Coordination of matrix attachment and ATP-dependent chromatin remodeling regulate auxin biosynthesis and <i>Arabidopsis</i> 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.下胚轴伸长广泛受激素信号网络调控。其中，生长素代谢与信号通路在光依赖型下胚轴生长中发挥关键作用。核基质（nuclear matrix）可介导细胞核内DNA的组织排布，核基质与DNA的动态互作与基因调控密切相关。保守的支架/基质附着区（S/MARs）可通过拟南芥中的含AT钩基序的核定位蛋白（AHL）锚定至核基质。本研究发现，ESCAROLA（ESC）/AHL27与PHYTOCHROME B-4 #3抑制因子（SOB3）/AHL29在调控下胚轴伸长的生长素生物合成过程中存在冗余调控作用。这类光诱导型AHL蛋白可直接结合YUCCA9（YUC9）启动子的S/MAR区域，并通过抑制该基因的表达，抑制光培养幼苗的下胚轴生长。此外，它们还可招募SWI2/SNF2相关1（SWR1）复合物，促进组蛋白变体H2A.Z在YUC9基因座处替换H2A组蛋白，进而进一步精细调控生长素生物合成。与上述研究结果一致，生长素运输抑制剂与YUC酶系的强效化学抑制剂可恢复AHL及H2A.Z替换组分的遗传突变体的光培养长下胚轴表型。以上结果表明，基质附着与染色质修饰的协同调控是光依赖型下胚轴生长中生长素生物合成的核心分子基础。