Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1 A903V and CESA3 T942I of cellulose synthase

Autores
Harris, Darby M.; Corbin, Kendall; Wang, Tuo; Gutierrez, Ryan; Bertolo, Ana L.; Petti, Carloalberto; Smilgies, Detlef M.; Estevez, Jose Manuel; Bonetta, Dario; Urbanowicz, Breeanna R.; Ehrhardt, David W.; Somerville, Chris R.; Rose, Jocelyn K. C.; Hong, Mei; DeBolt, Seth
Año de publicación
2012
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
The mechanisms underlying the biosynthesis of cellulose in plants are complex and still poorly understood. A central question concerns the mechanism of microfibril structure and how this is linked to the catalytic polymerization action of cellulose synthase (CESA). Furthermore, it remains unclear whether modification of cellulose microfibril structure can be achieved genetically, which could be transformative in a bio-based economy. To explore these processes in planta, we developed a chemical genetic toolbox of pharmacological inhibitors and corresponding resistance-conferring point mutations in the C-terminal transmembrane domain region of CESA1 A903V and CESA3 T942I in Arabidopsis thaliana. Using 13C solidstate nuclear magnetic resonance spectroscopy and X-ray diffraction, we show that the cellulose microfibrils displayed reduced width and an additional cellulose C4 peak indicative of a degree of crystallinity that is intermediate between the surface and interior glucans of wild type, suggesting a difference in glucan chain association during microfibril formation. Consistent with measurements of lower microfibril crystallinity, cellulose extracts from mutated CESA1 A903V and CESA3 T942I displayed greater saccharification efficiency than wild type. Using live-cell imaging to track fluorescently labeled CESA, we found that these mutants show increased CESA velocities in the plasma membrane, an indication of increased polymerization rate. Collectively, these data suggest that CESA1 A903Vand CESA3 T942I have modified microfibril structure in terms of crystallinity and suggest that in plants, as in bacteria, crystallization biophysically limits polymerization.
Fil: Harris, Darby M.. University of Kentucky; Estados Unidos
Fil: Corbin, Kendall. University of Kentucky; Estados Unidos
Fil: Wang, Tuo. University of Iowa; Estados Unidos
Fil: Gutierrez, Ryan. Carnegie Institution for Science; Estados Unidos
Fil: Bertolo, Ana L.. Cornell University; Estados Unidos
Fil: Petti, Carloalberto. University of Kentucky; Estados Unidos
Fil: Smilgies, Detlef M.. Cornell University; Estados Unidos
Fil: Estevez, Jose Manuel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Fisiología, Biología Molecular y Neurociencias. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Fisiología, Biología Molecular y Neurociencias; Argentina
Fil: Bonetta, Dario. University Of Ontario Institute Of Technology; Canadá
Fil: Urbanowicz, Breeanna R.. Cornell University; Estados Unidos. University of Georgia; Estados Unidos
Fil: Ehrhardt, David W.. Carnegie Institution for Science; Estados Unidos
Fil: Somerville, Chris R.. University of California at Berkeley; Estados Unidos
Fil: Rose, Jocelyn K. C.. Cornell University; Estados Unidos
Fil: Hong, Mei. University of Iowa; Estados Unidos
Fil: DeBolt, Seth. University of Kentucky; Estados Unidos
Materia
Cell Wall
Polysaccharide
Quinoxyphen
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/70115
Acceder
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oai_identifier_str oai:ri.conicet.gov.ar:11336/70115
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1 A903V and CESA3 T942I of cellulose synthaseHarris, Darby M.Corbin, KendallWang, TuoGutierrez, RyanBertolo, Ana L.Petti, CarloalbertoSmilgies, Detlef M.Estevez, Jose ManuelBonetta, DarioUrbanowicz, Breeanna R.Ehrhardt, David W.Somerville, Chris R.Rose, Jocelyn K. C.Hong, MeiDeBolt, SethCell WallPolysaccharideQuinoxyphenhttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1The mechanisms underlying the biosynthesis of cellulose in plants are complex and still poorly understood. A central question concerns the mechanism of microfibril structure and how this is linked to the catalytic polymerization action of cellulose synthase (CESA). Furthermore, it remains unclear whether modification of cellulose microfibril structure can be achieved genetically, which could be transformative in a bio-based economy. To explore these processes in planta, we developed a chemical genetic toolbox of pharmacological inhibitors and corresponding resistance-conferring point mutations in the C-terminal transmembrane domain region of CESA1 A903V and CESA3 T942I in Arabidopsis