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PIRIN2 suppresses S-type lignin accumulation in a noncell-autonomous manner in Arabidopsis xylem elements
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, Umeå Plant Science Centre (UPSC). Umeå University, Faculty of Science and Technology, Department of Plant Physiology.
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
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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. Vol. 225, no 5, p. 1923-1935
Keywords [en]
Arabidopsis, lignification, noncell-autonomy, PIRIN, xylem vessel element
National Category
Biochemistry and Molecular Biology
Identifiers
URN: urn:nbn:se:umu:diva-165740DOI: 10.1111/nph.16271ISI: 000495547800001PubMedID: 31625609Scopus ID: 2-s2.0-85074993523OAI: oai:DiVA.org:umu-165740DiVA, id: diva2:1376691
Funder
Swedish Research Council, 232-2011-1312Swedish Research Council Formas, 232-2011-1312Swedish Foundation for Strategic Research , RBP14-0011Vinnova, 201600504Knut and Alice Wallenberg Foundation, 20160341Bio4EnergyAvailable from: 2019-12-10 Created: 2019-12-10 Last updated: 2023-03-24Bibliographically approved
In thesis
1. New regulators of xylem lignification in arabidopsis
Open this publication in new window or tab >>New regulators of xylem lignification in arabidopsis
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
Xylem, lignin, Arabidopsis, secondary cell wall, transcriptional regulation, lignin-biosynthetic gene, S/G lignin ratio
National Category
Natural Sciences Developmental Biology
Identifiers
urn:nbn:se:umu:diva-176654 (URN)978-91-7855-429-4 (ISBN)978-91-7855-428-7 (ISBN)
Public defence
2020-12-10, KBC Glasburen (KBC Focus Environment), KBC huset, Umeå, 10:00 (Swedish)
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Supervisors
Available from: 2020-11-19 Created: 2020-11-12 Last updated: 2020-11-17Bibliographically approved

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Zhang, BoSztojka, BernadetteEscamez, SachaHedenström, MattiasWang, YinGorzsás, AndrásTuominen, Hannele

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