Disruption of allene oxide cyclase in maize reveals the necessity of enzymatically produced 12-OPDA for the induction of jasmonic acid during herbivory

Authors: Hunter Iii, Charles; Gorman, Zachary; Li, Qin Bao; Sorg, Ariel; Rering, Caitlin; Block, Anna; CHRISTENSEN, SHAWN - Brigham Young University

Submitted to: The Plant Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/25/2025
Publication Date: 5/9/2025
Citation: Hunter III, C.T., Gorman, Z.J., Li, Q., Sorg, A.M., Rering, C.C., Block, A.K., Christensen, S. 2025. Disruption of allene oxide cyclase in maize reveals the necessity of enzymatically produced 12-OPDA for the induction of jasmonic acid during herbivory. The Plant Journal. 122,e70209. https://doi.org/10.1111/tpj.70209.
DOI: https://doi.org/10.1111/tpj.70209

Interpretive Summary: Plant hormones such as 12-oxo-phydienoic acid (12-OPDA) and Jasmonic acid (JA) regulate defenses against insect pests and fungal pathogens. The biosynthesis of 12-OPDA and JA is regulated by allene oxide cyclase (AOC), the enzyme responsible for the first committed step in the pathway. ARS researchers at the Center for Medical, Agricultural, and Veterinary Entomology, in Gainesville FL have used gene editing to remove the function of AOC in maize in order to discern the effects of AOC-deficiency. Surprisingly, the AOC-deficient maize lines maintained a limited capacity for 12-OPDA synthesis, revealing an alternative route independent of AOC for12-OPDA biosynthesis. The mutants also revealed a disassociation between production of lipid-bound versus free 12-OPDA, providing evidence for independent regulation of these pathways. These findings are counter to current dogma and represent important advancements in our understanding of 12-OPDA and JA metabolism in plants. The gene edited maize lines developed in this study provide useful tools for continued studies of the roles of 12-OPDA and JA and will help facilitate development of crops with greater resiliency against pathogens and insects.

Technical Abstract: • The hormones 12-oxo-phydienoic acid (12-OPDA) and Jasmonic acid (JA) underly diverse developmental and plant defense processes. Allene oxide cyclase (AOC) catalyzes formation of 12-OPDA from allene oxide, a committed step in jasmonate formation. Here the effects of eliminating AOC function in maize are investigated. • Gene editing was employed to disrupt a pair of redundant AOC-coding genes. Bioassays with Spodoptera frugiperda, targeted metabolomics, and gene expression analyses were used to characterize AOC-deficient plants. • Disruption of AOC led to feminization of male florets and increased sensitivity to biotic stresses. Mutants retained the capacity to produce cyclopentones downstream of AOC, having 10-20% normal levels of 12-OPDA and 1-2% normal levels of JA. Mutants had lower levels of most free oxylipins and altered hormone profiles characteristic of JA deficiency. Counter to expectations, OPDA-containing galactolipids were not affected by loss of AOC. • This study improves our understanding about the roles of jasmonates in maize development and defense. Production of 12-OPDA in the mutants reveals the capacity for 12-OPDA formation in the absence of AOC, either by autocyclization of allene oxide or via alternative cyclases. The mutants also reveal an unexpected disconnect in the synthesis of free versus bound oxylipins.