thaliana. Using 13C solidstate nuclear magnetic resonance spectroscopy and X-ray diffraction, we show that the cellulose microfibrils displayed reduced width and an additional cellulose C4 peak indicative of a degree of crystallinity that is intermediate between the surface and interior glucans of wild type, suggesting a difference in glucan chain association during microfibril formation. Consistent with measurements of lower microfibril crystallinity, cellulose extracts from mutated CESA1 A903V and CESA3 T942I displayed greater saccharification efficiency than wild type. Using live-cell imaging to track fluorescently labeled CESA, we found that these mutants show increased CESA velocities in the plasma membrane, an indication of increased polymerization rate. Collectively, these data suggest that CESA1 A903Vand CESA3 T942I have modified microfibril structure in terms of crystallinity and suggest that in plants, as in bacteria, crystallization biophysically limits polymerization.Fil: Harris, Darby M.. University of Kentucky; Estados UnidosFil: Corbin, Kendall. University of Kentucky; Estados UnidosFil: Wang, Tuo. University of Iowa; Estados UnidosFil: Gutierrez, Ryan. Carnegie Institution for Science; Estados UnidosFil: Bertolo, Ana L.. Cornell University; Estados UnidosFil: Petti, Carloalberto. University of Kentucky; Estados UnidosFil: Smilgies, Detlef M.. Cornell University; Estados UnidosFil: Estevez, Jose Manuel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Fisiología, Biología Molecular y Neurociencias. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Fisiología, Biología Molecular y Neurociencias; ArgentinaFil: Bonetta, Dario. University Of Ontario Institute Of Technology; CanadáFil: Urbanowicz, Breeanna R.. Cornell University; Estados Unidos. University of Georgia; Estados UnidosFil: Ehrhardt, David W.. Carnegie Institution for Science; Estados UnidosFil: Somerville, Chris R.. University of California at Berkeley; Estados UnidosFil: Rose, Jocelyn K. C.. Cornell University; Estados UnidosFil: Hong, Mei. University of Iowa; Estados UnidosFil: DeBolt, Seth. University of Kentucky; Estados UnidosNational Academy of Sciences2012-03info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/70115Harris, Darby M.; Corbin, Kendall; Wang, Tuo; Gutierrez, Ryan; Bertolo, Ana L.; et al.; Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1 A903V and CESA3 T942I of cellulose synthase; National Academy of Sciences; Proceedings of the National Academy of Sciences of The United States of America; 109; 11; 3-2012; 4098-41030027-84241091-6490CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1073/pnas.1200352109info:eu-repo/semantics/altIdentifier/url/https://www.pnas.org/content/109/11/4098info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-29T10:00:08Zoai:ri.conicet.gov.ar:11336/70115instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-29 10:00:08.295CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1 A903V and CESA3 T942I of cellulose synthase
title Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1 A903V and CESA3 T942I of cellulose synthase
spellingShingle Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1 A903V and CESA3 T942I of cellulose synthase
Harris, Darby M.
Cell Wall
Polysaccharide
Quinoxyphen
title_short Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1 A903V and CESA3 T942I of cellulose synthase
title_full Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1 A903V and CESA3 T942I of cellulose synthase
title_fullStr Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1 A903V and CESA3 T942I of cellulose synthase
title_full_unstemmed Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1 A903V and CESA3 T942I of cellulose synthase
title_sort Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1 A903V and CESA3 T942I of cellulose synthase
dc.creator.none.fl_str_mv Harris, Darby M.
Corbin, Kendall
Wang, Tuo
Gutierrez, Ryan
Bertolo, Ana L.
Petti, Carloalberto
Smilgies, Detlef M.
Estevez, Jose Manuel
Bonetta, Dario
Urbanowicz, Breeanna R.
Ehrhardt, David W.
Somerville, Chris R.
Rose, Jocelyn K. C.
Hong, Mei
DeBolt, Seth
author Harris, Darby M.
author_facet Harris, Darby M.
Corbin, Kendall
Wang, Tuo
Gutierrez, Ryan
Bertolo, Ana L.
Petti, Carloalberto
Smilgies, Detlef M.
Estevez, Jose Manuel
Bonetta, Dario
Urbanowicz, Breeanna R.
Ehrhardt, David W.
Somerville, Chris R.
Rose, Jocelyn K. C.
Hong, Mei
DeBolt, Seth
author_role author
author2 Corbin, Kendall
Wang, Tuo
Gutierrez, Ryan
Bertolo, Ana L.
Petti, Carloalberto
Smilgies, Detlef M.
Estevez, Jose Manuel
Bonetta, Dario
Urbanowicz, Breeanna R.
Ehrhardt, David W.
Somerville, Chris R.
Rose, Jocelyn K. C.
