Skip to main content
Log in

Phospholipid and phospholipase changes by jasmonic acid during stolon to tuber transition of potato

  • Original Paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Potato tuber formation starts with the stolon swelling and is regulated by jasmonates. The cascade of events leading to tuber formation is not completely understood. The aim of this study was to evaluate phospholipid composition and phospholipase activities during four stages of stolon-to-tuber transition of Solanum tuberosum L., cv. Spunta, and involvement of phosphatidic acid (PA) in stolon cell expansion during early stages. Effects of jasmonic acid (JA) treatment on phospholipid content and activation of phospholipase D (PLD) (EC 3.1.4.4) and phosphatidylinositol-4,5-bisphosphate-specific phospholipase C (PIP2-PLC) (EC 3.1.4.3) were studied in the early stages (first stage, hooked apex stolon; second stage, initial swelling stolon) of tuberization. All the phospholipid species identified, phosphatidylinositol (PI), phosphatidylserine (PS), phosphatidylcholine (PC), phosphatidylethanolamine (PE), phosphatidylglycerol (PG), PA, and cardiolipin (CL), decreased as tuber formation progressed. PLD and PLC were activated in control tissues at an early stage. JA treatment caused a decrease of PC and PS in first stage stolons, accumulation of PA in second stage stolons, and modification of PLD and PLC activities. PA increased stolon cell area in the first and second stages. These findings indicate that phospholipid catabolism is activated from the early stages of tuber formation, and that JA treatment modifies the pattern of phospholipid (PC, PS, and PA) composition and phospholipase (PLD and PLC) activity. These phospholipids therefore may play a role in activation of an intracellular mechanism that switches the developmental fate of stolon meristem cells, causing differentiation into a tuber.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

Abbreviations

CL:

Cardiolipin

JA:

Jasmonic acid

PA:

Phosphatidic acid

PC:

Phosphatidylcholine

PE:

Phosphatidylethanolamine

PG:

Phosphatidylglycerol

PI:

Phosphatidylinositol

PIP2 :

Phosphatidylinositol-4,5-bisphosphate

PIP2-PLC:

Phosphatidylinositol-4,5-bisphosphate specific phospholipase C

PS:

Phosphatidylserine

PLD:

Phospholipase D

All solvent proportions are by volume

References

  • Abdala G, Castro G, Guiñazú M, Tizio R, Miersch O (1996) Occurrence of jasmonic acid in organs of Solanum tuberosum L. and its effect on tuberization. Plant Growth Regul 19:139–143. doi:10.1007/BF00024580

    Article  CAS  Google Scholar 

  • Abdala G, Castro G, Miersch O, Pearce D (2002) Changes in jasmonates and gibberellins during development of potato plant (Solanum tuberosum L.). Plant Growth Regul 36:121–126. doi:10.1023/A:1015065011536

    Article  CAS  Google Scholar 

  • Bligh E, Dyer W (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–918

    PubMed  CAS  Google Scholar 

  • Cenzano A, Vigliocco A, Kraus T, Abdala G (2003) Exogenously applied jasmonic acid induces changes in apical meristem morphology of potato stolons. Ann Bot (Lond) 91:917–921. doi:10.1093/aob/mcg098

    Article  CAS  Google Scholar 

  • Cenzano A, Vigliocco A, Miersch O, Abdala G (2006) Octadecanoid levels during stolon to tuber transition in potato. Potato Res 48:107–115. doi:10.1007/BF02742370

    Article  Google Scholar 

  • Chapman KD (1998) Phospholipase activity during plant growth and development and in response to environmental stress. Trends Plant Sci 3:419–426. doi:10.1016/S1360-1385(98)01326-0

    Article  Google Scholar 

  • Cowan AK (2006) Phospholipids as plant growth regulators. Plant Growth Regul 48:97–109. doi:10.1007/s10725-005-5481-7

    Article  CAS  Google Scholar 

  • D’ Ambrogio de Argüeso A (1986) Capítulo I: Parte general. In: D’ Ambrogio de Argüeso A (ed) Manual de técnicas en histología vegetal. Hemisferio Sur, Buenos Aires, Argentina, pp 5–12

    Google Scholar 

  • Dhonukshe P, Laxalt AM, Goedhart J, Gadella TWJ, Munnik T (2003) Phospholipase D activation correlates with microtubule reorganization in living cells. Plant Cell 15:2666–2679. doi:10.1105/tpc.014977

    Article  PubMed  CAS  Google Scholar 

  • Dobson G, Griffiths DW, Davies HV, McNicol JW (2004) Comparison of fatty acid and polar lipid contents of tubers from two potato species, Solanum tuberosum and Solanum phureja. J Agric Food Chem 52:6306–6314. doi:10.1021/jf049692r

