Capturing an Early Gene Induction Event during Wood Decay by the Brown Rot Fungus Rhodonia placenta

Brown rot fungi dominate wood decomposition in coniferous forests, and their carbohydrate-selective mechanisms are of commercial interest. Brown rot was recently described as a two-step, sequential mechanism orchestrated by fungi using differentially expressed genes (DEGs) and consisting of oxidatio...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Applied and environmental microbiology 2022-04, Vol.88 (8), p.e0018822-e0018822
Hauptverfasser: Anderson, Claire E, Zhang, Jiwei, Markillie, Lye Meng, Mitchell, Hugh D, Chrisler, William B, Gaffrey, Matthew J, Orr, Galya, Schilling, Jonathan S
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page e0018822
container_issue 8
container_start_page e0018822
container_title Applied and environmental microbiology
container_volume 88
creator Anderson, Claire E
Zhang, Jiwei
Markillie, Lye Meng
Mitchell, Hugh D
Chrisler, William B
Gaffrey, Matthew J
Orr, Galya
Schilling, Jonathan S
description Brown rot fungi dominate wood decomposition in coniferous forests, and their carbohydrate-selective mechanisms are of commercial interest. Brown rot was recently described as a two-step, sequential mechanism orchestrated by fungi using differentially expressed genes (DEGs) and consisting of oxidation via reactive oxygen species (ROS) followed by enzymatic saccharification. There have been indications, however, that the initial oxidation step itself might require induction. To capture this early gene regulation event, here, we integrated fine-scale cryosectioning with whole-transcriptome sequencing to dissect gene expression at the single-hyphal-cell scale (tens of micrometers). This improved the spatial resolution 50-fold, relative to previous work, and we were able to capture the activity of the first 100 μm of hyphal front growth by Rhodonia placenta in aspen wood. This early decay period was dominated by delayed gene expression patterns as the fungus ramped up its mechanism. These delayed DEGs included many genes implicated in ROS pathways (lignocellulose oxidation [LOX]) that were previously and incorrectly assumed to be constitutively expressed. These delayed DEGs, which include those with and without predicted functions, also create a focused subset of target genes for functional genomics. However, this delayed pattern was not universal, with a few genes being upregulated immediately at the hyphal front. Most notably, this included a gene commonly implicated in hydroquinone and iron redox cycling: benzoquinone reductase. Earth's aboveground terrestrial biomass is primarily wood, and fungi dominate wood decomposition. Here, we studied these fungal pathways in a common "brown rot"-type fungus, , that selectively extracts sugars from carbohydrates embedded within wood lignin. Using a space-for-time design to map fungal gene expression at the extreme hyphal front in wood, we made two discoveries. First, we found that many genes long assumed to be "on" (constitutively expressed) from the very beginning of decay were instead "off" before being upregulated, when mapped (via transcriptome sequencing [RNA-seq]) at a high resolution. Second, we found that the gene encoding benzoquinone reductase was "on" in incipient decay and quickly downregulated, implying a key role in "kick-starting" brown rot.
doi_str_mv 10.1128/aem.00188-22
format Article
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9040566</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2644947287</sourcerecordid><originalsourceid>FETCH-LOGICAL-a445t-8e820fdc87ae9d9e15a714b858e4745a0ad1ab35220f2971afe77688b31d5dcc3</originalsourceid><addsrcrecordid>eNp1kUFv1DAQhS0EokvhxhlZnKjUFNtxEueCBEtbKlWqVIE4WhN7djdVYm9tp9X-e7ykreDQ00gzn98bzyPkPWcnnAv1GXA8YYwrVQjxgiw4a1VRlWX9kiwYa9vcleyAvInxhjEmWa1ek4OyKqUqlVoQs4RtmkLv1hQcPYUw7Og5OqQXzk4m9T4379Alamfot_eWfkcDO9rtaNog_Rb8vaPXPtGzya2nSK833nrXA90OYPJTeEterWCI-O6hHpJfZ6c_lz-Ky6vzi-XXywKkrFKhUAm2skY1gK1tkVfQcNmpSqFsZAUMLIeurESmRNtwWGHT1Ep1JbeVNaY8JF9m3e3UjWj33gEGvQ39CGGnPfT6_4nrN3rt73Sb71LVdRb4OAv4mHodTZ_QbIx3Dk3SXGUvJTL06cEl-NsJY9JjHw0OAzj0U9SilrKVjVBNRo9n1AQfY8DV0y6c6X14Ooen_4anxV75aMYhjkLf-Cm4fK7n2A___vVJ-DHZ8g913aLk</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2644947287</pqid></control><display><type>article</type><title>Capturing