Suppression of xylan endotransglycosylase PtxtXyn10A affects cellulose microfibril angle in secondary wall in aspen wood
Certain xylanases from family GH10 are highly expressed during secondary wall deposition, but their function is unknown. We carried out functional analyses of the secondary‐wall specific PtxtXyn10A in hybrid aspen (Populus tremula × tremuloides). PtxtXyn10A function was analysed by expression studie...
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| Veröffentlicht in: | The New phytologist 2015-01, Vol.205 (2), p.666-681 |
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| creator | Derba‐Maceluch, Marta Awano, Tatsuya Takahashi, Junko Lucenius, Jessica Ratke, Christine Kontro, Inkeri Busse‐Wicher, Marta Kosik, Ondrej Tanaka, Ryo Winzéll, Anders Kallas, Åsa Leśniewska, Joanna Berthold, Fredrik Immerzeel, Peter Teeri, Tuula T Ezcurra, Ines Dupree, Paul Serimaa, Ritva Mellerowicz, Ewa J |
| description | Certain xylanases from family GH10 are highly expressed during secondary wall deposition, but their function is unknown. We carried out functional analyses of the secondary‐wall specific PtxtXyn10A in hybrid aspen (Populus tremula × tremuloides). PtxtXyn10A function was analysed by expression studies, overexpression in Arabidopsis protoplasts and by downregulation in aspen. PtxtXyn10A overexpression in Arabidopsis protoplasts resulted in increased xylan endotransglycosylation rather than hydrolysis. In aspen, the enzyme was found to be proteolytically processed to a 68 kDa peptide and residing in cell walls. Its downregulation resulted in a corresponding decrease in xylan endotransglycosylase activity and no change in xylanase activity. This did not alter xylan molecular weight or its branching pattern but affected the cellulose‐microfibril angle in wood fibres, increased primary growth (stem elongation, leaf formation and enlargement) and reduced the tendency to form tension wood. Transcriptomes of transgenic plants showed downregulation of tension wood related genes and changes in stress‐responsive genes. The data indicate that PtxtXyn10A acts as a xylan endotransglycosylase and its main function is to release tensional stresses arising during secondary wall deposition. Furthermore, they suggest that regulation of stresses in secondary walls plays a vital role in plant development. |
| doi_str_mv | 10.1111/nph.13099 |
| format | Article |
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We carried out functional analyses of the secondary‐wall specific PtxtXyn10A in hybrid aspen (Populus tremula × tremuloides). PtxtXyn10A function was analysed by expression studies, overexpression in Arabidopsis protoplasts and by downregulation in aspen. PtxtXyn10A overexpression in Arabidopsis protoplasts resulted in increased xylan endotransglycosylation rather than hydrolysis. In aspen, the enzyme was found to be proteolytically processed to a 68 kDa peptide and residing in cell walls. Its downregulation resulted in a corresponding decrease in xylan endotransglycosylase activity and no change in xylanase activity. This did not alter xylan molecular weight or its branching pattern but affected the cellulose‐microfibril angle in wood fibres, increased primary growth (stem elongation, leaf formation and enlargement) and reduced the tendency to form tension wood. Transcriptomes of transgenic plants showed downregulation of tension wood related genes and changes in stress‐responsive genes. The data indicate that PtxtXyn10A acts as a xylan endotransglycosylase and its main function is to release tensional stresses arising during secondary wall deposition. Furthermore, they suggest that regulation of stresses in secondary walls plays a vital role in plant development.