Ethylene‐responsive factor ERF114 mediates fungal pathogen effector PevD1‐induced disease resistance in <i>Arabidopsis thaliana</i>

Li, Ze; Zhang, Yi; Ren, Jie; Jia, Fenglian; Zeng, Hongmei; Li, Guangyue; Yang, Xiufen

doi:10.1111/mpp.13208

Cited by 32 publications

(16 citation statements)

References 61 publications

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“…4a). PAL1 has been thoroughly related to plant defense responses [31,32,17]. Our metabolomic analysis further corroborated transcriptomic ndings as we found signi cant enrichment of the phenylpropanoid pathway in the roots of Pima-S6 compared to Pima S-7.…”

Section: Discussionsupporting

confidence: 85%

Enhanced phenylpropanoid metabolism underlies resistance to Fusarium oxysporum vasinfectum f. sp. race 4 infection in the cotton cultivar Pima-S6 (Gossypium barbadense L.)

Ojeda-Rivera,

Ulloa,

Najera-Gonzalez

et al. 2023

Preprint

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Background Fusarium oxysporum f. sp. vasinfectum (FOV) race 4 (FOV4) is a highly pathogenic soil-borne fungus responsible for Fusarium wilt in cotton (Gossypium spp.) and represents a continuing threat to cotton production in the southwest states of the U.S., including California, New Mexico, and Texas. Even though the Pima (G. barbadense L.) cotton gene pool shows more susceptibility to this pathogen than Upland (G. hirsutum L.) cotton, fortunately, some Pima cultivars present resistance to FOV4 infection, like Pima-S6. To gain insights into the mechanism underlying FOV4 resistance, we performed comparative transcriptional and metabolomic profiling of FOV4-resistant Pima-S6 and FOV4-susceptible Pima S-7 and Pima 3–79 cotton. Results Comparative analysis of transcriptional FOV4 infection responses on these genotypes indicated a differential response between resistant Pima-S6 and susceptible Pima S-7 and 3–79. GO-enriched analysis found clusters related to various biological processes, including transmembrane transport, glycoside hydrolysis, metabolism of small molecules, and phenylpropanoid metabolism. Arabidopsis ortholog genes comparison with categories significantly enriched in Pima-S6 resulted in multiple categories clustered to similar biological processes such as the metabolism of small molecules, regulation of enzymatic activity, diterpenoid biosynthetic processes, and phytohormone signaling-related processes, being phenylpropanoid biosynthesis and metabolism highly enriched. These results correlated with the accumulation of secondary metabolites in Pima-S6 roots, specifically esculetin, a coumarin that inhibits the growth of Fusarium. Transcriptomic profiling enabled the identification of candidate genes potentially involved in the resistance mechanism of FOV4-resistance in protecting the Pima-S6 cotton cultivar from this pathogenic fungus. Some genes of this pathway were found to be in chromosome-QTL regions linked with resistance to FOV4. Conclusions Our results highlight an essential role for the phenylpropanoid synthesis pathway in FOV4 resistance and create opportunities for gene discovery and SNP development for marker-associated selection (MAS) for breeding for FOV4 resistance.

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Section: Discussionsupporting

confidence: 85%

Enhanced phenylpropanoid metabolism underlies resistance to Fusarium oxysporum vasinfectum f. sp. race 4 infection in the cotton cultivar Pima-S6 (Gossypium barbadense L.)

Ojeda-Rivera,

Ulloa,

Najera-Gonzalez

et al. 2023

Preprint

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“…Most DEGs of ethylene-responsive factors were upregulated in the double inoculation of AMF and C. camelliae , possibly implying that the transcription factors were one of the key pathways to resist the pathogen after AMF inoculation. Ethylene-responsive factors are excellent candidates for developing plant resistance to anthracnose and other fungal diseases ( Svoboda et al., 2021 ), and loss of ERF114 function caused impaired disease resistance ( Li et al., 2022 ). Therefore, future research could be focused on this field.…”

Section: Discussionmentioning

confidence: 99%

Arbuscular mycorrhizal fungus alleviates anthracnose disease in tea seedlings

Chen

Ye²,

Sun³

et al. 2023

Front. Plant Sci.

