Dataset Information

Alternaria TeA toxin activates a chloroplast retrograde signaling pathway to facilitate JA-dependent pathogenicity.

ABSTRACT: The chloroplast is a critical battleground in the arms race between plants and pathogens. Among microbe-secreted mycotoxins, tenuazonic acid (TeA), produced by the genus Alternaria and other phytopathogenic fungi, inhibits photosynthesis, leading to a burst of photosynthetic singlet oxygen (¹O₂) that is implicated in damage and chloroplast-to-nucleus retrograde signaling. Despite the significant crop damage caused by Alternaria pathogens, our understanding of the molecular mechanism by which TeA promotes pathogenicity and cognate plant defense responses remains fragmentary. We now reveal that A. alternata induces necrotrophic foliar lesions by harnessing EXECUTER1 (EX1)/EX2-mediated chloroplast-to-nucleus retrograde signaling activated by TeA toxin-derived photosynthetic ¹O₂ in Arabidopsis thaliana. Mutation of the ¹O₂-sensitive EX1-W643 residue or complete deletion of the EX1 singlet oxygen sensor domain compromises expression of ¹O₂-responsive nuclear genes and foliar lesions. We also found that TeA toxin rapidly induces nuclear genes implicated in jasmonic acid (JA) synthesis and signaling, and EX1-mediated retrograde signaling appears to be critical for establishing a signaling cascade from ¹O₂ to JA. The present study sheds new light on the foliar pathogenicity of A. alternata, during which EX1-dependent ¹O₂ signaling induces JA-dependent foliar cell death.

SUBMITTER: Shi J

PROVIDER: S-EPMC10943587 | biostudies-literature | 2024 Mar

REPOSITORIES: biostudies-literature

ACCESS DATA

Publications

Alternaria TeA toxin activates a chloroplast retrograde signaling pathway to facilitate JA-dependent pathogenicity.

Shi Jiale J Wang He H Li Mengping M Mi Liru L Gao Yazhi Y Qiang Sheng S Zhang Yu Y Chen Dan D Dai Xinbin X Ma Hongyu H Lu Huan H Kim Chanhong C Chen Shiguo S

Plant communications 20231204 3

The chloroplast is a critical battleground in the arms race between plants and pathogens. Among microbe-secreted mycotoxins, tenuazonic acid (TeA), produced by the genus Alternaria and other phytopathogenic fungi, inhibits photosynthesis, leading to a burst of photosynthetic singlet oxygen (<sup>1</sup>O<sub>2</sub>) that is implicated in damage and chloroplast-to-nucleus retrograde signaling. Despite the significant crop damage caused by Alternaria pathogens, our understanding of the molecular ...[more]

