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Mutations in the Pectin Methyltransferase QUASIMODO2 Influence Cellulose Biosynthesis and Wall Integrity in Arabidopsis
Pectins are abundant in the cell walls of dicotyledonous plants, but how they interact with other wall polymers and influence wall integrity and cell growth has remained mysterious. Here, we verified that QUASIMODO2 (QUA2) is a pectin methyltransferase and determined that QUA2 is required for normal...
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Published in: | The Plant cell 2020-11, Vol.32 (11), p.3576-3597 |
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creator | Du, Juan Kirui, Alex Huang, Shixin Wang, Lianglei Barnes, William J Kiemle, Sarah N Zheng, Yunzhen Rui, Yue Ruan, Mei Qi, Shiqian Kim, Seong H Wang, Tuo Cosgrove, Daniel J Anderson, Charles T Xiao, Chaowen |
description | Pectins are abundant in the cell walls of dicotyledonous plants, but how they interact with other wall polymers and influence wall integrity and cell growth has remained mysterious. Here, we verified that QUASIMODO2 (QUA2) is a pectin methyltransferase and determined that QUA2 is required for normal pectin biosynthesis. To gain further insight into how pectin affects wall assembly and integrity maintenance, we investigated cellulose biosynthesis, cellulose organization, cortical microtubules, and wall integrity signaling in two mutant alleles of Arabidopsis (
)
,
and
In both mutants, crystalline cellulose content is reduced, cellulose synthase particles move more slowly, and cellulose organization is aberrant. NMR analysis shows higher mobility of cellulose and matrix polysaccharides in the mutants. Microtubules in mutant hypocotyls have aberrant organization and depolymerize more readily upon treatment with oryzalin or external force. The expression of genes related to wall integrity, wall biosynthesis, and microtubule stability is dysregulated in both mutants. These data provide insights into how homogalacturonan is methylesterified upon its synthesis, the mechanisms by which pectin functionally interacts with cellulose, and how these interactions are translated into intracellular regulation to maintain the structural integrity of the cell wall during plant growth and development. |
doi_str_mv | 10.1105/tpc.20.00252 |
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)
,
and
In both mutants, crystalline cellulose content is reduced, cellulose synthase particles move more slowly, and cellulose organization is aberrant. NMR analysis shows higher mobility of cellulose and matrix polysaccharides in the mutants. Microtubules in mutant hypocotyls have aberrant organization and depolymerize more readily upon treatment with oryzalin or external force. The expression of genes related to wall integrity, wall biosynthesis, and microtubule stability is dysregulated in both mutants. These data provide insights into how homogalacturonan is methylesterified upon its synthesis, the mechanisms by which pectin functionally interacts with cellulose, and how these interactions are translated into intracellular regulation to maintain the structural integrity of the cell wall during plant growth and development.</description><identifier>ISSN: 1040-4651</identifier><identifier>EISSN: 1532-298X</identifier><identifier>DOI: 10.1105/tpc.20.00252</identifier><identifier>PMID: 32883711</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><subject>Arabidopsis - cytology ; Arabidopsis - genetics ; Arabidopsis - growth & development ; Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; BASIC BIOLOGICAL SCIENCES ; Cell Adhesion - genetics ; Cell Wall - genetics ; Cellulose - biosynthesis ; Cellulose - genetics ; Dinitrobenzenes - pharmacology ; Gene Expression Regulation, Plant ; Hypocotyl - cytology ; Hypocotyl - genetics ; Hypocotyl - growth & development ; MATERIALS SCIENCE ; Methyltransferases - genetics ; Methyltransferases - metabolism ; Microtubules - metabolism ; Mutation ; Pectins - biosynthesis ; Pectins - genetics ; Pectins - metabolism ; Plant Cells - drug effects ; Plant Cells - metabolism ; Plants, Genetically Modified ; Sulfanilamides - pharmacology ; Uronic Acids - metabolism</subject><ispartof>The Plant cell, 2020-11, Vol.32 (11), p.3576-3597</ispartof><rights>2020 American Society of Plant Biologists. All rights reserved.