Multiple pathways mediate chloroplast singlet oxygen stress signaling

Tano, David W.; Kozlowska, Marta A.; Easter, R. A.; Woodson, Jesse D.

doi:10.1007/s11103-022-01319-z

Cited by 14 publications

(29 citation statements)

References 80 publications

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“…However, this necessitates that the plants be screened as adults after being selected for transgenesis. It has been previously shown that when grown as adults in cycling light conditions, fc2 mutants do initiate 1 O 2 signaling (Woodson et al, 2015, Lemke et al, 2021, Tano et al, 2023). However, fts suppressor mutants have mostly been characterized as seedlings and it is unclear how they behave as adults (a summary of published fts mutants and their seedling phenotypes can be found in Table S7) .…”

Section: Resultsmentioning

confidence: 99%

A genetic screen for dominant chloroplast reactive oxygen species signaling mutants reveals life stage-specific singlet oxygen signaling networks

Lemke,

Woodson

2023

Preprint

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Plants employ intricate molecular mechanisms to respond to abiotic stresses, which often lead to the accumulation of reactive oxygen species (ROS) within organelles such as chloroplasts. Such ROS can produce stress signals that regulate cellular response mechanisms. One ROS, singlet oxygen (1O2), is predominantly produced in the chloroplast during photosynthesis and can trigger chloroplast degradation, programmed cell death (PCD), and retrograde (organelle-to-nucleus) signaling. However, little is known about the molecular mechanisms involved in these signaling pathways or how many different signaling1O2pathways may exist. TheArabidopsis thaliana plastid ferrochelatase two(fc2) mutant conditionally accumulates chloroplast1O2, makingfc2a valuable genetic system for studying chloroplast1O2-initiated signaling. Here, we have used activation tagging in a new forward genetic screen to identify eight dominantfc2activation-tagged (fas) mutations that suppress chloroplast1O2-initiated PCD. Whilefc2 fasmutants all block1O2-triggered PCD in the adult stage, only twofc2 fasmutants block such cellular degradation at the seedling stage, suggesting that life-stage-specific1O2-response pathways exist. In addition to PCD,fasmutations generally reduce1O2-induced retrograde signals. Furthermore,fasmutants have enhanced tolerance to excess light, a natural mechanism to produce chloroplast1O2. However, general abiotic stress tolerance was only observed in onefc2 fasmutant (fc2 fas2). Together, this suggests that plants can employ general stress tolerance mechanisms to overcome1O2production but that this screen was mostly specific to1O2signaling. We also observed that salicylic acid (SA) and jasmonate (JA) stress hormone response marker genes were induced in1O2-stressedfc2and generally reduced byfasmutations, suggesting that SA and JA signaling is correlated with active1O2signaling and PCD. Together, this work highlights the complexity of1O2signaling by demonstrating that multiple pathways may exist and introduces a suite of new1O2signaling mutants to investigate the mechanisms controlling chloroplast-initiated degradation, PCD, and retrograde signaling.

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Section: Resultsmentioning

confidence: 99%

A genetic screen for dominant chloroplast reactive oxygen species signaling mutants reveals life stage-specific singlet oxygen signaling networks

Lemke,

Woodson

2023

Preprint

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“…Here we report the cellular manifestations of osmotic stress in the root through the lens of singlet oxygen production. Most studies about singlet oxygen are confined to aerial organs where the creation of singlet oxygen through photodynamic processes occurs in high light or in mutant plants (Mattila et al, 2023; Tano et al, 2023; Zhang et al, 2023). In those cases, dysfunction of photosynthesis and the production of singlet oxygen generated chemical messengers were shown to dramatically effect plant physiology (Li and Kim, 2023).…”

Section: Discussionmentioning

confidence: 99%

Osmotic stress in roots drives lipoxygenase-dependent plastid remodeling through singlet oxygen production

