Changes in H+-ATPase activity and conjugated polyamine contents in plasma membrane purified from developing wheat embryos under short-time drought stress

Abstract Plasma membrane (PM) vesicles were isolated from developing embryos of wheat (Triticum aestivum L.) with different drought-tolerance under drought stress by the gradient centrifugation method. The activity of the PM H+-ATPase (EC 3.6.1.35) and contents of polyamine conjugated (covalently and noncovalently) to the PM vesicles were investigated. Results showed that after drought treatment for 3 d, embryo relative water content (ERWC), embryo relative dry weight increase rate (ERDWIR) of drought-sensitive Yumai No. 48 cultivar decreased more significantly than those of drought-tolerant Luomai No. 22 cultivar, while PM H+-ATPase activity, noncovalently conjugated (NCC) spermidine (Spd) and NCC spermine (Spm), the covalently conjugated (CC) putrescine (Put) and CC Spd of PM from Luomai No. 22 cultivar increased more obviously than those from Yumai No. 48 cultivar. As judged by increases in ERWC and ERDWIR, treatment with exogenous Spd alleviated markedly drought injuries to Yumai No. 48, coupled with significant increases in NCC Spd and NCC Spm levels and H+-ATPase activity in the embryo PM vesicle. Under drought stress, the treatment of drought-tolerant Luomai No. 22 cultivar with methylglyoxyl-bis (guanylhydrazone) (MGBG), an inhibitor of S-adenosylmethionine decarboxylase (SAMDC), and phenanthrolin (o−Phen), an inhibitor of transglutaminase (TGase) respectively, caused a decrease of the NCC Spd, NCC Spm, CC Put and CC Spd. Those decreases were associated with decreased PM-H+-ATPase activity and the tolerance of developing wheat embryos to osmotic stress, as judged by decreases in ERWC and ERDWIR. These results suggest that tolerance of the developing wheat embryos to drought stress is associated with the embryo PM H+-ATPase and the levels of NCC Spd, NCC Spm, CC Put and CC Spd in embryo PM vesicles.

[1]  M. L. Mayer,et al.  An improved assay of inorganic phosphate in the presence of extralabile phosphate compounds: application to the ATPase assay in the presence of phosphocreatine. , 1975, Analytical biochemistry.

[2]  M. Piotrowski,et al.  Phosphorylation of Thr-948 at the C Terminus of the Plasma Membrane H+-ATPase Creates a Binding Site for the Regulatory 14-3-3 Protein , 1999, Plant Cell.

[3]  S. Beninati,et al.  Polyamines in chloroplasts: identification of their glutamyl and acetyl derivatives. , 1995, The Biochemical journal.

[4]  R. Serrano.  Structure and Function of Plasma Membrane ATPase , 1989 .

[5]  W. Cao,et al.  Induction of chilling tolerance in wheat during germination by pre-soaking seed with nitric oxide and gibberellin , 2013, Plant Growth Regulation.

[6]  M. Sussman,et al.  Molecular biology of the plasma membrane of higher plants. , 1989, The Plant cell.

[7]  M. Sussman.  Molecular Analysis of Proteins in the Plant Plasma Membrane , 1994 .

[8]  M. Taylor,et al.  Recent advances in polyamine research , 1997 .

[9]  K. Shinozaki,et al.  Arabidopsis ADC genes involved in polyamine biosynthesis are essential for seed development , 2005, FEBS letters.

[10]  C. Qin,et al.  Relationship Between H+-ATPase Activity and Fluidity of Tonoplast in Barley Roots Under NaCl Stress , 2002 .

[11]  S. Huber,et al.  Polycations globally enhance binding of 14-3-3omega to target proteins in spinach leaves. , 2006, Plant & cell physiology.

[12]  M. Cacho,et al.  Role of polyamines in regulating silymarin production in Silybum marianum (L.) Gaertn (Asteraceae) cell cultures under conditions of calcium deficiency. , 2013, Journal of plant physiology.

[13]  S. Srivastava,et al.  Effect of amines and guanidines on ATPase from maize scutellum , 1983 .

[14]  M. M. Bradford.  A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.

