Disrupting two Arabidopsis thaliana xylosyltransferase genes results in plants deficient in thermomorphogenesis

Several cell-wall-modifying enzymes have been implicated in hypocotyl elongation; however, whether cell wall biosynthesis enzymes contribute to this process, particularly under warm temperature, remains largely unknown. In Arabidopsis, xyloglucan is a major component of the primary cell wall. Xyloglucan xylosyltransferase 1 (XXT1) and XXT2 are the major enzymes required for xyloglucan biosynthesis. Here, we investigated the roles of XXT1/2 in hypocotyl elongation with a focus under warm temperature using genetic, molecular, and transcriptomic approaches. We show that XXT1/2 are required for warm-temperature-promoted hypocotyl elongation and that the elongation phenotypes of PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) overexpression, Phytochrome B (phyB), and ELONGATED HYPOCOTYL 5 (hy5) depend partly on XXT1/2. PIF4 directly binds to and activates the promoters of XXT1 and XXT2, whereas HY5 binds to the same promoter regions and represses their expression. Importantly, the warm-temperature-induced increase in xyloglucan content is antagonistically regulated by PIF4 and HY5. Transcriptomic analyses identified warm-responsive genes whose induction depends on XXT1/2, including expansins (EXPs) and xyloglucan endotransglucosylase/hydrolases (XTHs). Mutants of some EXPs and XTHs showed compromised warm-induced hypocotyl elongation. Together, our findings identify XXT1/2 as new components of the phyB-PIF4-HY5 growth network, linking environmental signaling to the cell wall biosynthetic machinery required for hypocotyl elongation.