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Cellular Aspects of Lignin Biosynthesis in Xylem Vessels of Zinnia and Arabidopsis
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Lignin is the second most abundant biopolymer on earth and is found in the wood (xylem) of vascular land plants. To transport the hydro-mineral sap, xylem forms specialized conduit cells, called tracheary elements (TEs), which are hollow dead cylinders reinforced with lateral secondary cell walls (SCW). These SCWs incorporate lignin to gain mechanical strength, water impermeability and resistance against pathogens. The aim of this thesis is to understand the spatio-temporal deposition of lignin during TE differentiation and the relationship with its neighbouring cells. In vitro TE differentiating cell cultures of Zinnia elegans and Arabidopsis thaliana are ideal tools to study this process: cells differentiate simultaneously into 30-50% TEs while the rest remain parenchymatic (non-TEs). Live-cell imaging of such TEs indicated that lignification occurs after programmed cell death (PCD), in a non-cell autonomous manner, in which the non-TEs provide the lignin monomers.

This thesis confirms that lignification occurs and continues long after TE PCD in both in vitro TE cultures and whole plants using biochemical, pharmacological and cytological methods. The cooperative supply of lignin monomers by the non-TEs was demonstrated by using Zinnia and Arabidopsis in vitro TE cultures. Inhibitor experiments revealed further that the non-TEs supply reactive oxygen species (ROS) to TEs and that ROS are required for TE post-mortem lignification. Characterization of the non-TEs showed an enlarged nucleus with increased DNA content, thus indicating that non-TEs are in fact endoreplicated xylem parenchyma cells (XP). The cooperative lignification was confirmed in whole plants by using knock-out mutants in a lignin monomer synthesis gene, which exhibit reduced TE lignification. The XP specific complementation of these mutants led to nearly completely rescuing the TE lignin reduction. Using microscopic techniques, the spatial distribution of lignin was analyzed in TEs from in vitro cultures and whole plants, revealing that lignification is restricted to TE SCWs in both protoxylem and metaxylem. These specific deposition domains were established by phenoloxidases, i.e. laccases localized to SCWs and peroxidases, present in SCWs and the apoplastic space. Laccases were cell-autonomously produced by developing TEs, indicating that the deposition domains are defined before PCD.

Altogether, these results highlight that the hydro-mineral sap transport through TEs is enabled by the spatially and temporally controlled lignification of the SCW. Lignification occurs post-mortem by the supply of monomers and ROS from neighbouring XP cells and is restricted to specific deposition domains, defined by the pre-mortem sequestration of phenoloxidases.     

Place, publisher, year, edition, pages
Umeå: Umeå universitet , 2015. , 87 p.
Keyword [en]
Lignin, tracheary elements, xylem/wood, post-mortem lignification, non-cell autonomous process, xylem parenchyma, endoreplication, reactive oxygen species, laccases, peroxidases
National Category
Botany
Research subject
Molecular Cellbiology
Identifiers
URN: urn:nbn:se:umu:diva-109179ISBN: 978-91-7601-347-2 (print)OAI: oai:DiVA.org:umu-109179DiVA: diva2:855662
Public defence
2015-10-16, KB3A9, KBC huset, Umeå, 13:30 (English)
Opponent
Supervisors
Available from: 2015-09-25 Created: 2015-09-22 Last updated: 2015-11-16Bibliographically approved
List of papers
1. Non-Cell-Autonomous Postmortem Lignification of Tracheary Elements in Zinnia elegans
Open this publication in new window or tab >>Non-Cell-Autonomous Postmortem Lignification of Tracheary Elements in Zinnia elegans
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2013 (English)In: The Plant Cell, ISSN 1040-4651, E-ISSN 1532-298X, Vol. 25, no 4, 1314-1328 p.Article in journal (Refereed) Published
Abstract [en]

