← Back to Search
Factors Involved In The Rise Of Phosphoenolpyruvate Carboxylase-kinase Activity Caused By Salinity In Sorghum Leaves
J. Monreal, Cirenia Arias-Baldrich, F. Pérez-Montaño, J. Gandullo, C. Echevarria, S. García-Mauriño
Published 2013 · Biology, Medicine
Download PDFAnalyze on Scholarcy
Salinity increases phosphoenolpyruvate carboxylase kinase (PEPCase-k) activity in sorghum leaves. This work has been focused on the mechanisms responsible for this phenomenon. The light-triggered expression of SbPPCK1 gene, accountable for the photosynthetic C4-PEPCase-k, is controlled by a complex signal transduction chain involving phospholipases C and D (PLC and PLD). These two phospholipase-derived signalling pathways were functional in salinized plants. Pharmacological agents that act on PLC (U-73122, neomycin) or PLD (n-butanol) derived signals, blocked the expression of SbPPCK1, but had little effect on PEPCase-k activity. This discrepancy was further noticed when SbPPCK1-3 gene expression and PEPCase-k activity were studied in parallel. At 172 mM, the main effect of NaCl was to decrease the rate of PEPCase-k protein turnover. Meanwhile, 258 mM NaCl significantly increased both SbPPCK1 and SbPPCK2 gene expression and/or mRNA stability. The combination of these factors contributed to maintain a high PEPCase-k activity in salinity. LiCl increased calcium-dependent protein kinase (CDPK) activity in illuminated sorghum leaves while it decreased the rate of PEPCase-k degradation. The latter effect was restrained by W7, an inhibitor of CDPK activity. Recombinant PEPCase-k protein was phosphorylated in vitro by PKA. A conserved phosphorylation motif, which can be recognized by PKA and by plant CDPKs, is present in the three PEPCase-ks proteins. Thus, it is possible that a phosphorylation event could be controlling (increasing) the stability of PEPCase-k in salinity. These results propose a new mechanism of regulation of PEPCase-k levels, and highlight the relevance of the preservation of key metabolic elements during the bulk degradation of proteins, which is commonly associated to stress.
This paper references
The Ca2+-dependent protein kinase CPK3 is required for MAPK-independent salt-stress acclimation in Arabidopsis
Norbert Mehlmer (2010)
An increase in phosphoinositide-specific phospholipase C activity precedes induction of C4 phosphoenolpyruvate carboxylase phosphorylation in illuminated and NH4Cl-treated protoplasts from Digitaria sanguinalis.
S. Coursol (2000)
Phosphatidic acid: an emerging plant lipid second messenger.
T. Munnik (2001)
Eto Brute? Role of ACS turnover in regulating ethylene biosynthesis.
H. S. Chae (2005)
Regulatory Phosphorylation of C4 Phosphoenolpyruvate Carboxylase (A Cardinal Event Influencing the Photosynthesis Rate in Sorghum and Maize)
N. Bakrim (1993)
Thioredoxinmediated reductive activation of a protein kinase for the regulatory phosphorylation
H Saze (2001)
Phosphoenolpyruvate carboxylase: a new era of structural biology.
K. Izui (2004)
Abiotic stresses affecting water balance induce phosphoenolpyruvate carboxylase expression in roots of wheat seedlings
M. González (2003)
Phosphorylation of Phosphoenolpyruvate Carboxylase Is Not Essential for High Photosynthetic Rates in the C4 Species Flaveria bidentis1[OA]
Tsuyoshi Furumoto (2007)
Reversible light activation of the phosphoenolpyruvate carboxylase protein‐serine kinase in maize leaves
C. Echevarrı́a (1990)
Regulation of Phosphoenolpyruvate Carboxylase Phosphorylation by Metabolites and Abscisic Acid during the Development and Germination of Barley Seeds1[C][W]
A. Feria (2008)
Arabidopsis thaliana contains two phosphoenolpyruvate carboxylase kinase genes with different expression patterns
V. Fontaine (2002)
Phospho enolpyruvate carboxylase kinase involved in C 4 photosynthesis in Flaveria trinervia: cDNA cloning and characterization 1 1 The nucleotide sequence data reported in this paper have been submitted to the DDBJ/EMBL/GenBank databases under the accession number AB065100.
Y. Tsuchida (2001)
Maize Phosphoenolpyruvate Carboxylase
Akiko Takahashi-Terada (2005)
Distinct patterns of control and expression amongst members of the PEP carboxylase kinase gene family in C4 plants.
