Suppression of xylan endotransglycosylase PtxtXyn10A affects cellulose microfibril angle in secondary wall in aspen wood

Marta Derba-Maceluch; Tatsuya Awano; Junko Takahashi; Jessica Lucenius; Christine Ratke; Inkeri Kontro; Marta Busse-Wicher; Ondrej Kosik; Ryo Tanaka; Anders Winzell; Asa Kallas; Joanna Lesniewska; Fredrik Berthold; Peter Immerzeel; Tuula T. Teeri; Ines Ezcurra; Paul Dupree; Ritva Serimaa; Ewa J. Mellerowicz

doi:10.1111/nph.13099

Suppression of xylan endotransglycosylase PtxtXyn10A affects cellulose microfibril angle in secondary wall in aspen wood

Marta Derba-Maceluch
, Tatsuya Awano
, Junko Takahashi
, Jessica Lucenius
, Christine Ratke
, Inkeri Kontro
, Marta Busse-Wicher
, Ondrej Kosik
, Ryo Tanaka
, Anders Winzell
, Asa Kallas
, Joanna Lesniewska
, Fredrik Berthold
, Peter Immerzeel
, Tuula T. Teeri
, Ines Ezcurra
, Paul Dupree
, Ritva Serimaa
, Ewa J. Mellerowicz^*

^*Corresponding author for this work

Not published at Aalto University

Research output: Contribution to journal › Article › Scientific › peer-review

65 Citations (Web of Science)

Abstract

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 tremulaxtremuloides).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 68kDa 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.

Original language	English
Pages (from-to)	666-681
Number of pages	16
Journal	New Phytologist
Volume	205
Issue number	2
DOIs	https://doi.org/10.1111/nph.13099
Publication status	Published - Jan 2015
MoE publication type	A1 Journal article-refereed

Funding

We thank Kjell Olofsson, Andreas Sjodin and Oskar Skogstrom, Laszlo Bako, Kirsi Leppanen and Gaia Geiss for help with the anatomy, microarrays, protoplasts, X-ray and qPCR analyses, respectively, and Anne Gouget, Lorenz Gerber and Tarek Elhasi for preliminary experiments. Andras Gorzsas from the Vibrational Spectroscopy Platform at Umea University assisted with the FTIR spectroscopic analysis and Cheng Choo Lee at the Umea Electron Microscopy Core Facility with FESEM. Financial sources: Formas (including HemiPop and FuncFiber), Swedish Research Council (VR), Swedish Governmental Agency for Innovation Systems (VINNOVA), Swedish Center for Biomimetic Fiber Engineering (funded by the Knut & Alice Wallenberg Foundation and the Foundation for Strategic Research), European projects EDEN (QLK5-CT-2001-00443) and RENEWALL, FORE, Bio4Energy, Wood Ultrastructure Research Centre, SamNordisk Skogsforskning (project no. 107), Japan Society for the Promotion of Science (JSPS KAKENHI grant no. 24580243) and the Academy of Finland (1127759).

Keywords

endotransglycosylase
growth stresses
hybrid aspen
Populus
secondary cell wall
wood formation
xylan
xylanase
PLANT-CELL-WALL
CARBOHYDRATE-ACTIVE ENZYMES
ARABIDOPSIS-THALIANA
BARLEY-ALEURONE
ARABINOGALACTAN PROTEINS
POLYSACCHARIDE ANALYSIS
SCHIZOPHYLLUM-COMMUNE
CORTICAL MICROTUBULES
GLUCURONOYL ESTERASE
GEL-ELECTROPHORESIS

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10.1111/nph.13099

Cite this

Derba-Maceluch, M., Awano, T., Takahashi, J., Lucenius, J., Ratke, C., Kontro, I., Busse-Wicher, M., Kosik, O., Tanaka, R., Winzell, A., Kallas, A., Lesniewska, J., Berthold, F., Immerzeel, P., Teeri, T. T., Ezcurra, I., Dupree, P., Serimaa, R., & Mellerowicz, E. J. (2015). Suppression of xylan endotransglycosylase PtxtXyn10A affects cellulose microfibril angle in secondary wall in aspen wood. New Phytologist, 205(2), 666-681. https://doi.org/10.1111/nph.13099