Cohen-Hoch,

Chen,

Sharabi

et al. 2024

Preprint

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Osmotic stress, caused by the lack of water or by high salinity, is a common environmental problem in roots. Osmotic stress can be reproducibly simulated with the application of solutions of the high-molecular-weight and impermeable polyethylene glycol. Different reactive oxygen species such as singlet oxygen, superoxide and hydrogen peroxide accompany this stress. Among them, singlet oxygen, produced as a byproduct of lipoxygenase activity, was shown to be associated with limiting root growth. To better understand the source and effect of singlet oxygen, its production was followed at the cellular level. Osmotic stress initiated profound changes in plastid morphology and vacuole structure. By confocal and electron microscopy the plastids were shown to be a source of singlet oxygen accompanied by the appearance of multiple small extraplastidic bodies that were also an intense source of singlet oxygen. A marker protein, CRUMPLED LEAF, indicated that these small bodies originated from the plastid outer membrane. Remarkably a type 9 lipoxygenase, LOX5, was shown to change its distribution from uniformly cytoplasmic to a more clumped distribution together with plastids and the small bodies. In addition, oxylipin products of type 9 lipoxygenase increased while products of type 13 lipoxygenases decreased. Inhibition of lipoxygenase by SHAM inhibitor or in down-regulated lipoxygenase lines prevented cells from initiating the cellular responses leading to cell death. In contrast, singlet oxygen scavenging halted terminal cell death. These findings underscore the reversible nature of osmotic stress-induced changes, emphasizing the pivotal roles of lipoxygenases and singlet oxygen in root stress physiology.

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“…Thus, lesion formation in acd2 may be distinct from EL-induced 1 O2 signaling, which involves both PUB4 and OXI1 in wt and ch1 mutants 11,24 .…”

Section: Main Textmentioning

confidence: 98%

“…However, it is not known if these mutants represent one or multiple chloroplast signaling pathways. To this end, we recently used a meta-analysis of previously published whole transcriptome data sets of the three mutants to determine if they regulate the same set of genes 24 due to generating the same 1 O 2 signal. We observed that they share a small core transcriptional response to 1 O 2 stress (36 genes), but maintain unique patterns.…”

Section: Main Textmentioning

confidence: 99%

“…This result opened the possibility that these mutants use different 1 O 2 signals that report on specific stresses. Next, we combined the suppressor mutations described above with 1 O 2 -producing backgrounds in which they were not originally isolated 24 . We then tested the ability of these suppressor mutations to block or alter 1 O 2 signaling in these new genetic backgrounds.…”

Section: Main Textmentioning

confidence: 99%

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Investigating the mechanism of chloroplast singlet oxygen signaling in theArabidopsis thaliana accelerated cell death 2mutant

Lemke,

Abate,

Woodson

2024

Preprint

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As sessile organisms, plants have evolved complex signaling mechanisms to sense stress and acclimate. This includes the use of reactive oxygen species (ROS) generated during dysfunctional photosynthesis to initiate signaling. One such ROS, singlet oxygen (1O2), can trigger retrograde signaling, chloroplast degradation, and programmed cell death. However, the signaling mechanisms are largely unknown. Several proteins (e.g., PUB4, OXI1, EX1) are proposed to play signaling roles across threeArabidopsis thalianamutants that conditionally accumulate chloroplast1O2(fluorescent in blue light(flu),chlorina 1(ch1), andplastid ferrochelatase 2(fc2)). We previously demonstrated that these mutants reveal at least two chloroplast1O2signaling pathways (represented byfluandfc2/ch1). Here, we test if the1O2-accumulating lesion mimic mutant,accelerated cell death 2(acd2), also utilizes these pathways. Thepub4-6allele delayed lesion formation inacd2and restored photosynthetic efficiency and biomass. Conversely, anoxi1mutation had no measurable effect on these phenotypes.acd2mutants were not sensitive to excess light (EL) stress, yetpub4-6andoxi1both conferred EL tolerance within theacd2background, suggesting that EL-induced1O2signaling pathways are independent from spontaneous lesion formation. Thus,1O2signaling inacd2may represent a third (partially overlapping) pathway to control cellular degradation.

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Multiple pathways mediate chloroplast singlet oxygen stress signaling

Abstract: Chloroplast singlet oxygen initiates multiple pathways to control chloroplast degradation, cell death, and nuclear gene expression.

Cited by 14 publications

References 80 publications

A genetic screen for dominant chloroplast reactive oxygen species signaling mutants reveals life stage-specific singlet oxygen signaling networks

A genetic screen for dominant chloroplast reactive oxygen species signaling mutants reveals life stage-specific singlet oxygen signaling networks

Osmotic stress in roots drives lipoxygenase-dependent plastid remodeling through singlet oxygen production

Investigating the mechanism of chloroplast singlet oxygen signaling in theArabidopsis thaliana accelerated cell death 2mutant

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