Skip to main content
SpringerLink
Log in

A phosphatidylinositol phosphate-specific myo-inositol polyphosphate 5-phosphatase required for seedling growth

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

The phosphatidylinositol phosphate signaling pathway is involved in many crucial cellular functions. The myo-inositol polyphosphate 5-phosphatases (5PTases) (E.C. 3.1.3.56) comprise a large protein family that hydrolyze 5-phosphates from a variety of phosphatidylinositol phosphate and inositol phosphate substrates. We previously reported that the At5PTase11 enzyme (At1g47510), which is one of the smallest predicted 5PTases found in any organism, encodes an active 5PTase whose activity is restricted to tris- and bis-, but not mono-phosphorylated phosphatidylinositol phosphate substrates containing a 5-phosphate. This is in contrast to other unrestricted Arabidopsis 5PTases, which also hydrolyze tris- and bis inositol phosphate molecules. To further explore the function of At5PTase11, we have characterized two T-DNA mutants in the At5PTase11 gene, and have complemented this mutant. Seed from 5ptase11 mutants germinate slower than wildtype seed and mutant seedlings have decreased hypocotyl growth as compared to wildtype seedlings when grown in the dark. This phenotype is the opposite of the increased hypocotyl growth phenotype previously described for other 5ptase mutants defective in inositol phosphate-specific 5PTase enzymes. By labeling the endogenous myo-inositol pool in 5ptase11 mutants, we correlated these hypocotyl growth changes with a small increase in the 5PTase11 substrate, phosphatidylinositol (4,5) bisphosphate, and decreases in the potential products of 5PTase11, phosphatidylinositol (3) phosphate and phosphatidylinositol (4) phosphate. Surprisingly, we also found that dark-grown 5ptase11 mutants contain increases in inositol (1,4,5) trisphosphate and an inositol bisphosphate that is not a substrate for recombinant 5PTase11. We present a model for regulation of hypocotyl growth by specific molecules found in this pathway.

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

Access this article

Log in via an institution

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
Fig. 9
Fig. 10

Similar content being viewed by others

Abbreviations

PtdIns:

Phosphatidylinositol

PtdInsP:

Phosphatidylinositol phosphate

PtdIns(4,5)P2 :

PtdIns(4,5) bisphosphate

InsP:

Inositol phosphate

Ins(1,4,5)P3 :

Inositol 1,4,5-trisphosphate

5Ptases:

Myo-inositol polyphosphate 5-phosphatases

WT:

Wildtype

MS:

Murashige and Skoog

HPLC:

High performance liquid chromatography

References

  • Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, Gadrinab C, Heller C, Jeske A, Koesema E, Meyers CC, Parker H, Prednis L, Ansari Y, Choy N, Deen H, Geralt M, Hazari N, Hom E, Karnes M, Mulholland C, Ndubaku R, Schmidt I, Guzman P, Aguilar-Henonin L, Schmid M, Weigel D, Carter DE, Marchand T, Risseeuw E, Brogden D, Zeko A, Crosby WL, Berry CC, Ecker JR (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657

    Article  PubMed  Google Scholar 

  • An Y, McDowell J, Huang S, McKinney E, Chambliss S, Meagher R (1996) Strong, constitutive expression of the Arabidopsis ACT2/ACT8 actin subclass vegetative tissues. Plant J 10:107–2121

    Article  PubMed  CAS  Google Scholar 

  • Astle MV, Horan KA, Ooms LM, Mitchell CA (2007) The inositol polyphosphate 5-phosphatases: traffic controllers, waistline watchers and tumour suppressors? Biochem Soc Symp 74:161–181

    Article  PubMed  CAS  Google Scholar 

  • Augert G, Blackmore PF, Exton JH (1989) Changes in the concentration and fatty acid composition of phosphoinositides induced by hormones in hepatocytes. J Biol Chem 264(5):2574–2580

    PubMed  CAS  Google Scholar 

  • Bechtold N, Ellis J, Pelletier G (1993) In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants. C R Acad Sci Ser III, Sci Vie 316:1194–1199

    CAS  Google Scholar 

  • Berdy S, Kudla J, Gruissem W, Gillaspy G (2001) Molecular characterization of At5PTase1, an inositol phosphatase capable of terminating IP3 signaling. Plant Physiol 126:801–810

