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The plasma membrane H+-ATPase is related to the development of salicylic acid-induced thermotolerance in pea leaves

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Abstract

The plasma membrane H+-ATPase (PM H+-ATPase, EC.3.6.1.35) plays a key role in the plant response to environmental stress. In this study, a possible mechanistic link between the PM H+-ATPase and salicylic acid (SA)-induced thermotolerance was investigated in pea (Pisum sativum L. cv. NingXia) leaves. The burst of free SA in response to heat acclimation (38 ± 0.5°C) was observed, and peaks appeared subsequently both in activity and amount of PM H+-ATPase in pea leaves during heat acclimation. Similarly, exogenous SA also triggered the two peaks in the room temperature (25 ± 0.5°C). Paclobutrazol (PAC) was employed to infiltrate onto pea leaves prior to heat acclimation treatment. The results showed that the peaks of both free SA and activity of PM H+-ATPase still occurred after the PAC pretreatment. In acquired thermotolerance assessment (malondialdehyde content and degree of wilting), spraying SA and fusicoccin (FC, the activator of PM H+-ATPase) separately could protect pea leaves from heat injury. Results from RT-PCR and western blotting analysis indicated that the increase in activity of the PM H+-ATPase was due to its transcriptional and translational regulation. The subcellular localizations of PM H+-ATPase after the FC or SA pretreatment also showed that the PM H+-ATPase is important to maintain the integrity of plasma membrane against the heat stress. Taken together, these results suggest PM H+-ATPase is related to the development of SA-induced thermotolerance in pea leaves.

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Abbreviations

DTT:

Dithiothreitol

FC:

Fusicoccin

MDA:

Malondialdehyde

NBT/BCIP:

Nitro blue tetrazolium/5-bromo-4-chloro-3-indolyl phosphate

PAC:

Paclobutrazol

PIP2-PLC:

Phosphatidylinositol-4, 5-bisphosphate-specific phospholipase C

PM:

Plasma membrane

PM H+-ATPase:

Plasma membrane H+-ATPase

PMSF:

Phenylmethylsulfonyl

PVPP:

Polyvinylpyrrolidone

RT-PCR:

Reverse transcription-polymerase chain reactions

SA:

Salicylic acid

SAG:

Salicylic acid 2-O-β-D-glucose

SAR:

Systemic acquired resistance

TCA:

Trichloroacetic acid

References

  • Ahn JS, Im JY, Chung CG, Cho HB (1999) Inducible expression of plasma membrane H+-ATPase in the roots of figleaf gourd plants under chilling rot temperature. Physiol Plant 106:35–40

    Article  CAS  Google Scholar 

  • Ahn SJ, Sivaguru M, Osawa H, Chung GC, Matsumoto H (2001) Aluminum inhibits the H+-ATPase activity by permanently altering the plasma membrane surface potentials in squash roots. Plant Physiol 126:1381–1390

    Article  PubMed  CAS  Google Scholar 

  • Alsterfjord M, Sehnke P, Arkell A, Larsson H, Svennelid F, Rosenquist M, Ferl RJ, Sommarin M, Larsson C (2004) Plasma membrane H+-ATPase and 14-3-3 isoforms of Arabidopsis leaves: evidence for isoform specificity in the 14-3-3/H+-ATPase interaction. Plant Cell Physiol 45:1202–1210

    Article  PubMed  CAS  Google Scholar 

  • Ames BM (1966) Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol 8:115–118

    Article  CAS  Google Scholar 

  • Arango M, Gévaudant F, Oufattole M, Boutry M (2003) The plasma membrane proton pump-ATPase: the significance of gene subfamilies. Planta 216:355–365

    PubMed  CAS  Google Scholar 

  • Axelsen KB, Venema K, Jahn T, Baunsgaard L, Palmgren MG (1999) Molecular dissection of the C-terminal regulatory domain of the plant plasma membrane H+-ATPase AHA2: mapping of residues that when altered give rise to an activated enzyme. Biochemistry 38:7227–7337

    Article  PubMed  CAS  Google Scholar 

  • Babakov AV, Chelysheva VV, Klychnikov OI, Zorinyanz SE, Trofimova MS, De Boer AH (2000) Involvement of 14-3-3 proteins in the osmotic regulation of H+-ATPase in plant plasma membrane. Planta 211:446–448

