Dual Regulation of a Chimeric Plant Serine/Threonine Kinase by Calcium and Calcium/Calmodulin

Takezawa, Daisuke; Ramachandiran, Sampath; Paranjape, Vijay; Poovaiah, B. W.

doi:10.1074/jbc.271.14.8126

Cited by 115 publications

(133 citation statements)

References 46 publications

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“…Moreover, it can be argued that the proximal Ca 2ϩ -dependent effector in the signaling pathway may be similarly transiently activated, returning to its resting state when the activating Ca 2ϩ is removed. Signaling components such as the Ca 2ϩ -dependent protein kinases (55,56), calmodulin (57) and its responsive kinases (58,59), Ca 2ϩ -dependent phosphatases (60), Ca 2ϩ -gated channels (61), and Ca 2ϩ -activated phospholipases (62) are obvious candidates for this downstream effector.…”

Section: Fig 2 Effect Of Plant Defense Elicitors On Intracellular Cmentioning

confidence: 99%

Measurement of Ca2+ Fluxes during Elicitation of the Oxidative Burst in Aequorin-transformed Tobacco Cells

Chandra

Low

1997

Journal of Biological Chemistry

148

117

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We have employed suspension cultured aequorintransformed tobacco cells to examine the involvement of Ca 2؉ in signal transduction of the oxidative burst. Use of cultured cells for this purpose was validated by demonstrating that the cells responded to cold shock quantitatively and qualitatively similarly to the intact transgenic plants from which they were derived. Stimulation of the oxidative burst in the cell suspension was achieved by administration of oligogalacturonic acid, Mas-7 (a peptide known to activate G proteins and Ca 2؉ fluxes), hypo-osmotic stress, or harpin (a protein from the pathogenic bacterium Erwinia amylovora). The latter failed to promote any detectable increase in cytoplasmic Ca 2؉ concentration, whereas each of the former three triggered a rapid rise in cytosolic Ca 2؉ followed by a return within seconds to basal Ca 2؉ levels. Peak Ca 2؉ concentrations induced by the former three elicitors were ϳ0.7, 1.4, and 1.3 M, respectively. Three lines of evidence suggest that the observed Ca 2؉ pulses are essential to transduction of the oxidative burst signals by their respective elicitors: (i) inhibition of the Ca 2؉ transients with Ca 2؉ chelators or Ca 2؉ channel blockers prevented expression of the oxidative burst, (ii) introduction of exogenous Ca 2؉ into the same cells initiated the burst even in the absence of other inducers of the response, and (iii) the observed Ca 2؉ transients often returned to near basal levels well before any H 2 O 2 synthesis could be detected, suggesting that the Ca 2؉ influx is required to communicate the burst signal but not maintain the defense response. These data suggest that Ca 2؉ pulses serve frequently, but not invariably, to transduce an oxidative burst signal.The oxidative burst constitutes one of the more rapid responses of a plant cell to pathogen attack (1). Within minutes of pathogen recognition, reactive oxygen species are generated that may promote cross-linking and lignification of the cell wall (2, 3), transcription of defense-related genes (4, 5), secondary metabolite biosynthesis (6), the hypersensitive response (4,7,8), and direct pathogen cytotoxicity (9, 10), depending on the plant species examined. In cultured cell systems, the oxidative burst can be promoted by isolated elicitors including harpin (11, 12), oligouronides (13), elicitins (14), purified fungal peptides (15), and other molecules from the extracts of pathogens (7,16). Abiotic stimuli such as mechanical stress (17), the pesticide fenthion (18), cold shock (19), phosphatase inhibitors (4, 20), and hypo-osmotic stress (17) can also induce biosynthesis of reactive oxygen species in plant cells.Because of its rapid expression, ease of assay, and similarity to the analogous defense response in human neutrophils (21), the oxidative burst has recently served as a model for exploring signal transduction pathways in plants. As the numbers of elicitors examined have risen, it has become increasingly clear that different elicitors may inaugurate independent signal transduction pathways that...

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Section: Fig 2 Effect Of Plant Defense Elicitors On Intracellular Cmentioning

confidence: 99%

Measurement of Ca2+ Fluxes during Elicitation of the Oxidative Burst in Aequorin-transformed Tobacco Cells

Chandra

Low

1997

Journal of Biological Chemistry

148

117

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“…Although the presence of CCaMK has been indicated from different plants [31Ϫ33], most of the kinases characterised biochemically belong to the Ca 2ϩ -dependent family [11]. Cloning of cDNA sequences with similarity to various CaM kinases has been reported from various plants [35Ϫ40], and the encoded proteins are possibly involved in various regulatory processes [39,40]. The only CCaMK that has been characterised biochemically is an protein overexpressed in E. coli from a cDNA from lily anthers [39].…”

Section: Discussionmentioning

confidence: 99%

“…Cloning of cDNA sequences with similarity to various CaM kinases has been reported from various plants [35Ϫ40], and the encoded proteins are possibly involved in various regulatory processes [39,40]. The only CCaMK that has been characterised biochemically is an protein overexpressed in E. coli from a cDNA from lily anthers [39]. The CCaMK showed dual regulation of kinase activity by Ca 2ϩ and CaM [39], and its expression was restricted to anthers.…”

