13-Lipoxygenases(LOXs)initiate the synthesis of jasmonic acid(JA),the best-understood oxylipin hormone in herbivory defense.However,the roles of 9-LOX-derived oxylipins in insect resistance remain unclear.Here,we repo...13-Lipoxygenases(LOXs)initiate the synthesis of jasmonic acid(JA),the best-understood oxylipin hormone in herbivory defense.However,the roles of 9-LOX-derived oxylipins in insect resistance remain unclear.Here,we report a novel anti-herbivory mechanism mediated by a tonoplast-localized 9-LOX,ZmLOX5,and its linolenic acid-derived product,9-hydroxy-10-oxo-12(Z),15(Z)-octadecadienoic acid(9,10-KODA).Transposon-insertional disruption of ZmLOX5 resulted in the loss of resistance to insect herbivory.lox5 knockout mutants displayed greatly reduced wound-induced accumulation of multiple oxylipins and defense metabolites,including benzoxazinoids,abscisic acid(ABA),and JA-isoleucine(JA-Ile).However,exogenous JA-Ile failed to rescue insect defense in lox5 mutants,while applications of 1 mM 9,10-KODA or the JA precursor,12-oxo-phytodienoic acid(12-OPDA),restored wild-type resistance levels.Metabolite profiling revealed that exogenous 9,10-KODA primed the plants for increased production of ABA and 12-OPDA,but not JA-Ile.While none of the 9-oxylipins were able to rescue JA-Ile induction,the lox5 mutant accumulated lower wound-induced levels of Ca^(2+),suggesting this as a potential explanation for lower wound-induced JA.Seedlings pretreated with 9,10-KODA exhibited rapid or more robust woundinduced defense gene expression.In addition,an artificial diet supplemented with 9,10-KODA arrested fall armyworm larvae growth.Finally,analysis of single and double lox5 and lox10 mutants showed that ZmLOX5 also contributed to insect defense by modulating ZmLOX10-mediated green leaf volatile signaling.Collectively,our study uncovered a previously unknown anti-herbivore defense and hormonelike signaling activity for a major 9-oxylipin α-ketol.展开更多
The brown planthopper （BPH, Nilaparvata lugens） is a destructive, monophagous, piercing-sucking insect pest of rice. Previous studies indicated that jasmonic acid （JA） positively regulates rice defense against che...The brown planthopper （BPH, Nilaparvata lugens） is a destructive, monophagous, piercing-sucking insect pest of rice. Previous studies indicated that jasmonic acid （JA） positively regulates rice defense against chewing insect pests but negatively regulates it against the piercing-sucking insect of BPH. We here demonstrated that overexpression of allene oxide cyclase （AOC） but not OPR3 （cis-12-oxo-phytodienoic acid （OPDA） reductase 3, an enzyme adjacent to AOC in the JA synthetic pathway） significantly increased rice resistance to BPH, mainly by reducing the feeding activity and survival rate. Further anal- ysis revealed that plant response to BPH under AOC overexpression was independent of the JA pathway and that significantly higher OPDA levels stimulated rice resistance to BPH. Microarray analysis identified multiple candidate resistance-related genes underAOCoverexpression. OPDA treatment stimulated the resistance of radish seedlings to green peach aphid Myzus persicae, another piercing-sucking insect. These results imply that rice resistance to chewing insects and to sucking insects can be enhanced simultaneously through AOC-mediated increases of JA and OPDA and provide direct evidence of the potential application of OPDA in stimulating plant defense responses to piercing-sucking insect pests in agriculture.展开更多
基金supported by United States Department of Agriculture(USDA)-National Institute of Food and Agriculture(NIFA)2017-67013-26524 and 2021-67013-33568 grants awarded to M.V.K.
文摘13-Lipoxygenases(LOXs)initiate the synthesis of jasmonic acid(JA),the best-understood oxylipin hormone in herbivory defense.However,the roles of 9-LOX-derived oxylipins in insect resistance remain unclear.Here,we report a novel anti-herbivory mechanism mediated by a tonoplast-localized 9-LOX,ZmLOX5,and its linolenic acid-derived product,9-hydroxy-10-oxo-12(Z),15(Z)-octadecadienoic acid(9,10-KODA).Transposon-insertional disruption of ZmLOX5 resulted in the loss of resistance to insect herbivory.lox5 knockout mutants displayed greatly reduced wound-induced accumulation of multiple oxylipins and defense metabolites,including benzoxazinoids,abscisic acid(ABA),and JA-isoleucine(JA-Ile).However,exogenous JA-Ile failed to rescue insect defense in lox5 mutants,while applications of 1 mM 9,10-KODA or the JA precursor,12-oxo-phytodienoic acid(12-OPDA),restored wild-type resistance levels.Metabolite profiling revealed that exogenous 9,10-KODA primed the plants for increased production of ABA and 12-OPDA,but not JA-Ile.While none of the 9-oxylipins were able to rescue JA-Ile induction,the lox5 mutant accumulated lower wound-induced levels of Ca^(2+),suggesting this as a potential explanation for lower wound-induced JA.Seedlings pretreated with 9,10-KODA exhibited rapid or more robust woundinduced defense gene expression.In addition,an artificial diet supplemented with 9,10-KODA arrested fall armyworm larvae growth.Finally,analysis of single and double lox5 and lox10 mutants showed that ZmLOX5 also contributed to insect defense by modulating ZmLOX10-mediated green leaf volatile signaling.Collectively,our study uncovered a previously unknown anti-herbivore defense and hormonelike signaling activity for a major 9-oxylipin α-ketol.
基金This study was supported by the National Basic Research Program of China （2010CB126200） and the National Natural Science Foundation of China （31371949）.
文摘The brown planthopper （BPH, Nilaparvata lugens） is a destructive, monophagous, piercing-sucking insect pest of rice. Previous studies indicated that jasmonic acid （JA） positively regulates rice defense against chewing insect pests but negatively regulates it against the piercing-sucking insect of BPH. We here demonstrated that overexpression of allene oxide cyclase （AOC） but not OPR3 （cis-12-oxo-phytodienoic acid （OPDA） reductase 3, an enzyme adjacent to AOC in the JA synthetic pathway） significantly increased rice resistance to BPH, mainly by reducing the feeding activity and survival rate. Further anal- ysis revealed that plant response to BPH under AOC overexpression was independent of the JA pathway and that significantly higher OPDA levels stimulated rice resistance to BPH. Microarray analysis identified multiple candidate resistance-related genes underAOCoverexpression. OPDA treatment stimulated the resistance of radish seedlings to green peach aphid Myzus persicae, another piercing-sucking insect. These results imply that rice resistance to chewing insects and to sucking insects can be enhanced simultaneously through AOC-mediated increases of JA and OPDA and provide direct evidence of the potential application of OPDA in stimulating plant defense responses to piercing-sucking insect pests in agriculture.
