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. Jasmonate perception occurs through the COI nuclear receptor allowing to target the JAZs repressors for degradation by the 26S proteasome. Consequently, repressed transcription factors are released and expression of JA-responsive genes is induced. In rice, three OsCOI genes have been identified, OsCOI1a and the closely related OsCOI1b homolog, and OsCOI2. While a role for OsCOI-1a and -1b genes was previously established in plant defense or leaf senescence, evidence for an important role of OsCOI2 in plant development, jasmonate-signaling and defence emerged only recently. To decipher the role of OsCOI2 in regulating jasmonate responses, we used rice mutant lines, edited both in the OsCOI1a and OsCOI1b genes, or in the OsCOI2 gene. Rice roots from WT and oscoi lines were treated by jasmonate to establish the molecular responses of each line, at the transcriptomic and metabolomic levels. RNA-seq data indicate that OsCOI2 is the main actor of the large transcriptional reprogramming observed after a JA challenge in rice roots. A series of transcription factors with an OsCOI2-dependent expression was identified, including transcription factors known to have a role in root development or stress response. An OsCOI2-dependent expression was detected for genes involved in specific processes or pathways such as photosynthesis, cell-growth and secondary metabolite biosynthesis (phenylpropanoids and diterpene phytoalexins). Functional redundancy between OsCOI1a/b and OsCOI2 can be shown for some genes, even if a lower response usually occurred in oscoi2 plants compared to oscoi1ab plants. Metabolic data revealed a shift from the primary metabolism to the secondary metabolism that is mainly OsCOI2-dependent. Differential accumulation of oryzalexins was also observed in oscoi lines.These data validate the major role of OsCOI2 in JA responses in rice roots. OsCOI2 is the major regulator of specialized metabolic pathways related to development and production of secondary metabolites. This study suggests that OsCOI2 controls the growth-defense trade-off in response to JA. Overall design: To decipher the molecular responses controlled by the OsCOI receptors in rice roots, we used rice edited lines, either edited in both the oscoi1a and oscoi1b genes, or edited in the oscoi2 gene. Rice roots were submitted to JA treatment to compare the molecular responses of the oscoi edited plants to the WT plants.