Skip to main content

Advertisement

Springer Nature Link
Log in

Aluminum inhibits phosphatidic acid formation by blocking the phospholipase C pathway

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Aluminum (Al3+) has been recognized as a main toxic factor in crop production in acid lands. Phosphatidic acid (PA) is emerging as an important lipid signaling molecule and has been implicated in various stress-signaling pathways in plants. In this paper, we focus on how PA generation is affected by Al3+ using Coffea arabica suspension cells. We pre-labeled cells with [32P]orthophosphate (32Pi) and assayed for 32P-PA formation in response to Al3+. Treating cells for 15 min with either AlCl3 or Al(NO3)3 inhibited the formation of PA. In order to test how Al3+ affected PA signaling, we used the peptide mastoparan-7 (mas-7), which is known as a very potent stimulator of PA formation. The Al3+ inhibited mas-7 induction of PA response, both before and after Al3+ incubation. The PA involved in signaling is generated by two distinct phospholipid signaling pathways, via phospholipase D (PLD; EC: 3.1.4.4) or via Phospholipase C (PLC; EC: 3.1.4.3), and diacylglycerol kinase (DGK; EC 2.7.1.107). By labeling with 32Pi for short periods of time, we found that PA formation was inhibited almost 30% when the cells were incubated with AlCl3 suggesting the involvement of the PLC/DGK pathway. Incubation of cells with PLC inhibitor, U73122, affected PA formation, like AlCl3 did. PLD in vivo activation by mas-7 was reduced by Al3+. These results suggest that PA formation was prevented through the inhibition of the PLC activity, and it provides the first evidence for the role of Al toxicity on PA production.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Explore related subjects

Discover the latest articles, books and news in related subjects, suggested using machine learning.

Abbreviations

ABA:

Abscisic acid

DAG:

Diacylglycerol

DGK:

Diacylglycerol kinase

DGPP:

Diacylglycerol pyrophosphate

EtAc:

Ethyl acetate

IP3 :

Inositol 1,4,5-trisphosphate

LPA:

Lyso-phosphatidic acid

PC:

Phosphatidylcholine

PIP:

Phosphatidylinositol 4-phosphate

PIP2 :

Phosphatidylinositol 4,5-bisphosphate

Pbut:

Phosphatidylbutanol

PLC:

Phospholipase C

PLD:

Phospholipase D

PA:

Phosphatidic acid

PCA:

Perchloric acid

PEPC:

Phosphoenolpyruvate carboxylase

32Pi:

[32P]orthophosphate

References

  • Alexandre J, Lassalles JP, Kado RT (1990) Opening of Ca2+ channels in isolated red beet root vacuole membrane by inositol 1, 4,5-trisphosphate. Nature 343:567–570

    Article  CAS  Google Scholar 

  • Apone F, Alyeshmerni N, Wiens K, Chalmers D, Chrispeels MJ, Colucci G (2003) The G-protein-coupled receptor GCR1 regulates DNA synthesis through activation of phosphatidylinositol-specific phospholipase C. Plant Physiol 133:571–579

    Article  PubMed  CAS  Google Scholar 

  • Arroyo-Serralta GA, Kú-González Á, Hernández-Sotomayor SMT, Zúñiga-Aguilar JJ (2005) Exposure to toxic concentrations of aluminum activates a MAPK-like protein in cell suspension cultures of Coffea arabica. Plant Physiol Biochem 43:27–35

    Article  PubMed  CAS  Google Scholar 

  • de Jong CF, Latax AM, Bargmann BOR, de Wit PJGM, Joosten MHAJ, Munnik T (2004) Phosphatidic acid accumulation is an early response in the Cf-4/Avr4 interaction. Plant J 39:1–12

    Article  PubMed  CAS  Google Scholar 

  • Delhaize E, Ryan PR (1995) Aluminum toxicity and tolerance in plants. Plant Physiol 107:315–321

    PubMed  CAS  Google Scholar 

  • Delton C, Manifava M, Wood E, Thompson D, Krugmann S, Pyne S, Ktistakis NT (2004) Sphingosine Kinase 1 is an intracellular effector of phosphatidic acid. J Biol Chem 279:44763–44774

    Article  CAS  Google Scholar 

  • den Hartog M, Musgrave A, Munnik T (2001) Nod factor-induced phosphatidic acid and diacylglycerol pyrophosphate formation: a role for phospholipase C and D in root hair deformation. Plant J 25:55–66

    Article  Google Scholar 

  • Feng MJ, Ryan PR, Delhaize E (2001) Aluminium tolerance in plants and the complexing role of organic acid. Trends Plant Sci 6:273–278

