Ethylene Signaling Is Required for Fully Functional Tension Wood in Hybrid Aspen

Tension wood (TW) in hybrid aspen trees forms on the upper side of displaced stems to generate a strain that leads to uplifting of the stem. TW is characterized by increased cambial growth, reduced vessel frequency and diameter, and the presence of gelatinous, cellulose-rich (G-)fibers with its micr...

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Main Authors: Carolin Seyfferth, Bernard A. Wessels, András Gorzsás, Jonathan W. Love, Markus Rüggeberg, Nicolas Delhomme, Thomas Vain, Kamil Antos, Hannele Tuominen, Björn Sundberg, Judith Felten
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-09-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2019.01101/full
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spelling doaj-ca29d4554b8c4f2cb02f0cb08c63c1192020-11-25T02:11:05ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2019-09-011010.3389/fpls.2019.01101467791Ethylene Signaling Is Required for Fully Functional Tension Wood in Hybrid AspenCarolin Seyfferth0Bernard A. Wessels1András Gorzsás2Jonathan W. Love3Markus Rüggeberg4Markus Rüggeberg5Nicolas Delhomme6Thomas Vain7Kamil Antos8Hannele Tuominen9Björn Sundberg10Björn Sundberg11Judith Felten12Umeå Plant Science Centre, Department of Plant Physiology, Umeå University, Umeå, SwedenUmeå Plant Science Centre, Department of Plant Physiology, Umeå University, Umeå, SwedenDepartment of Chemistry, Umeå University, Umeå, SwedenArevo AB, Umeå, SwedenInstitute for Building Materials, Swiss Federal Institute of Technology Zurich (ETH Zurich), Zurich, SwitzerlandLaboratory of Wood Materials, Swiss Federal Laboratories of Materials Science and Technology, Dubendorf, SwitzerlandUmeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Umeå, SwedenDIADE, Univ Montpellier, IRD, Montpellier, FranceDepartment of Integrative Medical Biology, Umeå University, Umeå, SwedenUmeå Plant Science Centre, Department of Plant Physiology, Umeå University, Umeå, SwedenUmeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Umeå, SwedenStora Enso AB, Nacka, SwedenUmeå Plant Science Centre, Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences, Umeå, SwedenTension wood (TW) in hybrid aspen trees forms on the upper side of displaced stems to generate a strain that leads to uplifting of the stem. TW is characterized by increased cambial growth, reduced vessel frequency and diameter, and the presence of gelatinous, cellulose-rich (G-)fibers with its microfibrils oriented parallel to the fiber cell axis. Knowledge remains limited about the molecular regulators required for the development of this special xylem tissue with its characteristic morphological, anatomical, and chemical features. In this study, we use transgenic, ethylene-insensitive (ETI) hybrid aspen trees together with time-lapse imaging to show that functional ethylene signaling is required for full uplifting of inclined stems. X-ray diffraction and Raman microspectroscopy of TW in ETI trees indicate that, although G-fibers form, the cellulose microfibril angle in the G-fiber S-layer is decreased, and the chemical composition of S- and G-layers is altered than in wild-type TW. The characteristic asymmetric growth and reduction of vessel density is suppressed during TW formation in ETI trees. A genome-wide transcriptome profiling reveals ethylene-dependent genes in TW, related to cell division, cell wall composition, vessel differentiation, microtubule orientation, and hormone crosstalk. Our results demonstrate that ethylene regulates transcriptional responses related to the amount of G-fiber formation and their properties (chemistry and cellulose microfibril angle) during TW formation. The quantitative and qualitative changes in G-fibers are likely to contribute to uplifting of stems that are displaced from their original position.https://www.frontiersin.org/article/10.3389/fpls.2019.01101/fullxylemwoodethylenetension woodligninmicrofibril angle
collection DOAJ
language English
format Article
sources DOAJ
author Carolin Seyfferth
Bernard A. Wessels
András Gorzsás
Jonathan W. Love
Markus Rüggeberg
Markus Rüggeberg
Nicolas Delhomme
Thomas Vain
Kamil Antos
Hannele Tuominen
Björn Sundberg
Björn Sundberg
Judith Felten
spellingShingle Carolin Seyfferth
Bernard A. Wessels
András Gorzsás
Jonathan W. Love
Markus Rüggeberg
Markus Rüggeberg
Nicolas Delhomme
Thomas Vain
Kamil Antos
Hannele Tuominen
Björn Sundberg
Björn Sundberg
Judith Felten
Ethylene Signaling Is Required for Fully Functional Tension Wood in Hybrid Aspen
Frontiers in Plant Science
xylem
wood
ethylene
tension wood
lignin
microfibril angle
author_facet Carolin Seyfferth
Bernard A. Wessels
András Gorzsás
Jonathan W. Love
Markus Rüggeberg
Markus Rüggeberg
Nicolas Delhomme
Thomas Vain
Kamil Antos
Hannele Tuominen
Björn Sundberg
Björn Sundberg
Judith Felten
author_sort Carolin Seyfferth
title Ethylene Signaling Is Required for Fully Functional Tension Wood in Hybrid Aspen
title_short Ethylene Signaling Is Required for Fully Functional Tension Wood in Hybrid Aspen
title_full Ethylene Signaling Is Required for Fully Functional Tension Wood in Hybrid Aspen
title_fullStr Ethylene Signaling Is Required for Fully Functional Tension Wood in Hybrid Aspen
title_full_unstemmed Ethylene Signaling Is Required for Fully Functional Tension Wood in Hybrid Aspen
title_sort ethylene signaling is required for fully functional tension wood in hybrid aspen
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2019-09-01
description Tension wood (TW) in hybrid aspen trees forms on the upper side of displaced stems to generate a strain that leads to uplifting of the stem. TW is characterized by increased cambial growth, reduced vessel frequency and diameter, and the presence of gelatinous, cellulose-rich (G-)fibers with its microfibrils oriented parallel to the fiber cell axis. Knowledge remains limited about the molecular regulators required for the development of this special xylem tissue with its characteristic morphological, anatomical, and chemical features. In this study, we use transgenic, ethylene-insensitive (ETI) hybrid aspen trees together with time-lapse imaging to show that functional ethylene signaling is required for full uplifting of inclined stems. X-ray diffraction and Raman microspectroscopy of TW in ETI trees indicate that, although G-fibers form, the cellulose microfibril angle in the G-fiber S-layer is decreased, and the chemical composition of S- and G-layers is altered than in wild-type TW. The characteristic asymmetric growth and reduction of vessel density is suppressed during TW formation in ETI trees. A genome-wide transcriptome profiling reveals ethylene-dependent genes in TW, related to cell division, cell wall composition, vessel differentiation, microtubule orientation, and hormone crosstalk. Our results demonstrate that ethylene regulates transcriptional responses related to the amount of G-fiber formation and their properties (chemistry and cellulose microfibril angle) during TW formation. The quantitative and qualitative changes in G-fibers are likely to contribute to uplifting of stems that are displaced from their original position.
topic xylem
wood
ethylene
tension wood
lignin
microfibril angle
url https://www.frontiersin.org/article/10.3389/fpls.2019.01101/full
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