Unraveling the Role of Xylan in the Integrity of Secondary Cell Walls: insights from Arabidopsis and Aspen

Plants have conquered lands by developing wood, with cells having secondary cell walls (SCW), which allowed them to thrive in various environments and reach heights up to a hundred meters. Wood is also the main reservoir of the assimilated carbon. Given current societal challenges, there is a pressing need for better utilization of this renewable resource, underscoring the importance of understanding the dynamic process of SCW deposition. In this thesis, I explored the role of xylan in the SCW integrity of Arabidopsis and Populus, which allowed me to uncover some differences between herbaceous and tree species. As the SCW integrity sensing pathways are not understood, I first searched for the members of the CrRLK1L family expressed during SCW formation in Populus because these proteins function as primary cell wall integrity sensing. I discovered that Populus possesses an extended array of malectin domain receptors expressed in tissues forming SCWs, reflecting the trees' adaptation to withstand higher negative vascular pressures and support perennial growth. Moreover, I studied changes following mechanical stimuli in Populus stems because mechanosensing pathway overlaps with cell wall integrity sensing. I found that tree growth was increased after repetitive stem bending and that jasmonic acid and polyamine signaling were activated. To determine the role of xylan in SCW integrity, I studied transgenic plants with altered xylan structure. Removal of the xylan MeGlcA side chain affected the binding of suberin-like compounds to cell walls without inducing any SCW integrity stress responses. Conversely, xylan backbone-impaired plants exhibited altered abscisic acid, ethylene, and cytokinin levels and changes in the expression of signaling and stress-related genes, which could participate in SCW integrity sensing and signaling. Finally, I studied the effect of xylan backbone impairment on drought responses in Arabidopsis and Populus. Xylan backbone-impaired plants exhibited different susceptibilities to drought, underscoring xylan pivotal role in cell wall architecture and overall plant physiology. Through this thesis, I have advanced our understanding of plant SCW integrity maintenance and identified potential targets for priming and genetic engineering. These findings hold significant implications for enhancing biomass production for biorefinery and plant resilience.