    Article  PubMed  CAS  Google Scholar 

  • Baunsgaard L, Venema K, Axelsen KB, Villalba JM, Welling A, Wollenweber B, Palmgren MG (1996) Modified plant plasma membrane H+-ATPase with improved transport coupling efficiency identified by mutant selection in yeast. Plant J 10:451–458

    Article  PubMed  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Carratu L, Franceschelli S, Pardini CL, Kobayashi GS, Horvath I, Vigh L, Maresca B (1996) Membrane lipid perturbation modifies the set point of the temperature of heat shock response in yeast. Proc Natl Acad Sci USA 93:3870–3875

    Article  PubMed  CAS  Google Scholar 

  • Chang A, Slayman CW (1991) Maturation of the yeast plasma membrane H+-ATPase involves phosphorylation during intracellular transport. J Cell Biol 115:289–295

    Article  PubMed  CAS  Google Scholar 

  • Chelysheva VV, Smolenskaya IN, Trofimova MC, Babakov AV, Muromtsev GS (1999) Role of the 14-3-3 proteins in the regulation of H+-ATPase activity in the plasma membrane of suspension-cultured sugar beet cells under cold stress. FEBS Lett 456:22–26

    Article  PubMed  CAS  Google Scholar 

  • Clarke MS, Mur AJL, Wood EJ, Scott MI (2004) Salicylic acid dependent signaling promotes basal thermotolerance but is not essential for acquires thermotolerance in Arabidopsis thaliana. Plant J 38:432–447

    Article  PubMed  CAS  Google Scholar 

  • Coccetti P, Tisi R, Martegani E, Teixeira LS, Brandão RL, Castro IM, Thevelein JM (1998) The PLC1 encoded phospholipase C in the yeast Saccharomyces cerevisiae is essential for glucose-induced phosphatidylinositol turnover and activation of plasma membrane H+-ATPase. Biochim Biophys Acta 1405:147–154

    Article  PubMed  CAS  Google Scholar 

  • Coote PJ, Jones MV, Seymour IJ, Rowe DL, Ferdinando DP, Mcarthur AJ, Cole MB (1994) Activity of the plasma membrane H+-ATPase is a key physiological determinant of thermotolerance in Saccharomyces cerevisiae. Microbiology 140:1881–1890

    Article  PubMed  CAS  Google Scholar 

  • Dat JF, Foyer CH, Scott IM (1998) Change in salicylic acid and antioxidants during induction of thermotolerance in mustard seedlings. Plant Physiol 118:1455–1461

    Article  PubMed  CAS  Google Scholar 

  • Delaney PT, Uknes S, Vernooij B, Friedrich L, Weymann K, Negrotto D, Gaffney T, Gut-Rella M, Kessmann H, Ward E, Ryals J (1994) A central role of salicylic acid in plant disease resistance. Science 266:1247–1250

    Article  PubMed  CAS  Google Scholar 

  • Faraday CD, Spanswick RM (1992) Maize root plasma membranes isolated by aqueous polymer two-phase partitioning: assessment of residual tonoplast ATPase and pyrophosphatase activities. J Exp Bot 43:1583–1590

    Article  CAS  Google Scholar 

  • Fodor J, Gullner G, Adam AL, Barna B, Komives T, Kiraly Z (1997) Local and systemic responses of antioxidants to tobacco mosaic virus infection and to salicylic acid in tobacco. Plant Physiol 114:1443–1451

    PubMed  CAS  Google Scholar 

  • Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Mol Biol 51:463–499

    Article  CAS  Google Scholar 

  • Hays DB, Doa JH, Masona RE, Morgana G, Finlaysona SA (2007) Heat stress induced ethylene production in developing wheat grains induces kernel abortion and increased maturation in a susceptible cultivar. Plant Sci 172:1113–1123

    Article  CAS  Google Scholar 

  • Huang Y, Yang F (1996) Physical state change of phospholipids mediated by Na+ modulates activity and conformation of reconstituted mitochondrial F0-F1-ATPase. In: Yang F, Wang F (ed) Membrane lipid-protein interaction and its application in medicine and agriculture. Shandong Science Press, Jinan, China, pp 1–17

  • Kalampanayil BD, Wimmers LE (2001) Identification and characterization of a salt-stress-induced plasma membrane H+-ATPase in tomato. Plant Cell Environ 24:999–1005

