Cyclic AMP mediates heat stress response by the control of redox homeostasis and ubiquitin‐proteasome system

Abstract

Heat stress (HS), causing impairment in several physiological processes, is one of the most damaging environmental cues for plants. To counteract the harmful effects of high temperatures, plants activate complex signalling networks, indicated as HS response (HSR). Expression of heat shock proteins (HSPs) and adjustment of redox homeostasis are crucial events of HSR, required for thermotolerance. By pharmacological approaches, the involvement of cAMP in triggering plant HSR has been recently proposed. In this study, to investigate the role of cAMP in HSR signalling, tobacco BY-2 cells overexpressing the 'cAMP-sponge', a genetic tool that reduces intracellular cAMP levels, have been used. in vivo cAMP dampening increased HS susceptibility in a HSPs-independent way. The failure in cAMP elevation during HS caused a high accumulation of reactive oxygen species, due to increased levels of respiratory burst oxidase homolog D, decreased activities of catalase and ascorbate peroxidase, as well as down-accumulation of proteins involved in the control of redox homeostasis. In addition, cAMP deficiency impaired proteasome activity and prevented the accumulation of many proteins of ubiquitin-proteasome system (UPS). By a large-scale proteomic approach together with in silico analyses, these UPS proteins were identified in a specific cAMP-dependent network of HSR.

A metabolomics insight into the Cyclic Nucleotide Monophosphate signaling cascade in tomato under non-stress and salinity conditions

“…Similarly, 8-oxo-GMP (a marker of oxidative imbalance) and glutathione conjugates were impaired by SC, strengthening the involvement of cNMP in the NO and ROS crosstalk. Consistently, Paradiso et al ., (2020) recently determined that the minimization of intracellular cAMP by means of a cAMP-sponge caused the accumulation of reactive oxygen species and impaired ROS-related enzymes such as ascorbate peroxidase. On the other hand, Nitric Oxide Synthase□3 is post-translationally regulated by a cGMP dependent protein kinase in endothelial cells of animals (John et al ., 2006).…”

cAMP Is a Promising Regulatory Molecule for Plant Adaptation to Heat Stress

“…Plants promote resilience by altering their cellular homeostasis and morphology under heat stress. Molecular processes underlying these responses have been intensively studied and found to encompass diverse mechanisms operating across a broad range of cellular components [ 7 , 9 , 23 , 24 ]. The accumulating experimental evidence suggests that cAMP regulates thermotolerance in plants, despite the fact that the identification of cAMP target proteins remains far behind that in animals [ 3 , 6 ].…”

“…When maize was exposed to heat stress, exogenous cAMP application obviously increased the expression of CSC1-like protein (Ca 2+ transporter) and the uptake of Ca 2+ in roots [ 24 ], as well as the expression of calmodulin protein 2 in leaves [ 9 ]; In tobacco BY-2 cells overexpressing the ‘cAMP-sponge’ as a genetic tool reducing intracellular cAMP levels (named as cAS cell), and cAMP deficiency significantly changed the expression of calcium-dependent lipid-binding (CaLB domain) family protein, annexin 2, calreticulin 3, calcineurin B-like 3, calcium-dependent phosphotriesterase superfamily protein, and calcium-binding EF-hand family protein under heat stress [ 7 ]. Interestingly, when Arabidopsis was subjected to heat stress, heat-increased AMP activated cyclic nucleotide-gated channel 6 (AtCNGC6) activity and thus resulted in an influx of Ca 2+ into the cell via AtCNGC6, facilitating the expression of HSP genes and the acquisition of thermotolerance [ 25 ]; under the elevated cytosolic Ca 2+ concentration, CaM2, CaM3, CaM5, and CaM7 negatively regulated Ca 2+ conductivity of CNGC6 by binding its atypical isoleucine-glutamine motif, and thus led to a marked decrease in plasma membrane inward Ca 2+ current, suggesting that the atypical isoleucine-glutamine motif plays an important role in CaM binding and the feedback regulation of the CNGC6 channel [ 29 ].…”

“…Over the last twenty years, several studies about the biological functions of ACs and their catalytic product cAMP have been reported in plants. Particularly in plant biology research, recent advances supported by biochemical, genetic and omics studies have proven that cAMP, as a polyhedral molecule, is critically involved in the signaling pathways of both plant development and response to environmental stress [ 6 , 7 , 8 , 9 , 10 ].…”

Mass Cytometry Exploration of Immunomodulatory Responses of Human Immune Cells Exposed to Silver Nanoparticles

“…Understanding the immune responses to metallic nanoparticle exposure is essential for understanding NP cytotoxicity and cell–NP interaction, and will help in the development of nanomaterials engineered for various biomedical purposes. Innate immunity is a primary concern due to its crucial role in upholding tissue and cellular homeostasis [ 16 ]. However, the interaction of NP with cells might alter or affect homeostasis of the immune system through recognition of foreign particles entering the body and stimulating immunological responses [ 17 , 18 ].…”