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Activation of auxin signalling counteracts photorespiratory hydrogen peroxide dependent cell death

ABSTRACT: The high metabolic flux through photorespiration constitutes a significant part of the carbon cycle. Although, the major enzymatic steps of the photorespiratory pathway are well characterized, little information is available on the functional significance of photorespiration beyond carbon recycling. Particularly important in this respect is the peroxisomal catalase activity which removes photorespiratory H2O2 generated during the oxidation of glycolate to glyoxylate, thus maintaining the cellular redox homeostasis governing the perception, integration and execution of stress responses. By perfroming a chemical screen, we identified 34 small molecules that alleviate the negative effects of photorespiration in Arabidopsis thaliana mutants lacking photorespiratory catalase (cat2). The chlorophyll fluorescence parameter photosystem II maximum efficiency (Fv'/Fm') was used as a high-throughput readout. The most potent chemical that could rescue the photorespiratory phenotype of cat2 is a pro-auxin that contains a synthetic auxin-like substructure belonging to the phenoxy herbicide family which can be released in planta. The naturally occurring indole-3-acetic acid (IAA) and other chemically distinct synthetic auxins also inhibited the photorespiratory-dependent cell death in cat2 mutants, implying a role for auxin signaling in stress tolerance. We used global transcriptome profiling to characterize the effect of a novel pro-axin structure (2-(2,4-dichlorophenoxy)-N-[4-(isobutyrylamino)-3-methoxyphenyl]propanamide) on Arabidopsis Col0 seedlings

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE52013 | GEO | 2013/11/02

SECONDARY ACCESSION(S): PRJNA226106

REPOSITORIES: GEO

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Activation of auxin signalling counteracts photorespiratory hydrogen peroxide dependent cell death

Project description:The high metabolic flux through photorespiration constitutes a significant part of the carbon cycle. Although, the major enzymatic steps of the photorespiratory pathway are well characterized, little information is available on the functional significance of photorespiration beyond carbon recycling. Particularly important in this respect is the peroxisomal catalase activity which removes photorespiratory H2O2 generated during the oxidation of glycolate to glyoxylate, thus maintaining the cellular redox homeostasis governing the perception, integration and execution of stress responses. By perfroming a chemical screen, we identified 34 small molecules that alleviate the negative effects of photorespiration in Arabidopsis thaliana mutants lacking photorespiratory catalase (cat2). The chlorophyll fluorescence parameter photosystem II maximum efficiency (Fv'/Fm') was used as a high-throughput readout. The most potent chemical that could rescue the photorespiratory phenotype of cat2 is a pro-auxin that contains a synthetic auxin-like substructure belonging to the phenoxy herbicide family which can be released in planta. The naturally occurring indole-3-acetic acid (IAA) and other chemically distinct synthetic auxins also inhibited the photorespiratory-dependent cell death in cat2 mutants, implying a role for auxin signaling in stress tolerance. We used global transcriptome profiling to characterize the effect of a novel pro-axin structure (2-(2,4-dichlorophenoxy)-N-[4-(isobutyrylamino)-3-methoxyphenyl]propanamide) on Arabidopsis Col0 seedlings 2-(2,4-dichlorophenoxy)-N-[4-(isobutyrylamino)-3-methoxyphenyl]propanamid (5 μM) was added to seven-day-old Arabidopsis Col0 seedlings grown in a 96-well plate setup. Control plants were treated with solvent (DMSO) only. RNA was extracted 24 h following chemical addition.

2013-11-02 | E-GEOD-52013 | biostudies-arrayexpress

Transcriptomic responses of cat2-2 and shr-6 cat2-2 to photorespiratory conditions

