Ferroptosis contributes to developmental cell death in rice blast

Shen, Qin; Liang, Maojin; Yang, Fan; Deng, Yi Zhen; Naqvi, Naweed I.

doi:10.1101/850560

Cited by 10 publications

(29 citation statements)

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“…By using the DII-Venus auxin biosensor in the fungus, we observed that auxin accumulated in the conidia in a sequential manner (from terminal conidial cell to the one proximal to the appressorium), in the process of appressorium development (Figure 1A). Such auxin accumulation pattern coincides with that of conidial ferroptosis, an iron-dependent cell death mediated by peroxidation of membrane lipids [33], during appressorium formation and maturation [20], and thus intrigued us to infer that auxin may regulate conidial ferroptosis. Indeed, our results showed that inhibition of IAA production by AOA effectively suppressed such conidial cell death (Figure 3 A-C).…”

Section: Discussionmentioning

confidence: 90%

“…After validating the engineered DII-Venus as an auxin biosensor in M. oryzae, we then proceeded to monitor the endogenous auxin homeostasis during pathogenic development and invasive growth. We were interested to first address whether auxin synthesis and/or distribution is uniform in the three conidial cells, which undergo regulated cell death one by one sequentially [20]. Interestingly, such intrinsic (fungal) auxin first accumulated in the terminal cell (the conidial cell distal to appressorium) at the specific inhibitor amino-oxyacetic acid (AOA) (Figure 1A).…”

Section: Intrinsic Auxin Accumulation In M Oryzae During Pathogenic Development and Host Infectionmentioning

confidence: 99%

“…To test this hypothesis, we first examined the effect of cell density on conidial cell death during appressorium development, since we saw a close correlation between fungal auxin accumulation and ferroptotic cell death in the conidium, which is critical for appressorium function [20,[25][26]. At 15 hpi, the condia from a low-density group (0.5×10 5 ) displayed obviously longer germ tube, and delayed conidial cell death, as compared to the conidia from a high-density group (3×10 5 ; Figure 3A).…”

Section: Fungal Auxin Acts As a Quorum-sensing Molecule Regulating Pathogenic Developmentmentioning

confidence: 99%

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Fungal auxin is a quorum-based modulator of blast disease severity

Dong

Shen

Chen

et al. 2021

Preprint

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Auxin is an important phytohormone regulating plant growth and development, and can also be produced by microbial pathogens including the rice-blast fungus Magnaporthe oryzae. However, the detailed biosynthesis pathway, biological function(s), and cellular distribution of such fungal auxin in M. oryzae remain largely unknown. Here, we report a sequential accumulation of intrinsic auxin in the three conidial cells, the infection structure (appressorium), and the invasive hyphae in M. oryzae. Such fungus-derived auxin was also secreted out and perceived by the host plants. A mitochondria-associated Indole-3-pyruvate decarboxylase, Ipd1, is essential for auxin/Indole-3-acetic acid biosynthesis in M. oryzae. The ipd1 mutant was defective in pathogenicity whereas overexpression of IPD1 led to enhanced virulence in rice. Chemical inhibition of fungal IAA biosynthesis, or its increase via external supplementation decreased or increased the severity of blast disease, respectively, in a dose-dependent manner. Furthermore, the IAA produced and secreted by M. oryzae governed the incidence and severity of blast disease in a quorum-dependent manner. Appressorium formation, conidial cell death critical for appressorium function, and the transcription of infection-related genes, MPG1 and INV1, directly correlated with cell density and/or IAA levels within the conidial population at the early stages of pathogenic development. Overall, our study revealed that the severity of blast disease is regulated via quorum sensing with intrinsic IAA serving as an associated signal transducer in rice blast.

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Section: Discussionmentioning

confidence: 90%

Section: Intrinsic Auxin Accumulation In M Oryzae During Pathogenic Development and Host Infectionmentioning

confidence: 99%

Section: Fungal Auxin Acts As a Quorum-sensing Molecule Regulating Pathogenic Developmentmentioning

confidence: 99%

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Fungal auxin is a quorum-based modulator of blast disease severity

Dong

Shen

Chen

et al. 2021

Preprint

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“…For instance, lipid peroxidation and ferroptosis are used to guard against Plasmodium infection in mice (Kain et al, 2020), which is suppressed by erastin treatment. In plants, ferroptosis is activated in the blast fungus Magnaporthe oryzae during rice development (Dangol et al, 2019;Shen et al, 2019). Ferroptosis-like cell death also takes place in Arabidopsis thaliana in response to environmental stress such as heat shock (Disté fano et al, 2017).…”

Section: Ferroptosis In Physiologymentioning

confidence: 99%

Progress in Understanding Ferroptosis and Challenges in Its Targeting for Therapeutic Benefit

Zou

Schreiber

2020

Cell Chemical Biology

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Ferroptosis is an iron-dependent cell-death modality driven by oxidative phospholipid damage. In contrast to apoptosis, which enables organisms to eliminate targeted cells purposefully at specific times, ferroptosis appears to be a vulnerability of cells that otherwise use high levels of polyunsaturated lipids to their advantage. Cells in this high polyunsaturated lipid state generally have safeguards that mitigate ferroptotic risk. Since its recognition, ferroptosis has been implicated in degenerative diseases in tissues including kidney and brain, and is a targetable vulnerability in multiple cancers-each likely characterized by the high polyunsaturated lipid state with insufficient or overwhelmed ferroptotic safeguards. In this Perspective, we present progress toward defining the essential roles and key mediators of lipid peroxidation and ferroptosis in disease contexts. Moreover, we discuss gaps in our understanding of ferroptosis and list key challenges that have thus far limited the full potential of targeting ferroptosis for improving human health.

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“…Autophagy‐dependent conidial cell death is reportedly necessary for the appressorium to mature and infect rice (Veneault‐Fourrey et al, 2006). We recently demonstrated that such conidial death is ferroptotic in nature (Shen et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

Tangeretin inhibits fungal ferroptosis to suppress rice blast

Liang

Shen

et al. 2021

JIPB

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Flavonoids are polyphenolic secondary metabolites that function as signaling molecules, allopathic compounds, phytoalexins, detoxifying agents and antimicrobial defensive compounds in plants. Blast caused by the fungus Magnaporthe oryzae is a serious disease affecting rice cultivation. In this study, we revealed that a natural flavonoid, tangeretin, substantially delays the formation of M. oryzae appressoria and blocks the development of blast lesions on rice plants. Our data suggest that tangeretin has antioxidant activity that interferes with conidial cell death/ferroptosis, which is critical for M. oryzae pathogenicity. Tangeretin showed a ferroptosis inhibition efficacy comparable to the well‐established liproxstatin‐1. Furthermore, overexpression of the NADPH oxidases NOX1 or NOX2 significantly decreased sensitivity toward tangeretin treatment, suggesting Nox‐mediated lipid peroxidation as a possible target for tangeretin in regulating redox signaling and ferroptosis in M. oryzae. Our nursery and field tests showed that application of tangeretin can effectively mitigate overall disease symptoms and prevent leaf blast. Our study reveals the plant‐derived fungal ferroptosis inhibitor tangeretin as a potential and novel antifungal agrochemical for the sustainable prevention of the devastating blast disease in important cereal crops.

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Ferroptosis contributes to developmental cell death in rice blast

Cited by 10 publications

References 50 publications

Fungal auxin is a quorum-based modulator of blast disease severity

Fungal auxin is a quorum-based modulator of blast disease severity

Progress in Understanding Ferroptosis and Challenges in Its Targeting for Therapeutic Benefit

Tangeretin inhibits fungal ferroptosis to suppress rice blast

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