Jasmonic acid promotes degreening via MYC 2/3/4‐ and ANAC 019/055/072‐mediated regulation of major chlorophyll catabolic genes

Degreening caused by rapid chlorophyll (Chl) degradation is a characteristic event during green organ senescence or maturation. Pheophorbide a oxygenase gene ( PAO ) encodes a key enzyme of Chl degradation, yet its transcriptional regulation remains largely unknown. Using yeast one‐hybrid screening, coupled with in vitro and in vivo assays, we revealed that Arabidopsis MYC 2/3/4 basic helix‐loop‐helix proteins directly bind to PAO promoter. Overexpression of the MYC s significantly enhanced the transcriptional activity of PAO promoter in Arabidopsis protoplasts, and methyl jasmonate (Me JA ) treatment greatly induced PAO expression in wild‐type Arabidopsis plants, but the induction was abolished in myc2 myc3 myc4 . In addition, MYC 2/3/4 proteins could promote the expression of another Chl catabolic enzyme gene, NYC 1 , as well as a key regulatory gene of Chl degradation, NYE 1/ SGR 1 , by directly binding to their promoters. More importantly, the myc2 myc3 myc4 triple mutant showed a severe stay‐green phenotype, whereas the lines overexpressing the MYC s showed accelerated leaf yellowing upon Me JA treatment. These results suggest that MYC 2/3/4 proteins may mediate jasmonic acid ( JA )‐induced Chl degradation by directly activating these Chl catabolic genes ( CCG s). Three NAC family proteins, ANAC 019/055/072, downstream from MYC 2/3/4 proteins, could also directly promote the expression of a similar set of CCG s ( NYE 1 / SGR 1 , NYE 2 / SGR 2 and NYC 1 ) during Chl degradation. In particular, anac019 anac055 anac072 triple mutant displayed a severe stay‐green phenotype after Me JA treatment. Finally, we revealed that MYC 2 and ANAC 019 may interact with each other and synergistically enhance NYE 1 expression. Together, our study reveals a hierarchical and coordinated regulatory network of JA ‐induced Chl degradation. De‐greening, caused by rapid chlorophyll degradation, is the most obvious symptom of senescent leaves. Jasmonic acid promotes chlorophyll degradation, but the underlying molecular mechanism was unknown. Here we show that jasmonic acid‐responsive MYC and NAC transcription factors coordinately promote chlorophyll degradation by directly activating chlorophyll catabolic genes.