Project description:Hydrogen peroxide (H2O2) is a potent signaling molecule influencing various aspects of plant growth and development. Its limited lifetime and specific production sites in the plant cell necessitate the existence of specialized mechanisms that relay H2O2-encoded information. To discover such mechanisms, we focused on peroxisomal H2O2 production triggered by enhanced photorespiration in Arabidopsis mutants lacking catalase activity (cat2-2), and looked for second-site mutations that attenuate the negative effects (Fv'/Fm' decline and lesion formation) of H2O2 build up. A mutation residing in the GRAS family transcriptional regulator SHORT-ROOT (SHR) was found to underlie the increased performance of cat2-2 knock-outs under photorespiratory stress. In contrast to shr, introduction of the scr mutation in cat2-2 background did not improve the photorespiratory performance of plants lacking peroxisomal catalase. The absence of SHR negatively affected the activity of the photorespiratory enzymes glycolate oxidase and catalase, which was accompanied with elevated glycolate content and inability to accumulate glycine under conditions promoting photorespiration. The transcriptome signature of cat2-2 shr-6 double mutants exposed to photorespiratory stress lacked jasmonate-dependent signaling components, otherwise induced in cat2-2. The photorespiratory phenotype of cat2-2 was found to be modulated by exogenous sugars both in the presence and absence of shr. Taken together, these findings highlight a crucial role for SHR in H2O2 signal transduction and stress tolerance.

2016-06-10 | GSE66365 | GEO

Transcriptomic responses of cat2-2 and shr-6 cat2-2 to photorespiratory conditions

2016-06-10 | E-GEOD-66365 | biostudies-arrayexpress

Arabidopsis GLYCOLATE OXIDASE 1 and 2 display divergent roles under conditions promoting photorespiration

Project description:Hydrogen peroxide (H2O2) can act as a signaling molecule that influences various aspects of plant growth and development, including stress signaling and cell death. To unravel the molecular mechanisms that regulate the response towards an impact of increased H2O2 levels in plant cells, we focused on the photorespiration-dependent peroxisomal H2O2 production in Arabidopsis thaliana mutants lacking CATALASE2 (CAT2) activity (cat2-2) and screened for second-site mutations that attenuate the Fv'/Fm' decrease and lesion formation linked to the cat2-2 phenotype. A mutation in GLYCOLATE OXIDASE 1, encoding one of the two photorespiratory isoforms of glycolate oxidase rescued the cell death phenotype of cat2-2 plants under photorespiration-promoting conditions. Interestingly, introduction of gox2 into the cat2 background did not have the same effect and the double cat2 gox2 mutants were as affected as the parental cat2 mutants under conditions promoting photorespiration. Using a series of physiological, biochemical and metabolomic approaches we investigated the differential photorespiratory response of cat2 mutants underlied by the lack of GOX1 and GOX2. These differences are in line with the non-redundant functions of GOX1 and GOX2 which could be observed under enhanced photorespiration.

2016-06-10 | GSE77170 | GEO

Arabidopsis GLYCOLATE OXIDASE 1 and 2 display divergent roles under conditions promoting photorespiration

2016-06-10 | E-GEOD-77170 | biostudies-arrayexpress

SHORT-ROOT Deficiency Alleviates the Cell Death Phenotype of the Arabidopsis catalase2 Mutant under Photorespiration-Promoting Conditions

Project description:Hydrogen peroxide (H2O2) can act as a signaling molecule that influences various aspects of plant growth and development, including stress signaling and cell death. To unravel the molecular mechanisms that regulate the response towards an impact of increased H2O2 levels in plant cells, we focused on the photorespiration-dependent peroxisomal H2O2 production in Arabidopsis thaliana mutants lacking CATALASE2 (CAT2) activity (cat2-2) and screened for second-site mutations that attenuate the Fv'/Fm' decrease and lesion formation linked to the cat2-2 phenotype. A mutation in the transcriptional regulator SHORT-ROOT (SHR) of the GRAS family rescued the cell death phenotype of cat2-2 plants under photorespiration-promoting conditions in a SCR-independent way, and provoked perturbation of photorespiratory metabolites. SHR deficiency boosted ascorbate levels and prevented the oxidation of the glutathione pool in cat2-2 background upon exposure to photorespiratory stress. These results reveal an unanticipated role for SHR as a regulator of cellular redox homeostasis. Unstressed and stressed samples of 4 genotypes (Col-0, cat2, shr and cat2 shr) in triplicate

