Biochemical and proteomic analyses reveal that Populus cathayana males and females have different metabolic activities under chilling stress.

Male and female poplars (Populus cathayana Rehd.) respond differently to environmental stresses. However, little is known about sex-dependent responses to chilling at the proteome level. To better understand these differences, a comparative proteomics investigation combined with a biochemical approach was used in the current study. Three-month-old poplar cuttings were treated at 25 or 4 °C for 14 days. Results revealed significant sexual differences in nitrogen metabolic enzymes and free amino acid components in response to chilling. The chilling-treated males showed higher activities of nitrate reductase and glutamine synthetase and higher contents of reduced glutathione, serine, arginine, leucine, glycine, proline and methionine than chilling-treated females. A total of 65 chilling-responsive spots were found, of which 48 showed significant sexual differences. These proteins are involved in photosynthesis, carbon and energy metabolism, metabolic processes of proteins, lipid metabolism, vitamin metabolism, stress defense, and gene expression regulation. The study shows that males have more effective metabolic processes and protective systems to chilling than females.

[1]  W. Schulze,et al.  Cold acclimation induces changes in Arabidopsis tonoplast protein abundance and activity and alters phosphorylation of tonoplast monosaccharide transporters. , 2012, The Plant Journal.

[2]  Hao Jiang,et al.  Comparative proteomics analysis of salt response reveals sex-related photosynthetic inhibition by salinity in Populus cathayana cuttings. , 2011, Journal of proteome research.

[3]  M. Taliansky,et al.  A plant alternative to animal caspases: subtilisin-like proteases , 2011, Cell Death and Differentiation.

[4]  Dana Pascovici,et al.  Differential proteomic response of rice (Oryza sativa) leaves exposed to high‐ and low‐temperature stress , 2011, Proteomics.

[5]  Baiyi An,et al.  Comparative Profile of Rubisco-interacting Proteins From Arabidopsis : Photosynthesis Under Cold Conditions*: Comparative Profile of Rubisco-interacting Proteins From Arabidopsis : Photosynthesis Under Cold Conditions* , 2011 .

[6]  H. Vélëz,et al.  Identification and characterization of a pyridoxal reductase involved in the vitamin B6 salvage pathway in Arabidopsis , 2011, Plant Molecular Biology.

[7]  F. J. Corpas,et al.  Mechanical wounding induces a nitrosative stress by down-regulation of GSNO reductase and an increase in S-nitrosothiols in sunflower (Helianthus annuus) seedlings , 2010, Journal of experimental botany.

[8]  Hao Jiang,et al.  Sex-related differences in morphological, physiological, and ultrastructural responses of Populus cathayana to chilling , 2010, Journal of experimental botany.

[9]  G. Salekdeh,et al.  Cold acclimation proteome analysis reveals close link between the up-regulation of low-temperature associated proteins and vernalization fulfillment. , 2010, Journal of proteome research.

[10]  H. Korpelainen,et al.  Sex-specific responses and tolerances of Populus cathayana to salinity. , 2010, Physiologia plantarum.

[11]  Mengzhu Lu,et al.  Changes in freezing tolerance in hybrid poplar caused by up- and down-regulation of PtFAD2 gene expression , 2010, Transgenic Research.

[12]  S. Zhang,et al.  Comparative physiological, ultrastructural and proteomic analyses reveal sexual differences in the responses of Populus cathayana under drought stress , 2010, Proteomics.

[13]  J. Y. Kim,et al.  Zinc finger-containing glycine-rich RNA-binding protein in Oryza sativa has an RNA chaperone activity under cold stress conditions. , 2010, Plant, cell & environment.

[14]  J. Y. Kim,et al.  Glycine-rich RNA-binding proteins are functionally conserved in Arabidopsis thaliana and Oryza sativa during cold adaptation process , 2010, Journal of experimental botany.

[15]  Yan Li,et al.  Sex-related adaptive responses of Populus cathayana to photoperiod transitions. , 2009, Plant, cell & environment.

[16]  Xiaofeng Zhang,et al.  Proteomic analysis of the cold stress response in the moss, Physcomitrella patens , 2009, Proteomics.