    Article  Google Scholar 

  • Frank W, Munnik T, Kerkmann K, Salamini F, Bartels D (2000) Water deficit triggers phospholipase D activity in the resurrection plant Craterostigma plantagineum. Plant Cell 12:111–123

    Article  PubMed  CAS  Google Scholar 

  • Fujisawa Y, Sawaki S, Kato H, Asahi T, Iwasaki Y (2001) Biochemical responses of rice cells to mastoparan 7, an activator of heterotrimeric G proteins. Plant Biotechnol 18:241–249

    CAS  Google Scholar 

  • Hunt L, Mills LN, Pical C, Leckie CP, Kopka J, Muller-Roeber B, McAinsh MR, Hetherington AM, Gray JE (2003) Phospholipase C is required for the control stomatal aperture by ABA. Plant J 34:47–55

    Article  PubMed  CAS  Google Scholar 

  • Jones GA, Carpenter G (1993) The regulation of phospholipase C-g1 by phosphatidic acid. J Biol Chem 268:20828–20845

    Google Scholar 

  • Jones DL, Kochian LV (1995) Aluminum inhibition of the inositol 1,4,5-triphosphate signal transduction pathway in wheat roots: a role in aluminum toxicity? Plant Cell 7:1913–1922

    Article  PubMed  CAS  Google Scholar 

  • Jacob T, Ritchien S, Assmann SM, Gilroy S (1999) Abscisic acid signal transduction in guard cells is mediated by phospholipase D activity. Proc Natl Acad Sci USA 96:12192–12197

    Article  PubMed  CAS  Google Scholar 

  • Kochian LV, Hoekenga OA, Piñeros MA (2004) How do crop plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Biol 55:459–493

    Article  PubMed  CAS  Google Scholar 

  • Kuin H, Koerten H, Ghijsen EJM, Munnik T, van den Ende H, Musgrave A (2000) Chlamydomonas contains calcium stores that are mobilized when phospholipase C is activated. Planta 210:286–294

    Article  PubMed  CAS  Google Scholar 

  • Latax AM, Munnik T (2002) Phospholipid signalling in plant defence. Curr Opin Plant Biol 5:332–338

    Article  Google Scholar 

  • Latijnhouwers M, Munnik T, Govers F (2002) Phospholipase D in Phytophthora infestans and its role in Zoospore Encystment. Am Phytopathol Soc 15:939–946

    CAS  Google Scholar 

  • Lee S, Suh S, Kim S (1997) Systemic elevation of phosphatidic acid and lysophospholipid levels in wounded plants. Plant J 12:547–556

    Article  CAS  Google Scholar 

  • Lemtir-Chlieh F, MacRobbie EAC, Webb AAR, Manison NF, Brownlee C, Skepper JN, Chen J, Prestwich G, Brearley CA (2003) Inositol hexakisphosphate mobilizes an endomemebrane store of calcium in guard cells. Proc Natl Acad Sci USA 100:10091–10095

    Article  CAS  Google Scholar 

  • Ligaba A, Shen H, Shibata K, Yamamoto Y, Tanakamaru S, Matsumoto H (2004) The role of phosphorus in aluminium-induced citrate and malate exudation from rape (Brassic napus). Physiol Plantarum 120:575–584

    Article  PubMed  CAS  Google Scholar 

  • Liu K, Li L, Luan S (2005) An essential function of phosphatidylinositol phosphates in activation of plant shaker-type K channels. Plant J 42:433–443

    Article  PubMed  CAS  Google Scholar 

  • Loewen CJR, Gaspar ML, Jesch SA, Delton C, Ktistakis NT, Henry SA, Levine TP (2004) Phospholipid metabolism regulated by a transcription factor sensing phosphatidic acid. Science 304:1644–1647

    Article  PubMed  CAS  Google Scholar 

  • Martínez-Estévez M, Muñoz-Sánchez JA, Loyola-Vargas VM, Hernández-Sotomayor SMT (2001) Modification of the culture medium to produce aluminum toxicity in cell suspensions of coffee (Coffea arabica L.). Plant Cell Rep 20:469–474

    Article  CAS  Google Scholar 

  • Martínez-Estévez M, Racagni-Di Palma G, Muñoz-Sánchez JA, Brito-Argáez L, Loyola-Vargas VM, Hernández-Sotomayor SMT (2003) Aluminium differentially modifies lipid metabolism from the phosphoinositide pathway in Coffea arabica cells. J Plant Physiol 160:1297–1303

