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. 2021 Apr 12:12:633221.
doi: 10.3389/fpls.2021.633221. eCollection 2021.

Differential Responses of Cucurbita pepo to Podosphaera xanthii Reveal the Mechanism of Powdery Mildew Disease Resistance in Pumpkin

Shuwu Zhang  1   2 , Jia Liu  1 , Bingliang Xu  1   2 , Jingjiang Zhou  1
Affiliations

Differential Responses of Cucurbita pepo to Podosphaera xanthii Reveal the Mechanism of Powdery Mildew Disease Resistance in Pumpkin

Shuwu Zhang et al. Front Plant Sci. .

Abstract

Powdery mildew is one of the most destructive diseases and the major cause to the production losses of cucurbit worldwide. A number of strategies have been developed and applied to discover suitable and safer methods to manage the occurrence of powdery mildew disease in pumpkins (Cucurbita pepo L.), but information is limited in screening tolerant germplasms and exploring their mechanisms in preventing the disease occurrence at physiological, biochemical, and molecular levels. Therefore, we investigated the responses of two commercial pumpkin cultivars to Podosphaera xanthii infection. Compared with mock-inoculated seedlings, few small and sparse powdery areas were observed on the leaves of the Sixing F1 cultivar on the 13th day after inoculation with P. xanthii, whereas a large number of diseased powdery areas and a layer of white powdery mildew were observed on the surface of Jin12 F1 leaves. The inoculation duration (7, 9, 11, and 13 days) significantly and continuously increased the disease incidence and index of pumpkin seedlings. The contents of H2O2, MDA, lignin, and total phenolics in the leaves of Sixing F1 and Jin12 F1 cultivars were markedly increased after inoculation with P. xanthii. However, the Sixing F1 cultivar exhibited much less reactive oxygen species (ROS) accumulation, a lower rate of lipid peroxidation, and a higher level of lignin and total phenolics contents after inoculation than the Jin12 F1 cultivar. Compared with untreated control pumpkin seedlings, significantly higher activities and gene expressions of the phenylpropanoids pathway enzymes (PAL and PPO), ROS scavenging defense enzymes (SOD, CAT, POD, and APX), and other salicylic acid (SA) signaling pathway marker genes were observed in the leaves of both cultivars after P. xanthii inoculation at different inoculation time points. These enhancements were significantly higher in Sixing F1 than Jin12 F1. Our results indicate that the Sixing F1 cultivar exhibited a much stronger ability in resistance to P. xanthii infection than the Jin12 F1 cultivar. Our results suggest that one possible mechanism of C. pepo cultivars to prevent the pathogen P. xanthii infection is by activating and enhancing the activity and gene expression of the phenylpropanoids pathway to synthesize phenolic substances and lignin, ROS scavenging defense enzymes to eliminate the harmful effects of ROS, and signaling pathway marker gene expression to improve plant disease resistance.

Keywords: Cucurbita pepo; Podosphaera xanthii; antioxidative defense system; disease incidence and index; gene expression; phenylpropanoids and SA pathways; powdery mildew; reactive oxygen species.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

FIGURE 1
FIGURE 1
The symptoms of different cultivars of Cucurbita pepo on the 13th day after inoculation with the pathogen of Podosphaera xanthii. (A) The cultivar of Jin12 F1 after inoculation with P. xanthii; (B) the cultivar of Sixing F1 after inoculation with P. xanthii; (C) the cultivar of Jin12 F1 after inoculation with sterile water but not P. xanthii; and (D) the cultivar of Sixing F1 after inoculation with sterile water but not P. xanthii.
FIGURE 2
FIGURE 2
PAL and PPO activity in the leaves of Sixing F1 and Jin12 F1 at different time points after inoculation with Podosphaera xanthii. (A) The PAL activity in the leaves of Sixing F1; (B) the PAL activity in the leaves of Jin12 F1; (C) the PPO activity in the leaves of Sixing F1; and (D) the PPO activity in the leaves of Jin12 F1. The line bars represent the standard errors of the means. Different letters denote significant difference at the P < 0.05 level by Duncan’s new multiple range test (n = 12). The treatments are detailed in the footnote of Table 2.
FIGURE 3
FIGURE 3
Activities of ROS scavenging enzymes in the leaves of Sixing F1 and Jin12 F1 at different time points after inoculation with Podosphaera xanthii. (A,C,E,G) The activity of SOD, CAT, POD, and APX in Sixing F1, respectively; (B,D,F,H) the activity of SOD, CAT, POD, and APX in Jin12 F1, respectively. The line bars, different letters, and the treatments are detailed in the footnote of Figure 2 and Table 2.
FIGURE 4
FIGURE 4
Expression levels of PAL and PPO genes in the leaves of Sixing F1 and Jin12 F1 at different time points after being inoculated with Podosphaera xanthii. (A,B) The expression levels of the PAL gene in Sixing F1 and Jin12 F1, respectively; (C,D) the expression levels of the PPO gene in Sixing F1 and Jin12 F1, respectively. The line bars, different letters, and treatments are detailed in the footnote of Figure 2 and Table 2.
FIGURE 5
FIGURE 5
Expression levels of ROS scavenging enzyme genes in the leaves of Sixing F1 and Jin12 F1 at different time points after being inoculated with Podosphaera xanthii. (A,C,E,G) The expression levels of SOD, CAT, POD, and APX genes in Sixing F1, respectively; (B,D,F,H) the expression levels of SOD, CAT, POD, and APX genes in Jin12 F1, respectively. The line bars, different letters, and treatments are detailed in the footnote of Figure 2 and Table 2.
FIGURE 6
FIGURE 6
Expression levels of SA signaling pathway marker genes in the leaves of Sixing F1 and Jin12 F1 at different time points after being inoculated with Podosphaera xanthii. (A,C,E) The expression levels of PR1, PR2, and ICS1 genes in Sixing F1, respectively; (B,D,F) the expression levels of PR1, PR2, and ICS1 genes in Jin12 F1, respectively. The line bars, different letters, and treatments are detailed in the footnote of Figure 2 and Table 2.
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