Hong, Mei
DeBolt, Seth
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv Cell Wall
Polysaccharide
Quinoxyphen
topic Cell Wall
Polysaccharide
Quinoxyphen
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv The mechanisms underlying the biosynthesis of cellulose in plants are complex and still poorly understood. A central question concerns the mechanism of microfibril structure and how this is linked to the catalytic polymerization action of cellulose synthase (CESA). Furthermore, it remains unclear whether modification of cellulose microfibril structure can be achieved genetically, which could be transformative in a bio-based economy. To explore these processes in planta, we developed a chemical genetic toolbox of pharmacological inhibitors and corresponding resistance-conferring point mutations in the C-terminal transmembrane domain region of CESA1 A903V and CESA3 T942I in Arabidopsis thaliana. Using 13C solidstate nuclear magnetic resonance spectroscopy and X-ray diffraction, we show that the cellulose microfibrils displayed reduced width and an additional cellulose C4 peak indicative of a degree of crystallinity that is intermediate between the surface and interior glucans of wild type, suggesting a difference in glucan chain association during microfibril formation. Consistent with measurements of lower microfibril crystallinity, cellulose extracts from mutated CESA1 A903V and CESA3 T942I displayed greater saccharification efficiency than wild type. Using live-cell imaging to track fluorescently labeled CESA, we found that these mutants show increased CESA velocities in the plasma membrane, an indication of increased polymerization rate. Collectively, these data suggest that CESA1 A903Vand CESA3 T942I have modified microfibril structure in terms of crystallinity and suggest that in plants, as in bacteria, crystallization biophysically limits polymerization.
Fil: Harris, Darby M.. University of Kentucky; Estados Unidos
Fil: Corbin, Kendall. University of Kentucky; Estados Unidos
Fil: Wang, Tuo. University of Iowa; Estados Unidos
Fil: Gutierrez, Ryan. Carnegie Institution for Science; Estados Unidos
Fil: Bertolo, Ana L.. Cornell University; Estados Unidos
Fil: Petti, Carloalberto. University of Kentucky; Estados Unidos
Fil: Smilgies, Detlef M.. Cornell University; Estados Unidos
Fil: Estevez, Jose Manuel. Consejo Nacional de Investigaciones Científicas y Técnicas. Oficina de Coordinación Administrativa Ciudad Universitaria. Instituto de Fisiología, Biología Molecular y Neurociencias. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Fisiología, Biología Molecular y Neurociencias; Argentina
Fil: Bonetta, Dario. University Of Ontario Institute Of Technology; Canadá
Fil: Urbanowicz, Breeanna R.. Cornell University; Estados Unidos. University of Georgia; Estados Unidos
Fil: Ehrhardt, David W.. Carnegie Institution for Science; Estados Unidos
Fil: Somerville, Chris R.. University of California at Berkeley; Estados Unidos
Fil: Rose, Jocelyn K. C.. Cornell University; Estados Unidos
Fil: Hong, Mei. University of Iowa; Estados Unidos
Fil: DeBolt, Seth. University of Kentucky; Estados Unidos
description The mechanisms underlying the biosynthesis of cellulose in plants are complex and still poorly understood. A central question concerns the mechanism of microfibril structure and how this is linked to the catalytic polymerization action of cellulose synthase (CESA). Furthermore, it remains unclear whether modification of cellulose microfibril structure can be achieved genetically, which could be transformative in a bio-based economy. To explore these processes in planta, we developed a chemical genetic toolbox of pharmacological inhibitors and corresponding resistance-conferring point mutations in the C-terminal transmembrane domain region of CESA1 A903V and CESA3 T942I in Arabidopsis thaliana. Using 13C solidstate nuclear magnetic resonance spectroscopy and X-ray diffraction, we show that the cellulose microfibrils displayed reduced width and an additional cellulose C4 peak indicative of a degree of crystallinity that is intermediate between the surface and interior glucans of wild type, suggesting a difference in glucan chain association during microfibril formation. Consistent with measurements of lower microfibril crystallinity, cellulose extracts from mutated CESA1 A903V and CESA3 T942I displayed greater saccharification efficiency than wild type. Using live-cell imaging to track fluorescently labeled CESA, we found that these mutants show increased CESA velocities in the plasma membrane, an indication of increased polymerization rate. Collectively, these data suggest that CESA1 A903Vand CESA3 T942I have modified microfibril structure in terms of crystallinity and suggest that in plants, as in bacteria, crystallization biophysically limits polymerization.
publishDate 2012
dc.date.none.fl_str_mv 2012-03
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/70115
Harris, Darby M.; Corbin, Kendall; Wang, Tuo; Gutierrez, Ryan; Bertolo, Ana L.; et al.; Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1 A903V and CESA3 T942I of cellulose synthase; National Academy of Sciences; Proceedings of the National Academy of Sciences of The United States of America; 109; 11; 3-2012; 4098-4103
0027-8424
1091-6490
CONICET Digital
CONICET
url http://hdl.handle.net/11336/70115
identifier_str_mv Harris, Darby M.; Corbin, Kendall; Wang, Tuo; Gutierrez, Ryan; Bertolo, Ana L.; et al.; Cellulose microfibril crystallinity is reduced by mutating C-terminal transmembrane region residues CESA1 A903V and CESA3 T942I of cellulose synthase; National Academy of Sciences; Proceedings of the National Academy of Sciences of The United States of America; 109; 11; 3-2012; 4098-4103
0027-8424
1091-6490
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1073/pnas.1200352109
info:eu-repo/semantics/altIdentifier/url/https://www.pnas.org/content/109/11/4098
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv National Academy of Sciences
publisher.none.fl_str_mv National Academy of Sciences
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.070432

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