A COMPASS histone H3K4 trimethyltransferase pentamer transactivates drought tolerance and growth/biomass production in Populus trichocarpa

Summary Histone H3 lysine‐4 trimethylation (H3K4me3) activating drought‐responsive genes in plants for drought adaptation has long been established, but the underlying regulatory mechanisms are unknown. Here, using yeast two‐hybrid, bimolecular fluorescence complementation, biochemical analyses, transient and CRISPR‐mediated transgenesis in Populus trichocarpa , we unveiled in this adaptation a regulatory interplay between chromatin regulation and gene transactivation mediated by an epigenetic determinant, a PtrSDG2‐1–PtrCOMPASS (complex proteins associated with Set1)‐like H3K4me3 complex, PtrSDG2‐1–PtrWDR5a‐1–PtrRbBP5‐1–PtrAsh2‐2 (PtrSWRA). Under drought conditions, a transcription factor PtrAREB1‐2 interacts with PtrSWRA, forming a PtrSWRA–PtrAREB1‐2 pentamer, to recruit PtrSWRA to specific promoter elements of drought‐tolerant genes, such as PtrHox2 , PtrHox46 , and PtrHox52 , for depositing H3K4me3 to promote and maintain activated state of such genes for tolerance. CRISPR‐edited defects in the pentamer impaired drought tolerance and elevated expression of PtrHox2 , PtrHox46 , or PtrHox52 improved the tolerance as well as growth in P . trichocarpa . Our findings revealed the identity of the underlying H3K4 trimethyltransferase and its interactive arrangement with the COMPASS for catalysis specificity and efficiency. Furthermore, our study uncovered how the H3K4 trimethyltransferase–COMPASS complex is recruited to the effector genes for elevating H3K4me3 marks for improved drought tolerance and growth/biomass production in plants.