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Strigolactone Promotes Cytokinin Degradation Through Transcriptional Activation OfCYTOKININ OXIDASE/DEHYDROGENASE 9in Rice

Jingbo Duan, Hong Yu, Kun Yuan, Zhigang Liao, Xiangbing Meng, Yanhui Jing, Guifu Liu, Jinfang Chu, Jiayang Li

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Strigolactones (SLs), a group of terpenoid lactones derived from carotenoids, are plant hormones that control numerous aspects of plant development. Although the framework of SL signaling that the repressor DWARF 53 (D53) could be SL-dependently degraded via the SL receptor D14 and F-box protein D3 has been established, the downstream response genes to SLs remain to be elucidated. Here we show that the cytokinin (CK) content is dramatically increased in shoot bases of the rice SL signaling mutantd53. By examining transcript levels of all the CK metabolism-related genes after treatment with SL analog GR24, we identifiedCYTOKININ OXIDASE/DEHYDROGENASE 9(OsCKX9) as a primary response gene significantly up-regulated within 1 h of treatment in the wild type but not ind53. We also found that OsCKX9 functions as a cytosolic and nuclear dual-localized CK catabolic enzyme, and that the overexpression ofOsCKX9suppresses the browning ofd53calli. Both the CRISPR/Cas9-generatedOsCKX9mutants andOsCKX9-overexpressing transgenic plants showed significant increases in tiller number and decreases in plant height and panicle size, suggesting that the homeostasis ofOsCKX9plays a critical role in regulating rice shoot architecture. Moreover, we identified the CK-inducible rice type-A response regulatorOsRR5as the secondary SL-responsive gene, whose expression is significantly repressed after 4 h of GR24 treatment in the wild type but not inosckx9. These findings reveal a comprehensive plant hormone cross-talk in which SL can induce the expression ofOsCKX9to down-regulate CK content, which in turn triggers the response of downstream genes.