@article{1094646b98d747169a51c720d10c8d8f,

title = "Suppression of xylan endotransglycosylase PtxtXyn10A affects cellulose microfibril angle in secondary wall in aspen wood",

abstract = "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 tremulaxtremuloides).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 68kDa 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.",

keywords = "endotransglycosylase, growth stresses, hybrid aspen, Populus, secondary cell wall, wood formation, xylan, xylanase, PLANT-CELL-WALL, CARBOHYDRATE-ACTIVE ENZYMES, ARABIDOPSIS-THALIANA, BARLEY-ALEURONE, ARABINOGALACTAN PROTEINS, POLYSACCHARIDE ANALYSIS, SCHIZOPHYLLUM-COMMUNE, CORTICAL MICROTUBULES, GLUCURONOYL ESTERASE, GEL-ELECTROPHORESIS",

author = "Marta Derba-Maceluch and Tatsuya Awano and Junko Takahashi and Jessica Lucenius and Christine Ratke and Inkeri Kontro and Marta Busse-Wicher and Ondrej Kosik and Ryo Tanaka and Anders Winzell and Asa Kallas and Joanna Lesniewska and Fredrik Berthold and Peter Immerzeel and Teeri, \{Tuula T.\} and Ines Ezcurra and Paul Dupree and Ritva Serimaa and Mellerowicz, \{Ewa J.\}",

year = "2015",

month = jan,

doi = "10.1111/nph.13099",

language = "English",

volume = "205",

pages = "666--681",

journal = "New Phytologist",

issn = "0028-646X",

publisher = "Wiley",

number = "2",

}

Derba-Maceluch, M, Awano, T, Takahashi, J, Lucenius, J, Ratke, C, Kontro, I, Busse-Wicher, M, Kosik, O, Tanaka, R, Winzell, A, Kallas, A, Lesniewska, J, Berthold, F, Immerzeel, P, Teeri, TT, Ezcurra, I, Dupree, P, Serimaa, R & Mellerowicz, EJ 2015, 'Suppression of xylan endotransglycosylase PtxtXyn10A affects cellulose microfibril angle in secondary wall in aspen wood', New Phytologist, vol. 205, no. 2, pp. 666-681. https://doi.org/10.1111/nph.13099

TY - JOUR

T1 - Suppression of xylan endotransglycosylase PtxtXyn10A affects cellulose microfibril angle in secondary wall in aspen wood

AU - Derba-Maceluch, Marta

AU - Awano, Tatsuya

AU - Takahashi, Junko

AU - Lucenius, Jessica

AU - Ratke, Christine

AU - Kontro, Inkeri

AU - Busse-Wicher, Marta

AU - Kosik, Ondrej

AU - Tanaka, Ryo

AU - Winzell, Anders

AU - Kallas, Asa

AU - Lesniewska, Joanna

AU - Berthold, Fredrik

AU - Immerzeel, Peter

AU - Teeri, Tuula T.

AU - Ezcurra, Ines

AU - Dupree, Paul

AU - Serimaa, Ritva

AU - Mellerowicz, Ewa J.

PY - 2015/1

Y1 - 2015/1

N2 - 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 tremulaxtremuloides).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 68kDa 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.

AB - 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 tremulaxtremuloides).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 68kDa 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.

KW - endotransglycosylase

KW - growth stresses

KW - hybrid aspen

KW - Populus

KW - secondary cell wall

KW - wood formation

KW - xylan

KW - xylanase

KW - PLANT-CELL-WALL

KW - CARBOHYDRATE-ACTIVE ENZYMES

KW - ARABIDOPSIS-THALIANA

KW - BARLEY-ALEURONE

KW - ARABINOGALACTAN PROTEINS

KW - POLYSACCHARIDE ANALYSIS

KW - SCHIZOPHYLLUM-COMMUNE

KW - CORTICAL MICROTUBULES

KW - GLUCURONOYL ESTERASE

KW - GEL-ELECTROPHORESIS

U2 - 10.1111/nph.13099

DO - 10.1111/nph.13099

M3 - Article

SN - 0028-646X

VL - 205

SP - 666

EP - 681

JO - New Phytologist

JF - New Phytologist

IS - 2

ER -

Suppression of xylan endotransglycosylase PtxtXyn10A affects cellulose microfibril angle in secondary wall in aspen wood

Abstract

Funding

Keywords

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