</description><identifier>ISSN: 0028-646X</identifier><identifier>ISSN: 1469-8137</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.13099</identifier><identifier>PMID: 25307149</identifier><language>eng</language><publisher>England: Academic Press</publisher><subject>Arabidopsis ; Arabidopsis - cytology ; Arabidopsis - genetics ; Arabidopsis - metabolism ; Botanik ; Botany ; branching ; Cell Wall - enzymology ; Cell Wall - metabolism ; Cell walls ; Cellulose ; Cellulose - metabolism ; Chimera ; Elongation ; endotransglycosylase ; Enlargement ; gene expression regulation ; Gene Expression Regulation, Plant ; Genes ; growth stresses ; Hardwoods ; hybrid aspen ; hybrids ; Hydrolysis ; leaves ; Microfibrils ; Molecular weight ; Multigene Family ; plant development ; Plant Proteins - genetics ; Plant Proteins - metabolism ; Plants, Genetically Modified ; Populus ; Populus - cytology ; Populus - enzymology ; Populus - genetics ; Populus tremula ; Protoplasts ; secondary cell wall ; stem elongation ; Stresses ; Tension ; tension wood ; transcriptome ; Transgenic plants ; Wall deposition ; Wood ; Wood - chemistry ; Wood - cytology ; Wood - enzymology ; Wood fibers ; wood formation ; Xylan ; Xylanase ; xylanases ; Xylans - metabolism ; Xylem - cytology ; Xylem - growth & development ; Xylem - metabolism ; Xylosidases - genetics ; Xylosidases - metabolism</subject><ispartof>The New phytologist, 2015-01, Vol.205 (2), p.666-681</ispartof><rights>2015 New Phytologist Trust</rights><rights>2014 The Authors. New Phytologist © 2014 New Phytologist Trust</rights><rights>2014 The Authors. New Phytologist © 2014 New Phytologist Trust.</rights><rights>Copyright © 2014 New Phytologist Trust</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5929-e99d0a8a042eb45f1454f13c4285e3420fd3976720a64efd781e5778ab4c404d3</citedby><cites>FETCH-LOGICAL-c5929-e99d0a8a042eb45f1454f13c4285e3420fd3976720a64efd781e5778ab4c404d3</cites><orcidid>0000-0001-6817-1031</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/newphytologist.205.2.666$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/newphytologist.205.2.666$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,780,784,803,885,1417,1433,27924,27925,45574,45575,46409,46833,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25307149$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://urn.kb.se/resolve?urn=urn:nbn:se:kth:diva-160058$$DView record from Swedish Publication Index$$Hfree_for_read</backlink><backlink>$$Uhttps://res.slu.se/id/publ/77121$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Derba‐Maceluch, Marta</creatorcontrib><creatorcontrib>Awano, Tatsuya</creatorcontrib><creatorcontrib>Takahashi, Junko</creatorcontrib><creatorcontrib>Lucenius, Jessica</creatorcontrib><creatorcontrib>Ratke, Christine</creatorcontrib><creatorcontrib>Kontro, Inkeri</creatorcontrib><creatorcontrib>Busse‐Wicher, Marta</creatorcontrib><creatorcontrib>Kosik, Ondrej</creatorcontrib><creatorcontrib>Tanaka, Ryo</creatorcontrib><creatorcontrib>Winzéll, Anders</creatorcontrib><creatorcontrib>Kallas, Åsa</creatorcontrib><creatorcontrib>Leśniewska, Joanna</creatorcontrib><creatorcontrib>Berthold, Fredrik</creatorcontrib><creatorcontrib>Immerzeel, Peter</creatorcontrib><creatorcontrib>Teeri, Tuula T</creatorcontrib><creatorcontrib>Ezcurra, Ines</creatorcontrib><creatorcontrib>Dupree, Paul</creatorcontrib><creatorcontrib>Serimaa, Ritva</creatorcontrib><creatorcontrib>Mellerowicz, Ewa J</creatorcontrib><creatorcontrib>Sveriges lantbruksuniversitet</creatorcontrib><title>Suppression of xylan endotransglycosylase PtxtXyn10A affects cellulose microfibril angle in secondary wall in aspen wood</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Certain xylanases from family GH10 are highly expressed during secondary wall deposition, but their function is unknown. We carried out functional analyses of the secondary‐wall specific PtxtXyn10A in hybrid aspen (Populus tremula × tremuloides). PtxtXyn10A function was analysed by expression studies, overexpression in Arabidopsis protoplasts and by downregulation in aspen. PtxtXyn10A overexpression in Arabidopsis protoplasts resulted in increased xylan endotransglycosylation rather than hydrolysis. In aspen, the enzyme was found to be proteolytically processed to a 68 kDa peptide and residing in cell walls. Its downregulation resulted in a corresponding decrease in xylan endotransglycosylase activity and no change in xylanase activity. This did not alter xylan molecular weight or its branching pattern but affected the cellulose‐microfibril angle in wood fibres, increased primary growth (stem elongation, leaf formation and enlargement) and reduced the tendency to form tension wood. Transcriptomes of transgenic plants showed downregulation of tension wood related genes and changes in stress‐responsive genes. The data indicate that PtxtXyn10A acts as a xylan endotransglycosylase and its main function is to release tensional stresses arising during secondary wall deposition. Furthermore, they suggest that regulation of stresses in secondary walls plays a vital role in plant development.