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New regulators of xylem lignification in arabidopsis
Umeå University, Faculty of Science and Technology, Department of Plant Physiology. (Hannele Tuominen)
2020 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

The ability of land plants to grow upright, bear their own weight and withstand adverse environmental conditions is largely dependent on the secondary xylem tissues of the stem. The xylem cells acquire thick secondary cell walls which are composed of cellulose, hemicellulose and lignin. The chemical structure of lignin renders the secondary cell wall rigid and waterproof, facilitating the transport of water and solutes through the vascular system. Lignin is a polyphenolic polymer composed of three different types of lignin units, guaiacyl (G), syringyl (S) and p-hydroxyphenyl (H), derived from the coniferyl, sinapyl and p-coumaryl alcohol, respectively. Lignin biosynthesis, monolignol transport and lignin polymerization (collectively called as ”lignification”) are controlled by numerous transcription factors and other regulators.

This thesis work uncovers three novel regulators of lignification in the secondary xylem tissues of Arabidopsis (Arabidopsis thaliana) stem and hypocotyl. The cupin domain containing protein PIRIN2 (PRN2) suppresses S-type lignin accumulation. PRN2 functions in a non-cell-autonomous fashion: it is expressed in the cells next to the xylem vessel elements, but affects the lignin composition of the vessel and fiber cell walls of the neighbouring cells. Two protein interactors of PRN2 are characterized here in connection to lignification. Opposite to the function of PRN2, the chromatin-modifying protein HISTONE MONOUBIQUITINATION2 (HUB2) promotes S-type lignin deposition. In line with this, PRN2 and HUB2 antagonistically regulate the expression of FERULATE-5-HYDROXYLASE1 which encodes the key S-type lignin-biosynthetic enzyme. Possibly, PRN2 antagonizes the S-lignin promoting function of HUB2 to ensure that the cell walls of the vessel elements get enriched in G-type lignin. Finally, identification of a potential diurnal modulator of lignin biosynthesis is described in this work. The PRN2-interacting basic helix-loop-helix transcription factor (PIB) does not influence the lignin content or composition of the secondary cell walls. However, PIB affects the diurnal expression pattern and promoter activity of some lignin-biosynthetic genes. Altogether, PRN2, HUB2 and PIB highlight the importance of intercellular co-operation in lignification, and uncover novel regulatory aspects of this process.

Abstract [sv]

Växternas förmåga att växa upprätt, bära sin egen vikt och tåla ogynnsamma miljöförhållanden styrs till stor del av stammens vaskulär vävnad som består av floem- och xylemceller. Xylemceller ackumulerar tjocka sekundära cellväggar som är sammansatta av cellulosa, hemicellulosa och lignin. Den kemiska strukturen hos lignin gör cellväggen styv och vattentät, vilket möjliggör transport av vatten och näringsämnen genom det vaskulära systemet. Lignin är en polyfenol som består av tre olika typer av lignin enheter: guaiacyl (G), syringyl (S) och p-hydroxyfenol (H). Lignin biosyntes, monolignol transport och lignin polymerisering (kollektivt kallad som "lignifiering") styrs av ett flertal transkriptionsfaktorer och andra regulatorer.

Denna avhandling avslöjar tre nya regulatorer av lignifiering i xylemvävnader av Arabidopsis (Arabidopsis thaliana) stam och hypokotyl. Genetiska och kemiska analyser avslöjade ett nytt protein, PIRIN2 (PRN2), som dämpar S-typ lignin ackumulering. PRN2 fungerar på ett icke-cell-autonomt sätt: det uttrycks i cellerna bredvid xylemkärlselement, men påverkar ligninsammansättningen hos de angränsande kärlens cellväggar. I avhandlingsarbetet identifierades och karakteriserades också två andra proteiner som interagerar med PRN2 i lignifiering. I motsats till funktionen av PRN2, det kromatin-modifierande HISTONE MONOUBIQUITINATION2 (HUB2) främjar S-typ lignin ackumulering. I linje med detta reglerar PRN2 och HUB2 antagonistiskt uttrycket av FERULATE-5-HYDROXYLASE1 som kontrollerar biosyntes av S-typ lignin. Det verkar troligt att PRN2 motverkar S-lignin främjande funktion av HUB2 för att säkerställa anrikning av G-typ lignin i kärlelementens cellväggar. Slutligen beskrivs här en helix-loop-helix transkriptionsfaktor (PIB) som potentiellt modulerar lignin biosyntes enligt dygnsrytmen. PIB påverkar inte lignin innehållet eller sammansättningen av de sekundära cellväggarna men påverkar tajmningen av genuttrycket och promotoraktiviteten hos vissa lignin-biosyntetiska gener. Sammantaget belyser PRN2, HUB2 och PIB vikten av intercellulärt samarbete i lignifiering och avslöjar nya regleringsaspekter av denna process.

