Strigolactone promotes cytokinin degradation through transcriptional activation of CYTOKININ OXIDASE/DEHYDROGENASE 9 in rice

Proc Natl Acad Sci U S A. 2019 Jul 9;116(28):14319-14324. doi: 10.1073/pnas.1810980116. Epub 2019 Jun 24.

Abstract

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 mutant d53 By examining transcript levels of all the CK metabolism-related genes after treatment with SL analog GR24, we identified CYTOKININ OXIDASE/DEHYDROGENASE 9 (OsCKX9) as a primary response gene significantly up-regulated within 1 h of treatment in the wild type but not in d53 We also found that OsCKX9 functions as a cytosolic and nuclear dual-localized CK catabolic enzyme, and that the overexpression of OsCKX9 suppresses the browning of d53 calli. Both the CRISPR/Cas9-generated OsCKX9 mutants and OsCKX9-overexpressing transgenic plants showed significant increases in tiller number and decreases in plant height and panicle size, suggesting that the homeostasis of OsCKX9 plays a critical role in regulating rice shoot architecture. Moreover, we identified the CK-inducible rice type-A response regulator OsRR5 as the secondary SL-responsive gene, whose expression is significantly repressed after 4 h of GR24 treatment in the wild type but not in osckx9 These findings reveal a comprehensive plant hormone cross-talk in which SL can induce the expression of OsCKX9 to down-regulate CK content, which in turn triggers the response of downstream genes.

Keywords: OsCKX9; cytokinin; hormonal crosstalk; rice; strigolactone.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cytokinins / genetics
  • Cytokinins / metabolism*
  • F-Box Proteins / genetics*
  • F-Box Proteins / metabolism
  • Gene Expression Regulation, Plant / drug effects
  • Heterocyclic Compounds, 3-Ring / pharmacology*
  • Lactones / metabolism
  • Lactones / pharmacology*
  • Oryza / genetics
  • Oryza / metabolism
  • Oxidoreductases / genetics*
  • Oxidoreductases / metabolism
  • Plant Growth Regulators / genetics*
  • Plant Growth Regulators / metabolism
  • Plant Shoots / genetics
  • Plant Shoots / growth & development
  • Plants, Genetically Modified / genetics
  • Plants, Genetically Modified / growth & development
  • Protein Binding / genetics
  • Signal Transduction / genetics
  • Transcriptional Activation / genetics

Substances

  • Cytokinins
  • F-Box Proteins
  • GR24 compound
  • GR24 strigolactone
  • Heterocyclic Compounds, 3-Ring
  • Lactones
  • Plant Growth Regulators
  • Oxidoreductases
  • cytokinin oxidase