Tansley Review No. 106

Abstract

 For three decades, hypotheses relating to the occurrence and function of cyclic nucleotides in higher plants have been highly controversial. Although cyclic nucleotides had been shown to have key regulatory roles in animals and bacteria, investigations with higher plants in the 1970s and early 1980s were criticized on the basis of (i) a lack of specificity of effects apparently elicited by cyclic nucleotides, (ii) the equivocal identification of putative endogenous cyclic nucleotides and (iii) ambiguity in the identification of enzymes connected with cyclic nucleotide. More recent evidence based on more rigorous identification procedures has demonstrated conclusively the presence of cyclic nucleotides, nucleotidyl cyclases and cyclic nucleotide phosphodiesterases in higher plants, and has identified plant processes subject to regulation by cyclic nucleotides. Here we review the history of the debate, the recent evidence establishing the presence of these compounds and their role ; future research objectives are discussed.

The Phytosulfokine (PSK) Receptor Is Capable of Guanylate Cyclase Activity and Enabling Cyclic GMP-dependent Signaling in Plants

“…In higher plants, cGMP has been identified as an important molecule involved in regulating a wide variety of physiological effects ranging from chloroplast development and plant hormone-dependent responses to the induction of plant defense responses (for reviews, see Refs. [1][2][3]. Nitric oxide signaling is thought to stimulate cGMP production in defense and stress responses, but how it generates cGMP is still uncertain (4,5).…”

Product identification and kinetic studies of nucleotidyl cyclase activity in isolated chloroplasts by quantitative fast-atom bombardment mass spectrometry

“…While cyclic AMP and cyclic GMP have both previously been shown to be present in chloroplasts, 14,15 and mass spectrometric analysis has been the basis of several recent identifications and estimations of cyclic nucleotides in plant extracts, [35][36][37] the data here provides unequivocally a first demonstration of the existence of both guanylyl and adenylyl cyclase in spinach chloroplasts; as such it demonstrates the ability of a tandem MS technique to provide an unambiguous identification, while analogous attempts by molecular biological techniques have thus far ended in controversy. The association of guanylyl cyclase together with adenylyl cyclase is of immense significance given the recent indication of cyclic GMP function in plant defence and signal transduction mechanisms; [39][40][41] the ability of quantitative mass spectrometry to assay simultaneously both cyclic AMP and cyclic GMP synthesis, together with the turnover of any enzyme effectors, will prove invaluable in the elucidation of the regulatory mechanisms controlling these enzymes.…”

“…[12][13][14] In the absence of a mammalian-like hormone/neurotransmitter system it was argued that plants have no need of a second messenger-type system. Early reports of cyclic nucleotides in higher plant tissues were criticized on the basis of ambiguous identification protocols (see reviews 14,15 ), and the natural occurrence of cyclic AMP, [16][17][18] cyclic GMP, 19,20 and cyclic CMP, UMP, IMP and dTMP 21 was only unequivocally demonstrated and thence generally accepted after identification of the cyclic nucleotides in plant extracts by mass spectrometric analysis.…”

“…[12][13][14] In the absence of a mammalian-like hormone/neurotransmitter system it was argued that plants have no need of a second messenger-type system. Early reports of cyclic nucleotides in higher plant tissues were criticized on the basis of ambiguous identification protocols (see reviews 14,15 ), and the natural occurrence of cyclic AMP, [16][17][18] cyclic GMP, 19,20 and cyclic CMP, UMP, IMP and dTMP 21 was only unequivocally demonstrated and thence generally accepted after identification of the cyclic nucleotides in plant extracts by mass spectrometric analysis. 22 Unambiguous identification of endogenous cyclic nucleotides is made by virtue of the characteristic fragmentations 23,24 observed in the mass-analyzed ion kinetic energy (MIKE) spectra obtained after collisionallyinduced dissociation (CID) of the protonated molecule in the fast-atom bombardment (FAB) mass spectrum, enabling the differentiation of the 3',5'-cyclic nucleotides, 23,24 which are the biochemical second messengers, from the 2',3'-cyclic nucleotide isomers, which are merely intermediates of nucleic acid catabolism.…”

“…The presence of the enzyme adenylyl cyclase has similarly been a controversial topic and conventional histochemical and biochemical assays were similarly criticized on the basis of ambiguous identification of the putative cyclic nucleotide product (see review 14 ). Again mass spectrometric identification provided the conclusive evidence that protein preparations synthesize cyclic AMP.…”