    Article  PubMed  CAS  Google Scholar 

  • Berridge MJ (1993) Inositol trisphosphate and calcium signaling. Nature 361:315–325

    Article  PubMed  CAS  Google Scholar 

  • Bertelli DF, Araujo EP, Cesquini M, Stoppa GR, Gasparotto-Contessotto M, Toyama MH, Felix JV, Carvalheira JB, Michelini LC, Chiavegatto S, Boschero AC, Saad MJ, Lopes-Cendes I, Velloso LA (2006) Phosphoinositide-specific inositol polyphosphate 5-phosphatase IV inhibits inositide trisphosphate accumulation in hypothalamus and regulates food intake and body weight. Endocrinology 147:5385–5399

    Article  PubMed  CAS  Google Scholar 

  • Burnette RN, Gunesekera BM, Gillaspy GE (2003) An Arabidopsis inositol 5-phosphatase gain-of-function alters abscisic acid signaling. Plant Physiol 132:1011–1019

    Article  PubMed  CAS  Google Scholar 

  • Carland FM, Nelson T (2004) Cotyledon vascular pattern 2-mediated inositol (1,4,5) triphosphate signal transduction is essential for closed venation patterns of Arabidopsis foliar organs. Plant Cell 16:1263–1275

    Article  PubMed  CAS  Google Scholar 

  • Challiss RA, Chilvers ER, Willcocks AL, Nahorski SR (1990) Heterogeneity of [3H]inositol 1,4,5-trisphosphate binding sites in adrenal-cortical membranes characterization and validation of a radioreceptor assay. Biochem J 265:421–427

    PubMed  CAS  Google Scholar 

  • Chen X, Lin WH, Wang Y, Luan S, Xue HW (2008) An inositol polyphosphate 5-phosphatase functions in PHOTOTROPIN1 signaling in Arabidopsis by altering cytosolic Ca2+. Plant Cell (In press)

  • Cutler SR, Ehrhardt DW, Griffitts JS, Somerville CR (2000) Random GFP::cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. PNAS 97:3718–3723

    Article  PubMed  CAS  Google Scholar 

  • DeWald DB, Torabinejad J, Jones CA, Shope JC, Cangelosi AR, Thompson JE, Prestwich GD, Hama H (2001) Rapid accumulation of phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate correlates with calcium mobilization in salt-stressed Arabidopsis. Plant Physiol 126:759–769

    Article  PubMed  CAS  Google Scholar 

  • Dowd PE, Coursol S, Skirpan AL, Kao TH, Gilroy S (2006) Petunia phospholipase c1 is involved in pollen tube growth. Plant Cell 18:1438–1453

    Article  PubMed  CAS  Google Scholar 

  • Ercetin ME, Gillaspy GE (2004) Molecular characterization of an Arabidopsis gene encoding a phospholipid-specific inositol polyphosphate 5-phosphatase. Plant Physiol 135:938–946

    Article  PubMed  CAS  Google Scholar 

  • Gunesekera B, Torabinejad J, Robinson J, Gillaspy GE (2007) Inositol polyphosphate 5-phosphatases 1 and 2 are required for regulating seedling growth. Plant Physiol 143:1408–1417

    Article  PubMed  CAS  Google Scholar 

  • Hama H, Takemoto JY, DeWald DB (2000) Analysis of phosphoinositides in protein trafficking. Methods 20:465–473

    Article  PubMed  CAS  Google Scholar 

  • Hama H, Torabinejad J, Prestwich GD, DeWald DB (2004) Measurement and immunofluorescence of cellular phosphoinositides. Methods Mol Biol 284:243–258

    PubMed  CAS  Google Scholar 

  • Helling D, Possart A, Cottier S, Klahre U, Kost B (2006) Pollen tube tip growth depends on plasma membrane polarization mediated by tobacco PLC3 activity and endocytic membrane recycling. Plant Cell 18:3519–3534

    Article  PubMed  CAS  Google Scholar 

  • Im YJ, Perera IY, Brglez I, Davis AJ, Stevenson-Paulik J, Phillippy BQ, Johannes E, Allen NS, Boss WF (2007) Increasing plasma membrane phosphatidylinositol(4,5)bisphosphate biosynthesis increases phosphoinositide metabolism in Nicotiana tabacum. Plant Cell 19(5):1603–1616

