Autophagy is responsible for the accumulation of proteogenic dipeptides in response to heat stress in <i>Arabidopsis thaliana</i>

Thirumalaikumar, Venkatesh P.; Wagner, Mateusz; Balazadeh, Salma; Skirycz, Aleksandra

doi:10.1111/febs.15336

Cited by 30 publications

(39 citation statements)

References 34 publications

(58 reference statements)

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“…At the 30 min time point, the 2′,3′-cAMP-induced genes were involved in many biological processes, with the highest fold enrichment for genes responding to biotic and abiotic stress, such as heat shock factors, transcription factors, and response to JA. This parallels the metabolomics data, where the accumulation of mainly RNA-degradation products and dipeptides (29) (Figure 1C) are signatures for stress response (Doppler et al, 2019; Thirumalaikumar et al, 2020; Camilo Moreno et al, 2021) not only in plants (Luzarowski et al, 2021).…”

Section: Discussionsupporting

confidence: 79%

2’,3’-cAMP treatment mimics stress molecular response inArabidopsis thaliana

Chodasiewicz

Kerber

Górka

et al. 2021

Preprint

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For many years, 2′,3′-cyclic adenosine monophosphate (2′,3′-cAMP), a positional isomer of the second messenger 3′,5′-cAMP, has not received enough attention. Recent studies have reported that 2′,3′-cAMP exists in plants and might be involved in stress signaling because 1) its level increases upon wounding and 2) it was shown to participate in stress granule formation. Although 2′,3′-cAMP is known as RNA-degradation product, the effect of its accumulation in the cell remains unknown. Here, we unprecedentedly evaluate responses at the transcriptome, metabolome, and proteome levels to the accumulation of 2′,3′-cAMP in Arabidopsis plants. Data revealed that 2′,3′-cAMP is metabolized into adenosine, suggesting that a well-known cyclic nucleotide - adenosine pathway from human cells might exist also in plants. However, the control transcriptomic data indicated that, despite fewer overlaps, responses to 2′,3′-cAMP and to adenosine differ. Analysis of the transcriptome and proteome in response to 2′,3′-cAMP showed similar changes, known as signatures for abiotic stress response. This is further supported by the fact that adding to the role in facilitating of stress granules (SGs) formation, 2′,3′-cAMP induces changes at the level of proteins known as key components of SGs and can also induce movement of processing bodies (PBs) in the cell.

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Section: Discussionsupporting

confidence: 79%

2’,3’-cAMP treatment mimics stress molecular response inArabidopsis thaliana

Chodasiewicz

Kerber

Górka

et al. 2021

Preprint

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“…Finally, the regulatory role of dipeptides would become particularly important in conditions that promote protein degradation. We have recently shown that in response to abiotic stress, such as heat and dark, plants accumulate dipeptides in the autophagydependent manner 57 . Autophagy was also shown to account for the increase in dipeptides reported in the mammalian pro-tumorigenic cell lines 48 .…”

Section: Discussionmentioning

confidence: 99%

Global mapping of protein–metabolite interactions in Saccharomyces cerevisiae reveals that Ser-Leu dipeptide regulates phosphoglycerate kinase activity

et al. 2021

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Protein–metabolite interactions are of crucial importance for all cellular processes but remain understudied. Here, we applied a biochemical approach named PROMIS, to address the complexity of the protein–small molecule interactome in the model yeast Saccharomyces cerevisiae. By doing so, we provide a unique dataset, which can be queried for interactions between 74 small molecules and 3982 proteins using a user-friendly interface available at https://promis.mpimp-golm.mpg.de/yeastpmi/. By interpolating PROMIS with the list of predicted protein–metabolite interactions, we provided experimental validation for 225 binding events. Remarkably, of the 74 small molecules co-eluting with proteins, 36 were proteogenic dipeptides. Targeted analysis of a representative dipeptide, Ser-Leu, revealed numerous protein interactors comprising chaperones, proteasomal subunits, and metabolic enzymes. We could further demonstrate that Ser-Leu binding increases activity of a glycolytic enzyme phosphoglycerate kinase (Pgk1). Consistent with the binding analysis, Ser-Leu supplementation leads to the acute metabolic changes and delays timing of a diauxic shift. Supported by the dipeptide accumulation analysis our work attests to the role of Ser-Leu as a metabolic regulator at the interface of protein degradation and central metabolism.

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“…The similarities and clear differences in dipeptide production in these two coral species suggest that their production may not be explained solely by proteolysis due to metabolic shutdown prior to cell death and that they are bona fide early metabolic signals of bleaching in response to thermal stress. We did not determine which component of the holobiont produced each metabolite, however, an accumulation of proteogenic dipeptides in Arabidopsis thaliana during a time-course stress experiment is linked to autophagy 24 . Dipeptides also serve a diversity of other functions such as small molecule regulators (e.g., H + buffers 25 , antioxidants 26 , and glucose regulators 27 ).…”

Section: Figmentioning

confidence: 99%

Metabolome shift associated with thermal stress in coral holobionts

Williams

Chiles

Conetta

et al. 2020

Preprint

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23Coral reef systems are under global threat due to warming and acidifying oceans 1 . 24Understanding the response of the coral holobiont to environmental change is crucial to aid 25 conservation efforts. The most pressing problem is "coral bleaching", usually precipitated 26 by prolonged thermal stress that disrupts the algal symbiosis sustaining the holobiont 2,3 . We 27 used metabolomics to understand how the coral holobiont metabolome responds to heat 28 stress with the goal of identifying diagnostic markers prior to bleaching onset. We studied 29 the heat tolerant Montipora capitata and heat sensitive Pocillopora acuta coral species from 30 the Hawaiian reef system in Kāne'ohe Bay, O'ahu. Untargeted LC-MS analysis uncovered 31 both known and novel metabolites that accumulate during heat stress. Among those showing 32 the highest differential accumulation were a variety of co-regulated dipeptides present in 33 both species. The structures of four of these compounds were determined (Arginine-34 Glutamine, Lysine-Glutamine, Arginine-Valine, and Arginine-Alanine). These dipeptides 35 also showed differential accumulation in symbiotic and aposymbiotic (alga free) individuals 36 of the sea anemone model Aiptasia 4 , suggesting their animal provenance and algal symbiont 37 related function. Our results identify a suite of metabolites associated with thermal stress 38 that can be used to diagnose coral health in wild samples. 39 40 The exchange of metabolites, either between organism-environment or organism-organism, gave 41 rise not only to early life, but complex life systems on Earth. Examples include bacterial deep vent 42communities 5 , the plant rhizosphere 6 , the human microbiome 7 , and the coral holobiont 8 . Exchange 43 of metabolites between stony corals (Scleractinia), their dinoflagellate algal photosymbionts 44 (Symbiodiniaceae), and associated microbes is the foundation for modern coral reef ecosystems 1,9 45 that cover ca. 255,000 km 2 of the planet surface 10 . Under ambient conditions, the algal cells 46 provide 90-95% of host energy needs in the form of lipids, carbohydrates, amino acids, and O2 11 . 47

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Autophagy is responsible for the accumulation of proteogenic dipeptides in response to heat stress in Arabidopsis thaliana

Cited by 30 publications

References 34 publications

2’,3’-cAMP treatment mimics stress molecular response inArabidopsis thaliana

2’,3’-cAMP treatment mimics stress molecular response inArabidopsis thaliana

Global mapping of protein–metabolite interactions in Saccharomyces cerevisiae reveals that Ser-Leu dipeptide regulates phosphoglycerate kinase activity

Metabolome shift associated with thermal stress in coral holobionts

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