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Disruption of mitochondrial dynamics increases stress resistance through activation of multiple stress response pathways.

ABSTRACT: Mitochondria are dynamic organelles that can change shape and size depending on the needs of the cell through the processes of mitochondrial fission and fusion. In this work, we investigated the role of mitochondrial dynamics in organismal stress response. By using C. elegans as a genetic model, we could visualize mitochondrial morphology in a live organism with well-established stress assays and well-characterized stress response pathways. We found that disrupting mitochondrial fission (DRP1/drp-1) or fusion (OPA1/eat-3, MFN/fzo-1) genes caused alterations in mitochondrial morphology that impacted both mitochondrial function and physiologic rates. While both mitochondrial fission and mitochondrial fusion mutants showed increased sensitivity to osmotic stress and anoxia, surprisingly we found that the mitochondrial fusion mutants eat-3 and fzo-1 are more resistant to both heat stress and oxidative stress. In exploring the mechanism of increased stress resistance, we found that disruption of mitochondrial fusion genes resulted in the upregulation of multiple stress response pathways. Overall, this work demonstrates that disrupting mitochondrial dynamics can have opposite effects on resistance to different types of stress. Our results suggest that disruption of mitochondrial fusion activates multiple stress response pathways that enhance resistance to specific stresses.

SUBMITTER: Machiela E

PROVIDER: S-EPMC7313680 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Disruption of mitochondrial dynamics increases stress resistance through activation of multiple stress response pathways.

Machiela Emily E Liontis Thomas T Dues Dylan J DJ Rudich Paige D PD Traa Annika A Wyman Leslie L Kaufman Corah C Cooper Jason F JF Lew Leira L Nadarajan Saravanapriah S Senchuk Megan M MM Van Raamsdonk Jeremy M JM

FASEB journal : official publication of the Federation of American Societies for Experimental Biology 20200508 6

Mitochondria are dynamic organelles that can change shape and size depending on the needs of the cell through the processes of mitochondrial fission and fusion. In this work, we investigated the role of mitochondrial dynamics in organismal stress response. By using C. elegans as a genetic model, we could visualize mitochondrial morphology in a live organism with well-established stress assays and well-characterized stress response pathways. We found that disrupting mitochondrial fission (DRP1/dr ...[more]

PMID: 32385951

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Project description:Plant oxylipins are signaling molecules produced from fatty acids by oxidative pathways, mainly initiated by 9- and 13-lipoxygenases (9-LOX and 13-LOX), alpha-dioxygenases or non-enzymatic oxidation. Oxylipins from the 9-LOX pathway induce oxidative stress and control root development and plant defense. These activities have been associated with mitochondrial processes, but precise cellular targets and pathways remain unknown. In order to study oxylipin signaling, we previously generated a collection of Arabidopsis thaliana mutants that were insensitive to the 9-LOX products 9(S)-hydroxy-10,12, 15-octadecatrienoic acid (9-HOT) and its ketone derivative 9-KOT (noxy mutants). Here, we describe noxy1, noxy3, noxy5, noxy23, and noxy54 mutants, all affected in nucleus-encoded mitochondrial proteins, and use them to study the role of mitochondria in oxylipin signaling. Functional and phenotypic analyses showed that noxy plants displayed mitochondrial aggregation, reduced respiration rates and resistance to the complex III inhibitor Antimycin A (AA), thus indicating a close similarity of the oxylipin signaling and mitochondrial stress. Application of 9-HOT and 9-KOT protected plants against subsequent mitochondrial stress, whereas they boosted root growth reduction when applied in combination with complex III inhibitors but did not with inhibitors of other respiratory complexes. A similar effect was caused by linear-chain oxylipins from 13-LOX or non-enzymatic pathways having α,β-unsaturated hydroxyl or keto groups in their structure. Studies to investigate 9-HOT and 9-KOT activity indicated that they do not reduce respiration rates, but their action is primarily associated with enhanced ROS responses. This was supported by the results showing that 9-HOT or 9-KOT combined with AA amplified the expression of oxylipin- and ROS-responding genes but not of the AA marker AOX1a, thus implying the activation of a specific mitochondria retrograde signaling pathway. Our results implicate mitochondrial complex III as a hub in the signaling activity of multiple oxylipin pathways and point at downstream ROS responses as components of oxylipin function.

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Disruption of mitochondrial dynamics increases stress resistance through activation of multiple stress response pathways.

Publications

Disruption of mitochondrial dynamics increases stress resistance through activation of multiple stress response pathways.

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