Transcriptomic and metabolomic reveal OsCOI2 as the jasmonate-receptor master switch in rice root

Jasmonate is an essential phytohormone involved in plant development and stress responses. Its perception occurs through the CORONATINE INSENSITIVE (COI) nuclear receptor allowing to target the Jasmonate-ZIM domain (JAZ) repressors for degradation by the 26S proteasome. Consequently, repressed transcription factors are released and expression of jasmonate responsive genes is induced. In rice, three OsCOI genes have been identified, OsCOI1a and the closely related OsCOI1b homolog, and OsCOI2. While the roles of OsCOI1a and OsCOI1b in plant defense and leaf senescence are well-established, the significance of OsCOI2 in plant development and jasmonate signaling has only emerged recently. To unravel the role of OsCOI2 in regulating jasmonate signaling, we examined the transcriptomic and metabolomic responses of jasmonate-treated rice lines mutated in both the OsCOI1a and OsCOI1b genes or OsCOI2. RNA-seq data highlight OsCOI2 as the primary driver of the extensive transcriptional reprogramming observed after a jasmonate challenge in rice roots. A series of transcription factors exhibiting an OsCOI2-dependent expression were identified, including those involved in root development or stress responses. OsCOI2-dependent expression was also observed for genes involved in specific processes or pathways such as cell-growth and secondary metabolite biosynthesis (phenylpropanoids and diterpene phytoalexins). Although functional redundancy exists between OsCOI1a/b and OsCOI2 in regulating some genes, oscoi2 plants generally exhibit a weaker response compared to oscoi1ab plants. Metabolic data revealed a shift from the primary metabolism to the secondary metabolism primarily governed by OsCOI2. Additionally, differential accumulation of oryzalexins was also observed in oscoi1ab and oscoi2 lines. These findings underscore the pivotal role of OsCOI2 in jasmonate signaling and suggest its involvement in the control of the growth-defense trade-off in rice.