an Early Gene Induction Event during Wood Decay by the Brown Rot Fungus Rhodonia placenta</title><source>American Society for Microbiology</source><source>MEDLINE</source><source>PubMed Central</source><source>Alma/SFX Local Collection</source><creator>Anderson, Claire E ; Zhang, Jiwei ; Markillie, Lye Meng ; Mitchell, Hugh D ; Chrisler, William B ; Gaffrey, Matthew J ; Orr, Galya ; Schilling, Jonathan S</creator><contributor>Druzhinina, Irina S</contributor><creatorcontrib>Anderson, Claire E ; Zhang, Jiwei ; Markillie, Lye Meng ; Mitchell, Hugh D ; Chrisler, William B ; Gaffrey, Matthew J ; Orr, Galya ; Schilling, Jonathan S ; Pacific Northwest National Lab. (PNNL), Richland, WA (United States) ; Druzhinina, Irina S</creatorcontrib><description>Brown rot fungi dominate wood decomposition in coniferous forests, and their carbohydrate-selective mechanisms are of commercial interest. Brown rot was recently described as a two-step, sequential mechanism orchestrated by fungi using differentially expressed genes (DEGs) and consisting of oxidation via reactive oxygen species (ROS) followed by enzymatic saccharification. There have been indications, however, that the initial oxidation step itself might require induction. To capture this early gene regulation event, here, we integrated fine-scale cryosectioning with whole-transcriptome sequencing to dissect gene expression at the single-hyphal-cell scale (tens of micrometers). This improved the spatial resolution 50-fold, relative to previous work, and we were able to capture the activity of the first 100 μm of hyphal front growth by Rhodonia placenta in aspen wood. This early decay period was dominated by delayed gene expression patterns as the fungus ramped up its mechanism. These delayed DEGs included many genes implicated in ROS pathways (lignocellulose oxidation [LOX]) that were previously and incorrectly assumed to be constitutively expressed. These delayed DEGs, which include those with and without predicted functions, also create a focused subset of target genes for functional genomics. However, this delayed pattern was not universal, with a few genes being upregulated immediately at the hyphal front. Most notably, this included a gene commonly implicated in hydroquinone and iron redox cycling: benzoquinone reductase. Earth's aboveground terrestrial biomass is primarily wood, and fungi dominate wood decomposition. Here, we studied these fungal pathways in a common "brown rot"-type fungus, , that selectively extracts sugars from carbohydrates embedded within wood lignin. Using a space-for-time design to map fungal gene expression at the extreme hyphal front in wood, we made two discoveries. First, we found that many genes long assumed to be "on" (constitutively expressed) from the very beginning of decay were instead "off" before being upregulated, when mapped (via transcriptome sequencing [RNA-seq]) at a high resolution. Second, we found that the gene encoding benzoquinone reductase was "on" in incipient decay and quickly downregulated, implying a key role in "kick-starting" brown rot.</description><identifier>ISSN: 0099-2240</identifier><identifier>EISSN: 1098-5336</identifier><identifier>DOI: 10.1128/aem.00188-22</identifier><identifier>PMID: 35348388</identifier><language>eng</language><publisher>United States: American Society for Microbiology</publisher><subject>BASIC BIOLOGICAL SCIENCES ; Benzoquinones - metabolism ; Biodegradation ; Gene Expression ; Mycology ; Oxidoreductases - metabolism ; Polyporales ; Reactive Oxygen Species - metabolism ; RNA, biodegradation, decomposition, lignocellulose, transcriptomics ; Spotlight ; Spotlight Selection ; Wood - microbiology</subject><ispartof>Applied and environmental microbiology, 2022-04, Vol.88 (8), p.e0018822-e0018822</ispartof><rights>Copyright © 2022 Anderson et al.</rights><rights>Copyright © 2022 Anderson et al. 2022 Anderson et al.