Pexophagy is critical for fungal development, stress response, and virulence in <i>Alternaria alternata</i>

Wu, Pei-Ching; Choo, Celine Yen Ling; Lu, Hsin-Yu; Wei, Xian-Yong; Chen, Yu-Kun; Yago, Jonar I.; Chung, Kuang-Ren

doi:10.1111/mpp.13247

Cited by 13 publications

(15 citation statements)

References 75 publications

(122 reference statements)

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“…Autophagy is a highly conserved process where proteins, membranes, and organelles are broken down and repurposed to sustain energy balance within eukaryotic cells [39,40]. In this study, the ATG8, a marker to monitor autophagosome formation [36], was characterized in A. flavus. We identified the atg8 gene and found that the ATG8 protein plays a crucial role in various aspects of A. flavus biology, including vegetative growth, conidial development, pathogenicity, resistance to ROS, and AFB1 biosynthesis.…”

Section: Discussionmentioning

confidence: 98%

“…The abovementioned data indicate the involvement of ATG8 in responding to these stress stimuli in A. flavus. In fungi, autophagy has been recognized as essential for oxidative stress resistance [36]. Therefore, the resistance ability of Δatg8 mutant against oxidative stress was measured.…”

Section: Response Of Atg8 To Multiple Stresses In a Flavusmentioning

confidence: 99%

“…The Δatg8 hyphae, stained with DCFH-DA, emitted significantly brighter green fluorescence compared to WT and atg8 C strains, indicating a higher accumulation of ROS in the Δatg8 strain (Figure 6C). RT-qPCR In fungi, autophagy has been recognized as essential for oxidative stress resistance [36]. Therefore, the resistance ability of ∆atg8 mutant against oxidative stress was measured.…”

Section: Response Of Atg8 To Multiple Stresses In a Flavusmentioning

confidence: 99%

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The Autophagy-Related Protein ATG8 Orchestrates Asexual Development and AFB1 Biosynthesis in Aspergillus flavus

Geng,

Hu,

et al. 2024

JoF

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Autophagy, a conserved cellular recycling process, plays a crucial role in maintaining homeostasis under stress conditions. It also regulates the development and virulence of numerous filamentous fungi. In this study, we investigated the specific function of ATG8, a reliable autophagic marker, in the opportunistic pathogen Aspergillus flavus. To investigate the role of atg8 in A. flavus, the deletion and complemented mutants of atg8 were generated according to the homologous recombination principle. Deletion of atg8 showed a significant decrease in conidiation, spore germination, and sclerotia formation compared to the WT and atg8Cstrains. Additionally, aflatoxin production was found severely impaired in the ∆atg8 mutant. The stress assays demonstrated that ATG8 was important for A. flavus response to oxidative stress. The fluorescence microscopy showed increased levels of reactive oxygen species in the ∆atg8 mutant cells, and the transcriptional result also indicated that genes related to the antioxidant system were significantly reduced in the ∆atg8 mutant. We further found that ATG8 participated in regulating the pathogenicity of A. flavus on crop seeds. These results revealed the biological role of ATG8 in A. flavus, which might provide a potential target for the control of A. flavus and AFB1 biosynthesis.

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Section: Discussionmentioning

confidence: 98%

Section: Response Of Atg8 To Multiple Stresses In a Flavusmentioning

confidence: 99%

Section: Response Of Atg8 To Multiple Stresses In a Flavusmentioning

confidence: 99%

See 1 more Smart Citation

The Autophagy-Related Protein ATG8 Orchestrates Asexual Development and AFB1 Biosynthesis in Aspergillus flavus

Geng,

Hu,

et al. 2024

JoF

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“…Midbody rings recognize autophagy receptors such as SQSTM1 and NBR1 during selective autophagy [ 26 ]. Pexophagy is the selective destruction of peroxisomes via autophagy; peroxisomes recognize autophagy adaptors autophagy-related 36 (ATG36), ATG40, and peroxisomal biogenesis factor 3 (PEX3), and autophagy receptors SQSTM1 and NBR1 [ 27 ]. Zymophagy selectively degrades damaged or surplus zymogen granules via autophagy; zymogen particles bind to autophagy receptors, including SQSTM1 [ 28 ].…”

Section: Mechanism Of Autophagy Pathwaysmentioning

confidence: 99%

The Emerging Role of Autophagy as a Target of Environmental Pollutants: An Update on Mechanisms