M. Shenton (2006)
Reversible light activation of phosphoenolpyruvate carboxylase protein-serine kinase in maize
C Echevarrı́a (1990)
Turnover of LeACS2, a wound-inducible 1-aminocyclopropane-1-carboxylic acid synthase in tomato, is regulated by phosphorylation/dephosphorylation.
Y. Kamiyoshihara (2010)
A novel C-terminal proteolytic processing of cytosolic pyruvate kinase, its phosphorylation and degradation by the proteasome in developing soybean seeds.
Guo-Qing Tang (2003)
The neighbor-joining method
N. Saitou (1987)
A protease activity copurified with the C 4 PEPC from sorghum leaves is specifically activated by a synthetic peptide from its C-terminal
J Gandullo (2008)
Biotic and abiotic stress responses through calcium-dependent protein kinase (CDPK) signaling in wheat (Triticum aestivum L.)
Aili Li (2008)
A Ca(2+)-dependent protein kinase with characteristics of protein kinase C in leaves and mesophyll cell protoplasts from Digitaria sanguinalis: possible involvement in the C(4)-phosphoenolpyruvate carboxylase phosphorylation cascade.
Lidia Osuna (2004)
Maize phosphoenolpyruvate carboxylase. Cloning and characterization of mRNAs encoding isozymic forms.
M. Harpster (1986)
Generation and maintenance
M Stitt (1985)
A Ca protein kinase with characteristics of protein kinase C in leaves and mesophyll cell protoplasts from Digitaria sanguinalis: possible involvement
L Osuna (2004)
In vivo regulatory phosphorylation of the phosphoenolpyruvate carboxylase AtPPC1 in phosphate-starved Arabidopsis thaliana
A. L. Gregory (2009)
PLANT CELLULAR AND MOLECULAR RESPONSES TO HIGH SALINITY.
P. Hasegawa (2000)
Partial purification and characterization of a protein inhibitor of phosphoenolpyruvate carboxylase kinase
G. A. Nimmo (2001)
Echevarrı́a C, Garcı́aMauriño S (2007a) ABA modulates the degradation of phosphoenolpyruvate carboxylase kinase in sorghum
JA Monreal (2007)
Exogenous ABA as a Modulator of the Response of Sorghum to High Salinity
G. N. Amzallag (1990)
The effect of pH on the covalent and metabolic control of C4 phosphoenolpyruvate carboxylase from Sorghum leaf.
C. Echevarria (1994)
The unique phosphoenolpyruvate carboxylase kinase
C. Echevarria (2003)
Sand and Water Culture Methods Used in the Study of Plant Nutrition
J. Doe (1952)
G Protein Activation Stimulates Phospholipase D Signaling in Plants.
T. Munnik (1995)
Enzymes of ethylene biosynthesis.
H. Kende (1989)
Kinetic and calcium-binding properties of three calcium-dependent protein kinase isoenzymes from soybean.
J. Lee (1998)
The Ubiquitin – Proteasome Pathway is Involved in Rapid Degradation of Phosphoenolpyruvate Carboxylase Kinase for C 4 Photosynthesis
Masakazu Agetsuma (2005)
Arabidopsis phosphoenolpyruvate carboxylase genes encode immunologically unrelated polypeptides and are differentially expressed in response to drought and salt stress
R. Sánchez (2005)
Immunological analysis of the phosphorylation state of maize C4-form phosphoenolpyruvate carboxylase with specific antibodies raised against a synthetic phosphorylated peptide.
Y. Ueno (2000)
Genome-wide identification of the rice calcium-dependent protein kinase and its closely related kinase gene families: comprehensive analysis of the CDPKs gene family in rice.
T. Asano (2005)
Arabidopsis phosphoenolpyruvate carboxylase genes encode immunologically unrelated 1412
R Sanchez (2006)
Water for Agriculture: Maintaining Food Security Under Growing Scarcity
M. Rosegrant (2009)
The ubiquitin-proteasome pathway is involved in rapid degradation of phosphoenolpyruvate carboxylase kinase for C4 photosynthesis.
Masakazu Agetsuma (2005)
The PROSITE database, its status in 2002
L. Falquet (2002)
Calcium Signaling through Protein Kinases. The Arabidopsis Calcium-Dependent Protein Kinase Gene Family1
Shu-Hua Cheng (2002)
polypeptides and are differentially expressed in response to drought and salt stress
An increase in phosphoinositide-specific phospholipase C activity precedes induction of C 4 phosphoenolpyruvate carboxylase in illuminated and NH 4 Cl-treated protoplasts from Digitaria sanguinalis
S Coursol (2000)
Protein kinase recognition sequence motifs.
