Priming maize resistance by its neighbors: activating 1,4-benzoxazine-3-ones synthesis and defense gene expression to alleviate leaf disease

Abstract

Plant disease can be effectively suppressed in intercropping systems. Our previous study demonstrated that neighboring maize plants can restrict the spread of soil-borne pathogens of pepper plants by secreting defense compounds into the soil. However, whether maize plant can receive benefits from its neighboring pepper plants in an intercropping system is little attention. We examined the effects of maize roots treated with elicitors from the pepper pathogen Phytophthora capsici and pepper root exudates on the synthesis of 1,4-benzoxazine-3-ones (BXs), the expression of defense-related genes in maize, and their ability to alleviate the severity of southern corn leaf blight (SCLB) caused by Bipolaris maydis. We found that SCLB was significantly reduced after the above treatments. The contents of 1,4-benzoxazine-3-ones (BXs: DIBOA, DIMBOA, and MBOA) and the expression levels of BX synthesis and defense genes in maize roots and shoots were up-regulated. DIMBOA and MBOA effectively inhibited the mycelium growth of Bipolaris maydis at physiological concentrations in maize shoots. Further studies suggested that the defense related pathways or genes in maize roots and shoots were activated by elicitors from the P. capsici or pepper root exudates. In conclusion, maize increased the levels of BXs and defense gene expression both in roots and shoots after being triggered by root exudates and pathogen from neighboring pepper plants, eventually enhancing its resistance.

Keywords: DIMBOA; antimicrobial activity; defense genes; intercropping; resistance induction.

Figure 1

Induced systemic resistance evaluation after maize roots induced by five elicitors. (A) Symptoms on maize leaves infected with B. maydis after the roots were induced by five elicitors or mock treated; (B) The percentage of lesion area on the maize leaves (n = 5 plants per treatment, from three independent experiments). CK, mock treated; SP, spore suspension; SL, spore lysis suspension; CS, culture suspension; HRE, healthy root exudate; NRE, nosogenic root exudate. Treatments were statistically different (p < 0.05; Turkey Post-hoc ANOVA).

Figure 2

Accumulation of DIBOA, DIMBOA, and MBOA in maize crown roots and shoots after treated with five elicitors. Maize crown roots and shoots were collected at 0, 12, 24, 48, and 72 h post-elicitor induction. The content of DIBOA, DIMBOA, and MBOA in crown root (A–C) and shoot (D–F) was analyzed by HPLC (n = 3 replicates, with each replicate consisting of five plants). Treatments were statistically different (p < 0.05; Turkey Post-hoc ANOVA).

Figure 3

Antimicrobial activities of DIMBOA and MBOA against the mycelium growth of B. maydis. Average mycelium growth inhibition (±SE) of B. maydis observed on media supplemented with different concentrations of DIMBOA (A) or MBOA (B). Different letters indicate significant differences between the mycelium growth inhibition at different concentrations of DIMBOA or MBOA. Treatments were statistically different (p < 0.05; Turkey Post-hoc ANOVA).

Figure 4

Gene expression profiles in maize crown roots and shoots from 12 to 72 h of maize roots treated with five elicitors. Maize was collected at 0, 12, 24, 48, and 72 h post-elicitor induction. Gene expression in maize crown roots (A) and shoots (B) were indicated in terms of the fold induction compared to the mock-treated plant, and the bars show their fold changes. The 21 stress gene expression profiles in crown roots (C) and shoots (D) were analyzed by hierarchical cluster analysis (n = 3 replicates, with each replicate consisting of five plants).