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-a445t-8e820fdc87ae9d9e15a714b858e4745a0ad1ab35220f2971afe77688b31d5dcc3</citedby><cites>FETCH-LOGICAL-a445t-8e820fdc87ae9d9e15a714b858e4745a0ad1ab35220f2971afe77688b31d5dcc3</cites><orcidid>0000-0002-1441-0735 ; 0000-0003-0810-3007 ; 0000000308103007 ; 0000000214410735 ; 0000000255522151</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://journals.asm.org/doi/pdf/10.1128/aem.00188-22$$EPDF$$P50$$Gasm2$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://journals.asm.org/doi/full/10.1128/aem.00188-22$$EHTML$$P50$$Gasm2$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,3175,27901,27902,52726,52727,52728,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35348388$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/servlets/purl/1868882$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><contributor>Druzhinina, Irina S</contributor><creatorcontrib>Anderson, Claire E</creatorcontrib><creatorcontrib>Zhang, Jiwei</creatorcontrib><creatorcontrib>Markillie, Lye Meng</creatorcontrib><creatorcontrib>Mitchell, Hugh D</creatorcontrib><creatorcontrib>Chrisler, William B</creatorcontrib><creatorcontrib>Gaffrey, Matthew J</creatorcontrib><creatorcontrib>Orr, Galya</creatorcontrib><creatorcontrib>Schilling, Jonathan S</creatorcontrib><creatorcontrib>Pacific Northwest National Lab. (PNNL), Richland, WA (United States)</creatorcontrib><title>Capturing an Early Gene Induction Event during Wood Decay by the Brown Rot Fungus Rhodonia placenta</title><title>Applied and environmental microbiology</title><addtitle>Appl Environ Microbiol</addtitle><addtitle>Appl Environ Microbiol</addtitle><description>Brown rot fungi dominate wood decomposition in coniferous forests, and their carbohydrate-selective mechanisms are of commercial interest. Brown rot was recently described as a two-step, sequential mechanism orchestrated by fungi using differentially expressed genes (DEGs) and consisting of oxidation via reactive oxygen species (ROS) followed by enzymatic saccharification. There have been indications, however, that the initial oxidation step itself might require induction. To capture this early gene regulation event, here, we integrated fine-scale cryosectioning with whole-transcriptome sequencing to dissect gene expression at the single-hyphal-cell scale (tens of micrometers). This improved the spatial resolution 50-fold, relative to previous work, and we were able to capture the activity of the first 100 μm of hyphal front growth by Rhodonia placenta in aspen wood. This early decay period was dominated by delayed gene expression patterns as the fungus ramped up its mechanism. These delayed DEGs included many genes implicated in ROS pathways (lignocellulose oxidation [LOX]) that were previously and incorrectly assumed to be constitutively expressed. These delayed DEGs, which include those with and without predicted functions, also create a focused subset of target genes for functional genomics. However, this delayed pattern was not universal, with a few genes being upregulated immediately at the hyphal front. Most notably, this included a gene commonly implicated in hydroquinone and iron redox cycling: benzoquinone reductase. Earth's aboveground terrestrial biomass is primarily wood, and fungi dominate wood decomposition. Here, we studied these fungal pathways in a common "brown rot"-type fungus, , that selectively extracts sugars from carbohydrates embedded within wood lignin. Using a space-for-time design to map fungal gene expression at the extreme hyphal front in wood, we made two discoveries. First, we found that many genes long assumed to be "on" (constitutively expressed) from the very beginning of decay were instead "off" before being upregulated, when mapped (via transcriptome sequencing [RNA-seq]) at a high resolution. Second, we found that the gene encoding benzoquinone reductase was "on" in incipient decay and quickly downregulated, implying a key role in "kick-starting" brown rot.