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Tea has been gaining increasing popularity all over the world in recent years, and its yield and quality depend on the growth and development of tea plants [Camellia sinensis (L.) Kuntze] in various environments. Nowadays, biotic stress and extreme weather, such as high temperature, drought, waterlogging, pests, and diseases, bring about much pressure on the production of tea with high quality. Wherein anthracnose, which is the most common and serious disease of tea plants, has earned more and more attention, as its control mainly relies on chemical pesticides. Arbuscular mycorrhizal fungi (AMF), forming symbiosis with most terrestrial plants, participate in plant resistance against the anthracnose disease, which was found by previous studies in a few herbaceous plants. However, there are a few studies about arbuscular mycorrhizal (AM) fungal regulation of the resistance to the anthracnose pathogen in woody plants so far. In this paper, we investigated the effect of AMF on the development of anthracnose caused by Colletotrichum camelliae and tried to decipher the pertinent mechanism through transcriptome analysis. Results showed that inoculating AMF significantly reduced the damage of anthracnose on tea seedlings by reducing the lesion area by 35.29% compared to that of the control. The content of superoxide anion and activities of catalase and peroxidase significantly increased (P < 0.05) in mycorrhizal treatment in response to the pathogen with 1.23, 2.00, and 1.39 times higher, respectively, than those in the control. Pathways of plant hormone signal transduction, mitogen-activated protein kinase (MAPK) signaling, and phenylpropanoid biosynthesis might play roles in this regulation according to the transcriptomic results. Further redundancy analysis (RDA) and partial least squares structural equation modeling (PLS-SEM) analysis found that plant hormones, such as auxin and ethylene, and the antioxidant system (especially peroxidase) were of great importance in the AM fungal alleviation of anthracnose. Our results preliminarily indicated the mechanisms of enhanced resistance in mycorrhizal tea seedlings to the anthracnose pathogen and provided a theoretical foundation for the application of AMF as one of the biological control methods in tea plantations.

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“…Similarly, ERF114 positively regulates the immunity of N. benthamiana plants against bacterial speck [ P. syringae pv. tomato (Pst)] DC3000 by modulating the accumulation of lignin and salicylic acid induced by the effector PevD1 (Li et al., 2022). In this study, we showed that infection with R. solanacearum and the exogenous application of ABA both significantly induce the accumulation of ERF098 transcripts (Figure S8).…”

Section: Discussionmentioning

confidence: 99%

Ralstonia solanacearum effector RipAK suppresses homodimerization of the host transcription factor ERF098 to enhance susceptibility and the sensitivity of pepper plants to dehydration

Liu,

Shi,

Luo

et al. 2023

The Plant Journal

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SUMMARYPlants have evolved a sophisticated immune system to defend against invasion by pathogens. In response, pathogens deploy copious effectors to evade the immune responses. However, the molecular mechanisms used by pathogen effectors to suppress plant immunity remain unclear. Herein, we report that an effector secreted by Ralstonia solanacearum, RipAK, modulates the transcriptional activity of the ethylene‐responsive factor ERF098 to suppress immunity and dehydration tolerance, which causes bacterial wilt in pepper (Capsicum annuum L.) plants. Silencing ERF098 enhances the resistance of pepper plants to R. solanacearum infection not only by inhibiting the host colonization of R. solanacearum but also by increasing the immunity and tolerance of pepper plants to dehydration and including the closure of stomata to reduce the loss of water in an abscisic acid signal‐dependent manner. In contrast, the ectopic expression of ERF098 in Nicotiana benthamiana enhances wilt disease. We also show that RipAK targets and inhibits the ERF098 homodimerization to repress the expression of salicylic acid‐dependent PR1 and dehydration tolerance‐related OSR1 and OSM1 by cis‐elements in their promoters. Taken together, our study reveals a regulatory mechanism used by the R. solanacearum effector RipAK to increase virulence by specifically inhibiting the homodimerization of ERF098 and reprogramming the transcription of PR1, OSR1, and OSM1 to boost susceptibility and dehydration sensitivity. Thus, our study sheds light on a previously unidentified strategy by which a pathogen simultaneously suppresses plant immunity and tolerance to dehydration by secreting an effector to interfere with the activity of a transcription factor and manipulate plant transcriptional programs.

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Ethylene‐responsive factor ERF114 mediates fungal pathogen effector PevD1‐induced disease resistance in Arabidopsis thaliana

Cited by 32 publications

References 61 publications

Enhanced phenylpropanoid metabolism underlies resistance to Fusarium oxysporum vasinfectum f. sp. race 4 infection in the cotton cultivar Pima-S6 (Gossypium barbadense L.)

Enhanced phenylpropanoid metabolism underlies resistance to Fusarium oxysporum vasinfectum f. sp. race 4 infection in the cotton cultivar Pima-S6 (Gossypium barbadense L.)

Arbuscular mycorrhizal fungus alleviates anthracnose disease in tea seedlings

Ralstonia solanacearum effector RipAK suppresses homodimerization of the host transcription factor ERF098 to enhance susceptibility and the sensitivity of pepper plants to dehydration

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