Place, publisher, year, edition, pages
Umeå: Umeå University , 2020. , p. 70
Keywords [en]
Xylem, lignin, Arabidopsis, secondary cell wall, transcriptional regulation, lignin-biosynthetic gene, S/G lignin ratio
National Category
Natural Sciences Developmental Biology
Identifiers
URN: urn:nbn:se:umu:diva-176654ISBN: 978-91-7855-429-4 (electronic)ISBN: 978-91-7855-428-7 (print)OAI: oai:DiVA.org:umu-176654DiVA, id: diva2:1500629
Public defence
2020-12-10, KBC Glasburen (KBC Focus Environment), KBC huset, Umeå, 10:00 (Swedish)
Opponent
Supervisors
Available from: 2020-11-19 Created: 2020-11-12 Last updated: 2020-11-17Bibliographically approved
List of papers
1. PIRIN2 suppresses S-type lignin accumulation in a noncell-autonomous manner in Arabidopsis xylem elements
Open this publication in new window or tab >>PIRIN2 suppresses S-type lignin accumulation in a noncell-autonomous manner in Arabidopsis xylem elements
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2020 (English)In: New Phytologist, ISSN 0028-646X, E-ISSN 1469-8137, Vol. 225, no 5, p. 1923-1935Article in journal (Refereed) Published
Abstract [en]
  • PIRIN (PRN) genes encode cupin domain‐containing proteins that function as transcriptional co‐regulators in humans but that are poorly described in plants. A previous study in xylogenic cell cultures of Zinnia elegans suggested a role for a PRN protein in lignification. This study aimed to identify the function of Arabidopsis (Arabidopsis thaliana) PRN proteins in lignification of xylem tissues.
  • Chemical composition of the secondary cell walls was analysed in Arabidopsis stems and/or hypocotyls by pyrolysis–gas chromatography/mass spectrometry, 2D‐nuclear magnetic resonance and phenolic profiling. Secondary cell walls of individual xylem elements were chemotyped by Fourier transform infrared and Raman microspectroscopy.
  • Arabidopsis PRN2 suppressed accumulation of S‐type lignin in Arabidopsis stems and hypocotyls. PRN2 promoter activity and PRN2:GFP fusion protein were localised specifically in cells next to the vessel elements, suggesting a role for PRN2 in noncell‐autonomous lignification of xylem vessels. Accordingly, PRN2 modulated lignin chemistry in the secondary cell walls of the neighbouring vessel elements.
  • These results indicate that PRN2 suppresses S‐type lignin accumulation in the neighbourhood of xylem vessels to bestow G‐type enriched lignin composition on the secondary cell walls of the vessel elements. Gene expression analyses suggested that PRN2 function is mediated by regulation of the expression of the lignin‐biosynthetic genes.
Place, publisher, year, edition, pages
New Phytologist Trust, 2020
Keywords
Arabidopsis, lignification, noncell-autonomy, PIRIN, xylem vessel element
National Category
Biochemistry and Molecular Biology
Identifiers
urn:nbn:se:umu:diva-165740 (URN)10.1111/nph.16271 (DOI)000495547800001 ()31625609 (PubMedID)2-s2.0-85074993523 (Scopus ID)
Funder
Swedish Research Council, 232-2011-1312Swedish Research Council Formas, 232-2011-1312Swedish Foundation for Strategic Research , RBP14-0011Vinnova, 201600504Knut and Alice Wallenberg Foundation, 20160341Bio4Energy
Available from: 2019-12-10 Created: 2019-12-10 Last updated: 2023-03-24Bibliographically approved
2. The chromatin-modifying protein HUB2 is involved in the regulation of lignin composition in xylem vessels
Open this publication in new window or tab >>The chromatin-modifying protein HUB2 is involved in the regulation of lignin composition in xylem vessels
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2020 (English)In: Journal of Experimental Botany, ISSN 0022-0957, E-ISSN 1460-2431, Vol. 71, no 18, p. 5484-5494Article in journal (Refereed) Published
Abstract [en]

PIRIN2 (PRN2) was earlier reported to suppress syringyl (S)-type lignin accumulation of xylem vessels of Arabidopsis thaliana. In the present study, we report yeast two-hybrid results supporting the interaction of PRN2 with HISTONE MONOUBIQUITINATION2 (HUB2) in Arabidopsis. HUB2 has been previously implicated in several plant developmental processes, but not in lignification. Interaction between PRN2 and HUB2 was verified by β-galactosidase enzymatic and co-immunoprecipitation assays. HUB2 promoted the deposition of S-type lignin in the secondary cell walls of both stem and hypocotyl tissues, as analysed by pyrolysis-GC/MS. Chemical fingerprinting of individual xylem vessel cell walls by Raman and Fourier transform infrared microspectroscopy supported the function of HUB2 in lignin deposition. These results, together with a genetic analysis of the hub2 prn2 double mutant, support the antagonistic function of PRN2 and HUB2 in deposition of S-type lignin. Transcriptome analyses indicated the opposite regulation of the S-type lignin biosynthetic gene FERULATE-5-HYDROXYLASE1 by PRN2 and HUB2 as the underlying mechanism. PRN2 and HUB2 promoter activities co-localized in cells neighbouring the xylem vessel elements, suggesting that the S-type lignin-promoting function of HUB2 is antagonized by PRN2 for the benefit of the guaiacyl (G)-type lignin enrichment of the neighbouring xylem vessel elements.

Place, publisher, year, edition, pages
Oxford University Press, 2020
Keywords
Arabidopsis, cell wall chemistry, HUB2, lignin, PIRIN2, syringyl-type lignin, xylem vessels
National Category
Botany
Identifiers
urn:nbn:se:umu:diva-176306 (URN)10.1093/jxb/eraa264 (DOI)000577073500017 ()32479638 (PubMedID)2-s2.0-85096472238 (Scopus ID)
Available from: 2020-11-05 Created: 2020-11-05 Last updated: 2023-03-24Bibliographically approved
3. PIB – a potential modulator of lignification in Arabidopsis
Open this publication in new window or tab >>PIB – a potential modulator of lignification in Arabidopsis
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(English)Manuscript (preprint) (Other academic)
National Category
Natural Sciences
Identifiers
urn:nbn:se:umu:diva-176649 (URN)
Available from: 2020-11-12 Created: 2020-11-12 Last updated: 2020-11-13

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Sztojka, Bernadette

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