</description><subject>BASIC BIOLOGICAL SCIENCES</subject><subject>Benzoquinones - metabolism</subject><subject>Biodegradation</subject><subject>Gene Expression</subject><subject>Mycology</subject><subject>Oxidoreductases - metabolism</subject><subject>Polyporales</subject><subject>Reactive Oxygen Species - metabolism</subject><subject>RNA, biodegradation, decomposition, lignocellulose, transcriptomics</subject><subject>Spotlight</subject><subject>Spotlight Selection</subject><subject>Wood - microbiology</subject><issn>0099-2240</issn><issn>1098-5336</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kUFv1DAQhS0EokvhxhlZnKjUFNtxEueCBEtbKlWqVIE4WhN7djdVYm9tp9X-e7ykreDQ00gzn98bzyPkPWcnnAv1GXA8YYwrVQjxgiw4a1VRlWX9kiwYa9vcleyAvInxhjEmWa1ek4OyKqUqlVoQs4RtmkLv1hQcPYUw7Og5OqQXzk4m9T4379Alamfot_eWfkcDO9rtaNog_Rb8vaPXPtGzya2nSK833nrXA90OYPJTeEterWCI-O6hHpJfZ6c_lz-Ky6vzi-XXywKkrFKhUAm2skY1gK1tkVfQcNmpSqFsZAUMLIeurESmRNtwWGHT1Ep1JbeVNaY8JF9m3e3UjWj33gEGvQ39CGGnPfT6_4nrN3rt73Sb71LVdRb4OAv4mHodTZ_QbIx3Dk3SXGUvJTL06cEl-NsJY9JjHw0OAzj0U9SilrKVjVBNRo9n1AQfY8DV0y6c6X14Ooen_4anxV75aMYhjkLf-Cm4fK7n2A___vVJ-DHZ8g913aLk</recordid><startdate>20220426</startdate><enddate>20220426</enddate><creator>Anderson, Claire E</creator><creator>Zhang, Jiwei</creator><creator>Markillie, Lye Meng</creator><creator>Mitchell, Hugh D</creator><creator>Chrisler, William B</creator><creator>Gaffrey, Matthew J</creator><creator>Orr, Galya</creator><creator>Schilling, Jonathan S</creator><general>American Society for Microbiology</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>OIOZB</scope><scope>OTOTI</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-1441-0735</orcidid><orcidid>https://orcid.org/0000-0003-0810-3007</orcidid><orcidid>https://orcid.org/0000000308103007</orcidid><orcidid>https://orcid.org/0000000214410735</orcidid><orcidid>https://orcid.org/0000000255522151</orcidid></search><sort><creationdate>20220426</creationdate><title>Capturing an Early Gene Induction Event during Wood Decay by the Brown Rot Fungus Rhodonia placenta</title><author>Anderson, Claire E ; Zhang, Jiwei ; Markillie, Lye Meng ; Mitchell, Hugh D ; Chrisler, William B ; Gaffrey, Matthew J ; Orr, Galya ; Schilling, Jonathan S</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a445t-8e820fdc87ae9d9e15a714b858e4745a0ad1ab35220f2971afe77688b31d5dcc3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>BASIC BIOLOGICAL SCIENCES</topic><topic>Benzoquinones - metabolism</topic><topic>Biodegradation</topic><topic>Gene Expression</topic><topic>Mycology</topic><topic>Oxidoreductases - metabolism</topic><topic>Polyporales</topic><topic>Reactive Oxygen Species - metabolism</topic><topic>RNA, biodegradation, decomposition, lignocellulose, transcriptomics</topic><topic>Spotlight</topic><topic>Spotlight Selection</topic><topic>Wood - microbiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Anderson, Claire E</creatorcontrib><creatorcontrib>Zhang, Jiwei</creatorcontrib><creatorcontrib>Markillie, Lye Meng</creatorcontrib><creatorcontrib>Mitchell, Hugh D</creatorcontrib><creatorcontrib>Chrisler, William B</creatorcontrib><creatorcontrib>Gaffrey, Matthew J</creatorcontrib><creatorcontrib>Orr, Galya</creatorcontrib><creatorcontrib>Schilling, Jonathan S</creatorcontrib><creatorcontrib>Pacific Northwest National Lab. (PNNL), Richland, WA (United States)</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>OSTI.GOV - Hybrid</collection><collection>OSTI.GOV</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Applied and environmental microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Anderson, Claire E</au><au>Zhang, Jiwei</au><au>Markillie, Lye Meng</au><au>Mitchell, Hugh D</au><au>Chrisler, William B</au><au>Gaffrey, Matthew J</au><au>Orr, Galya</au><au>Schilling, Jonathan S</au><au>Druzhinina, Irina S</au><aucorp>Pacific Northwest National Lab. (PNNL), Richland, WA (United States)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Capturing an Early Gene Induction Event during Wood Decay by the Brown Rot Fungus Rhodonia placenta</atitle><jtitle>Applied and environmental microbiology</jtitle><stitle>Appl Environ Microbiol</stitle><addtitle>Appl Environ Microbiol</addtitle><date>2022-04-26</date><risdate>2022</risdate><volume>88</volume><issue>8</issue><spage>e0018822</spage><epage>e0018822</epage><pages>e0018822-e0018822</pages><issn>0099-2240</issn><eissn>1098-5336</eissn><abstract>Brown rot fungi dominate wood decomposition in coniferous