    Article  PubMed  Google Scholar 

  • Meijer HJG, Arisz SA, van Himbergen JAJ, Musgrave A, Munnik T (2001) Hyperosmotic stress rapidly generates lyso-phosphatidic acid in Chlamydomonas. Plant J 25:541–548

    Article  PubMed  CAS  Google Scholar 

  • Meijer HJG, Munnik T (2003) Phospholipid-based signaling in plants. Annu Rev Plant Biol 54:256–306

    Article  CAS  Google Scholar 

  • Meijer HJG, ter Riet B, van Himbergen JAJ, Musgrave A, Munnik T (2002) KCl activates phospholipase D at two different concentration ranges: distinguishing between hyperosmotic stress and membrane depolarization. Plant J 31:51–59

    Article  PubMed  CAS  Google Scholar 

  • Munnik T (2001) Phosphatidic acid: an emerging plant lipid second messenger. Trends Plant Sci 6:227–233

    Article  PubMed  CAS  Google Scholar 

  • Munnik T, Arisz SA, de Vrije T, Musgrave A (1995) G protein activation stimulates phospholipase D signaling in plants. Plant Cell 7:2197–2210

    Article  PubMed  CAS  Google Scholar 

  • Munnik T, de Vrije T, Irvine RF, Musgrave A (1996) Identification of diacylglycerol pyrophosphate as a novel metabolic product of phosphatidic acid during G-protein activation in plants. J Biol Chem 271:15708–15715

    Article  PubMed  CAS  Google Scholar 

  • Munnik T, Meijer HJG (2001) Osmotic stress activates distinct lipid and MAPK signalling pathways in plants. FEBS Lett 498:172–178

    Article  PubMed  CAS  Google Scholar 

  • Munnik T, van Himbergen JAJ, ter Riet B, Braun F-J, Irvine RF, van der Ende H, Musgrave A (1998) Detailed analysis of the turnover of polyphosphoinositides and phosphatidic acid upon activation of phospholipase C and D in Chlamydomonas cells treated with non-permeabilizing concentrations of mastoparan. Planta 207:133–145

    Article  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–495

    Article  CAS  Google Scholar 

  • Osawa H, Matsumoto H (2001) Possible involvement of protein phosphorylation in aluminum-responsive malate efflux. Plant Physiol 126:411–420

    Article  PubMed  CAS  Google Scholar 

  • Palicz A, Foubert TR, Jesaitis AJ, Marodi L, McPhail LC (2001) Phosphatidic acid and diacylglycerol directly activate NADPH oxidase by interacting with enzyme components. J Biol Chem 276:3090–3097

    Article  PubMed  CAS  Google Scholar 

  • Park J, Gu Y, Lee Y, Yang Z, Lee Y (2004) Phosphatidic acid induces leaf cell death in Arabidopsis by activating the Rho-related small G protein GTPase-mediated pathway of reactive oxygen species generation. Plant Physiol 134:129–136

    Article  PubMed  CAS  Google Scholar 

  • Piña-Chable ML, Hernández-Sotomayor SMT (2001) Phospholipase C activity from Catharanthus roseus transformed roots: aluminum effect. Prostaglandins Other Lipid Mediat 65:45–56

    Article  PubMed  Google Scholar 

  • Rengel Z, Robinson DL (1989) Competitive Al3+ inhibition of net Mg2+ uptake by intact Lolium multiflorum roots. Plant Physiol 91:1407–1413

    Article  PubMed  CAS  Google Scholar 

  • Ritchien S, Gilroy S (1998) Abscisic acid signal transduction in the barley aleurone is mediated by phospholipase D activity. Proc Natl Acad Sci USA 95:2697–2702

    Article  Google Scholar 

  • Rizzo MA, Shome K, Watkins SC, Romero G (2000) The recruitment of Raf-1 to membranes is mediated by direct interaction with phosphatidic acid and is independent of association with Ras. J Biol Chem 275:23911–23918

    Article  PubMed  CAS  Google Scholar 

  • Ruelland E, Cantrel C, Gawer M, Kader J-C, Zachowski A (2002) Activation of phospholipase C and D is an early response to a cold exposure in Arabidopsis suspension cells. Plant Physiol 130:999–1007

    Article  PubMed  CAS  Google Scholar 

  • Sivaguru M, Ezaki B, He Z-H, Tong H, Osawa H, Balušek F, Volkmann D, Matsumoto H (2003) Aluminum-induced gene expression and protein localization of cell wall-associated receptor kinase in Arabidopsis. Plant Physiol 132:2256–2266