[17]  R. Tognetti,et al.  Low temperature induces different cold sensitivity in two poplar clones (Populus x canadensis Monch 'I-214' and P. deltoides Marsh. 'Dvina'). , 2009, Journal of experimental botany.

[18]  Jin-yuan Liu,et al.  Comparative Proteomics Analysis Reveals an Intimate Protein Network Provoked by Hydrogen Peroxide Stress in Rice Seedling Leaves*S , 2008, Molecular & Cellular Proteomics.

[19]  S. Zhang,et al.  Sex-specific responses of Populus cathayana to drought and elevated temperatures. , 2008, Plant, cell & environment.

[20]  A. Good,et al.  NAD(H)-dependent glutamate dehydrogenase is essential for the survival of Arabidopsis thaliana during dark-induced carbon starvation. , 2008, Journal of experimental botany.

[21]  Junying Wang,et al.  Expression Analysis of Low Temperature Responsive Genes in Eupatorium Adenophorum Spreng Using cDNA-AFLP , 2007, Plant Molecular Biology Reporter.

[22]  Klaus-Dieter Scharf,et al.  Complexity of the heat stress response in plants. , 2007, Current opinion in plant biology.

[23]  S. Komatsu,et al.  Proteomic analysis of rice seedlings during cold stress , 2007, Proteomics.

[24]  A. Tripathi,et al.  Gender-specific responses of Piper betle L. to low temperature stress: changes in chlorophyllase activity , 2006, Biologia Plantarum.

[25]  J. Botella,et al.  Tobacco Isoenzyme 1 of NAD(H)-Dependent Glutamate Dehydrogenase Catabolizes Glutamate in Vivo[OA] , 2006, Plant Physiology.

[26]  V. Vona,et al.  Temperature dependence of nitrate reductase in the psychrophilic unicellular alga Koliella antarctica and the mesophilic alga Chlorella sorokiniana. , 2006, Plant, cell & environment.

[27]  F. J. Corpas,et al.  Localization of S-nitrosoglutathione and expression of S-nitrosoglutathione reductase in pea plants under cadmium stress. , 2006, Journal of experimental botany.

[28]  C. Lenz,et al.  Variation in the holm oak leaf proteome at different plant developmental stages, between provenances and in response to drought stress , 2006, Proteomics.

[29]  Zhangcheng Tang,et al.  Comparative Proteomic Analysis Provides New Insights into Chilling Stress Responses in Rice* , 2006, Molecular & Cellular Proteomics.

[30]  Y. Charng,et al.  Arabidopsis Hsa32, a Novel Heat Shock Protein, Is Essential for Acquired Thermotolerance during Long Recovery after Acclimation1[W] , 2006, Plant Physiology.

[31]  J. Weinman,et al.  Low Temperature Treatment at the Young Microspore Stage Induces Protein Changes in Rice Anthers*S , 2006, Molecular & Cellular Proteomics.

[32]  L. Hoffmann,et al.  Biochemical and physiological mechanisms related to cold acclimation and enhanced freezing tolerance in poplar plantlets , 2005 .

[33]  Tal Isaacson,et al.  Dual Role for Tomato Heat Shock Protein 21: Protecting Photosystem II from Oxidative Stress and Promoting Color Changes during Fruit Maturation , 2005, The Plant Cell Online.

[34]  O. Junttila,et al.  Sexual differences in cold acclimation and freezing tolerance development in sea buckthorn (Hippophae rhamnoides L.) ecotypes , 2005 .

[35]  Gilles Caraux,et al.  PermutMatrix: a graphical environment to arrange gene expression profiles in optimal linear order , 2005, Bioinform..

[36]  Jörg Durner,et al.  Proteomic Identification of S-Nitrosylated Proteins in Arabidopsis1[w] , 2005, Plant Physiology.

[37]  V. Vona,et al.  Temperature responses of growth, photosynthesis, respiration and NADH: nitrate reductase in cryophilic and mesophilic algae. , 2004, The New phytologist.

[38]  T. Wolpert,et al.  Purification and Characterization of Serine Proteases That Exhibit Caspase-Like Activity and Are Associated with Programmed Cell Death in Avena sativa , 2004, The Plant Cell Online.