PMID: 38050356

Similar Datasets

Project description:Alternaria brassicicola is a successful saprophyte and necrotrophic plant pathogen. Molecular determinants of its life style shift between saprophyte and pathogen, however, are unknown. To identify these determinants we studied nonpathogenic mutants of a transcription factor-coding gene, AbPf2. Frequency and timing of germination and appressorium formation on host plants were similar between the nonpathogenic Δabpf2 mutants and wild-type A. brassicicola. The mutants were also similar in vitro to wild-type A. brassicicola in vegetative growth, conidium production, and responses to chemical stressors, such as a phytoalexin, reactive oxygen species, and osmolites. The mutants, however, did not penetrate host plant tissues, though their hyphae continued to grow on the plant surface. Transcripts of the AbPf2 gene increased exponentially soon after wild-type conidia encountered their host plants. A small amount of AbPf2 protein, monitored by fused green fluorescent protein, was located in both the cytoplasm and nuclei of young, mature conidia. The protein level decreased during saprophytic growth but increased several-fold during pathogenesis. Levels of both the proteins and transcripts sharply declined following colonization of host tissues beyond the initial infection site. When the transcription factor was expressed at an induced level in the wild type during early pathogenesis, the expression of 106 fungal genes was down-regulated in the Δabpf2 mutants. Notably, 33 of the 106 genes encoded secreted proteins, including eight putative effector proteins. Plants inoculated with Δabpf2 mutants expressed higher levels of genes associated with photosynthesis, the pentose phosphate pathway, and primary metabolism, but lower levels of defense-related genes. Our results suggest that conidia of A. brassicicola are programmed as saprophytes, but become parasites upon contact with their hosts. AbPf2 coordinates this transformation by expressing pathogenesis-associated genes, including those coding for effectors. Twenty seven Ar. thaliana (Col-0) were spray-inoculated until run-off with 5x105 conidia per milliliter of Δabpf2-5 mutant or the wild type. Tissues containing both host plant tissue and fungal hyphae were harvested at 12 hours postinoculation and 48 hours postinoculation from three plants for each sample and immediately frozen in liquid nitrogen to fix gene expression profiles. The frozen tissues were ground and total RNA was extracted using an RNeasy kit. Residual DNA was digested in columns with RNase-free DNase following the manufacturer’s protocol (Qiagen, Palo Alto, CA). Three biological replicates were prepared for the mutant and three for the wild type and their gene expression profiles compared. We constructed strand-specific sequencing libraries using the TruSeq™ RNA Sample Prep Kit (Illumina, San Diego, CA) from total RNA following the manufacturer’s protocol. Each sample RNA was used to construct a library with a unique index primer. A total of six index primers were used to construct six libraries. All six libraries were mixed and determined 100 nucleotide-long sequence tags using Illumina Hiseq2000 (Illumina, San Diego, CA, USA) according to the manufacturer’s protocol. Image analysis, base-calling, and quality checks were performed with the Illumina data analysis pipeline CASAVA v1.8.0.

Project description:BackgroundGlutathione transferases (GSTs) represent an extended family of multifunctional proteins involved in detoxification processes and tolerance to oxidative stress. We thus anticipated that some GSTs could play an essential role in the protection of fungal necrotrophs against plant-derived toxic metabolites and reactive oxygen species that accumulate at the host-pathogen interface during infection.ResultsMining the genome of the necrotrophic Brassica pathogen Alternaria brassicicola for glutathione transferase revealed 23 sequences, 17 of which could be clustered into the main classes previously defined for fungal GSTs and six were 'orphans'. Five isothiocyanate-inducible GSTs from five different classes were more thoroughly investigated. Analysis of their catalytic properties revealed that two GSTs, belonging to the GSTFuA and GTT1 classes, exhibited GSH transferase activity with isothiocyanates (ITC) and peroxidase activity with cumene hydroperoxide, respectively. Mutant deficient for these two GSTs were however neither more susceptible to ITC nor less aggressive than the wild-type parental strain. By contrast mutants deficient for two other GSTs, belonging to the Ure2pB and GSTO classes, were distinguished by their hyper-susceptibility to ITC and low aggressiveness against Brassica oleracea. In particular AbGSTO1 could participate in cell tolerance to ITC due to its glutathione-dependent thioltransferase activity. The fifth ITC-inducible GST belonged to the MAPEG class and although it was not possible to produce the soluble active form of this protein in a bacterial expression system, the corresponding deficient mutant failed to develop normal symptoms on host plant tissues.ConclusionsAmong the five ITC-inducible GSTs analyzed in this study, three were found essential for full aggressiveness of A. brassicicola on host plant. This, to our knowledge is the first evidence that GSTs might be essential virulence factors for fungal necrotrophs.

Dataset Information

Alternaria TeA toxin activates a chloroplast retrograde signaling pathway to facilitate JA-dependent pathogenicity.

Publications

Alternaria TeA toxin activates a chloroplast retrograde signaling pathway to facilitate JA-dependent pathogenicity.

Similar Datasets

OmicsDI is part of the ELIXIR infrastructure

Tweets