</rights><rights>2020 American Society of Plant Biologists. All rights reserved. 2020</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c477t-9c025225279156cdcd9f26a9bbc78a9d7c1ebf6f9013343ac1c58a1acb66a7793</citedby><cites>FETCH-LOGICAL-c477t-9c025225279156cdcd9f26a9bbc78a9d7c1ebf6f9013343ac1c58a1acb66a7793</cites><orcidid>0000-0003-4499-7474 ; 0000-0002-4020-5786 ; 0000-0001-9380-8831 ; 0000-0001-7481-3571 ; 0000-0002-7081-2392 ; 0000-0002-8575-7269 ; 0000-0003-0757-4608 ; 0000-0001-8981-8367 ; 0000-0002-9087-4283 ; 0000-0002-7589-8877 ; 0000-0002-0291-0062 ; 0000-0002-1903-5356 ; 0000-0002-1801-924X ; 0000-0003-3297-4136 ; 0000-0001-8232-4284 ; 0000000344997474 ; 0000000189818367 ; 0000000202910062 ; 0000000193808831 ; 0000000290874283 ; 0000000275898877 ; 0000000270812392 ; 0000000332974136 ; 0000000240205786 ; 0000000307574608 ; 0000000182324284 ; 0000000219035356 ; 000000021801924X ; 0000000174813571 ; 0000000285757269</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,315,786,790,891,27957,27958</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32883711$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://www.osti.gov/biblio/1657865$$D View this record in Osti.gov$$Hfree_for_read</backlink></links><search><creatorcontrib>Du, Juan</creatorcontrib><creatorcontrib>Kirui, Alex</creatorcontrib><creatorcontrib>Huang, Shixin</creatorcontrib><creatorcontrib>Wang, Lianglei</creatorcontrib><creatorcontrib>Barnes, William J</creatorcontrib><creatorcontrib>Kiemle, Sarah N</creatorcontrib><creatorcontrib>Zheng, Yunzhen</creatorcontrib><creatorcontrib>Rui, Yue</creatorcontrib><creatorcontrib>Ruan, Mei</creatorcontrib><creatorcontrib>Qi, Shiqian</creatorcontrib><creatorcontrib>Kim, Seong H</creatorcontrib><creatorcontrib>Wang, Tuo</creatorcontrib><creatorcontrib>Cosgrove, Daniel J</creatorcontrib><creatorcontrib>Anderson, Charles T</creatorcontrib><creatorcontrib>Xiao, Chaowen</creatorcontrib><creatorcontrib>Pennsylvania State Univ., University Park, PA (United States)</creatorcontrib><title>Mutations in the Pectin Methyltransferase QUASIMODO2 Influence Cellulose Biosynthesis and Wall Integrity in Arabidopsis</title><title>The Plant cell</title><addtitle>Plant Cell</addtitle><description>Pectins are abundant in the cell walls of dicotyledonous plants, but how they interact with other wall polymers and influence wall integrity and cell growth has remained mysterious. Here, we verified that QUASIMODO2 (QUA2) is a pectin methyltransferase and determined that QUA2 is required for normal pectin biosynthesis. To gain further insight into how pectin affects wall assembly and integrity maintenance, we investigated cellulose biosynthesis, cellulose organization, cortical microtubules, and wall integrity signaling in two mutant alleles of Arabidopsis (
)
,
and
In both mutants, crystalline cellulose content is reduced, cellulose synthase particles move more slowly, and cellulose organization is aberrant. NMR analysis shows higher mobility of cellulose and matrix polysaccharides in the mutants. Microtubules in mutant hypocotyls have aberrant organization and depolymerize more readily upon treatment with oryzalin or external force. The expression of genes related to wall integrity, wall biosynthesis, and microtubule stability is dysregulated in both mutants. These data provide insights into how homogalacturonan is methylesterified upon its synthesis, the mechanisms by which pectin functionally interacts with cellulose, and how these interactions are translated into intracellular regulation to maintain the structural integrity of the cell wall during plant growth and development.