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Arabidopsis XTH4 and XTH9 Contribute to Wood Cell Expansion and Secondary Wall Formation

Kushwah, Sunita and Banasiak, Alicja and Nishikubo, Nobuyuki and Derba-Maceluch, Marta and Majda, Mateusz and Endo, Satoshi and Kumar, Vikash and Gomez, Leonardo and Gorzsas, Andras and McQueen-Mason, Simon and Braam, Janet and Sundberg, Björn and Mellerowicz, Ewa (2020). Arabidopsis XTH4 and XTH9 Contribute to Wood Cell Expansion and Secondary Wall Formation. Plant Physiology. 182 , 1946-1965
[Research article]

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Abstract

Xylem cell expansion and fiber intrusive tip growth require the activity of enzymes that rearrange xyloglucan in cell walls, and their deficiency not only affects cell expansion but alters subsequent secondary wall formation via cell wall integrity-sensing mechanisms.Xyloglucan is the major hemicellulose of dicotyledon primary cell walls, affecting the load-bearing framework with the participation of xyloglucan endo-transglycosylase/hydrolases (XTHs). We used loss- and gain-of function approaches to study functions of XTH4 and XTH9 abundantly expressed in cambial regions during secondary growth of Arabidopsis (Arabidopsis thaliana). In secondarily thickened hypocotyls, these enzymes had positive effects on vessel element expansion and fiber intrusive growth. They also stimulated secondary wall thickening but reduced secondary xylem production. Cell wall analyses of inflorescence stems revealed changes in lignin, cellulose, and matrix sugar composition indicating an overall increase in secondary versus primary walls in mutants, indicative of higher xylem production compared with the wild type (since secondary walls were thinner). Intriguingly, the number of secondary cell wall layers compared with the wild type was increased in xth9 and reduced in xth4, whereas the double mutant xth4x9 displayed an intermediate number of layers. These changes correlated with specific Raman signals from the walls, indicating changes in lignin and cellulose. Secondary walls were affected also in the interfascicular fibers, where neither XTH4 nor XTH9 was expressed, indicating that these effects were indirect. Transcripts involved in secondary wall biosynthesis and cell wall integrity sensing, including THESEUS1 and WALL ASSOCIATED KINASE2, were highly induced in the mutants, indicating that deficiency in XTH4 and XTH9 triggers cell wall integrity signaling, which, we propose, stimulates xylem cell production and modulates secondary wall thickening. Prominent effects of XTH4 and XTH9 on secondary xylem support the hypothesis that altered xyloglucan affects wood properties both directly and via cell wall integrity sensing.

Authors/Creators:Kushwah, Sunita and Banasiak, Alicja and Nishikubo, Nobuyuki and Derba-Maceluch, Marta and Majda, Mateusz and Endo, Satoshi and Kumar, Vikash and Gomez, Leonardo and Gorzsas, Andras and McQueen-Mason, Simon and Braam, Janet and Sundberg, Björn and Mellerowicz, Ewa
Title:Arabidopsis XTH4 and XTH9 Contribute to Wood Cell Expansion and Secondary Wall Formation
Series Name/Journal:Plant Physiology
Year of publishing :2020
Volume:182
Page range:1946-1965
Number of Pages:20
Publisher:AMER SOC PLANT BIOLOGISTS
ISSN:0032-0889
Language:English
Publication Type:Research article
Article category:Scientific peer reviewed
Version:Published version
Full Text Status:Public
Subjects:(A) Swedish standard research categories 2011 > 1 Natural sciences > 106 Biological Sciences (Medical to be 3 and Agricultural to be 4) > Botany
(A) Swedish standard research categories 2011 > 1 Natural sciences > 106 Biological Sciences (Medical to be 3 and Agricultural to be 4) > Cell Biology
URN:NBN:urn:nbn:se:slu:epsilon-p-105613
Permanent URL:
http://urn.kb.se/resolve?urn=urn:nbn:se:slu:epsilon-p-105613
Additional ID:
Type of IDID
DOI10.1104/pp.19.01529
Web of Science (WoS)000526827500048
ID Code:24584
Faculty:S - Faculty of Forest Sciences
Department:(S) > Dept. of Forest Genetics and Plant Physiology
Deposited By: SLUpub Connector
Deposited On:21 Jun 2021 14:46
Metadata Last Modified:21 Jun 2021 14:51

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