[15]  S. Huber,et al.  Divalent cations and polyamines bind to loop 8 of 14-3-3 proteins, modulating their interaction with phosphorylated nitrate reductase. , 2002, The Plant journal : for cell and molecular biology.

[16]  G. Lester.  Polyamines and their cellular anti-senescence properties in honey dew muskmelon fruit. , 2000, Plant science : an international journal of experimental plant biology.

[17]  L. Camoni,et al.  Binding of phosphatidic acid to 14‐3‐3 proteins hampers their ability to activate the plant plasma membrane H+‐ATPase , 2012, IUBMB life.

[18]  Z. Fu.  Effects of Salinity Stress on the Levels of Covalently and Noncovalently Conjugated Polyamines in Plasma Membrane and Tonoplast Isolated from Barley Seedlings , 2000 .

[19]  Da-Peng Zhang,et al.  Abscisic acid activates ATPase in developing apple fruit especially in fruit phloem cells , 2003 .

[20]  P. K. Nagar,et al.  The effect of polyamines on leaf senescence in two diverse rose species , 2003, Plant Growth Regulation.

[21]  E. Weiler,et al.  Binding of Regulatory 14-3-3 Proteins to the C Terminus of the Plant Plasma Membrane H+-ATPase Involves Part of Its Autoinhibitory Region* , 2001, The Journal of Biological Chemistry.

[22]  I. N. Suwastika,et al.  The plasma membrane H+-ATPase from Tradescantia stem and leaf tissue is modulated in vitro by cGMP. , 1999, Archives of biochemistry and biophysics.

[23]  R. Serrano,et al.  Identification of an autoinhibitory domain in the C-terminal region of the plant plasma membrane H(+)-ATPase. , 1991, The Journal of biological chemistry.

[24]  S. Shabala,et al.  Polyamines Interact with Hydroxyl Radicals in Activating Ca2+ and K+ Transport across the Root Epidermal Plasma Membranes1[W] , 2011, Plant Physiology.

[25]  J. Boyer,et al.  Low water potentials affect expression of genes encoding vegetative storage proteins and plasma membrane proton ATPase in soybean , 1991, Plant Molecular Biology.

[26]  J. Kubiś.  Exogenous spermidine differentially alters activities of some scavenging system enzymes, H(2)O(2) and superoxide radical levels in water-stressed cucumber leaves. , 2008, Journal of plant physiology.

[27]  A. Knapp,et al.  Relationship between changes in endogenous polyamines and seed quality during development of sh2 sweet corn (Zea mays L.) seed , 2010 .

[28]  Wei Tang,et al.  Polyamines reduce salt-induced oxidative damage by increasing the activities of antioxidant enzymes and decreasing lipid peroxidation in Virginia pine , 2005, Plant Growth Regulation.

[29]  Bingjun Yu,et al.  Effects of spermidine and spermine levels on salt tolerance associated with tonoplast H+-ATPase and H+-PPase activities in barley roots , 2006, Plant Growth Regulation.

[30]  C. Larsson,et al.  Fusicoccin Activates the Plasma Membrane H+-ATPase by a Mechanism Involving the C-Terminal Inhibitory Domain. , 1993, The Plant cell.

[31]  B. Carver,et al.  Water relations in winter wheat as drought resistance indicators , 1988 .

[32]  T. Kinoshita,et al.  Cytosolic Concentration of Ca2+ Regulates the Plasma Membrane H+-ATPase in Guard Cells of Fava Bean. , 1995, The Plant cell.

[33]  Arthur W. Galston,et al.  Polyamines in plants : An overview , 2005 .

[34]  L. Astarita,et al.  Changes in polyamines content associated with zygotic embryogenesis in the Brazilian pine, Araucaria angustifolia (Bert.) O. Ktze. , 2003 .

[35]  Yang Zhang,et al.  Relationship between osmotic stress and the levels of free, conjugated and bound polyamines in leaves of wheat seedlings , 2004 .

[36]  M. Boutry,et al.  A plant plasma membrane proton-ATPase gene is regulated by development and environment and shows signs of a translational regulation. , 1994, The Plant cell.