    Article  CAS  Google Scholar 

  • Kasamo K (2003) Regulation of plasma membrane H+-ATPase activity by the membrane environment. J Plant Res 116:517–523

    Article  PubMed  CAS  Google Scholar 

  • Kinoshita T, Nishimura M, Shimazaki K (1995) Cytosolic concentration of Ca2+ regulates the plasma membrane H+-ATPase in guard cells of fava bean. Plant Cell 7:1333–1342

    Article  PubMed  CAS  Google Scholar 

  • Kratsch HA, Wise RR (2000) The ultrastructure of chilling stress. Plant Cell Environ 23:337–350

    Article  CAS  Google Scholar 

  • Kuhlbrandt W (2004) Biology, structure and mechanism of P-type ATPases. Nat Rev Mol Cell Biol 5:282–295

    Article  PubMed  CAS  Google Scholar 

  • Laemmli UK (1970) Cleavage of structural protein during the assembly of the head bacteriophage T4. Nature 227:680–685

    Article  PubMed  CAS  Google Scholar 

  • Lee HI, Raskin I (1998) Glucosylation of salicylic acid in Nicotiana tabacum cv. Xanthi-nc. Phytopathology 88:692–697

    Article  PubMed  CAS  Google Scholar 

  • León J, Shulaev V, Yalpani N, Lawton MA, Raskin I (1995) Benzoic acid 2-hydroxylase, a soluble oxygenase from tobacco, catalyzes salicylic acid biosynthesis. Proc Natl Acad Sci USA 92:10413–10417

    Article  PubMed  Google Scholar 

  • Liu HT, Huang WD, Pan QH, Weng FH, Zhan JC, Liu Y, Wan SB, Liu YY (2006a) Contributions of PIP2-specific-phospholipase C and free salicylic acid to heat acclimation-induced thermotolerance in pea leaves. J Plant Physiol 163:405–416

    Article  PubMed  CAS  Google Scholar 

  • Liu HT, Liu YY, Pan QH, Yang HR, Zhan JC, Huang WD (2006b) Novel interrelationship between salicylic acid, abscisic acid and PIP2-specific-phospholipase C in heat acclimation-induced thermotolerance in pea leaves. J Exp Bot 57:3337–3347

    Article  PubMed  CAS  Google Scholar 

  • Logemann J, Schell J, Willmitzer L (1987) Improved method for the isolation of RNA from plant issues. Anal Biochem 163:16–20

    Article  PubMed  CAS  Google Scholar 

  • Mauch-Mani B, Métraux J (1998) Salicylic acid and systemic acquired resistance to pathogen attack. Ann Bot 82:535–540

    Article  CAS  Google Scholar 

  • Michelet B, Boutry M (1995) The plasma membrane H+-ATPase: a highly regulated enzyme with multiple physiological functions. Plant Physiol 108:1–6

    PubMed  CAS  Google Scholar 

  • Morsomme P, de Kerchove d’Exaerde A, De Meester S, Thines D, Goffeau A, Boutry M (1996) Single point mutations in various domains of a plant plasma membrane H+-ATPase expressed in Saccharomyces cerevisiae increased H+ pumping and permit yeast growth at low pH. EMBO J 15:5513–5526

    PubMed  CAS  Google Scholar 

  • Olsson A, Svennelid F, EK B, Sommarin M, Larsson C (1998) A phosphothreonine residue at the C-terminal end of the plasma membrane H+-ATPase is protected by fusicoccin-induced 14-3-3 binding. Plant Physiol 118:551–555

    Article  PubMed  CAS  Google Scholar 

  • Ottmann C, Marco S, Jaspert N, Marcon C, Schauer N, Weyand M, Vandermeeren C, Duby G, Boutry M, Wittinghofer A, Rigaud J-Louis, Oecking C (2007) Structure of a 14-3-3 coordinated hexamer of the plant plasma membrane H+-ATPase by combining X-Ray crystallography and electron cryomicroscopy. Mol Cell 25:427–440

    Article  PubMed  CAS  Google Scholar 

  • Palmgren MG (1998) Proton gradients and plant growth: role of the plasma membrane H+-ATPase. Adv Bot Res 28:1–70

    Article  CAS  Google Scholar 

  • Palva TK, Hurtig M, Saindrenan P, Palva ET (1994) Salicylic acid induced resistance to Erwinia carotovora subsp. Carotavora in tobacco. Mol Plant Microbe In 7:356–363