    Article  PubMed  CAS  Google Scholar 

  • Fiske G, Subbarow J (1925) The colorimetric determination of phosphorus. J Biol Chem 66:375–400

    CAS  Google Scholar 

  • Helder H, Miersch O, Vreugdenhil D, Sembdner G (1993) Ocurrence of hydroxylated jasmonic acids in leaflets of Solanum demissum plants grown under long- and short-days conditions. Physiol Plant 88:647–653. doi:10.1111/j.1399-3054.1993.tb01384.x

    Article  CAS  Google Scholar 

  • Hernández-Sotomayor SMT, De Los Santos-Briones C, Muñoz-Sánchez JA, Loyola-Vargas VM (1999) Kinetic analysis of phospholipase C from Catharanthus roseus transformed roots using different assays. Plant Physiol 120:1075–1081. doi:10.1104/pp.120.4.1075

    Article  PubMed  Google Scholar 

  • Hirschberg HJHB, Simons JWFA, Dekker N, Egmond MA (2001) Cloning, expression, purification and characterization of patatin, a novel phospholipase A. Eur J Biochem 268:5037–5044. doi:10.1046/j.0014-2956.2001.02411.x

    Article  PubMed  CAS  Google Scholar 

  • Ishiguro S, Kawai-Oda A, Ueda J, Nishida I, Okada K (2001) The defective in anther dehiscence1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13:2191–2209

    Article  PubMed  CAS  Google Scholar 

  • Jackson SD (1999) Multiple signaling pathways control tuber induction in potato. Plant Physiol 119:1–8. doi:10.1104/pp.119.1.1

    Article  PubMed  CAS  Google Scholar 

  • Johansen DA (1940) Plant microtechnique. McGraw-Hill Book Company, Inc, New York

    Google Scholar 

  • Jung KM, Kim DK (2000) Purification and characterization of a membrane-associated 48-kilodalton phospholipase A2 in leaves of broad bean. Plant Physiol 123:1057–1068. doi:10.1104/pp.123.3.1057

    Article  PubMed  CAS  Google Scholar 

  • Kirchner JG (1978) Detection of colorless compounds. In: Weissberger A (ed) Techniques of chemistry. Thin layer chromatography, vol 14. Wiley-Interscience Publishers, USA, pp 193–264

    Google Scholar 

  • Koda Y (1997) Possible involvement of jasmonates in various morphogenic events. Physiol Plant 100:639–646. doi:10.1111/j.1399-3054.1997.tb03070.x

    Article  CAS  Google Scholar 

  • Koda Y, Omer EA, Yoshihara T, Shibata H, Sakamura S, Okazawa Y (1988) Isolation of a specific potato tuber-inducing substance from potato leaves. Plant Cell Physiol 29:969–974

    CAS  Google Scholar 

  • Koda Y, Kikuta Y, Tazaki H, Tsujino Y, Sakamura S, Toshihara T (1991) Potato tuber-inducing activities of jasmonic acid and related compounds. Phytochemistry 30:1435–1438. doi:10.1016/0031-9422(91)84180-Z

    Article  CAS  Google Scholar 

  • Lee S, Suh S, Kim S, Crain CR, Kwak JM, Nam HG et al (1997) Systemic elevation of phosphatidic acid and lysophospholipid levels in wounded plants. Plant J 12:547–556. doi:10.1046/j.1365-313X.1997.00547.x

    Article  CAS  Google Scholar 

  • Lloyd C, Hussey P (2001) Microtubule-associated proteins in plants: why we need a MAP. Nat Rev Mol Cell Biol 2:40–47. doi:10.1038/35048005

    Article  PubMed  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 metabolism from the phosphoinositide pathway in Coffea Arabica cells. J Plant Physiol 160:1297–1303. doi:10.1078/0176-1617-01168

    Article  PubMed  Google Scholar 

  • Matsuki T, Tazaki H, Fujimori T, Hogetsu T (1992) The influences of jasmonic acid methyl ester on microtubules in potato cells and formation of potato tubers. Biosci Biotechnol Biochem 56:1329–1330

    Article  CAS  Google Scholar 

  • Munnik T (2001) Phosphatidic acid: an emerging plant lipid second messenger. Trends Plant Sci 6:227–233. doi:10.1016/S1360-1385(01)01918-5

    Article  PubMed  CAS  Google Scholar 

  • Munnik T, Irvine RF, Musgrave A (1998) Phospholipid signalling in plants. Biochim Biophys Acta 1389:222–272

    PubMed  CAS  Google Scholar 

  • Novotná Z, Martinec J, Profotová B, Ždárová Š, Kader J-C, Valentová O (2003) In vitro distribution and characterization of membrane-associated PLD and PI-PLC in Brassica napus. J Exp Bot 54:691–698. doi:10.1093/jxb/erg070

