Wood-specific modification of glucuronoxylan can enhance growth in Populus

Abstract

Xylem cells are surrounded by primary and secondary cell walls. Formation of primary walls is regulated by the cell wall integrity surveillance system, but it is unclear if the deposition of secondary walls is similarly regulated. To study this question, we introduced to aspen three different enzymes cleaving cell wall-localized xylan and we suppressed xylan synthase components either ubiquitously or specifically during secondary wall formation using the Populus trichocarpa GT43B promoter. When xylan was ubiquitously altered, 95% of lines showed reduced growth, whereas when it was altered during secondary wall deposition, 30% of lines grew better, with the rest having no growth impairment, suggesting opposite effects of primary and secondary wall disturbances. To detect the mechanism of growth stimulation by disturbed deposition of the secondary wall, we analyzed changes in wood quality traits, chemistry, transcriptomics, metabolomics and hormonomics in transgenic lines. We found increased tension wood production, reduced S- and H-lignin, and changes in several metabolites in common in these lines. Remorin REM1.3 and NRL2 (NPH3 family) transcripts increased, and changes in jasmonates, abscisic acid, and salicylic acid occurred in secondary wall-forming xylem, suggesting their involvement in secondary wall integrity surveyance and signaling. The data indicate that a unique program mediates responses to secondary wall impairment that induces growth.Perturbation of deposition of secondary walls that are responsible for the mechanical strength of plant bodies can increase growth, with discrete changes in gene expression, hormone levels, and metabolism.

Keywords

Aspen; cell wall integrity sensing; glucuronoxylan; secondary cell wall; secondary cell wall integrity; transgenic Populus trees; wood development

Published in

Journal of Experimental Botany
2025
Publisher: OXFORD UNIV PRESS

SLU Authors

• Urbancsok, Janos

  • Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences
    

• Donev, Evgeniy

  • Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences
    
  • Center of Plant Systems Biology and Biotechnology

• Derba-Maceluch, Marta

  • Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences
    

• Sivan, Pramod

  • Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences
    
  • Royal Institute of Technology (KTH)

• Barbut, Félix

  • Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences
    

• Mitra, Madhusree

  • Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences
    

• Simura, Jan

  • Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences
    

• Mellerowicz, Ewa

  • Department of Forest Genetics and Plant Physiology, Swedish University of Agricultural Sciences
    

UKÄ Subject classification

Cell Biology
Wood Science

Publication identifier

• DOI: https://doi.org/10.1093/jxb/eraf364

Permanent link to this page (URI)

https://res.slu.se/id/publ/144785