forests, and their carbohydrate-selective mechanisms are of commercial interest. Brown rot was recently described as a two-step, sequential mechanism orchestrated by fungi using differentially expressed genes (DEGs) and consisting of oxidation via reactive oxygen species (ROS) followed by enzymatic saccharification. There have been indications, however, that the initial oxidation step itself might require induction. To capture this early gene regulation event, here, we integrated fine-scale cryosectioning with whole-transcriptome sequencing to dissect gene expression at the single-hyphal-cell scale (tens of micrometers). This improved the spatial resolution 50-fold, relative to previous work, and we were able to capture the activity of the first 100 μm of hyphal front growth by Rhodonia placenta in aspen wood. This early decay period was dominated by delayed gene expression patterns as the fungus ramped up its mechanism. These delayed DEGs included many genes implicated in ROS pathways (lignocellulose oxidation [LOX]) that were previously and incorrectly assumed to be constitutively expressed. These delayed DEGs, which include those with and without predicted functions, also create a focused subset of target genes for functional genomics. However, this delayed pattern was not universal, with a few genes being upregulated immediately at the hyphal front. Most notably, this included a gene commonly implicated in hydroquinone and iron redox cycling: benzoquinone reductase. Earth's aboveground terrestrial biomass is primarily wood, and fungi dominate wood decomposition. Here, we studied these fungal pathways in a common "brown rot"-type fungus, , that selectively extracts sugars from carbohydrates embedded within wood lignin. Using a space-for-time design to map fungal gene expression at the extreme hyphal front in wood, we made two discoveries. First, we found that many genes long assumed to be "on" (constitutively expressed) from the very beginning of decay were instead "off" before being upregulated, when mapped (via transcriptome sequencing [RNA-seq]) at a high resolution. Second, we found that the gene encoding benzoquinone reductase was "on" in incipient decay and quickly downregulated, implying a key role in "kick-starting" brown rot.</abstract><cop>United States</cop><pub>American Society for Microbiology</pub><pmid>35348388</pmid><doi>10.1128/aem.00188-22</doi><tpages>8</tpages><orcidid>https://orcid.org/0000-0002-1441-0735</orcidid><orcidid>https://orcid.org/0000-0003-0810-3007</orcidid><orcidid>https://orcid.org/0000000308103007</orcidid><orcidid>https://orcid.org/0000000214410735</orcidid><orcidid>https://orcid.org/0000000255522151</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0099-2240
ispartof Applied and environmental microbiology, 2022-04, Vol.88 (8), p.e0018822-e0018822
issn 0099-2240
1098-5336
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9040566
source American Society for Microbiology; MEDLINE; PubMed Central; Alma/SFX Local Collection
subjects BASIC BIOLOGICAL SCIENCES
Benzoquinones - metabolism
Biodegradation
Gene Expression
Mycology
Oxidoreductases - metabolism
Polyporales
Reactive Oxygen Species - metabolism
RNA, biodegradation, decomposition, lignocellulose, transcriptomics
Spotlight
Spotlight Selection
Wood - microbiology
title Capturing an Early Gene Induction Event during Wood Decay by the Brown Rot Fungus Rhodonia placenta
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-21T15%3A14%3A47IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Capturing%20an%20Early%20Gene%20Induction%20Event%20during%20Wood%20Decay%20by%20the%20Brown%20Rot%20Fungus%20Rhodonia%20placenta&rft.jtitle=Applied%20and%20environmental%20microbiology&rft.au=Anderson,%20Claire%20E&rft.aucorp=Pacific%20Northwest%20National%20Lab.%20(PNNL),%20Richland,%20WA%20(United%20States)&rft.date=2022-04-26&rft.volume=88&rft.issue=8&rft.spage=e0018822&rft.epage=e0018822&rft.pages=e0018822-e0018822&rft.issn=0099-2240&rft.eissn=1098-5336&rft_id=info:doi/10.1128/aem.00188-22&rft_dat=%3Cproquest_pubme%3E2644947287%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2644947287&rft_id=info:pmid/35348388&rfr_iscdi=true