Section: Discussionmentioning

confidence: 99%

“…apple [35Ϫ37], lily [38,39], and maize [40]. All these homologues show considerable similarity with their animal counterparts at cDNA level.…”

mentioning

confidence: 99%

“…The Nterminal region of the encoded protein contains all eleven conserved subdomains characteristic of serine/threonine protein kinases, and the CaM-binding region has high similarity (79 %) to a subunit of mammalian CCaMK [38]. The cDNA clone from lily anthers has been over expressed in Escherichia coli, and its biochemical properties indicate it to be a CCaMK regulated by Ca 2ϩ and Ca 2ϩ /CaM [39]. CCaMK from maize roots [40] contains all eleven subdomains characteristic of protein-kinase catalytic domains with all the conserved amino acid residues, and shares sequence identity in this region with yeast CMK 1 (42 %), with a rat CaMK II subunit (37%) and apple CB 1 (34%).…”

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Biochemical evidence for a calmodulin‐stimulated calcium‐dependent protein kinase in maize

Pandey

Sopory

1998

European Journal of Biochemistry

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We provide biochemical evidence for the presence of a Ca 2ϩ -dependent calmodulin (CaM)-stimulated protein kinase (CCaMK) from etiolated maize coleoptiles. The kinase, with a molecular mass of 72.3 kDa, was purified to homogeneity by means of ammonium sulphate precipitation, DEAE-Sephacel chromatography, CaM-Sepharose chromatography and gel purification. The purified kinase required 5 mM Mg 2ϩ for activity and had an optimum pH of 7.5. The kinase is a Ca 2ϩ -binding protein, as was evident by 45 Ca 2ϩ -binding and Ca 2ϩ mobility-gel-shift assays. 1 µM Ca 2ϩ stimulated the kinase activity about 12-fold and was further stimulated by the addition of exogenous CaM (Ϸ100 nM). Addition of Ca 2ϩ and CaM antagonists decreased the kinase activity. Under in vitro assay conditions the kinase phosphorylated preferentially syntide-2, histone IIIS and casein. Syntide-2 and histone IIIS were phosphorylated at serine residues, showing that the kinase belongs to the serine/threonine family of protein kinases. Autophosphorylation of CCaMK occurred on threonine residue(s) and was Ca 2ϩ dependent. Addition of exogenous CaM had no effect on autophosphorylation. The properties of the maize kinase suggests that it is a CCaMK that shows dual stimulation with Ca 2ϩ and CaM for substrate phosphorylation and only Ca 2ϩ requirement for autophosphorylation. Antibodies raised against the kinase cross-reacted with maize total proteins to give a single band of 72 kDa and precipitated substrate (syntide-2 and histone IIIS)-phosphorylation and autophosphorylation activities in a specific manner. Localisation studies with antibodies showed that the kinase is ubiquitous.Keywords : calmodulin; Ca 2ϩ /calmodulin-dependent kinase ; Zea mays; protein kinase. Ca 2ϩ are one of the most common second messengers, and couple a large number of diverse stimuli to their characteristic responses in a very specific and precise manner in plant and animal systems [1Ϫ3]. In animal systems, the role of Ca 2ϩ as a second messenger has been very well established. Changes in intracellular Ca 2ϩ levels are perceived by various Ca 2ϩ -binding proteins, e.g. calmodulin (CaM) and CaM-like proteins, which either by themselves or by modifying other proteins and/or factors transduce the signal downstream to elicit the final response. Protein kinases are one of the main targets of these proteins, which by their reversible phosphorylation/dephosphorylation activate other constituents of signal-transduction pathways [1, 4Ϫ5].Ca 2ϩ is known to regulate two families of protein kinases, i.e. Ca 2ϩ /phospholipid-dependent protein kinases [6] and Ca 2ϩ / CaM-dependent protein kinases (CCaMK) [7Ϫ9]. In animal systems, various members of these families have been purified, and characterised, and their regulation has been understood [10]. In plants a third, biochemically distinct family of protein kinases, Ca 2ϩ -dependent protein kinases, is more common [11]. These kinases do not require lipid or CaM for their activation. These kinases are single polypeptides, containing conserved cata...

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Calcium signaling and transcriptional regulation in arbuscular mycorrhizal symbiosis

Luginbuehl

Oldroyd

2016

Molecular Mycorrhizal Symbiosis

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Dual Regulation of a Chimeric Plant Serine/Threonine Kinase by Calcium and Calcium/Calmodulin

Cited by 115 publications

References 46 publications

Measurement of Ca2+ Fluxes during Elicitation of the Oxidative Burst in Aequorin-transformed Tobacco Cells

Measurement of Ca2+ Fluxes during Elicitation of the Oxidative Burst in Aequorin-transformed Tobacco Cells

Biochemical evidence for a calmodulin‐stimulated calcium‐dependent protein kinase in maize

Calcium signaling and transcriptional regulation in arbuscular mycorrhizal symbiosis

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