    CAS  Google Scholar 

  • Pan QH, Zhan JC, Liu HT, Zhang JH, Chen JY, Wen PF, Huang WD (2006) Salicylic acid synthesized by benzonic acid 2-hydroxylase catalysis was involved in the induction of thermotolerance in pea plants. Plant Sci 171:226–233

    Article  CAS  Google Scholar 

  • Pastori GM, Foyer CH (2002) Common components, networks and pathways of cross-tolerance to stress: the central role of ‘redox’ and abscisic acid-mediated controls. Plant Physiol 129:460–468

    Article  PubMed  CAS  Google Scholar 

  • Peng YB, Lu YF, Zhang DP (2003) Abscisic acid activates ATPase in developing apple fruit especially in fruit phloem cells. Plant Cell Environ 26:1329–1342

    Article  CAS  Google Scholar 

  • Portillo F (2000) Regulation of plasma membrane H+-ATPase in fungi and plants. Biochim Biophys Acta 1469:31–42

    PubMed  CAS  Google Scholar 

  • Prince AH, Hendry GAF (1991) Iron-catalyzed oxygen radical formation and its possible contribution to drought damage in nine native grasses and three cereals. Plant Cell Environ 14:451–477

    Google Scholar 

  • Rao MV, Davis KR (1999) Ozone-induced cell death occurs via two distinct mechanisms in Arabidopsis: the role of salicylic acid. Plant J 17:603–614

    Article  PubMed  CAS  Google Scholar 

  • Rao MV, Paliyath G, Ormrod P, Murr DP, Watkins CB (1997) Influence of salicylic acid on H2O2 production, oxidative stress, and H2O2-metabolizing enzymes. Plant Physiol 115:137–149

    Article  PubMed  CAS  Google Scholar 

  • Rasmussen JB, Hammerschimidt R, Zook MN (1991) Systemic induction of salicylic acid accumulation in cucumber after inoculation with Pseudomonus syringae pv. Syringae. Plant Physiol 97:1342–1347

    Article  PubMed  CAS  Google Scholar 

  • Ruelland E, Campalans A, Selman-Housein G, Puigdomenech P, Rigau J (2003) Cellular and subcellular localization of the lignin biosynthetic enzymes caffeic acid-O-methyltransferase, cinnamyl alcohol dehydrogenase and cinnamoyl-coenzyme A reductase in two monocots, sugarcane and maize. Physiol Plant 117:93–99

    Article  CAS  Google Scholar 

  • Sangwan V, Örvar BL, Beyerly J, Hirt H, Dhindsa RS (2002) Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. Plant J 31:629–638

    Article  PubMed  CAS  Google Scholar 

  • Schaller A, Oecking C (1999) Modulation of plasma membrane H+-ATPase activity differentially activates wound and pathogen defense responses in tomato plants. Plant Cell 11:263–272

    Article  PubMed  CAS  Google Scholar 

  • Senaratna T, Touchell D, Bunn T, Dixon K (2000) Acetyl salicylic acid (Aspirin) and salicylic acid induce multiple stress tolerance in bean and tomato plants. Plant Growth Regul 30:157–161

    Article  CAS  Google Scholar 

  • Serrano R (1983) In vivo glucose activation of the yeast plasma membrane ATPase. FEBS Lett 156:11–14

    Article  PubMed  CAS  Google Scholar 

  • Shen H, He LF, Sasaki T, Yamamoto Y, Zheng SJ, Ligaba A, Yan XL, Ahn SJ, Yamaguchi M, Sasakawa H, Matsumoto H (2005) Citrate secretion coupled with the modulation of soybean root tip under aluminum stress: up-regulation of transcription, translation, and threonin-oriented phosphorylation of plasma membrane H+-ATPase. Plant Physiol 138:287–296

    Article  PubMed  CAS  Google Scholar 

  • Shen H, Chen JH, Wang ZY, Yang CY, Sasaki T, Yamamoto Y, Matsumto H, Yan XL (2006) Root plasma membrane H+-ATPase is involved in the adaptation of soybean to phosphorus starvation. J Exp Bot 57:1353–1362

    Article  PubMed  CAS  Google Scholar 

  • Souza MAA, Trópia MJ, Brandão RL (2001) New aspects of glucose activation of the H+-ATPase in the yeast Saccharomyces cerevisiae. Microbiology 147:2849–2855