    Article  PubMed  CAS  Google Scholar 

  • Kisseleva MV, Wilson MP, Majerus PW (2000) The isolation and characterization of a cDNA encoding phospholipid-specific inositol polyphosphate 5-phosphatase. J Biol Chem 275:20110–20116

    Article  PubMed  CAS  Google Scholar 

  • Kisseleva MV, Cao L, Majerus PW (2002) Phosphoinositide-specific inositol polyphosphate 5-phosphatase IV inhibits Akt/protein kinase B phosphorylation and leads to apoptotic cell death. J Biol Chem 277:6266–6272

    Article  PubMed  CAS  Google Scholar 

  • König S, Mosblech A, Heilmann I (2007) Stress-inducible and constitutive phosphoinositide pools have distinctive fatty acid patterns in Arabidopsis thaliana. FASEB J 21:1958–1967

    Article  PubMed  CAS  Google Scholar 

  • Kost B, Lemichez E, Spielhofer P, Hong Y, Tolias K, Carpenter C, Chua NH (1999) Rac homologues and compartmentalized phosphatidylinositol 4,5-bisphosphate act in a common pathway to regulate polar pollen tube growth. J Cell Biol 19:317–330

    Article  Google Scholar 

  • Kusano H, Testerink C, Vermeer JE, Tsuge T, Shimada H, Oka A, Munnik T, Aoyama T (2008) The Arabidopsis phosphatidylinositol phosphate 5-kinase PIP5K3 is a key Regulator of Root Hair Tip Growth. Plant Cell (In press)

  • Lanzetta PA, Alvarez LJ, Reinach PS, Candia OA (1979) An improved assay for nanomole amounts of inorganic phosphate. Anal Biochem 100:95–97

    Article  PubMed  CAS  Google Scholar 

  • Meijer HJ, Munnik TM (2003) Phospholipid-based signaling in plants. Annu Rev Plant Biol 54:265–306

    Article  PubMed  CAS  Google Scholar 

  • Meijer H, Divecha N, van den Ende H, Musgrave A, Munnik T (1999) Hyperosmostic stress induces rapid synthesis of phosphatidyl-d-inositol 3,5-bisphosphate in plant cells. Planta 208:294–298

    Article  CAS  Google Scholar 

  • Meijer HJ, Berrie CP, Iurisci C, Divecha N, Musgrave A, Munnik T (2001) Identification of a new polyphosphoinositide in plants, phosphatidylinositol 5-monophosphate (PtdIns5P), and its accumulation upon osmotic stress. Biochem J 360:491–498

    Article  PubMed  CAS  Google Scholar 

  • Perera IY, Love J, Heilmann I, Thompson WF, Boss WF (2002) Up-regulation of phosphoinositide metabolism in tobacco cells constitutively expressing the human type I inositol polyphosphate 5-phosphatase. Plant Physiol 129:1795–1806

    Article  PubMed  CAS  Google Scholar 

  • Preuss ML, Schmitz AJ, Thole JM, Bonner HK, Otegui MS, Nielsen E (2006) A role for the RabA4b effector protein PI-4Kbeta1 in polarized expansion of root hair cells in Arabidopsis thaliana. J Cell Biol 172(7):991–998

    Article  PubMed  CAS  Google Scholar 

  • Sanchez JP, Chua NH (2001) Arabidopsis PLC1 is required for secondary responses to abscisic acid signals. Plant Cell 13:1143–1154

    Article  PubMed  CAS  Google Scholar 

  • Schmid AC, Wise HM, Mitchell CA, Nussbaum R, Woscholski R (2004) Type II phosphoinositide 5-phosphatases have unique sensitivities towards fatty acid composition and head group phosphorylation. FEBS Lett 576:9–13

    Article  PubMed  CAS  Google Scholar 

  • Schneider A, Hausler RE, Kolukisaoglu U, Kunze R, van der Graaff E, Schwacke R, Catoni E, Desimone M, Flugge UI (2002) An Arabidopsis thaliana knock-out mutant of the chloroplast triose phosphate/phosphate translocator is severely compromised only when starch synthesis, but not starch mobilisation is abolished. Plant J 32:685–699

