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We have previously reported that disruption of a maize root-expressed 9-lipoxygenase (9-LOX) gene,  ZmLOX3 , results in dramatic increase in resistance to diverse leaf and stalk pathogens. Despite evident economic significance of these findings, the mechanism behind this increased resistance remained elusive. In this study, we found that increased resistance of the  lox3-4  mutants is due to constitutive activation of induced systemic resistance (ISR) signaling. We showed that  ZmLOX3  lacked expression in leaves in response to anthracnose leaf blight pathogen  Colletotrichum graminicola , but was expressed constitutively in the roots, thus, prompting our hypothesis: the roots of  lox3-4  mutants are the source of increased resistance in leaves. Supporting this hypothesis, treatment of wild-type plants (WT) with xylem sap of  lox3-4  mutant induced resistance to  C. graminicola  to the levels comparable to those observed in  lox3-4  mutant. Moreover, treating mutants with the sap collected from WT plants partially restored the susceptibility to  C. graminicola .  lox3-4  mutants showed primed defense responses upon infection, which included earlier and greater induction of defense-related PAL and GST genes compared to WT. In addition to the greater expression of the octadecanoid pathway genes,  lox3-4  mutant responded earlier and with a greater accumulation of H 2 O 2  in response to  C. graminicola  infection or treatment with alamethicin. These findings suggest that  lox3-4  mutants display constitutive ISR-like signaling. In support of this idea, root colonization by  Trichoderma virens  strain GV29-8 induced the same level of disease resistance in WT as the treatment with the mutant sap, but had no additional resistance effect in  lox3-4  mutant. While treatment with  T. virens  GV29 strongly and rapidly suppressed Zm LOX3  expression in hydroponically grown WT roots,  T. virens  Δsml mutant, which is deficient in ISR induction, was unable to suppress expression of  ZmLOX3 , thus, providing genetic evidence that SM1 function in ISR, at least in part, by suppressing host  ZmLOX3  gene. This study and the genetic tools generated herein will allow the identification of the signals regulating the induction of resistance to aboveground attackers by beneficial soil microorganisms in the future.

Root-expressed maize lipoxygenase 3 negatively regulates induced systemic resistance to Colletotrichum graminicola in shoots