[39]  D. Werck-Reichhart,et al.  Cloning, characterization and regulation of a family of phi class glutathione transferases from wheat , 2003, Plant Molecular Biology.

[40]  P. Streb,et al.  Malate metabolism and reactions of oxidoreduction in cold-hardened winter rye (Secale cereale L.) leaves. , 2003, Journal of experimental botany.

[41]  O. Junttila,et al.  Cold acclimation in silver birch (Betula pendula). Development of freezing tolerance in different tissues and climatic ecotypes , 2002 .

[42]  J. Schulze,et al.  Malate plays a central role in plant nutrition , 2002, Plant and Soil.

[43]  Yves Gibon,et al.  Steps towards an integrated view of nitrogen metabolism. , 2002, Journal of experimental botany.

[44]  J. Hausman,et al.  Compared responses of poplar cuttings and in vitro raised shoots to short-term chilling treatments , 2000, Plant Cell Reports.

[45]  M. Van Montagu,et al.  Phenylcoumaran benzylic ether reductase, a prominent poplar xylem protein, is strongly associated with phenylpropanoid biosynthesis in lignifying cells , 2000, Planta.

[46]  G. Smith,et al.  Temperature dependence of nitrate reductase activity in marine phytoplankton: biochemical analysis and ecological implications , 2000 .

[47]  A. B. Hope,et al.  Electron transfers amongst cytochrome f, plastocyanin and photosystem I: kinetics and mechanisms. , 2000, Biochimica et biophysica acta.

[48]  Mark Stitt,et al.  Accumulation of nitrate in the shoot acts as a signal to regulate shoot‐root allocation in tobacco† , 1997 .

[49]  R. L. Warner,et al.  Expression of NADH-Specific and NAD(P)H-Bispecific Nitrate Reductase Genes in Response to Nitrate in Barley , 1995, Plant physiology.

[50]  R. Häusler,et al.  Control of photosynthesis in barley leaves with reduced activities of glutamine synthetase or glutamate synthase , 1994, Planta.

[51]  S. Robinson,et al.  Regulation of glutamate dehydrogenase activity in relation to carbon limitation and protein catabolism in carrot cell suspension cultures. , 1992, Plant physiology.

[52]  C. Vogel,et al.  Nitrate reductase activity, nitrogenase activity and photosynthesis of black alder exposed to chilling temperatures , 1991 .

[53]  C. A. Loulakakis,et al.  Intracellular Localization and Properties of NADH-Glutamate Dehydrogenase from Vitis vinifera L.: Purification and Characterization of the Major Leaf Isoenzyme , 1990 .

[54]  J. Snel,et al.  The use of chlorophyll fluorescence nomenclature in plant stress physiology , 1990, Photosynthesis Research.

[55]  A. Guri.  VARIATION IN GLUTATHIONE AND ASCORBIC ACID CONTENT AMONG SELECTED CULTIVARS OF Phaseolus vulgaris PRIOR TO AND AFTER EXPOSURE TO OZONE , 1983 .

[56]  Y. Charng,et al.  Arabidopsis Hsa 32 , a Novel Heat Shock Protein , Is Essential for Acquired Thermotolerance during Long Recovery after Acclimation 1 [ W ] , 2006 .

[57]  J. Renaut,et al.  Proteomics and low-temperature studies : bridging the gap between gene expression and metabolism , 2006 .

[58]  D. Ort,et al.  Low temperature induces expression of nitrate reductase in tomato that temporarily overrides circadian regulation of activity , 2004, Photosynthesis Research.

[59]  L. Hoffmann,et al.  Responses of poplar to chilling temperatures: proteomic and physiological aspects. , 2004, Plant biology.

[60]  R. Tischner,et al.  Nitrate reductase from winter wheat leaves is activated at low temperature via protein dephosphorylation. , 2002, Physiologia plantarum.

[61]  R. V. van Montfort,et al.  Structure and function of the small heat shock protein/alpha-crystallin family of molecular chaperones. , 2001, Advances in protein chemistry.

[62]  T. Gaspar,et al.  Early Biochemical Changes during Acclimation of Poplar to Low Temperature , 1995 .

[63]  A. Portis.  Regulation of Ribulose 1,5-Bisphosphate Carboxylase/Oxygenase Activity , 1992 .