Cyclic Nucleotide Monophosphates and Their Cyclases in Plant Signaling

Abstract

The cyclic nucleotide monophosphates (cNMPs), and notably 3′,5′-cyclic guanosine monophosphate (cGMP) and 3′,5′-cyclic adenosine monophosphate (cAMP) are now accepted as key signaling molecules in many processes in plants including growth and differentiation, photosynthesis, and biotic and abiotic defense. At the single molecule level, we are now beginning to understand how cNMPs modify specific target molecules such as cyclic nucleotide-gated channels, while at the systems level, a recent study of the Arabidopsis cNMP interactome has identified novel target molecules with specific cNMP-binding domains. A major advance came with the discovery and characterization of a steadily increasing number of guanylate cyclases (GCs) and adenylate cyclases (ACs). Several of the GCs are receptor kinases and include the brassinosteroid receptor, the phytosulfokine receptor, the Pep receptor, the plant natriuretic peptide receptor as well as a nitric oxide sensor. We foresee that in the near future many more molecular mechanisms and biological roles of GCs and ACs and their catalytic products will be discovered and further establish cNMPs as a key component of plant responses to the environment.

Genetic buffering of cyclic AMP in Arabidopsis thaliana compromises the plant immune response triggered by an avirulent strain of Pseudomonas syringae pv. tomato

“…An increase in intracellular cAMP content has been reported in different plants treated with elicitors of defence responses (Bolwell, ; Kurosaki and Nishi, ; Cooke et al ., ; Zhao et al ., ; Jiang et al ., ; Ma et al ., ; Lu et al ., ). However, as little information is known on enzymes responsible for cAMP synthesis and degradation in plants, the study of cAMP‐mediated signalling pathways in plant defence has always relied on the use of cell‐permeable cAMP analogues and stimulators or inhibitors of mammalian ACs and PDEs (Gehring and Turek, ). In order to study the specific cAMP‐dependent pathways in plant immune response, we used here a genetic approach by overexpressing the cAMP‐sponge, which specifically binds cAMP (Lefkimmiatis et al ., ).…”

“…In higher plants, the presence and the biological role of 3′,5′‐cyclic adenosine monophosphate (cAMP) have been, for a long time, a matter of debate. This situation is firstly due to its low cellular concentration (typically between 40 and 170 pmol g −1 fresh weight (FW)) and secondly to the technical difficulties related to its detection (Gehring, ; Gehring and Turek, ). Moreover, plant adenylyl‐cyclases (AC) and cAMP phosphodiesterases (PDE), responsible for cAMP synthesis and catabolism, respectively, have not been isolated and/or fully characterized, although evidence of their activity has been reported (Gehring and Turek, ; Bianchet et al ., ).…”

PLANT NATRIURETIC PEPTIDE A antagonizes salicylic acid-primed cell death

“…The resulting increased cellular cGMP acts as a second messenger in the intracellular signal transduction mostly by activating kinases, which is implicated in ion channel conductance, glycogenolysis, relaxation of smooth muscle tissues, and inhibition of platelet aggregation 39 . In plants, cGMP is also a crucial signaling molecule involved in stress responses 16,40,41 , ion homeostasis through the regulation of cyclic nucleotide gated channels 42,43 , nitric oxide (NO)-dependent signaling 44,45 , hormonal signaling 46,47 , and phytochrome-dependent transcriptional regulation 48 . Importantly, it was previously reported that PNP-A interacts with a novel leucine-rich repeat (LRR) protein, namely PNP-R1, which is predicted to contain a putative N-terminal SP, a LRR N-terminal (LRRNT) domain, a transmembrane (TM) domain, two LRR domains, and a PK domain followed by a GC catalytic center at the C-terminus 15 .…”

“…Plant natriuretic peptides (PNPs), functional analogs to vertebrate atrial natriuretic peptides (ANPs) 12 , are a novel type of peptide hormones that signal via guanosine 3’,5’-cyclic monophosphate (cGMP) 13–16 . In animals, the synthesis of cGMP from guanosine triphosphate (GTP) is catalyzed by natriuretic peptide receptors (NPRs), which possess protein kinase (PK) and guanylyl cyclase (GC) activities, following perception of ANPs 17 .…”

The Brassica napus Wall-Associated Kinase-Like (WAKL) gene Rlm9 provides race-specific blackleg resistance

“…Rlm9 contains an identical GC motif (SFGVVLAELITGEK) within the PK domain. GCs convert guanosine 5ʹ-triphosphate (GTP) into guanosine 3ʹ,5ʹ-cyclic monophosphate (cGMP), an important signaling molecule during biotic interactions (Durner et al, 1998;Gehring & Turek, 2017). Plant cGMP-binding proteins include several actors in defense response pathways, including hydrogen peroxide production (Donaldson et al, 2016).…”