Wood-specific modification of glucuronoxylan can enhance growth in <i>Populus</i>

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.