Botrytis cinerea methyl isocitrate lyase mediates oxidative stress tolerance and programmed cell death by modulating cellular succinate levels

Oren-Young, Liat; Llorens, Eugenio; Bi, Kai; Zhang, Mingzhe; Sharon, Amir

doi:10.1016/j.fgb.2020.103484

Cited by 10 publications

(4 citation statements)

References 45 publications

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“…The positive correlation between the CLSM calcium signature (Figure 2) and the upregulation of both calcium-binding EF-hand family protein member (Solyc10g006700) that is homologous to a S. tuberosum calcium-binding protein which is involved in resistance to Phytophthora infestans (Muktar et al, 2015) and calmodulin (Solyc04g058160) (Figure 6A) is interesting. EF-hand motifs in the hydrophilic C-terminal domain of tomato have been correlated to Ca 2+ cyt regulation of ROS production (Amicucci et al, 1999), whereas calmodulin, a calcium-binding protein with a helix-loop-helix (EF-hand) motif and one of the key mediators in plant immune responses (Cheval et al, 2013), is required for a successful defense response to pathogens (Zheng et al, 2018) and is upregulated by Botrytis cinerea infection (Yu and Du, 2018) a plant pathogen that causes cell disruption and death (Camejo et al, 2016;Oren-Young et al, 2021). On the other hand, the downregulation of the calcium-binding phospholipase D (Solyc01g091910), a protein that hydrolyses different membrane phospholipids and that is implicated in plant-pathogen interactions (Zhao, 2015), has also been shown to interfere with ethylene signaling regulation (Dek et al, 2018).…”

Section: Edna Induces Early Tomato Events Which Are Typical Of the Biotic Stress Responsementioning

confidence: 99%

Extracellular Fragmented Self-DNA Is Involved in Plant Responses to Biotic Stress

2021

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A growing body of evidence indicates that extracellular fragmented self-DNA (eDNA), by acting as a signaling molecule, triggers inhibitory effects on conspecific plants and functions as a damage-associated molecular pattern (DAMP). To evaluate early and late events in DAMP-dependent responses to eDNA, we extracted, fragmented, and applied the tomato (Solanum lycopersicum) eDNA to tomato leaves. Non-sonicated, intact self-DNA (intact DNA) was used as control. Early event analyses included the evaluation of plasma transmembrane potentials (Vm), cytosolic calcium variations (Ca2+cyt), the activity and subcellular localization of both voltage-gated and ligand-gated rectified K+ channels, and the reactive oxygen species (ROS) subcellular localization and quantification. Late events included RNA-Seq transcriptomic analysis and qPCR validation of gene expression of tomato leaves exposed to tomato eDNA. Application of eDNA induced a concentration-dependent Vm depolarization which was correlated to an increase in (Ca2+)cyt; this event was associated to the opening of K+ channels, with particular action on ligand-gated rectified K+ channels. Both eDNA-dependent (Ca2+)cyt and K+ increases were correlated to ROS production. In contrast, application of intact DNA produced no effects. The plant response to eDNA was the modulation of the expression of genes involved in plant–biotic interactions including pathogenesis-related proteins (PRPs), calcium-dependent protein kinases (CPK1), heat shock transcription factors (Hsf), heat shock proteins (Hsp), receptor-like kinases (RLKs), and ethylene-responsive factors (ERFs). Several genes involved in calcium signaling, ROS scavenging and ion homeostasis were also modulated by application of eDNA. Shared elements among the transcriptional response to eDNA and to biotic stress indicate that eDNA might be a common DAMP that triggers plant responses to pathogens and herbivores, particularly to those that intensive plant cell disruption or cell death. Our results suggest the intriguing hypothesis that some of the plant reactions to pathogens and herbivores might be due to DNA degradation, especially when associated to the plant cell disruption. Fragmented DNA would then become an important and powerful elicitor able to trigger early and late responses to biotic stress.

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Section: Edna Induces Early Tomato Events Which Are Typical Of the Biotic Stress Responsementioning

confidence: 99%

Extracellular Fragmented Self-DNA Is Involved in Plant Responses to Biotic Stress

2021

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“…Interestingly, a probable succinyl-coenzyme A (CoA)-ligase-encoding gene (Bcin11g03450) was upregulated in the Δ bcxyr1 strain. Recently, succinate was shown to be connected to stress responses and cell death ( 35 ), suggesting this gene might play a role in the host-pathogen interaction.…”

Section: Resultsmentioning

confidence: 99%

Botrytis cinerea Transcription Factor BcXyr1 Regulates (Hemi-)Cellulase Production and Fungal Virulence

Liu

Zhang³

et al. 2022

mSystems

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“…The increase in ROS levels in P. nicotianae indicated the potential damage to mitochondria caused by DDA. Succinic acid, a molecule that inhibits ROS-mediated lipid peroxidation in mitochondria ( 35 ), was decreased by DDA treatment. Similarly, significant transcription of MPV17 (mediating antioxidant and antiapoptotic functions in mitochondria) was also observed.…”

Section: Discussionmentioning

confidence: 99%

2 E ,4 E -Decadienoic Acid, a Novel Anti-Oomycete Agent from Coculture of Bacillus subtilis and Trichoderma asperellum

Zhang

Wang

et al. 2022

Microbiol Spectr

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Botrytis cinerea methyl isocitrate lyase mediates oxidative stress tolerance and programmed cell death by modulating cellular succinate levels

Cited by 10 publications

References 45 publications

Extracellular Fragmented Self-DNA Is Involved in Plant Responses to Biotic Stress

Extracellular Fragmented Self-DNA Is Involved in Plant Responses to Biotic Stress

Botrytis cinerea Transcription Factor BcXyr1 Regulates (Hemi-)Cellulase Production and Fungal Virulence

2 E ,4 E -Decadienoic Acid, a Novel Anti-Oomycete Agent from Coculture of Bacillus subtilis and Trichoderma asperellum

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