2′,3′-cAMP treatment mimics the stress molecular response in<i>Arabidopsis thaliana</i>

Chodasiewicz, Monika; Kerber, Olga; Górka, Michał; Beltran, Juan Camilo Moreno; Maruri-López, Israel; Minen, Romina Inés; Sampathkumar, Arun; Nelson, Andrew D. L.; Skirycz, Aleksandra

doi:10.1093/plphys/kiac013

Cited by 22 publications

(7 citation statements)

References 56 publications

(92 reference statements)

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“…We speculate that 2′,3′-cAMP and 2′,3′-cGMP may up-regulate the expression of genes required for EDS1 signaling. This model agrees with a recent study showing that 2′,3′-cAMP induces many stress-related Arabidopsis genes ( 41 ).…”

Section: Discussionsupporting

confidence: 93%

TIR-catalyzed ADP-ribosylation reactions produce signaling molecules for plant immunity

Jia

Huang

Song

et al. 2022

Science

120

108

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Plant pathogen-activated immune signaling by nucleotide-binding leucine-rich repeat (NLR) receptors with an N-terminal Toll/Interleukin-1 receptor (TIR) domain converges on Enhanced Disease Susceptibility 1 (EDS1) and its direct partners Phytoalexin Deficient 4 (PAD4) or Senescence-Associated Gene 101 (SAG101). TIR-encoded NADases produce signaling molecules to promote exclusive EDS1-PAD4 and EDS1-SAG101 interactions with helper NLR sub-classes. Here we show that TIR-containing proteins catalyze adenosine diphosphate (ADP)-ribosylation of adenosine triphosphate (ATP) and ADP ribose (ADPR) via ADPR polymerase-like and NADase activity, forming ADP-ribosylated ATP (ADPr-ATP) and ADPr-ADPR (di-ADPR), respectively. Specific binding of ADPr-ATP or di-ADPR allosterically promotes EDS1-SAG101 interaction with helper NLR N requirement gene 1A (NRG1A) in vitro and in planta . Our data reveal an enzymatic activity of TIRs that enables specific activation of the EDS1-SAG101-NRG1 immunity branch.

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Section: Discussionsupporting

confidence: 93%

TIR-catalyzed ADP-ribosylation reactions produce signaling molecules for plant immunity

Jia

Huang

Song

et al. 2022

Science

120

108

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“…Examples of RNP condensates are the evolutionarily conserved processing bodies (PBs), and stress granules (SGs) ( Solis-Miranda et al 2023 ). The numbers and sizes of PBs and SGs depend on conditions; furthermore, the size of SGs depends on small metabolic molecules ( Chodasiewicz et al 2022 ). Under heat stress (HS), PB size can increase ( Gutierrez-Beltran et al 2015 ).…”

Section: Introductionmentioning

confidence: 99%

A proxitome-RNA-capture approach reveals that processing bodies repress coregulated hub genes

Liu,

Mentzelopoulou,

Hatzianestis

et al. 2023

The Plant Cell

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Cellular condensates are usually ribonucleoprotein assemblies with liquid- or solid-like properties. Because these subcellular structures lack a delineating membrane, determining their compositions is difficult. Here we describe a proximity-biotinylation approach for capturing the RNAs of the condensates known as processing bodies (PBs) in Arabidopsis (Arabidopsis thaliana). By combining this approach with RNA detection, in silico, and high-resolution imaging approaches, we studied PBs under normal conditions and heat stress. PBs showed a much more dynamic RNA composition than the total transcriptome. RNAs involved in cell wall development and regeneration, plant hormonal signaling, secondary metabolism/defense, and RNA metabolism were enriched in PBs. RNA-binding proteins and the liquidity of PBs modulated RNA recruitment, while RNAs were frequently recruited together with their encoded proteins. In PBs, RNAs follow distinct fates: in small liquid-like PBs, RNAs get degraded while in more solid-like larger ones, they are stored. PB properties can be regulated by the actin-polymerizing SCAR (suppressor of the cyclic AMP)-WAVE (WASP family verprolin homologous) complex. SCAR/WAVE modulates the shuttling of RNAs between PBs and the translational machinery, thereby adjusting ethylene signaling. In summary, we provide an approach to identify RNAs in condensates that allowed us to reveal a mechanism for regulating RNA fate.

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“…Treatment with 10 μ m Br‐adenosine did not rescue the short‐hypocotyl phenotype of the act2act7 (Figure S3; Table S10), asserting the specificity of the 3′,5′‐cAMP action. No rescue was also measured for the positional isomer of 3′,5′‐cAMP, 2′,3’‐cAMP known as a stress signaling molecule (Chodasiewicz et al., 2022; Kosmacz et al., 2018) (Figure 4a,b). Finally, we showed that Br‐3′,5′‐cAMP concentrations as low as 100 n m , corresponding to the reported 3′,5′‐cAMP concentrations (low to middle range n m ) in plant cells (Moutinho et al., 2001), rescued the short‐hypocotyl phenotype of the act2act7 mutant (Figure 3d; Figure S4, Table S11).…”

Section: Resultsmentioning

confidence: 98%

Protein interactome of 3′,5′‐cAMP reveals its role in regulating the actin cytoskeleton

Figueroa,

Franz,

Luzarowski

et al. 2023

The Plant Journal

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SUMMARYIdentification of protein interactors is ideally suited for the functional characterization of small molecules. 3′,5′‐cAMP is an evolutionary ancient signaling metabolite largely uncharacterized in plants. To tap into the physiological roles of 3′,5′‐cAMP, we used a chemo‐proteomics approach, thermal proteome profiling (TPP), for the unbiased identification of 3′,5′‐cAMP protein targets. TPP measures shifts in the protein thermal stability upon ligand binding. Comprehensive proteomics analysis yielded a list of 51 proteins significantly altered in their thermal stability upon incubation with 3′,5′‐cAMP. The list contained metabolic enzymes, ribosomal subunits, translation initiation factors, and proteins associated with the regulation of plant growth such as CELL DIVISION CYCLE 48. To functionally validate obtained results, we focused on the role of 3′,5′‐cAMP in regulating the actin cytoskeleton suggested by the presence of actin among the 51 identified proteins. 3′,5′‐cAMP supplementation affected actin organization by inducing actin‐bundling. Consistent with these results, the increase in 3′,5′‐cAMP levels, obtained either by feeding or by chemical modulation of 3′,5′‐cAMP metabolism, was sufficient to partially rescue the short hypocotyl phenotype of the actin2 actin7 mutant, severely compromised in actin level. The observed rescue was specific to 3′,5′‐cAMP, as demonstrated using a positional isomer 2′,3′‐cAMP, and true for the nanomolar 3′,5′‐cAMP concentrations reported for plant cells. In vitro characterization of the 3′,5′‐cAMP–actin pairing argues against a direct interaction between actin and 3′,5′‐cAMP. Alternative mechanisms by which 3′,5′‐cAMP would affect actin dynamics, such as by interfering with calcium signaling, are discussed. In summary, our work provides a specific resource, 3′,5′‐cAMP interactome, as well as functional insight into 3′,5′‐cAMP‐mediated regulation in plants.

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

Cited by 22 publications

References 56 publications

TIR-catalyzed ADP-ribosylation reactions produce signaling molecules for plant immunity

TIR-catalyzed ADP-ribosylation reactions produce signaling molecules for plant immunity

A proxitome-RNA-capture approach reveals that processing bodies repress coregulated hub genes

Protein interactome of 3′,5′‐cAMP reveals its role in regulating the actin cytoskeleton

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