Rahman

Parvez

et al. 2023

Toxics

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Autophagy is an evolutionarily conserved cellular system crucial for cellular homeostasis that protects cells from a broad range of internal and extracellular stresses. Autophagy decreases metabolic load and toxicity by removing damaged cellular components. Environmental contaminants, particularly industrial substances, can influence autophagic flux by enhancing it as a protective response, preventing it, or converting its protective function into a pro-cell death mechanism. Environmental toxic materials are also notorious for their tendency to bioaccumulate and induce pathophysiological vulnerability. Many environmental pollutants have been found to influence stress which increases autophagy. Increasing autophagy was recently shown to improve stress resistance and reduce genetic damage. Moreover, suppressing autophagy or depleting its resources either increases or decreases toxicity, depending on the circumstances. The essential process of selective autophagy is utilized by mammalian cells in order to eliminate particulate matter, nanoparticles, toxic metals, and smoke exposure without inflicting damage on cytosolic components. Moreover, cigarette smoke and aging are the chief causes of chronic obstructive pulmonary disease (COPD)-emphysema; however, the disease’s molecular mechanism is poorly known. Therefore, understanding the impacts of environmental exposure via autophagy offers new approaches for risk assessment, protection, and preventative actions which will counter the harmful effects of environmental contaminants on human and animal health.

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“…The biosynthesis of fungal secondary metabolites is regulated or impacted by a wide variety of proteins, signals, and environmental factors ( 19 , 20 ). Studies in the tangerine pathotype have identified components in the mitogen-activated protein (MAP) kinase pathways, peroxisome complex activities, and autophagy-related processes that are required for ACT biosynthesis and virulence ( 21 – 24 ). A basal transcription factor II H subunit (tfb5) and a GATA transcription factor (AreA) have also been shown to be required for ACT biosynthesis, sporulation, and virulence in the tangerine pathotype ( 25 , 26 ).…”

Section: Introductionmentioning

confidence: 99%

The Alternaria alternata StuA transcription factor interacting with the pH-responsive regulator PacC for the biosynthesis of host-selective toxin and virulence in citrus

Chen,

Cao,

Jiao

et al. 2023

Microbiol Spectr

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The tangerine pathotype of Alternaria alternata produces a host-selective toxin termed Alternaria citri toxin (ACT). The molecular mechanisms underlying the global regulation and biosynthesis of ACT remain unknown. In the present study, the function of an APSES transcription factor StuA was investigated. StuA was shown to be required for ACT biosynthesis and fungal virulence. StuA was found, for the first time, to physically interact with a pH-responsive transcription regulator PacC using yeast two-hybrid, bimolecular fluorescence complementation, and GST pull-down assays. Functional analyses revealed that StuA and PacC regulate the expression of genes involved in toxin biosynthesis and virulence. Mutation of stuA via targeted gene deletion or silencing pacC yielded fungal strains that decreased the expression of seven toxin biosynthetic genes ( ACCT ) and toxin production. EMSA analyses revealed that PacC could bind to the promoters of ACTT6 encoding an enoyl-CoA hydratase and ACTTR encoding an ACT pathway-specific transcription factor. Site-directed mutagenesis of five potential protein kinase A (PKA) phosphorylation sites in StuA revealed that none of the sites was involved in ACT production, indicating that the function of StuA in the regulation of ACT gene expression is not dependent on phosphorylation. Overall, our results confirmed that PacC is one of the key regulators interacting with StuA for the biosynthesis of ACT. Environmental pH may play a decisive role during A. alternata pathogenesis. Our results also revealed a previously unrecognized (StuA-PacC)→ACTTR module for the biosynthesis of ACT in A. alternata . IMPORTANCE In this study, we used Alternaria alternata as a biological model to report the role of StuA in phytopathogenic fungi. Our findings indicated that StuA is required for Alternaria citri toxin (ACT) biosynthesis and fungal virulence. In addition, StuA physically interacts with PacC. Disruption of stuA or pacC led to decreased expression of seven toxin biosynthetic genes (ACCT) and toxin production. PacC could recognize and bind to the promoter regions of ACTT6 and ACTTR . Our results revealed a previously unrecognized (StuA-PacC)→ACTTR module for the biosynthesis of ACT in A. alternata , which also provides a framework for the study of StuA in other fungi.

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Pexophagy is critical for fungal development, stress response, and virulence in Alternaria alternata

Cited by 13 publications

References 75 publications

The Autophagy-Related Protein ATG8 Orchestrates Asexual Development and AFB1 Biosynthesis in Aspergillus flavus

The Autophagy-Related Protein ATG8 Orchestrates Asexual Development and AFB1 Biosynthesis in Aspergillus flavus

The Emerging Role of Autophagy as a Target of Environmental Pollutants: An Update on Mechanisms

The Alternaria alternata StuA transcription factor interacting with the pH-responsive regulator PacC for the biosynthesis of host-selective toxin and virulence in citrus

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