Jasmonic acid promotes degreening via MYC2/3/4‐ and ANAC019/055/072‐mediated regulation of major chlorophyll catabolic genes

Abstract

Summary 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 MYC2/3/4 basic helix‐loop‐helix proteins directly bind to PAO promoter. Overexpression of the MYCs significantly enhanced the transcriptional activity of PAO promoter in Arabidopsis protoplasts, and methyl jasmonate (MeJA) treatment greatly induced PAO expression in wild‐type Arabidopsis plants, but the induction was abolished in myc2 myc3 myc4. In addition, MYC2/3/4 proteins could promote the expression of another Chl catabolic enzyme gene, NYC1, as well as a key regulatory gene of Chl degradation, NYE1/SGR1, 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 MYCs showed accelerated leaf yellowing upon MeJA treatment. These results suggest that MYC2/3/4 proteins may mediate jasmonic acid (JA)‐induced Chl degradation by directly activating these Chl catabolic genes (CCGs). Three NAC family proteins, ANAC019/055/072, downstream from MYC2/3/4 proteins, could also directly promote the expression of a similar set of CCGs (NYE1/SGR1, NYE2/SGR2 and NYC1) during Chl degradation. In particular, anac019 anac055 anac072 triple mutant displayed a severe stay‐green phenotype after MeJA treatment. Finally, we revealed that MYC2 and ANAC019 may interact with each other and synergistically enhance NYE1 expression. Together, our study reveals a hierarchical and coordinated regulatory network of JA‐induced Chl degradation.

The Jasmonate-Activated Transcription Factor MdMYC2 Regulates ETHYLENE RESPONSE FACTOR and Ethylene Biosynthetic Genes to Promote Ethylene Biosynthesis during Apple Fruit Ripening

“…A similar phenomenon was observed for JA-promoted chlorophyll degradation in Arabidopsis (Zhu et al, 2015). In that study, AtMYC2 bound to the promoter of pheophorbide a oxygenase (PAO) gene, a key gene in chlorophyll degradation.…”

“…In that study, AtMYC2 bound to the promoter of pheophorbide a oxygenase (PAO) gene, a key gene in chlorophyll degradation. Following JA treatment, AtPAO expression was enhanced in control plants but was not altered in AtMYC2-silenced plants, whereas in the absence of JA treatment, AtPAO expression did not significantly differ between the control and AtMYC2-silenced plants (Zhu et al, 2015). These results suggest that MYC2 cannot activate the transcription of downstream genes without JA.…”

BrWRKY65, a WRKY Transcription Factor, Is Involved in Regulating Three Leaf Senescence-Associated Genes in Chinese Flowering Cabbage

“…Accordingly, whether BrWRKY65 and BrWRKY75 act together or individually to regulate SAGs is an interesting research issue in the future. Moreover, it has been reported other types of Arabidopsis TFs, such as ABSCISIC ACID INSENSITIVE3 (ABI3) [47], ABI5, ENHANCED EM LEVEL (EEL) [48], phytochrome-interacting factor 4 (PIF4) [49], MYC2/3/4 [50], ANAC072 [43], and ERF [51], are reported to activate genes related to chlorophyll degradation such as NYE1 (also known as SGR1 ), NYC1 , and PAO (pheophorbide a oxygenase) via directly binding to their promoters, leading to accelerated chlorophyll degradation during leaf senescence, seed or fruit degreening. Intriguingly, Arabidopsis ETHYLENE INSENSITIVE3 (EIN3) and ORE1/NAC2 establish a network controlling ethylene-induced leaf senescence via directly targeting NYE1 , NYC1 , and PAO [52].…”

The Role of Specialized Photoreceptors in the Protection of Energy‐Rich Tissues

“…There is good evidence that wounding actively suppresses photosynthesis, as the decrease in photosynthesis is greater than the amount of tissue damaged and requires intact JA signaling [52,53]. Recently, the key defense regulator MYC2 was shown to directly trigger expression of genes involved in chlorophyll degradation, suggesting a mechanism of JA-mediated suppression of photosynthesis [54,55]. However, other evidence questions whether photosynthesis is genuinely suppressed during defense responses.…”