B. Kemp (1990)
Characterization of StABF1, a stress-responsive bZIP transcription factor from Solanum tuberosum L. that is phosphorylated by StCDPK2 in vitro
María Noelia Muñiz García (2011)
Structure and Expression of Phosphoenolpyruvate Carboxylase Kinase Genes in Solanaceae. A Novel Gene Exhibits Alternative Splicing1
J. Marsh (2003)
Characterization and functional analysis of phosphoenolpyruvate carboxylase kinase genes in rice.
H. Fukayama (2006)
Phosphoenolpyruvate Carboxylase Kinase in Tobacco Leaves Is Activated by Light in a Similar but Not Identical Way as in Maize
B. Li (1996)
Characterization of salt stress-enhanced phosphoenolpyruvate carboxylase kinase activity in leaves of Sorghumvulgare: independence from osmotic stress, involvement of ion toxicity and significance of dark phosphorylation
S. García-Mauriño (2002)
A protease activity copurified with the C4 PEPC from sorghum leaves is specifically activated by a synthetic peptide from its C-terminal
J Gandullo (2008)
Sand and Water Culture Methods Used in the Study of Plant Nutrition
E. J. Hewitt (1966)
The Sorghum bicolor genome and the diversification of grasses
A. Paterson (2009)
Thioredoxin-mediated reductive activation of a protein kinase for the regulatory phosphorylation of C4-form phosphoenolpyruvate carboxylase from maize.
H. Saze (2001)
MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.
K. Tamura (2011)
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.
M. M. Bradford (1976)
Regulation of balance between C3 and C4 pathway: Role of abscisic acid
N. Sankhla (1975)
Salt stress increases the Ca2+-independent phosphoenolpyruvate carboxylase kinase activity in Sorghum leaves
C. Echevarria (2001)
Plant salt tolerance.
J. K. Zhu (2001)
Involvement of abscisic acid in photosynthetic process in Hordeum vulgare L. during salinity stress
L. Popova (2004)
A Conserved 19-Amino Acid Synthetic Peptide from the Carboxy Terminus of Phosphoenolpyruvate Carboxylase Inhibits the in Vitro Phosphorylation of the Enzyme by the Calcium-Independent Phosphoenolpyruvate Carboxylase Kinase1
R. Álvarez (2003)
N-(6-aminohexyl)-5-chloro-1-naphthalenesulfonamide, a calmodulin antagonist, inhibits cell proliferation.
H. Hidaka (1981)
Effect of LiCl on phosphoenolpyruvate carboxylase kinase and the phosphorylation of phosphoenolpyruvate carboxylase in leaf disks and leaves of Sorghum vulgare
J. Monreal (2006)
Changes in the kinetic properties and phosphorylation state of phosphoenolpyruvate carboxylase in Zea mays leaves in reponse to light and dark
G. A. Nimmo (1987)
Roots, Cycles and Leaves. Expression of the Phosphoenolpyruvate Carboxylase Kinase Gene Family in Soybean1
S. Sullivan (2004)
A rice calcium-dependent protein kinase OsCPK12 oppositely modulates salt-stress tolerance and blast disease resistance.
T. Asano (2012)
The Arabidopsis CDPK-SnRK Superfamily of Protein Kinases
E. M. Hrabak (2003)
Roots, cycles and leaves
S Sullivan (2004)
Biotic and abiotic stress responses through calcium-dependent protein kinase (CDPK) signaling in wheat
A Li (2008)
Involvement of phospholipase D and phosphatidic acid in the light-dependent up-regulation of sorghum leaf phosphoenolpyruvate carboxylase-kinase
J. Monreal (2010)
PHOSPHOENOLPYRUVATE CARBOXYLASE: A Ubiquitous, Highly Regulated Enzyme in Plants.
R. Chollet (1996)
Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants.
Y. Saijo (2000)
Generation and maintenance of concentration gradients between the mesophyll and bundle sheath in maize leaves
M. Stitt (1985)
Metabolite and post-translational control of phosphoenolpyruvate carboxylase from leaves and mesophyll cell protoplasts of
A. Gousset-Dupont (2005)
Phosphoenolpyruvate carboxylase kinase is a novel protein kinase regulated at the level of expression.
J. Hartwell (1999)
The Light-Dependent Transduction Pathway Controlling the Regulatory Phosphorylation of C4 Phosphoenolpyruvate Carboxylase in Protoplasts from Digitaria sanguinalis.