2016-07-28 | E-GEOD-77017 | biostudies-arrayexpress

Respiratory burst oxidase homologues D and F in catalase2 deficient plants

Project description:Hydrogen peroxide (H2O2) can act as a signaling molecule that influences various aspects of plant growth and development, including stress signaling and cell death. Catalase deficient plants are pioneering systems which accumulate hydrogen peroxide (H2O2) from peroxisomal origin during photorespiratory challenges. Respiratory burst oxidase homologues D and F are known to participate in intracellular oxidative stress response launched in cat2 mutants (Chaouch et al., 2012). We studied the compared the transcriptional response of cat2 rbohD and cat2 rbohF double mutants versus the cat2 background to further adress their role during photorespiratory stress.

2016-06-10 | GSE81516 | GEO

SHORT-ROOT Deficiency Alleviates the Cell Death Phenotype of the Arabidopsis catalase2 Mutant under Photorespiration-Promoting Conditions

Project description:Hydrogen peroxide (H2O2) can act as a signaling molecule that influences various aspects of plant growth and development, including stress signaling and cell death. To unravel the molecular mechanisms that regulate the response towards an impact of increased H2O2 levels in plant cells, we focused on the photorespiration-dependent peroxisomal H2O2 production in Arabidopsis thaliana mutants lacking CATALASE2 (CAT2) activity (cat2-2) and screened for second-site mutations that attenuate the Fv'/Fm' decrease and lesion formation linked to the cat2-2 phenotype. A mutation in the transcriptional regulator SHORT-ROOT (SHR) of the GRAS family rescued the cell death phenotype of cat2-2 plants under photorespiration-promoting conditions in a SCR-independent way, and provoked perturbation of photorespiratory metabolites. SHR deficiency boosted ascorbate levels and prevented the oxidation of the glutathione pool in cat2-2 background upon exposure to photorespiratory stress. These results reveal an unanticipated role for SHR as a regulator of cellular redox homeostasis.

2016-07-28 | GSE77017 | GEO

Respiratory burst oxidase homologues D and F in catalase2 deficient plants

Project description:Hydrogen peroxide (H2O2) can act as a signaling molecule that influences various aspects of plant growth and development, including stress signaling and cell death. Catalase deficient plants are pioneering systems which accumulate hydrogen peroxide (H2O2) from peroxisomal origin during photorespiratory challenges. Respiratory burst oxidase homologues D and F are known to participate in intracellular oxidative stress response launched in cat2 mutants (Chaouch et al., 2012). We studied the compared the transcriptional response of cat2 rbohD and cat2 rbohF double mutants versus the cat2 background to further adress their role during photorespiratory stress. After 3 weeks of growth, leaf tissue from the three different genotypes was harvested in triplicate.

2016-06-10 | E-GEOD-81516 | biostudies-arrayexpress

Photorespiration is crucial to the dynamic response of photosynthetic metabolism and stomatal movement to altered CO2 availability

Project description:The photorespiratory pathway, short photorespiration, is an essential process in oxygenic photosynthetic organisms but also reduces the efficiency of photosynthetic carbon assimilation and is hence frequently considered as a wasteful process. By comparing the response of wild-type plants and mutants impaired in photorespiration to a shift in ambient CO2 concentrations, we demonstrate that photorespiration also plays a beneficial role during short-term acclimation to reduced CO2 availability. Wild-type plants responded with few differentially expressed genes, mostly involved in drought stress, which is likely a consequence of enhanced opening of stomata and concomitant water loss upon shift toward low CO2. In contrast, mutants with impaired activity of photorespiratory enzymes were highly stressed and not able to adjust stomatal conductance to reduced external CO2 availability. The mutants´ transcriptional response was congruent, indicating a general reprogramming to deal with the consequences of reduced CO2 availability, signaled by enhanced oxygenation of ribulose-1,5 bisphosphate and amplified by the artificially impaired photorespiratory metabolism. Central in this reprogramming was the pronounced reallocation of resources from growth processes to stress responses. In conclusion, we demonstrate that unrestricted photorespiratory metabolism is a prerequisite for rapid physiological acclimation to a reduction in CO2 availability.

2016-10-15 | GSE87329 | GEO

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