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PsDMAP1/PsTIP60-regulated H4K16ac is required for ROS-dependent virulence adaptation of Phytophthora sojae on host plants
Friday, 2025/01/10 | 07:24:50

Fan ZhangShanshan ChenCan ZhangZhiwen WangJianqiang MiaoTan DaiJianjun Hao, and Xili Liu

PNAS December 30, 2024, 122 (1) e2413127122; https://doi.org/10.1073/pnas.2413127122

Significance

Our findings underscore the crucial involvement of epigenetic-associated proteins in the intricate interplay between chromatin remodeling and DNA repair mechanisms under reactive oxygen species (ROS) stress conditions. Specifically, PsDMAP1/PsTIP60 mediated H4K16ac acts as an epigenetic mark that mediates the transmission of oxidative stress adaptation to asexual and sexual progeny in Phytophthora sojae, enhancing offspring resilience to host plant defense mechanisms and increasing their resistance to fungicides. Moreover, the epigenetically inherited adaptation to ROS allows P. sojae on plants to exhibit greater resistance to fungicides compared to P. sojae cultured on artificial media under field conditions. Significantly, our results offer fresh insights and strategic avenues for mitigating oomycete diseases and addressing challenges associated with agricultural fungicide resistance.

Abstract

Host plants and various fungicides inhibit plant pathogens by inducing the release of excessive reactive oxygen species (ROS) and causing DNA damage, either directly or indirectly leading to cell death. The mechanisms by which the oomycete Phytophthora sojae manages ROS stress resulting from plant immune responses and fungicides remains unclear. This study elucidates the role of histone acetylation in ROS-induced DNA damage responses (DDR) to adapt to stress. Mechanistically, the P. sojae DNA methyltransferase 1-associated protein (PsDMAP1) binds Tat-interactive protein 60 (PsTIP60) to comediate histone H4 acetylation on lysine 16 (H4K16ac). This regulation affects RNA polymerase II (pol II) recruitment, transcriptional induction of DDR-related genes, and the enrichment of histone H2Ax phosphorylated on serine 137 (γH2Ax) in response to both plant immunity and fungicide stress. The resulting H4K16ac serves as a crucial transgenerational epigenetic signal for virulence adaptation of P. sojae on plants, as a result of adaptation to ROS stress.

 

See https://www.pnas.org/doi/10.1073/pnas.2413127122

 

Figure 1:

PsDMAP1 mediates the response of P. sojae to ROS stress. (A) ROS produced in P. sojae-infected soybean seedlings. Seven-day-old soybean seedlings were inoculated with mycelial plugs of P. sojae and then stained at 24 hpi by DCFH-DA with or without 1 μM DPI as ROS scavenger. Bar: 50 μm. (B) 1 µg/mL (ppm) AZX induced ROS production in P. sojae. Each strain was cultured in V8 liquid medium with 0.1% DMSO, 1 ppm AZX, or 1 ppm AZX+1 μM DPI for 48 h. The resulting mycelia of each strain were stained with DCFH-DA. ROS fluorescence was detected by confocal microscopy. Bar: 20 μm. (C) PsDMAP1 knockdown mutants showed increased sensitivity to H2O2 and AZX. A 5-mm mycelial plug from the wild-type P6497, empty vector strain (EV), the PsDMAP1 knockdown mutants (DMAP1-1 and DMAP1-2), and the PsDMAP1-overexpressed strain (DMAP1-OE) was incubated on V8 plates supplemented with 0.1% DMSO, 10 mM H2O2, 1 ppm AZX, 0.1% DMSO+1 μM DPI, 10 mM H2O2+1 μM DPI, or 1 ppm AZX+1 μM DPI for 5 d. (D) Mycelial growth inhibition of the H2O2 or AZX relative to the DMSO-treated control and mycelial inhibition by H2O2+DPI or AZX+DPI relative to the DMSO+DPI-treated control. Relative inhibition was calculated as (CK−Growth rate on plates with treatment)/CK×100%. Statistical significance of the mycelial inhibition of above strains compared to the wild type P6497 was determined using Student’s t test (**P < 0.01, ns: not significant). (E) The treatment with 1 μM DPI restored the impaired virulence of PsDMAP1 knockdown strains. Left panels: soybean seedlings were inoculated with mycelial plugs of each strain and then stained at 24 hpi by DCFH-DA with or without 1 μM DPI as ROS scavenger. Right panels: disease symptoms at 48 hpi of above strains when soybean seedlings were treated with H2O (control) or DPI. (F) Lesion length and (G) pathogen biomass of each strain under treatments with H2O (control) or DPI, measured at 48 hpi. Statistical significance of the lesion length and biomass of above strains compared to the P6497 at H2O or DPI treatment was determined using Student’s t test (**P < 0.01, ns: not significant). Data in D, F, and G are presented as the mean ± SD from three biological replicates.

 

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