N. Giglioli-Guivarc’h (1996)
What can enzymes of C₄ photosynthesis do for C₃ plants under stress?
V. Doubnerová (2011)
ABA modulates the degradation of phosphoenolpyruvate carboxylase kinase in sorghum leaves
J. Monreal (2007)
Cloning of a Calcium-Dependent Protein Kinase Gene NtCDPK12, and Its Induced Expression by High-Salt and Drought in Nicotiana tabacum
Shuai Chen (2011)
Expressional Analysis and Role of Calcium Regulated Kinases in Abiotic Stress Signaling
R. Das (2010)
This paper is referenced by
Phosphoenolpyruvate carboxylase (PEPC) and PEPC-kinase (PEPC-k) isoenzymes in Arabidopsis thaliana: role in control and abiotic stress conditions
A. B. Feria (2016)
PHYSIOLOGICAL AND BIOCHEMICAL BASIS FOR STAY-GREEN TRAIT IN SORGHUM I.K.A. GALYUON, A. GAY, A.K. BORRELL and C.J. HOWARTH
Isaac K. A. Galyuon (2019)
Phosphoproteomic profiling of microsomal fractions in leaves of Cogon grass ('Imperata cylindrica')
Ting-ying Wu (2015)
Genomic and Expression Analysis Indicate the Involvement of Phospholipase C family in Abiotic Stress Signaling in Chickpea (Cicer arietinum).
S. Sagar (2020)
Insights Into the Nitric Oxide Mediated Stress Tolerance in Plants
P. Santisree (2019)
Phosphorylation of bacterial-type phosphoenolpyruvate carboxylase by a Ca2+-dependent protein kinase suggests a link between Ca2+ signalling and anaplerotic pathway control in developing castor oil seeds.
A. T. Hill (2014)
Genome-wide Analysis of Phosphoenolpyruvate Carboxylase Gene Family and Their Response to Abiotic Stresses in Soybean
N. Wang (2016)
The Sinorhizobium (Ensifer) fredii HH103 Type 3 Secretion System Suppresses Early Defense Responses to Effectively Nodulate Soybean.
I. Jiménez-Guerrero (2015)
Nitric oxide regulation of leaf phosphoenolpyruvate carboxylase-kinase activity: implication in sorghum responses to salinity
J. Monreal (2013)
Improved short-term drought response of transgenic rice over-expressing maize C4 phosphoenolpyruvate carboxylase via calcium signal cascade.
X. Liu (2017)
Ectopic Expression of GsPPCK3 and SCMRP in Medicago sativa Enhances Plant Alkaline Stress Tolerance and Methionine Content
M. Sun (2014)
Nitric Oxide Alleviates Salt Stress Inhibited Photosynthetic Performance by Interacting with Sulfur Assimilation in Mustard
M. Fatma (2016)
Enzymatic activity, gene expression and posttranslational modifications of photosynthetic and non-photosynthetic phosphoenolpyruvate carboxylase in ammonium-stressed sorghum plants.
Cirenia Arias-Baldrich (2017)
Phosphoenolpyruvate carboxylase regulation in C4-PEPC-expressing transgenic rice during early responses to drought stress.
X. Liu (2017)
Phosphoenolpyruvate Carboxylase during Maturation and Germination Sorghum Seeds: Enzyme Activity and Regulation
Y. Bouargalne (2018)
Comparative Transcriptome Analysis of Seedling Stage of Two Sorghum Cultivars Under Salt Stress
Jiang-hui Cui (2018)
In silico Expression Profile of Maize Genes in Response to Osmotic Stress
玉米响应渗透胁迫的数字基因表达谱分析 葛淑娟 (2014)
In vivo monoubiquitination of anaplerotic phosphoenolpyruvate carboxylase occurs at Lys624 in germinating sorghum seeds
Isabel Ruiz-Ballesta (2014)
Salinity promotes opposite patterns of carbonylation and nitrosylation of C4 phosphoenolpyruvate carboxylase in sorghum leaves
G. Baena (2017)
Exogenous ATP enhance signal response of suspension cells of transgenic rice (Oryza sativa L.) expressing maize C4-pepc encoded phosphoenolpyruvate carboxylase under PEG treatment
K. Huo (2016)
Plant phosphoinositide-dependent phospholipases C: variations around a canonical theme.
I. Pokotylo (2014)
Plant phospholipase C family: Regulation and functional role in lipid signaling.
A. Singh (2015)
Investigating the Genetic Basis of Agronomically Important Traits in Sorghum
Nikhil Y. Patil (2016)