Cyclic AMP: A Polyhedral Signalling Molecule in Plants

Abstract

The cyclic nucleotide cAMP (3',5'-cyclic adenosine monophosphate) is nowadays recognised as an important signalling molecule in plants, involved in many molecular processes, including sensing and response to biotic and abiotic environmental stresses. The validation of a functional cAMP-dependent signalling system in higher plants has spurred a great scientific interest on the polyhedral role of cAMP, as it actively participates in plant adaptation to external stimuli, in addition to the regulation of physiological processes. The complex architecture of cAMP-dependent pathways is far from being fully understood, because the actors of these pathways and their downstream target proteins remain largely unidentified. Recently, a genetic strategy was effectively used to lower cAMP cytosolic levels and hence shed light on the consequences of cAMP deficiency in plant cells. This review aims to provide an integrated overview of the current state of knowledge on cAMP's role in plant growth and response to environmental stress. Current knowledge of the molecular components and the mechanisms of cAMP signalling events is summarised.

Keywords: abiotic stress; cAMP; cyclic nucleotides-gated channels; plant innate immunity.

Figure 1

Schematic representation of the “cAMP sponge” overexpression in Nicotiana tabacum Bright yellow-2 (BY-2) cells and Arabidopsis thaliana plants. The cAMP-sponge construct used for tobacco BY-2 and Arabidopsis genetic transformations is reported on the top of the figure. The two following panels illustrate the characterisation of different transgenic lines (cAS lines) overexpressing the cAMP sponge in tobacco BY-2 cells (left) and in Arabidopsis plants (right). RT-PCR products show the integration of the transgene in the transformed cAS lines. Total and free cAMP content in wild type (WT) and cAS lines are reported in the histogram graphs. The presence of cAMP sponge protein is visualised by mCherry fluorescence. (Adapted from Sabetta et al. (2016) and Sabetta et al. (2019) [32,33]).

Figure 2

cAMP involvement in plant physiological processes. Literature data indicate a role for cAMP in ion homeostasis, mainly through the regulation of membrane-localised ion channels [29,34,35,36,40,48,49,50,51,52,53,54] and in stomatal opening, through Ca²⁺ and K⁺ flux regulation [39,40,52,53], cAMP was also shown to influence pollen tube orientation and growth, by the regulation of Ca²⁺ channels and choline acetyltransferase activity [14,54,55,56,57,58]. Seed germination [59,60,61,62,63] and cell cycle progression [32,33,37,38,64] are also regulated by cAMP. More details are provided in the text.

Figure 3

Molecular mechanisms of cAMP involvement in plant innate immunity. Elicitor recognition elevates cytosolic cAMP, which can activate CNGCs or PLC2, inducing Ca²⁺ accumulation and oxidative burst, through the activation of NADPH oxidase. cAMP-dependent oxidative burst can also be due to apoplastic peroxidases. Ca²⁺ stimulates NO production, which, together with ROS, induces defence response and HR. cAMP accumulation also activates PAL expression and production of SA and phytoalexins. More details are provided in the text. Question marks indicate pathways not completely characterised. Abbreviations: AC, adenylate cyclase; cAMP, 3′,5′-cyclic adenosine monophosphate; CNGCs, cyclic nucleotides-gated channels; DAG, diacylglycerol; HR, hypersensitive response; IP₃, inositol triphosphate; NO, nitric oxide; PA, phosphatidic acid; PAL, phenylalanine ammonia lyase; PIP, monophosphatidylinosotol; PKA, protein kinase A, PLC₂, phospholipase C₂; PR-1, pathogenesis-related genes; PRRs, pattern recognition receptors; SA, salicylic acid; SOD, superoxide dismutase.