Cyclic AMP as a Second Messenger in Higher Plants (Status and Future Prospects)

Pollen tube growth and reorientation is a prerequisite for fertilization and seed formation. Here we report imaging of cAMP distribution in living pollen tubes microinjected with the protein kinase A-derived fluorosensor. Growing tubes revealed a uniform distribution of cAMP with a resting concentration of Ϸ100 -150 nM. Modulators of adenylyl cyclase (AC), forskolin, and dideoxyadenosine could alter these values. Transient elevations in the apical region could be correlated with changes in the tube-growth axis, suggesting a role for cAMP in polarized growth. Changes in cAMP arise through the activity of a putative AC identified in pollen. This signaling protein shows homology to functional motifs in fungal AC. Expression of the cDNA in Escherichia coli resulted in cAMP increase and complemented a catabolic defect in the fermentation of carbohydrates caused by the absence of cAMP in a cyaA mutant. Antisense assays performed with oligodeoxynucleotide probes directed against conserved motifs perturbed tip growth, suggesting that modulation of cAMP concentration is vital for tip growth.

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“…2). These values, although regarded as estimates, are similar to measurements performed in animal cells (12).…”

Section: Measurements Of [Camp]i In Pollen Tubessupporting

confidence: 61%

“…Many reports have claimed the identification of cAMPdependent processes in plant cells mainly by biochemical methods (12,13). Nevertheless, the cAMP signaling pathway remains largely unknown because of the lack of evidence for its biological role and identification of a plant AC.…”

mentioning

confidence: 99%

cAMP acts as a second messenger in pollen tube growth and reorientation

Moutinho

Hussey

Trewavas

et al. 2001

Proc. Natl. Acad. Sci. U.S.A.

221

209

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“…Interestingly, cAMP-mediated regulation, well known in fungi and bacteria, still seems to operate in algae and mosses and selected higher plants (see Assmann, 1995;. For instance, 3',5'-cAMP and 3',5'-cGMP are present in the duckweed Lemna paucicostata and have been implicated in the flowering response and circadian rhythmicity (Gangwani et al, 1991, Hasunuma et al, 1988.…”

Section: Stimulation Of Chloronema Differentiation By 3'5'-cyclic Ampmentioning

confidence: 99%

“…3',5'-cGMP is now accepted as an important second messenger in plants and a functional guanylyl cyclase from Arabidopsis has also been characterized (Ludidi and Gehring, 2003). As pointed out by Assmann (1995), future studies on systems such as the growth of incompatible pollen tubes, which is stimulated by exogenous cAMP, or on etiolated grass protoplasts, where the swelling response may be cAMP regulated, will help in unravelling the in vivo role of cAMP in some of the higher plants.…”

Section: Stimulation Of Chloronema Differentiation By 3'5'-cyclic Ampmentioning

confidence: 99%

Hormonal regulation in green plant lineage families

Johri

2008

Physiol Mol Biol Plants

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The patterns of phytohormones distribution, their native function and possible origin of hormonal regulation across the green plant lineages (chlorophytes, charophytes, bryophytes and tracheophytes) are discussed. The five classical phytohormonesauxins, cytokinins, gibberellins (GA), abscisic acid (ABA) and ethylene occur ubiquitously in green plants. They are produced as secondary metabolites by microorganisms. Some of the bacterial species use phytohormones to interact with the plant as a part of their colonization strategy. Phytohormone biosynthetic pathways in plants seem to be of microbial origin and furthermore, the origin of high affinity perception mechanism could have preceded the recruitment of a metabolite as a hormone. The bryophytes represent the earliest land plants which respond to the phytohormones with the exception of gibberellins. The regulation by auxin and ABA may have evolved before the separation of green algal lineage. Auxin enhances rhizoid and caulonemal differentiation while cytokinins enhance shoot bud formation in mosses. Ethylene retards cell division but seems to promote cell elongation. The presence of responses specific to cytokinins and ethylene strongly suggest the origin of their regulation in bryophytes. The hormonal role of GAs could have evolved in some of the ferns where antheridiogens (compounds related to GAs) and GAs themselves regulate the formation of antheridia.During migration of life forms to land, the tolerance to desiccation may have evolved and is now observed in some of the microorganisms, animals and plants. Besides plants, sequences coding for late embryogenesis abundant-like proteins occur in the genomes of other anhydrobiotic species of microorganisms and nematodes. ABA acts as a stress signal and increases rapidly upon desiccation or in response to some of the abiotic stresses in green plants. As the salt stress also increases ABA release in the culture medium of cyanobacterium Trichormus variabilis, the recruitment of ABA in the regulation of stress responses could have been derived from prokaryotes and present at the level of common ancestor of green plants. The overall hormonal action mechanisms in mosses are remarkably similar to that of the higher plants. As plants are thought to be monophyletic in origin, the existence of remarkably similar hormonal mechanisms in the mosses and higher plants, suggests that some of the basic elements of regulation cascade could have also evolved at the level of common ancestor of plants. The networking of various steps in a cascade or the crosstalk between different cascades is variable and reflects the dynamic interaction between a species and its specific environment.

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“…As a consequence, although there were a few reports after the production of MS evidence of the identity of cAMP in plant extracts that claimed the absence of cAMP from plant cells (Spiteri et al, 1989), several reviews have appeared that show a shift in the balance of opinion. Although most reviews in the initial phase expressed the opinion that cAMP did not, or was unlikely to, function in higher plants (Keates, 1973 ;Lin, 1974 ;Amrhein, 1974aAmrhein, , 1977, these have been superseded by commentaries suggesting potential functions (Brown & Newton, 1981 ;Francko, 1983 ;Newton & Brown, 1986 ;Assmann, 1995 ;Bolwell, 1995 ;Trewavas, 1997). As will be detailed in the sections below, conclusive evidence of the existence of cAMP, adenylyl cyclase, phosphodiesterase and cAMP-binding proteins is now available and systematic studies of the function of the cyclic nucleotide are appearing, for example in studies of its role in the cell cycle, in stress response systems and in the regulation of ion channels.…”

Section:       C   mentioning

confidence: 99%

Tansley Review No. 106

et al. 1999

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 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.

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Cyclic AMP as a Second Messenger in Higher Plants (Status and Future Prospects)

Cited by 103 publications

References 32 publications

cAMP acts as a second messenger in pollen tube growth and reorientation

cAMP acts as a second messenger in pollen tube growth and reorientation

Hormonal regulation in green plant lineage families

Tansley Review No. 106

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