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GmPAO-mediated polyamine catabolism enhances soybean Phytophthora resistance without growth penalty

Plant immunity is activated upon perception of pathogens and often affects growth when it is constitutively active. It is still a challenge to balance plant immunity and growth in disease resistance breeding. Here, we demonstrated that soybean (Glycine max) polyamine oxidase (GmPAO) confers resistance to multiple Phytophthora pathogens, but has no obvious adverse impact on agronomic traits. GmPAO produces H2O2 by oxidizing spermidine and spermine. Phytophthora sojae induces an increase in these two substrates, and thus promotes GmPAO-mediated polyamine catabolism specifically during infection.

Kun YangQiang YanYi WangHao PengMaofeng Jing & Daolong Dou

Phytopathology ResearchSept. 2022; 35 (2022) (Published: 16 September 2022)

ABSTRACT

Plant immunity is activated upon perception of pathogens and often affects growth when it is constitutively active. It is still a challenge to balance plant immunity and growth in disease resistance breeding. Here, we demonstrated that soybean (Glycine max) polyamine oxidase (GmPAO) confers resistance to multiple Phytophthora pathogens, but has no obvious adverse impact on agronomic traits. GmPAO produces H2O2 by oxidizing spermidine and spermine. Phytophthora sojae induces an increase in these two substrates, and thus promotes GmPAO-mediated polyamine catabolism specifically during infection. Interestingly, we found that the two substrates showed higher accumulation in transgenic soybean lines overexpressing GmPAO than in WT and CK after inoculation with P. sojae to ensure H2O2 production during infection, rather than directly inhibit P. sojae. In these transgenic soybean plants, the significantly enhanced resistance to different P. sojae isolates was achieved; PAMP-induced H2O2 accumulation was enhanced by GmPAO overexpression. Moreover, transient expression of GmPAO also significantly improved Nicotiana benthamiana resistance to Phytophthora capsici and Phytophthora parasitica in agroinfiltration assays. Our results provide a novel approach to allow rapid defense responses in plants upon pathogen infection while minimizing growth penalties under normal conditions, with a clear mechanism in which plant promotes H2O2 production via pathogen-activated substrates.

 

See: GmPAO-mhytopathology Research | Full Text (biomedcentral.com)

 

Figure 2: GmPAO promotes PAMP (flg22 or chitin)-induced H2O2 accumulation. ab GmPAO promoted PAMP (flg22 or chitin)-induced H2O2 accumulation in transgenic soybean lines. The leaves (2-week-old) were subjected to flg22- (a) or chitin-induced (b) ROS examination, and the relative luminescence unit (RLU) value was recorded. Error bar represents mean ± SD, n ≥ 8, n represents sample number. cd GmPAO promoted PAMP (flg22 or chitin)-induced H2O2 accumulation in N. benthamiana. The indicated constructs were transiently expressed by Agrobacterium-mediated transient expression for 2 days and subjected to flg22- (c) or chitin-induced (d) ROS examination. GFP was used as a control. The protein expression is shown in the right panel. Error bar represents mean ± SD, n = 8, n represents sample number. All the experiments were performed three times (biological replicates) with similar results. The data were analyzed by Shapiro–Wilk test to determine the Normality and Lognormality Tests across groups, and then analyzed by unpaired t test for groups that had passed the normality test (**P < 0.01). The exact n, SD values, and P values are shown in the data.

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