Coordination of matrix attachment and ATP-dependent chromatin remodeling regulate auxin biosynthesis and Arabidopsis hypocotyl elongation

Hypocotyl elongation is extensively controlled by hormone signaling networks. In particular, auxin metabolism and signaling play key roles in light-dependent hypocotyl growth. The nuclear matrix facilitates organization of DNA within the nucleus, and dynamic interactions between nuclear matrix and DNA are related to gene regulation. Conserved scaffold/matrix attachment regions (S/MARs) are anchored to the nuclear matrix by the AT-HOOK MOTIF CONTAINING NUCLEAR LOCALIZED (AHL) proteins in Arabidopsis. Here, we found that ESCAROLA (ESC)/AHL27 and SUPPRESSOR OF PHYTOCHROME B-4 #3 (SOB3)/AHL29 redundantly regulate auxin biosynthesis in the control of hypocotyl elongation. The light-inducible AHL proteins bind directly to an S/MAR region of the YUCCA 9 (YUC9) promoter and suppress its expression to inhibit hypocotyl growth in light-grown seedlings. In addition, they recruit the SWI2/SNF2-RELATED 1 (SWR1) complex and promote exchange of H2A with the histone variant H2A.Z at the YUC9 locus to further elaborately control auxin biosynthesis. Consistent with these results, the long hypocotyl phenotypes of light-grown genetic mutants of the AHLs and H2A.Z-exchanging components were suppressed by potent chemical inhibitors of auxin transport and YUC enzymes. These results suggest that the coordination of matrix attachment and chromatin modification underlies auxin biosynthesis in light-dependent hypocotyl growth.