    Article  PubMed  CAS  Google Scholar 

  • O’Brien TP, Mc Cully ME (1981) Chapter 4: anatomical methods. In: O’Brien TP, Mc Cully ME (eds) The study of plant structure: principles and selected methods. Termacarphi Pty Ltd, Melbourne, Australia, pp 4.1–4.55

    Google Scholar 

  • Potocký M, Elías M, Profotová B, Novotná Z, Valentová O, Zárský V (2003) Phosphatidic acid produced by phospholipase D is required for tobacco pollen tube growth. Planta 217:122–130

    PubMed  Google Scholar 

  • Prat S (2004) Hormonal and daylength control of potato tuberization. In: Davies PJ (ed) Plant hormones: biosynthesis, signal transduction, action. Kluwer Academic Publishers, The Netherlands, pp 538–560

    Google Scholar 

  • Racagni G, García de Lema M, Domenech CE, Machado de Domenech EE (1992) Phospholipids in Trypanosoma cruzi: phosphoinositide composition and turnover. Lipids 27:275–278. doi:10.1007/BF02536475

    Article  PubMed  CAS  Google Scholar 

  • Racusen D, Foote M (1980) A major soluble glycoprotein of potato tubers. J Food Biochem 4:43–52. doi:10.1111/j.1745-4514.1980.tb00876.x

    Article  CAS  Google Scholar 

  • Regente M, Corti Monzón G, de la Canal L (2008) Phospholipids are present in extracellular fluids of imbibing sunflower seeds and are modulated by hormonal treatments. J Exp Bot 59:553–562. doi:10.1093/jxb/erm329

    Article  PubMed  CAS  Google Scholar 

  • Ryu SB (2004) Phospholipid-derived signaling mediated by phospholipase A in plants. Trends Plant Sci 9:229–235. doi:10.1016/j.tplants.2004.03.004

    Article  PubMed  CAS  Google Scholar 

  • Ryu BS, Wang X (1998) Increase in free linolenic and linoleic acids associated with phospholipase D-mediated hydrolysis of phospholipids in wounded castor bean leaves. Biochim Biophys Acta 1393:193–202

    PubMed  CAS  Google Scholar 

  • Schaller F, Schaller A, Stintzi A (2005) Biosynthesis and metabolism of jasmonates. J Plant Growth Regul 23:179–199

    Google Scholar 

  • Senda K, Yoshioka H, Doke N, Kawakita K (1996) A cytosolic phospholipase A2 from potato tissues appears to be patatin. Plant Cell Physiol 37:347–353

    PubMed  CAS  Google Scholar 

  • Shewry P (2003) Tuber storage proteins. Ann Bot (Lond) 91:755–769. doi:10.1093/aob/mcg084

    Article  CAS  Google Scholar 

  • Shibaoka H (1994) Plant hormone-induced changes in the orientation of cortical microtubules. Annu Rev Plant Physiol Plant Mol Biol 45:527–544

    CAS  Google Scholar 

  • Van der Luit AH, Piatti T, van Doorn A, Musgrave A, Felix G, Boller T et al (2000) Elicitation of suspension-cultured tomato cells triggers the formation of phosphatidic acid and diacylglycerol pryrophosphate. Plant Physiol 123:1507–1516. doi:10.1104/pp.123.4.1507

    Article  PubMed  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. doi:10.1016/S0163-7827(00)00002-3

    Article  PubMed  CAS  Google Scholar 

  • Wang X (2001) Plant phospholipases. Annu Rev Plant Physiol Plant Mol Biol 52:211–231. doi:10.1146/annurev.arplant.52.1.211

    Article  PubMed  CAS  Google Scholar 

  • Wang X (2002) Phospholipase D in hormonal and stress signalling. Curr Opin Plant Biol 5:408–414. doi:10.1016/S1369-5266(02)00283-2

    Article  PubMed  CAS  Google Scholar 

  • Wang X, Wang C, Sang Y, Qin C, Welti R (2002) Networking of phospholipases in plant signal transduction. Physiol Plant 115:331–335. doi:10.1034/j.1399-3054.2002.1150301.x

    Article  PubMed  CAS  Google Scholar 

  • Xu X, Vreugdenhil D, van Lammeren AAM (1998) Cell division and cell enlargement during potato tuber formation. J Exp Bot 320:573–582. doi:10.1093/jexbot/49.320.573

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from SECYT-UNRC and CONICET to G.A., and fellowships from CONICET to A.C.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ana Cenzano.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cenzano, A., Cantoro, R., Racagni, G. et al. Phospholipid and phospholipase changes by jasmonic acid during stolon to tuber transition of potato. Plant Growth Regul 56, 307–316 (2008). https://doi.org/10.1007/s10725-008-9311-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-008-9311-6

Keywords

Navigation