War Andr as N. Spaan, Bas G.J. Surewaard, Reindert Nijland, and Jos A.G. van Strijp p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 629
Index Cumulative Index of Contributing Authors, Volumes 6367 p p p p p p p p p p p p p p p p p p p p p p p p p p p 651 Errata An online log of corrections to Annual Review of Microbiology articles may be found at http://micro.annualreviews.org/
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Contents

Capit. Plant Cell Wall Deconstruction

Diunggah oleh

Informasi Dokumen

Deskripsi Asli:

Hak Cipta

Format Tersedia

Bagikan dokumen Ini

Bagikan atau Tanam Dokumen

Opsi Berbagi

Apakah menurut Anda dokumen ini bermanfaat?

Apakah konten ini tidak pantas?

Hak Cipta:

Format Tersedia

Capit. Plant Cell Wall Deconstruction

Diunggah oleh

Hak Cipta:

Format Tersedia

ANNUAL REVIEWS

Plant Cell Wall Deconstruction by Ascomycete Fungi

CELL WALL DECONSTRUCTION Cellulose Deconstruction

Polysaccharide monooxygenase (PMO/GH61) Cellobiose dehydrogenase (CDH)

-Xylosidase (GH31) -Galactosidase (GH1, GH2, GH3, GH35, GH42)

-Fucosidase (GH1, GH29, GH30, GH95) -L-Arabinofuranosidase

-Galactosidase (GH27, GH36)

Arabinanase (GH43, GH93)

Pectin methylesterase (CE8, CE12) Pectin acetylesterase (CE12)

D-glucose D-galactose D-mannose

D-glucuronic acid D-galacturonic acid D-arabinofuranose

D-xylose L-rhamnose L-fucose

Feruloyl group O-acetyl O-methyl

CAZy gene count and expression data

REGULATORY MECHANISMS Carbon Catabolite Repression

Transcription Factors Involved in Cellulose Deconstruction

Transcription Factors Involved in Hemicellulose and Pectin Deconstruction

ClrA ClrB XlnR

ACE1 Xyr1 ACE1

cbh-2 gh5-1 ------gh3-4 gh1-1 gh3-3 gh3-6 ------Complex substrates BglR

Strict dependence Partial dependence

Crosstalk Between Regulatory Pathways

ENVIRONMENTAL AND DEVELOPMENTAL REGULATION OF PLANT CELL WALLDEGRADING CAPACITY Light

GNG1 gna3 GNA3 gna1

Light responsiveness of gene expression

PKAC1 LL xyr1 cbh1 cbh2 DD P

Expression of plant cell walldegrading enzymes

Heterotrimeric G-Protein Pathway

Annual Review of Microbiology Volume 67, 2013

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