    PubMed  CAS  Google Scholar 

  • Sun WN, Montagu VM, Verbruggen N (2002) Small heat shock proteins and stress tolerance in plants. Biochim Biophys Acta 1577:1–9

    PubMed  CAS  Google Scholar 

  • Sung JA, Yang JJ, Gap CC, Baik HC (1999) Inducible expression of plasma membrane H+-ATPase in the roots of figleaf gourd plants under chilling rot temperature. Physiol Plant 106:35–40

    Article  Google Scholar 

  • Suwastika IN, Gehring CA (1999) The plasma membrane H+-ATPase from Tradescantia stem and leaf tissue is modulated in Vitro by cGMP. Arch Biochem Biophys 367:137–139

    Article  PubMed  CAS  Google Scholar 

  • Sze H, Li XH, Palmgren GM (1999) Energization of plant cell membranes by H+-pumping ATPase: regulation and biosynthesis. Plant cell 11:677–689

    Article  PubMed  CAS  Google Scholar 

  • Vani B, Saradhi P, Mohanty P (2001) Alteration in chloroplast structure and thylakoid membrane composition due to in vivo heat treatment of rise seedlings: correlation with the functional changes. J Plant Physiol 158:583–592

    Article  CAS  Google Scholar 

  • Venema K, Palmgren MG (1995) Metabolic modulation of transport coupling ratio in yeast plasma membrane H+-ATPase. J Biol Chem 270:19659–19667

    Article  PubMed  CAS  Google Scholar 

  • Veselov AP, Kurganova LN, Likhacheva AV, Sushkova UA (2002) Possible regulatory effect of lipid peroxidation on the H+-ATPase activity of the plasmalemma under stress conditions. Russ Plant Physiol 49:385–389

    Google Scholar 

  • Vitart V, Baxter I, Doerner P, Harper JF (2001) Evidence for a role in growth and salt resistance of a plasma membrane H+-ATPase in the root endodermis. Plant J 27:191–201

    Article  PubMed  CAS  Google Scholar 

  • Wang WX, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252

    Article  PubMed  CAS  Google Scholar 

  • Woloszynska M, Kanczewska J, Drabkin A, Maudoux O, Dambly S, Boutry M (2003) Function and regulation of the two major plant plasma membrane H+-ATPase. Ann N Y Acad Sci 986:198–203

    PubMed  CAS  Google Scholar 

  • Yang YL, Zhang F, Zhao MG, An LZ, Zhang LX, Chen NL (2007) Properties of plasma membrane H+-ATPase in salt-treated Populus euphratica callus. Plant Cell Rep 26:229–235

    Article  PubMed  CAS  Google Scholar 

  • Zhang DP, Lu YM, Wang YZ, Duan CQ, Yan HY (2001) Acid invertase is predominantly localized to cell walls of both the practically symplasmically isolated sieve element/companion cell complex and parenchyma cells in developing apple fruits. Plant Cell Env 24:691–702

    Article  CAS  Google Scholar 

  • Zhang JH, Huang WD, Liu YP, Pan QH (2005) Effects of temperature acclimation pretreatment on the ultrastructure of mesophyll cells in young grape plants (Vitis vinifera L. cv. Jingxiu) under cross-temperature stresses. J Integr Plant Biol 47:959–970

    Article  Google Scholar 

  • Zhang JH, Liu YP, Pan QH, Zhan JC, Wang XQ, Huang WD (2006) Changes in membrane-associated H+-ATPase activities and amounts in young grape plants during the cross adaptation to temperature stresses. Plant Sci 170:768–777

    Article  CAS  Google Scholar 

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Acknowledgments

We are grateful to Dr. R. Serrano and Dr. Jennifer Corrigan for their kindly providing the antibody against PM H+-ATPase and Hsps. This research was supported by the National Natural Science Foundation of China (Grant Numbers 30471192 and 30671468), Specialized Research Fund for the Doctoral Program of Higher Education of China (No. 20050019015) and The Significant Program of Beijing Municipal Science and Technology Commission (No. D07060500160701).

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Liu, Y., Liu, H., Pan, Q. et al. The plasma membrane H+-ATPase is related to the development of salicylic acid-induced thermotolerance in pea leaves. Planta 229, 1087–1098 (2009). https://doi.org/10.1007/s00425-009-0897-3

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