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Non-Cell-Autonomous Postmortem Lignification of Tracheary Elements in Zinnia elegans
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).ORCID iD: 0000-0002-6959-3284
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. Umeå University, Faculty of Science and Technology, Umeå Plant Science Centre (UPSC).
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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. Vol. 25, no 4, 1314-1328 p.
National Category
Botany Cell Biology
Identifiers
URN: urn:nbn:se:umu:diva-76275DOI: 10.1105/tpc.113.110593ISI: 000319450500012OAI: oai:DiVA.org:umu-76275DiVA: diva2:635954
Available from: 2013-07-08 Created: 2013-07-08 Last updated: 2017-12-06Bibliographically approved
In thesis
1. Cellular Aspects of Lignin Biosynthesis in Xylem Vessels of Zinnia and Arabidopsis
Open this publication in new window or tab >>Cellular Aspects of Lignin Biosynthesis in Xylem Vessels of Zinnia and Arabidopsis
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
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:nbn:se:umu:diva-109179 (URN)978-91-7601-347-2 (ISBN)
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
2. Xylem cells cooperate in the control of lignification and cell death during plant vascular development
Open this publication in new window or tab >>Xylem cells cooperate in the control of lignification and cell death during plant vascular development
2016 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The evolutionary success of land plants was fostered by the acquisition of the xylem vascular tissue which conducts water and minerals upwards from the roots. The xylem tissue of flowering plants is composed of three main types of cells: the sap-conducting tracheary elements (TE), the fibres which provide mechanical support and the parenchyma cells which provide metabolic support to the tissue. Both the TEs and the fibres deposit thick polysaccharidic secondary cell walls (SCWs), reinforced by a rigid phenolic polymer called lignin. The cell walls of TEs form efficient water conducting hollow tubes after the TEs have undergone programmed cell death (PCD) and complete protoplast degradation as a part of their differentiation. The work presented in this thesis studied the regulation of TE PCD by characterizing the function of the candidate PCD regulator METACASPASE 9 (MC9) in Arabidopsis thaliana xylogenic cell suspensions. These cell suspensions can be externally induced to differentiate into a mix of TEs and parenchymatic non-TE cells, thus representing an ideal system to study the cellular processes of TE PCD. In this system, TEs with reduced expression of MC9 were shown to have increased levels of autophagy and to trigger the ectopic death of the non-TE cells. The viability of the non-TE cells could be restored by down-regulating autophagy specifically in the TEs with reduced MC9 expression. Therefore, this work showed that MC9 must tightly regulate the level of autophagy during TE PCD in order to prevent the TEs from becoming harmful to the non-TEs. Hence, this work demonstrated the existence of a cellular cooperation between the TEs and the surrounding parenchymatic cells during TE PCD. The potential cooperation between the TEs and the neighbouring parenchyma during the biosynthesis of lignin was also investigated. The cupin domain containing protein PIRIN2 was found to regulate TE lignification in a non-cell autonomous manner in Arabidopsis thaliana. More precisely, PIRIN2 was shown to function as an antagonist of positive transcriptional regulators of lignin biosynthetic genes in xylem parenchyma cells. Part of the transcriptional regulation by PIRIN2 involves chromatin modifications, which represent a new type of regulation of lignin biosynthesis. Because xylem constitutes the wood in tree species, this newly discovered regulation of non-cell autonomous lignification represents a potential target to modify lignin biosynthesis in order to overcome the recalcitrance of the woody biomass for the production of biofuels.

Place, publisher, year, edition, pages
Umeå University, 2016. 76 p.
Keyword
Xylem, Arabidopsis, programmed cell death, tracheary element, xylem vessel, autophagy, metacaspase, lignin, secondary cell wall, chromatin, gene expression
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-115787 (URN)978-91-7601-400-4 (ISBN)
Public defence
2016-03-04, KB3A9, KBC building, Umeå University, Umeå, 13:00 (English)
Opponent
Supervisors
Available from: 2016-02-12 Created: 2016-02-04 Last updated: 2016-02-11Bibliographically approved

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Pesquet, EdouardZhang, BoSerk, HenrikEscamez, SachaTuominen, Hannele

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Pesquet, EdouardZhang, BoPuhakainen, TuulaSerk, HenrikEscamez, SachaCourtois-Moreau, CharleenTuominen, Hannele
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