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Xylem cells cooperate in the control of lignification and cell death during plant vascular development
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: 0000-0001-7049-6978
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 [en]
Xylem, Arabidopsis, programmed cell death, tracheary element, xylem vessel, autophagy, metacaspase, lignin, secondary cell wall, chromatin, gene expression
National Category
Botany
Identifiers
URN: urn:nbn:se:umu:diva-115787ISBN: 978-91-7601-400-4 (print)OAI: oai:DiVA.org:umu-115787DiVA: diva2:900504
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
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. METACASPASE9 modulates autophagy to confine cell death tothe target cells during Arabidopsis vascular xylem differentiation
Open this publication in new window or tab >>METACASPASE9 modulates autophagy to confine cell death tothe target cells during Arabidopsis vascular xylem differentiation
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2016 (English)In: Biology Open, ISSN 2046-6390, Vol. 5, no 2, 122-129 p.Article in journal (Refereed) Published
Abstract [en]

We uncovered that the level of autophagy in plant cells undergoingprogrammed cell death determines the fate of the surrounding cells.Our approach consisted of using Arabidopsis thaliana cell culturescapable of differentiating into two different cell types: vasculartracheary elements (TEs) that undergo programmed cell death(PCD) and protoplast autolysis, and parenchymatic non-TEs thatremain alive. The TE cell type displayed higher levels of autophagywhen expression of the TE-specific METACASPASE9 (MC9) wasreduced using RNAi (MC9-RNAi). Misregulation of autophagy in theMC9-RNAi TEs coincided with ectopic death of the non-TEs, implyingthe existence of an autophagy-dependent intercellular signallingfrom within the TEs towards the non-TEs. Viability of the non-TEswas restored when AUTOPHAGY2 (ATG2) was downregulatedspecifically in MC9-RNAi TEs, demonstrating the importance ofautophagy in the spatial confinement of cell death. Our resultssuggest that other eukaryotic cells undergoing PCD might also needto tightly regulate their level of autophagy to avoid detrimentalconsequences for the surrounding cells.

Place, publisher, year, edition, pages
The Company of Biologists ltd, 2016
Keyword
Arabidopsis thaliana, Autophagy, Intercellular signalling, Metacaspase, Programmed cell death, Tracheary element
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-115784 (URN)10.1242/bio.015529 (DOI)000370240300005 ()26740571 (PubMedID)
Available from: 2016-02-04 Created: 2016-02-04 Last updated: 2016-04-08Bibliographically approved
3. PIRIN2 controls chromatin modification of lignin biosynthetic genes and modulates the non-cell autonomous xylem lignification in Arabidopsis thaliana
Open this publication in new window or tab >>PIRIN2 controls chromatin modification of lignin biosynthetic genes and modulates the non-cell autonomous xylem lignification in Arabidopsis thaliana
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(English)Manuscript (preprint) (Other academic)
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-116697 (URN)
Available from: 2016-02-10 Created: 2016-02-10 Last updated: 2016-02-11Bibliographically approved
4. The bHLH62 transcription factor is involved in the PIRIN2-dependent regulation of lignification in the xylem of Arabidopsis thaliana
Open this publication in new window or tab >>The bHLH62 transcription factor is involved in the PIRIN2-dependent regulation of lignification in the xylem of Arabidopsis thaliana
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(English)Manuscript (preprint) (Other academic)
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-116698 (URN)
Available from: 2016-02-10 Created: 2016-02-10 Last updated: 2016-02-11Bibliographically approved

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