Postmortem lignification of xylem tracheary elements (TEs) has been debated for decades. Here, we provide evidence in Zinnia elegans TE cell cultures, using pharmacological inhibitors and in intact Z. elegans plants using Fourier transform infrared microspectroscopy, that TE lignification occurs postmortem (i.e., after TE programmed cell death). In situ RT-PCR verified expression of the lignin monomer biosynthetic cinnamoyl CoA reductase and cinnamyl alcohol dehydrogenase in not only the lignifying TEs but also in the unlignified non-TE cells of Z. elegans TE cell cultures and in living, parenchymatic xylem cells that surround TEs in stems. These cells were also shown to have the capacity to synthesize and transport lignin monomers and reactive oxygen species to the cell walls of dead TEs. Differential gene expression analysis in Z. elegans TE cell cultures and concomitant functional analysis in Arabidopsis thaliana resulted in identification of several genes that were expressed in the non-TE cells and that affected lignin chemistry on the basis of pyrolysis-gas chromatography/mass spectrometry analysis. These data suggest that living, parenchymatic xylem cells contribute to TE lignification in a non-cellautonomous manner, thus enabling the postmortem lignification of TEs.

Place, publisher, year, edition, pages
American Society of Plant Biologists, 2013
National Category
Botany Cell Biology
Identifiers
urn:nbn:se:umu:diva-76275 (URN)10.1105/tpc.113.110593 (DOI)000319450500012 ()
Available from: 2013-07-08 Created: 2013-07-08 Last updated: 2017-12-06Bibliographically approved
2. Cooperative lignification of xylem tracheary elements
Open this publication in new window or tab >>Cooperative lignification of xylem tracheary elements
2015 (English)In: Plant Signalling & Behavior, ISSN 1559-2316, E-ISSN 1559-2324, Vol. 10, no 4, e1003753Article in journal (Refereed) Published
Abstract [en]

The development of xylem tracheary elements (TEs) – the hydro-mineral sap conducting cells - has been an evolutionary breakthrough to enable long distance nutrition and upright growth of vascular land plants. To allow sap conduction, TEs form hollow laterally reinforced cylinders by combining programmed cell death and secondary cell wall formation. To ensure their structural resistance for sap conduction, TE cell walls are reinforced with the phenolic polymer lignin, which is deposited after TE cell death by the cooperative supply of monomers and other substrates from the surrounding living cells.

Place, publisher, year, edition, pages
Taylor & Francis Group, 2015
Keyword
lignin, non-cell autonomous process, post-mortem lignification, secondary cell wall, tracheary elements, xylem/wood vessels
National Category
Cell Biology
Identifiers
urn:nbn:se:umu:diva-108895 (URN)10.1080/15592324.2014.1003753 (DOI)000362317900003 ()
Funder
Swedish Research Council, 2010-4620
Available from: 2015-09-21 Created: 2015-09-17 Last updated: 2017-12-04Bibliographically approved
3. The post-mortem spatial restriction of lignification in protoxylem and metaxylem vessels of Zinnia elegans is controlled by laccases and peroxidases
Open this publication in new window or tab >>The post-mortem spatial restriction of lignification in protoxylem and metaxylem vessels of Zinnia elegans is controlled by laccases and peroxidases
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(English)Manuscript (preprint) (Other academic)
National Category
Botany
Research subject
Molecular Cellbiology
Identifiers
urn:nbn:se:umu:diva-109150 (URN)
Available from: 2015-09-21 Created: 2015-09-21 Last updated: 2015-09-22
4. The formation and function of plant vascular system requires intra-tissular cell cooperation
Open this publication in new window or tab >>The formation and function of plant vascular system requires intra-tissular cell cooperation
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(English)Manuscript (preprint) (Other academic)
National Category
Botany
Research subject
Molecular Cellbiology
Identifiers
urn:nbn:se:umu:diva-109152 (URN)
Available from: 2015-09-21 Created: 2015-09-21 Last updated: 2015-09-22

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