    Article  PubMed  CAS  Google Scholar 

  • Stenzel I, Ischebeck T, König S, Holubowska A, Sporysz M, Hause B, Heilmann I (2008) The type B phosphatidylinositol-4-phosphate 5-kinase 3 is essential for root hair formation in Arabidopsis thaliana. Plant Cell 20:124–141

    Article  PubMed  CAS  Google Scholar 

  • Stevenson JM, Perera IY, Heilmann II, Persson S, Boss WF (2000) Inositol signaling and plant growth. Trends Plant Sci 5:357

    Article  PubMed  Google Scholar 

  • Thole JM, Vermeer JE, Zhang Y, Gadella TW Jr, Nielsen E (2008) ROOT HAIR DEFECTIVE4 encodes a phosphatidylinositol-4-phosphate phosphatase required for proper root hair development in Arabidopsis thaliana. Plant Cell (In press)

  • Toker A (1998) The synthesis and cellular roles of phosphatidylinositol 4,5-bisphosphate. Curr Opin Cell Biol 10:254–261

    Article  PubMed  CAS  Google Scholar 

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

    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

    Article  PubMed  CAS  Google Scholar 

  • Williams ME, Torabinejad J, Cohick E, Parker K, Drake EJ, Thompson JE, Hortter M, Dewald DB (2005) Mutations in the Arabidopsis phosphoinositide phosphatase gene SAC9 lead to overaccumulation of PtdIns(4,5)P2 and constitutive expression of the stress-response pathway. Plant Physiol 138:686–700

    Article  PubMed  CAS  Google Scholar 

  • Zhong R, Ye ZH (2004) Molecular and biochemical characterization of three WD-repeat-domain-containing inositol polyphosphate 5-phosphatases in Arabidopsis thaliana. Plant Cell Physiol 45:1720–1728

    Article  PubMed  CAS  Google Scholar 

  • Zhong R, Burk DH, Morrison WH 3rd, Ye ZH (2004) FRAGILE FIBER3, an Arabidopsis gene encoding a type II inositol polyphosphate 5-phosphatase, is required for secondary wall synthesis and actin organization in fiber cells. Plant Cell 16:3242–3259

    Article  PubMed  CAS  Google Scholar 

  • Zhong R, Burk DH, Nairn CJ, Wood-Jones A, Morrison WH 3rd, Ye ZH (2005) Mutation of SAC1, an Arabidopsis SAC domain phosphoinositide phosphatase, causes alterations in cell morphogenesis, cell wall synthesis, and actin organization. Plant Cell 17:1449–1466

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W (2004) GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 136:2621–2632

    Article  PubMed  CAS  Google Scholar 

  • Zonia L, Munnik T (2006) Cracking the green paradigm: functional coding of phosphoinositide signals in plant stress responses. Subcell Biochem 39:207–237

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

This work is dedicated to the memory of Ryan Christopher Clark. We are grateful to SIGnAL and the Arabidopsis Biological Resource Center for supplying mutant seeds, to Ryan Burnette for assistance in isolating mutants and to Janet Donahue for technical assistance. This work was supported by an award from the USDA (2003-35318-13690) and NSF (MCB0641954) to G.E.G. and by Hatch project (no. VA-135583).

Author information

Authors and Affiliations

  1. Department of Biochemistry, Virginia Tech, 542 Latham Hall, Blacksburg, VA, 24061, USA

    Mustafa E. Ercetin, Elitsa A. Ananieva, Natasha M. Safaee, Javad Torabinejad, Jamille Y. Robinson & Glenda E. Gillaspy

Authors
  1. Mustafa E. Ercetin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elitsa A. Ananieva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Natasha M. Safaee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Javad Torabinejad
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jamille Y. Robinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Glenda E. Gillaspy
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Glenda E. Gillaspy.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplemental Fig. 1

Genvestigator expression analysis of At5PTase11. Data from the Genvestigator web site was analyzed and plotted. Note that only NASC data from the 8k array chip and the indicated tissues is available, and that the highest expression level noted (leaf) is only slightly above the general background level specified by Genvestigator (TIF 33823 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ercetin, M.E., Ananieva, E.A., Safaee, N.M. et al. A phosphatidylinositol phosphate-specific myo-inositol polyphosphate 5-phosphatase required for seedling growth. Plant Mol Biol 67, 375–388 (2008). https://doi.org/10.1007/s11103-008-9327-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-008-9327-3

Keywords

Search

Navigation