</description><subject>Arabidopsis</subject><subject>Arabidopsis - cytology</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Botanik</subject><subject>Botany</subject><subject>branching</subject><subject>Cell Wall - enzymology</subject><subject>Cell Wall - metabolism</subject><subject>Cell walls</subject><subject>Cellulose</subject><subject>Cellulose - metabolism</subject><subject>Chimera</subject><subject>Elongation</subject><subject>endotransglycosylase</subject><subject>Enlargement</subject><subject>gene expression regulation</subject><subject>Gene Expression Regulation, Plant</subject><subject>Genes</subject><subject>growth stresses</subject><subject>Hardwoods</subject><subject>hybrid aspen</subject><subject>hybrids</subject><subject>Hydrolysis</subject><subject>leaves</subject><subject>Microfibrils</subject><subject>Molecular weight</subject><subject>Multigene Family</subject><subject>plant development</subject><subject>Plant Proteins - genetics</subject><subject>Plant Proteins - metabolism</subject><subject>Plants, Genetically Modified</subject><subject>Populus</subject><subject>Populus - cytology</subject><subject>Populus - enzymology</subject><subject>Populus - genetics</subject><subject>Populus tremula</subject><subject>Protoplasts</subject><subject>secondary cell wall</subject><subject>stem elongation</subject><subject>Stresses</subject><subject>Tension</subject><subject>tension wood</subject><subject>transcriptome</subject><subject>Transgenic plants</subject><subject>Wall deposition</subject><subject>Wood</subject><subject>Wood - chemistry</subject><subject>Wood - cytology</subject><subject>Wood - enzymology</subject><subject>Wood fibers</subject><subject>wood formation</subject><subject>Xylan</subject><subject>Xylanase</subject><subject>xylanases</subject><subject>Xylans - metabolism</subject><subject>Xylem - cytology</subject><subject>Xylem - growth & development</subject><subject>Xylem - metabolism</subject><subject>Xylosidases - 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Transcriptomes of transgenic plants showed downregulation of tension wood related genes and changes in stress‐responsive genes. The data indicate that PtxtXyn10A acts as a xylan endotransglycosylase and its main function is to release tensional stresses arising during secondary wall deposition. Furthermore, they suggest that regulation of stresses in secondary walls plays a vital role in plant development.</abstract><cop>England</cop><pub>Academic Press</pub><pmid>25307149</pmid><doi>10.1111/nph.13099</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0001-6817-1031</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | The New phytologist, 2015-01, Vol.205 (2), p.666-681 |
| issn | 0028-646X 1469-8137 1469-8137 |
| language | eng |
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| source | MEDLINE; JSTOR Archive Collection A-Z Listing; Wiley Free Content; IngentaConnect Free/Open Access Journals; EZB-FREE-00999 freely available EZB journals; Wiley Online Library All Journals |
| subjects | Arabidopsis Arabidopsis - cytology Arabidopsis - genetics Arabidopsis - metabolism Botanik Botany branching Cell Wall - enzymology Cell Wall - metabolism Cell walls Cellulose Cellulose - metabolism Chimera Elongation endotransglycosylase Enlargement gene expression regulation Gene Expression Regulation, Plant Genes growth stresses Hardwoods hybrid aspen hybrids Hydrolysis leaves Microfibrils Molecular weight Multigene Family plant development Plant Proteins - genetics Plant Proteins - metabolism Plants, Genetically Modified Populus Populus - cytology Populus - enzymology Populus - genetics Populus tremula Protoplasts secondary cell wall stem elongation Stresses Tension tension wood transcriptome Transgenic plants Wall deposition Wood Wood - chemistry Wood - cytology Wood - enzymology Wood fibers wood formation Xylan Xylanase xylanases Xylans - metabolism Xylem - cytology Xylem - growth & development Xylem - metabolism Xylosidases - genetics Xylosidases - metabolism |
| title | Suppression of xylan endotransglycosylase PtxtXyn10A affects cellulose microfibril angle in secondary wall in aspen wood |
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