[37]  Bhaskar Gupta,et al.  Plant polyamines in abiotic stress responses , 2013, Acta Physiologiae Plantarum.

[38]  V. Silveira,et al.  Polyamines affect the cellular growth and structure of pro-embryogenic masses in Araucaria angustifolia embryogenic cultures through the modulation of proton pump activities and endogenous levels of polyamines. , 2013, Physiologia plantarum.

[39]  A. Galston,et al.  Polyamines in Plants , 1985, Advances in Agricultural Biotechnology.

[40]  J. Martin-Tanguy.  Metabolism and function of polyamines in plants: recent development (new approaches) , 2001, Plant Growth Regulation.

[41]  A. Tiburcio,et al.  Recent advances in the understanding of polyamine functions during plant development , 1993, Plant Growth Regulation.

[42]  R. Lieberei,et al.  Establishment of suspension culture in Theobroma cacao and polyamines associated with cacao embryogenesis , 2012, Plant Growth Regulation.

[43]  C. Larsson,et al.  The Plant Plasma Membrane , 2007, Springer Berlin Heidelberg.

[44]  M. Goyal,et al.  Polyamine catabolism influences antioxidative defense mechanism in shoots and roots of five wheat genotypes under high temperature stress , 2009, Plant Growth Regulation.

[45]  L. Camoni,et al.  Polyamines as physiological regulators of 14-3-3 interaction with the plant plasma membrane H+-ATPase. , 2007, Plant & cell physiology.

[46]  M. Ashraf,et al.  Changes in growth, photosynthetic capacity and ionic relations in spring wheat (Triticum aestivum L.) due to pre-sowing seed treatment with polyamines , 2005, Plant Growth Regulation.

[47]  R. Jia,et al.  Physiological and biochemical responses induced by lead stress in Spirodela polyrhiza , 2012, Plant Growth Regulation.

[48]  J. Zwiazek,et al.  Effects of triadimefon and osmotic stress on plasma membrane composition and ATPase activity in white spruce (Picea glauca) needles , 1993 .

[49]  A. Wahid,et al.  Exogenously applied polyamines increase drought tolerance of rice by improving leaf water status, photosynthesis and membrane properties , 2009, Acta Physiologiae Plantarum.

[50]  Q. Qiu,et al.  The influence of extracellular-side Ca2+ on the activity of the plasma membrane H+-ATPase from wheat roots , 1998 .

[51]  A. Michael,et al.  A protective role for the polyamine spermine against drought stress in Arabidopsis. , 2007, Biochemical and biophysical research communications.

[52]  C. Larsson,et al.  A Critical Evaluation of Markers Used in Plasma Membrane Purification , 1990 .

[53]  E. Młodzińska,et al.  The role of polyamines in the regulation of the plasma membrane and the tonoplast proton pumps under salt stress. , 2010, Journal of plant physiology.

[54]  L. Kochian,et al.  Putrescine-induced wounding and its effects on membrane integrity and ion transport processes in roots of intact corn seedlings. , 1989, Plant physiology.

[55]  A. Galston,et al.  Polyamines as Endogenous Growth Regulators , 1987 .

[56]  D. Hincha,et al.  Dissecting Rice Polyamine Metabolism under Controlled Long-Term Drought Stress , 2013, PloS one.

[57]  M. Boutry,et al.  The Plasma Membrane H+-ATPase (A Highly Regulated Enzyme with Multiple Physiological Functions) , 1995, Plant physiology.

[58]  P. Adiga,et al.  Biosynthesis and regulation of polyamines in higher plants , 1985, Plant Growth Regulation.

[59]  M. Rajam,et al.  Spatial and Temporal Changes in Endogenous Polyamine Levels Associated with Somatic Embryogenesis from Different Hypocotyl Segments of Eggplant (Solanum melongena L.) , 1995 .

[60]  S. Zaina,et al.  Plasmalemma ATPase in rice coleoptiles; Stimulation by putrescine and polyamines , 1992 .

[61]  Qiu Quan.  STRUCTURE AND FUNCTION OF PLANT PLASMA MEMBRANE H + ATPase , 1999 .