</description><subject>Arabidopsis - cytology</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - growth & development</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>BASIC BIOLOGICAL SCIENCES</subject><subject>Cell Adhesion - genetics</subject><subject>Cell Wall - genetics</subject><subject>Cellulose - biosynthesis</subject><subject>Cellulose - genetics</subject><subject>Dinitrobenzenes - pharmacology</subject><subject>Gene Expression Regulation, Plant</subject><subject>Hypocotyl - cytology</subject><subject>Hypocotyl - genetics</subject><subject>Hypocotyl - growth & development</subject><subject>MATERIALS SCIENCE</subject><subject>Methyltransferases - genetics</subject><subject>Methyltransferases - metabolism</subject><subject>Microtubules - metabolism</subject><subject>Mutation</subject><subject>Pectins - biosynthesis</subject><subject>Pectins - genetics</subject><subject>Pectins - metabolism</subject><subject>Plant Cells - drug effects</subject><subject>Plant Cells - metabolism</subject><subject>Plants, Genetically Modified</subject><subject>Sulfanilamides - pharmacology</subject><subject>Uronic Acids - metabolism</subject><issn>1040-4651</issn><issn>1532-298X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><recordid>eNpVkc9rFDEUx4NYbK3ePMvgyYOzJplJMrkI6_qjC11W0aK3kHmT6UayyTbJKPvfm3XbUiGQwPvwyXvvi9ALgmeEYPY272BG8QxjyugjdEZYQ2squ5-Pyxu3uG45I6foaUq_MMZEEPkEnTa06xpByBn6s5qyzjb4VFlf5Y2pvhjI5bkyebN3OWqfRhN1MtXXq_m35Wr9YU2rpR_dZDyYamGcm1wo5fc2pL0vhmRTpf1Q_dDOFTKb62jz_qCfR93bIewK8QydjNol8_z2PkdXnz5-X1zUl-vPy8X8soZWiFxLOIxVjpCEcRhgkCPlWvY9iE7LQQAx_chHiUnTtI0GAqzTREPPuRZCNufo3dG7m_qtGcD4MpJTu2i3Ou5V0Fb9X_F2o67DbyU4wVTSInh1FISUrUpgs4ENBO_LmhThTHScFej17S8x3EwmZbW1CcpqtDdhSoq2LW4FK8KCvjmiEENK0Yz3vRCsDoGqEqiiWP0LtOAvH_Z_D98l2PwFeuWeIw</recordid><startdate>20201101</startdate><enddate>20201101</enddate><creator>Du, Juan</creator><creator>Kirui, Alex</creator><creator>Huang, Shixin</creator><creator>Wang, Lianglei</creator><creator>Barnes, William J</creator><creator>Kiemle, Sarah N</creator><creator>Zheng, Yunzhen</creator><creator>Rui, Yue</creator><creator>Ruan, Mei</creator><creator>Qi, Shiqian</creator><creator>Kim, Seong H</creator><creator>Wang, Tuo</creator><creator>Cosgrove, Daniel J</creator><creator>Anderson, Charles T</creator><creator>Xiao, Chaowen</creator><general>Oxford University Press</general><general>American Society of Plant Biologists</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>OTOTI</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-4499-7474</orcidid><orcidid>https://orcid.org/0000-0002-4020-5786</orcidid><orcidid>https://orcid.org/0000-0001-9380-8831</orcidid><orcidid>https://orcid.org/0000-0001-7481-3571</orcidid><orcidid>https://orcid.org/0000-0002-7081-2392</orcidid><orcidid>https://orcid.org/0000-0002-8575-7269</orcidid><orcidid>https://orcid.org/0000-0003-0757-4608</orcidid><orcidid>https://orcid.org/0000-0001-8981-8367</orcidid><orcidid>https://orcid.org/0000-0002-9087-4283</orcidid><orcidid>https://orcid.org/0000-0002-7589-8877</orcidid><orcidid>https://orcid.org/0000-0002-0291-0062</orcidid><orcidid>https://orcid.org/0000-0002-1903-5356</orcidid><orcidid>https://orcid.org/0000-0002-1801-924X</orcidid><orcidid>https://orcid.org/0000-0003-3297-4136</orcidid><orcidid>https://orcid.org/0000-0001-8232-4284</orcidid><orcidid>https://orcid.org/0000000344997474</orcidid><orcidid>https://orcid.org/0000000189818367</orcidid><orcidid>https://orcid.org/0000000202910062</orcidid><orcidid>https://orcid.org/0000000193808831</orcidid><orcidid>https://orcid.org/0000000290874283</orcidid><orcidid>https://orcid.org/0000000275898877</orcidid><orcidid>https://orcid.org/0000000270812392</orcidid><orcidid>https://orcid.org/0000000332974136</orcidid><orcidid>https://orcid.org/0000000240205786</orcidid><orcidid>https://orcid.org/0000000307574608</orcidid><orcidid>https://orcid.org/0000000182324284</orcidid><orcidid>https://orcid.org/0000000219035356</orcidid><orcidid>https://orcid.org/000000021801924X</orcidid><orcidid>https://orcid.org/0000000174813571</orcidid><orcidid>https://orcid.org/0000000285757269</orcidid></search><sort><creationdate>20201101</creationdate><title>Mutations in the Pectin Methyltransferase QUASIMODO2 Influence Cellulose Biosynthesis and Wall Integrity in Arabidopsis</title><author>Du, Juan ; Kirui, Alex ; Huang, Shixin ; Wang, Lianglei ; Barnes, William J ; Kiemle, Sarah N ; Zheng, Yunzhen ; Rui, Yue ; Ruan, Mei ; Qi, Shiqian ; Kim, Seong H ; Wang, Tuo ; Cosgrove, Daniel J ; Anderson, Charles T ; Xiao, Chaowen</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c477t-9c025225279156cdcd9f26a9bbc78a9d7c1ebf6f9013343ac1c58a1acb66a7793</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Arabidopsis - cytology</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - growth & development</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>BASIC BIOLOGICAL SCIENCES</topic><topic>Cell Adhesion - genetics</topic><topic>Cell Wall - genetics</topic><topic>Cellulose - biosynthesis</topic><topic>Cellulose - genetics</topic><topic>Dinitrobenzenes - pharmacology</topic><topic>Gene Expression Regulation, Plant</topic><topic>Hypocotyl - cytology</topic><topic>Hypocotyl - genetics</topic><topic>Hypocotyl - growth & development</topic><topic>MATERIALS SCIENCE</topic><topic>Methyltransferases - genetics</topic><topic>Methyltransferases - metabolism</topic><topic>Microtubules - metabolism</topic><topic>Mutation</topic><topic>Pectins - biosynthesis</topic><topic>Pectins - genetics</topic><topic>Pectins - metabolism</topic><topic>Plant Cells - drug effects</topic><topic>Plant Cells - metabolism</topic><topic>Plants, Genetically Modified</topic><topic>Sulfanilamides - pharmacology</topic><topic>Uronic Acids - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Du, Juan</creatorcontrib><creatorcontrib>Kirui, Alex</creatorcontrib><creatorcontrib>Huang, Shixin</creatorcontrib><creatorcontrib>Wang, Lianglei</creatorcontrib><creatorcontrib>Barnes, William J</creatorcontrib><creatorcontrib>Kiemle, Sarah N</creatorcontrib><creatorcontrib>Zheng, Yunzhen</creatorcontrib><creatorcontrib>Rui, Yue</creatorcontrib><creatorcontrib>Ruan, Mei</creatorcontrib><creatorcontrib>Qi, Shiqian</creatorcontrib><creatorcontrib>Kim, Seong H</creatorcontrib><creatorcontrib>Wang, Tuo</creatorcontrib><creatorcontrib>Cosgrove, Daniel J</creatorcontrib><creatorcontrib>Anderson, Charles T</creatorcontrib><creatorcontrib>Xiao, Chaowen</creatorcontrib><creatorcontrib>Pennsylvania State Univ., University Park, PA (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</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Plant cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Du, Juan</au><au>Kirui, Alex</au><au>Huang, Shixin</au><au>Wang, Lianglei</au><au>Barnes, William J</au><au>Kiemle, Sarah N</au><au>Zheng, Yunzhen</au><au>Rui, Yue</au><au>Ruan, Mei</au><au>Qi, Shiqian</au><au>Kim, Seong H</au><au>Wang, Tuo</au><au>Cosgrove, Daniel J</au><au>Anderson, Charles T</au><au>Xiao, Chaowen</au><aucorp>Pennsylvania State Univ., University Park, PA (United States)</aucorp><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Mutations in the Pectin Methyltransferase QUASIMODO2 Influence Cellulose Biosynthesis and Wall Integrity in Arabidopsis</atitle><jtitle>The Plant cell</jtitle><addtitle>Plant Cell</addtitle><date>2020-11-01</date><risdate>2020</risdate><volume>32</volume><issue>11</issue><spage>3576</spage><epage>3597</epage><pages>3576-3597</pages><issn>1040-4651</issn><eissn>1532-298X</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><notes>China Postdoctoral Science Foundation</notes><notes>SC0001090</notes><notes>USDOE Office of Science (SC), Basic Energy Sciences (BES)</notes><notes>Central Universities</notes><notes>Current address: Complex Carbohydrate Research Center, University of Georgia, Athens, Georgia 30602.</notes><notes>Current address: Science Center, Mount Holyoke College, South Hadley, Massachusetts 01075.</notes><notes>www.plantcell.org/cgi/doi/10.1105/tpc.20.00252</notes><notes>Current address: Department of Biology, Stanford University, Stanford, California 94305.</notes><notes>The authors responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) are: Charles T. Anderson (cta3@psu.edu) and Chaowen Xiao (cwxiao@scu.edu.cn).</notes><abstract>Pectins are abundant in the cell walls of dicotyledonous plants, but how they interact with other wall polymers and influence wall integrity and cell growth has remained mysterious. Here, we verified that QUASIMODO2 (QUA2) is a pectin methyltransferase and determined that QUA2 is required for normal pectin biosynthesis. To gain further insight into how pectin affects wall assembly and integrity maintenance, we investigated cellulose biosynthesis, cellulose organization, cortical microtubules, and wall integrity signaling in two mutant alleles of Arabidopsis (