    Article  PubMed  CAS  Google Scholar 

  • Testerink C, Dekker HL, Lim Z-Y, Johns MK, Holmes AB, de Koster CG, Ktistakis NT, Munnik T (2004) Isolation and identification of phosphatidic acid targets from plants. Plant J 39:527–536

    Article  PubMed  CAS  Google Scholar 

  • Testerink C, Munnik T (2005) Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci 10:368–375

    Article  PubMed  CAS  Google Scholar 

  • van der Luit AH, Piatti T, van Doorn A, Musgrave A, Felix G, Boller T, Munnik T (2000) Elicitation of suspension-cultured tomato cells triggers the formation of phosphatidic acid and diacylglycerol pyrophosphate. Plant Physiol 123:1507–1515

    Article  PubMed  Google Scholar 

  • van Himbergen JAJ, ter Riet B, Meijer HJG, van der Ende H, Musgrave A, Munnik T (1999) Mastoparan analogues stimulate phospholipase C- and phospholipase D-activity in Chlamydomonas: a comparative study. J Biol Chem 50:1735–1742

    Google Scholar 

  • van Leeuwen W, Ökrész L, Bögre L, Munnik T (2004) Learning the lipid language of plant signalling. Trends Plant Sci 9:378–384

    Article  PubMed  CAS  Google Scholar 

  • Verstraeten SV, Villaverde MS, Oteiza PI (2003) Al3+-mediated changes on membrane fluidity affects the activity of PI-PLC but not PLC. Chem Phys Lipids 122:159–163

    Article  PubMed  CAS  Google Scholar 

  • Wang X (1999) The role of phospholipase D in Signaling cascades. Plant Physiol 120:645–651

    Article  PubMed  CAS  Google Scholar 

  • Wang X (2001) Plant phospholipases. Annu Rev Plant Physiol Mol Biol 52:211–231

    Article  CAS  Google Scholar 

  • Wang X (2000) Multiple forms of phospholipase D in plants: the gene family, catalytic and regulatory properties, and cellular functions. Prog Lipid Res 39:109–149

    Article  PubMed  CAS  Google Scholar 

  • Zhang W-H, Ryan Peter R, Tyerman SD (2001) Malate-permeable channels and cation channels activated by aluminum in the apical cells of wheat roots. Plant Physiol 125:1459–1472

    Article  PubMed  CAS  Google Scholar 

  • Zhao J, Wang X (2004) Arabidopsis phospholipasa Da1 interacts with the heterotrimeric G-protein a-subunit through a motif with heterotrimeric G-protein a-subunit through a motif analogous to the DRY motif in G-protein-coupled receptors. J Biol Chem 279:1794–1800

    Article  PubMed  CAS  Google Scholar 

  • Zonia L, Munnik T (2004) Osmotically induced cell swelling versus shrinking elicits specific changes in phospholipid signals in tobacco pollen tubes. Plant Physiol 134:813–823

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors thank Rafael Tobeña and Armando Muñoz-Sánchez for their technical assistance. This work was supported by Consejo Nacional de Ciencia y Tecnología grant to SMTH-S (45798-Z) and a fellowship to AR-D (165087). T. Munnik’s lab is financially supported by the Netherlands Organization for Scientific Research (NWO; CW 99002, ALW 863.04.004), The European Commission (HP RN-CT-2002-00251), and the Royal Netherlands Academy of Arts and Sciences (KN AW).

Author information

Authors and Affiliations

  1. Centro de Investigación Científica de Yucatán (CICY), Unidad de Bioquímica y Biología Molecular de Plantas, Calle 43, 130 Col. Chuburná de Hidalgo, 97200, Mérida Yucatán, México

    Ana Ramos-Díaz, Ligia Brito-Argáez & S. M. Teresa Hernández-Sotomayor

  2. Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, Netherlands

    Teun Munnik

Authors
  1. Ana Ramos-Díaz
    View author publications

    Search author on:PubMed Google Scholar

  2. Ligia Brito-Argáez
    View author publications

    Search author on:PubMed Google Scholar

  3. Teun Munnik
    View author publications

    Search author on:PubMed Google Scholar

  4. S. M. Teresa Hernández-Sotomayor
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to S. M. Teresa Hernández-Sotomayor.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ramos-Díaz, A., Brito-Argáez, L., Munnik, T. et al. Aluminum inhibits phosphatidic acid formation by blocking the phospholipase C pathway. Planta 225, 393–401 (2007). https://doi.org/10.1007/s00425-006-0348-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-006-0348-3

Keywords

Profiles

  1. Teun Munnik View author profile