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Panax notoginseng WRKY Transcription Factor 9 Is a Positive Regulator in Responding to Root Rot Pathogen Fusarium solani

ABSTRACT: Panax notoginseng (Burk) F.H. Chen is a rare and valuable Chinese herb, but root rot mainly caused by Fusarium solani severely affects the yield and quality of P. notoginseng herbal materials. In this study, we isolated 30 P. notoginseng WRKY transcription factors (TFs), which were divided into three groups (I, II, and III) on the basis of a phylogenetic analysis. The expression levels of 10 WRKY genes, including PnWRKY9, in P. notoginseng roots increased in response to a methyl jasmonate (MeJA) treatment and the following F. solani infection. Additionally, PnWRKY9 was functionally characterized. The PnWRKY9 protein was localized to the nucleus. The overexpression of PnWRKY9 in tobacco (Nicotiana tabacum) considerably increased the resistance to F. solani, whereas an RNAi-mediated decrease in the PnWRKY9 expression level in P. notoginseng leaves increased the susceptibility to F. solani. The RNA sequencing and hormone content analyses of PnWRKY9-overexpression tobacco revealed that PnWRKY9 and the jasmonic acid (JA) signaling pathway synergistically enhance disease resistance. The PnWRKY9 recombinant protein was observed to bind specifically to the W-box sequence in the promoter of a JA-responsive and F. solani resistance-related defensin gene (PnDEFL1). A yeast one-hybrid assay indicated that PnWRKY9 can activate the transcription of PnDEFL1. Furthermore, a co-expression assay in tobacco using β-glucuronidase (GUS) as a reporter further verified that PnWRKY9 positively regulates PnDEFL1 expression. Overall, in this study, we identified P. notoginseng WRKY TFs and demonstrated that PnWRKY9 positively affects plant defenses against the root rot pathogen. The data presented herein provide researchers with fundamental information regarding the regulatory mechanism mediating the coordinated activities of WRKY TFs and the JA signaling pathway in P. notoginseng responses to the root rot pathogen.

SUBMITTER: Zheng L

PROVIDER: S-EPMC9331302 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Harnessing indigenous soil microbial suppression is an emerging strategy for managing soilborne plant diseases. Soil moisture is a vital factor in soil microbiomes, but its role in the regulation of microbial suppression is poorly understood. Here, we investigated the correlation of root rot disease of Panax notoginseng with rhizosphere microbial communities mediated by soil moisture gradients from 55% to 100% field capacity (FC); then, we captured the disease-suppressive and disease-inductive microbiomes and validated their functions by a culture experiment with synthetic microbiotas containing keystone species. We found that proper soil moisture at 75% to 95% FC could maintain a disease-suppressive microbiome to alleviate root rot disease. However, extremely low or high soil moistures (>95% FC or <75% FC) could aggravate root rot disease by depleting the disease-suppressive microbiome while enriching the disease-inductive microbiome. Both the low-soil-moisture-enriched pathogen Monographella cucumerina and the high-soil-moisture-enriched pathogen Ilyonectria destructans could synergize with different disease-inductive microbiomes to aggravate disease. Metagenomic data confirmed that low- and high-moisture conditions suppressed antibiotic biosynthesis genes but enriched pathogenicity-related genes, resulting in a change in the soil state from disease suppressive to inductive. This study highlights the importance of soil moisture when indigenous microbial suppression is harnessed for disease control. IMPORTANCE Soilborne diseases pose a major problem in high-intensity agricultural systems due to the imbalance of microbial communities in soil, resulting in the buildup of soilborne pathogens. Harnessing indigenous soil microbial suppression is an emerging strategy for overcoming soilborne plant diseases. In this study, we showed that soil moisture is a key factor in balancing microbiome effects on root rot disease. Proper soil moisture management represent an effective approach to maintain microbial disease resistance by enriching disease-suppressive microbiomes. Conversely, moisture stresses may enrich for a disease-inductive microbiome and aid accumulation of host-specific soilborne pathogens threatening crop production. This work could provide a new strategy for sustainable control of soilborne diseases by enriching the indigenous disease-suppressive microbiome through soil moisture management.

Project description:The root of Panax notoginseng (P. notoginseng) is one of the most highly valuable medicinal herbs in China owing to its pronounced hemostatic and restorative properties. Despite this important fact, growing P. notoginseng is seriously limited by root-rot diseases. In studies aimed at developing a solution to this problem, environment-friendly essential oils (EOs) of five medicinal plants of the family Zingiberaceae were tested for their inhibitory effects on the growth of three main soil pathogens associated with the root-rot diseases of P. notoginseng. The results showed that the EOs of Alpinia katsumadai Hayata and Zingiber officinale Roscoe promote significant reductions in the mycelium growth of the pathogen in vitro at a concentration of 50 mg mL-1, which is much higher than that needed (5 mg mL-1) to reduce growth by the positive control, flutriafol. Furthermore, the chemical components of the two EOs were determined by using GC-MS analysis. Eucalyptol was found to account for more than 30% of the oils of the two plants, with the second major components being geranyl acetate and ?-terpineol. These substances display different degrees of fungistasis in vitro. To further determine the effects of the EO of Zingiber officinale (Z. officinale) in vivo, soilless cultivation of P. notoginseng with pathogen inoculation was conducted in a greenhouse. Addition of the petroleum ether extract (approximately equal to EO) of Z. officinale to the culture matrix causes a large decrease in both the occurrence and severity of the P. notoginseng root-rot disease. The decreasing trend of net photosynthetic rate (Pn), stomatal conductance (gs), intercellular CO2 concentration (Ci), and transpiration rate (Tr) were all alleviated. In addition, the activities of catalase (CAT), peroxidase (POD), and the malondialdehyde (MDA) content were also largely reduced after pathogen infection, with the root activity being higher than that of the control. Taken together, the findings reveal that the EOs from plants might serve as promising sources of eco-friendly natural pesticides with less chemical resistance.

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Panax notoginseng WRKY Transcription Factor 9 Is a Positive Regulator in Responding to Root Rot Pathogen Fusarium solani

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