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.

Center of Plant Systems Biology and Biotechnology 14 St Knyaz Boris 1 Pokrastitel str Plovdiv 4023 Bulgaria

Department of Forest Genetics and Plant Physiology Umeå Plant Science Centre Swedish University of Agricultural Sciences Umeå 901 83 Sweden

Division of Glycoscience Department of Chemistry KTH Royal Institute of Technology AlbaNova University Centre Stockholm 106 91 Sweden

Laboratory of Growth Regulators Institute of Experimental Botany the Czech Academy of Sciences and Palacký University Šlechtitelů 27 Olomouc CZ 779 00 Czech Republic

RISE Research Institutes of Sweden Drottning Kristinas väg 61 Stockholm 11428 Sweden

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