)
,
and
In both mutants, crystalline cellulose content is reduced, cellulose synthase particles move more slowly, and cellulose organization is aberrant. NMR analysis shows higher mobility of cellulose and matrix polysaccharides in the mutants. Microtubules in mutant hypocotyls have aberrant organization and depolymerize more readily upon treatment with oryzalin or external force. The expression of genes related to wall integrity, wall biosynthesis, and microtubule stability is dysregulated in both mutants. These data provide insights into how homogalacturonan is methylesterified upon its synthesis, the mechanisms by which pectin functionally interacts with cellulose, and how these interactions are translated into intracellular regulation to maintain the structural integrity of the cell wall during plant growth and development.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>32883711</pmid><doi>10.1105/tpc.20.00252</doi><tpages>22</tpages><orcidid>https://orcid.org/0000-0003-4499-7474</orcidid><orcidid>https://orcid.org/0000-0002-4020-5786</orcidid><orcidid>https://orcid.org/0000-0001-9380-8831</orcidid><orcidid>https://orcid.org/0000-0001-7481-3571</orcidid><orcidid>https://orcid.org/0000-0002-7081-2392</orcidid><orcidid>https://orcid.org/0000-0002-8575-7269</orcidid><orcidid>https://orcid.org/0000-0003-0757-4608</orcidid><orcidid>https://orcid.org/0000-0001-8981-8367</orcidid><orcidid>https://orcid.org/0000-0002-9087-4283</orcidid><orcidid>https://orcid.org/0000-0002-7589-8877</orcidid><orcidid>https://orcid.org/0000-0002-0291-0062</orcidid><orcidid>https://orcid.org/0000-0002-1903-5356</orcidid><orcidid>https://orcid.org/0000-0002-1801-924X</orcidid><orcidid>https://orcid.org/0000-0003-3297-4136</orcidid><orcidid>https://orcid.org/0000-0001-8232-4284</orcidid><orcidid>https://orcid.org/0000000344997474</orcidid><orcidid>https://orcid.org/0000000189818367</orcidid><orcidid>https://orcid.org/0000000202910062</orcidid><orcidid>https://orcid.org/0000000193808831</orcidid><orcidid>https://orcid.org/0000000290874283</orcidid><orcidid>https://orcid.org/0000000275898877</orcidid><orcidid>https://orcid.org/0000000270812392</orcidid><orcidid>https://orcid.org/0000000332974136</orcidid><orcidid>https://orcid.org/0000000240205786</orcidid><orcidid>https://orcid.org/0000000307574608</orcidid><orcidid>https://orcid.org/0000000182324284</orcidid><orcidid>https://orcid.org/0000000219035356</orcidid><orcidid>https://orcid.org/000000021801924X</orcidid><orcidid>https://orcid.org/0000000174813571</orcidid><orcidid>https://orcid.org/0000000285757269</orcidid><oa>free_for_read</oa></addata></record> |
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ispartof | The Plant cell, 2020-11, Vol.32 (11), p.3576-3597 |
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source | Oxford Academic Journals (OUP) |
subjects | Arabidopsis - cytology Arabidopsis - genetics Arabidopsis - growth & development Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism BASIC BIOLOGICAL SCIENCES Cell Adhesion - genetics Cell Wall - genetics Cellulose - biosynthesis Cellulose - genetics Dinitrobenzenes - pharmacology Gene Expression Regulation, Plant Hypocotyl - cytology Hypocotyl - genetics Hypocotyl - growth & development MATERIALS SCIENCE Methyltransferases - genetics Methyltransferases - metabolism Microtubules - metabolism Mutation Pectins - biosynthesis Pectins - genetics Pectins - metabolism Plant Cells - drug effects Plant Cells - metabolism Plants, Genetically Modified Sulfanilamides - pharmacology Uronic Acids - metabolism |
title | Mutations in the Pectin Methyltransferase QUASIMODO2 Influence Cellulose Biosynthesis and Wall Integrity in Arabidopsis |
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