Maize OPR2 and LOX10 Mediate Defense against Fall Armyworm and Western Corn Rootworm by Tissue-Specific Regulation of Jasmonic Acid and Ketol Metabolism

Abstract

Foliage-feeding fall armyworm (FAW; Spodoptera frugiperda) and root-feeding western corn rootworm (WCR; Diabrotica virgifera virgifera) are maize (Zea mays L.) pests that cause significant yield losses. Jasmonic acid (JA) plays a pivotal defense role against insects. 12-oxo-phytodienoic acid (12-OPDA) is converted into JA by peroxisome-localized OPDA reductases (OPR). However, little is known about the physiological functions of cytoplasmic OPRs. Here, we show that disruption of ZmOPR2 reduced wound-induced JA production and defense against FAW while accumulating more JA catabolites. Overexpression of ZmOPR2 in Arabidopsis enhanced JA production and defense against beet armyworm (BAW; Spodoptera exigua). In addition, lox10opr2 double mutants were more susceptible than either single mutant, suggesting that ZmOPR2 and ZmLOX10 uniquely and additively contributed to defense. In contrast to the defensive roles of ZmOPR2 and ZmLOX10 in leaves, single mutants did not display any alteration in root herbivory defense against WCR. Feeding on lox10opr2 double mutants resulted in increased WCR mortality associated with greater herbivory-induced production of insecticidal death acids and ketols. Thus, ZmOPR2 and ZmLOX10 cooperatively inhibit the synthesis of these metabolites during herbivory by WCR. We conclude that ZmOPR2 and ZmLOX10 regulate JA-mediated resistance in leaves against FAW while suppressing insecticidal oxylipin synthesis in roots during WCR infestation.

Genome-wide identification of ZmMYC2 binding sites and target genes in maize

“…In these hormone related genes, some have been characterized functionally in maize growth or stress response. For instance, JA related genes, ZmLOX10 and ZmJAZ9 were involved in insect resistance, and ZmJAZ8 played roles in defense to C. graminicola infection [ 31 , 35 , 36 ]. Auxin biosynthesis genes, ZmYucca6 and ZmYucca9 were reported to participate into root geotropism and lodging resistance [ 37 ].…”

Trichoderma virens and Pseudomonas chlororaphis Differentially Regulate Maize Resistance to Anthracnose Leaf Blight and Insect Herbivores When Grown in Sterile versus Non-sterile Soils

“…In this study, we showed that T. virens colonization significantly enhanced mortality and suppressed weight gain of WCR larvae. Our previous report showed that increased WCR mortality was correlated with greater levels of herbivory-induced production of insecticidal death acids and ketols [16]. Therefore, one of the potential mechanisms of T. virens-mediated WCR defense may be to activate the production of insecticidal defensive compounds.…”

“…The laboratory strain of fall armyworm (FAW; Spodoptera frugiperda) was purchased from Benzon Research (Carlisle, PA, USA). Two weeks after incubation with the beneficial microorganisms, six FAW neonates were placed to the whorls of maize seedlings contained in individual plastic jars and allowed to move and feed on the plants freely for 7 days, as described in Huang et al (2023b) [16]. FAW larvae were removed from the plants, and the total weight was determined 7 days post-infestation.…”

“…WCR larvae were removed from the soil, and the total weight was determined 10 days post-infestation. The fresh weights of shoot and root tissues was measured after the soil was removed and the ratio was analyzed as larvae damaged over control root mass, as described in Huang et al, (2023) [16].…”

“…WCR larvae cause the most significant damage through feeding on the corn root while WCR adult beetles damage the silks [8,11]. Published evidence indicates that the plant phytohormone salicylic acid (SA) plays a critical role in maize defense against C. graminicola [12,13], while resistance to chewing insects, including FAW, is mainly mediated by the lipid-derived phytohormone jasmonic acid (JA) [14][15][16]. However, resistance mechanisms against root-feeding WCR remain largely unknown [17].…”