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. 1996 Jun;111(2):459–467. doi: 10.1104/pp.111.2.459

Mastoparan-Induced Intracellular Ca2+ Fluxes May Regulate Cell-to-Cell Communication in Plants.

E B Tucker 1, W F Boss 1
PMCID: PMC157856  PMID: 12226302

Abstract

The relationship of Ca2+ and plasmodesmatal closure was examined in staminal hairs of Setcreasea purpurea by microinjecting cells with active mastoparan (Mas-7), inactive mastoparan (Mas-17), active inositol-1,4,5-trisphosphate (IP3), or inactive IP3. Calcium green dextran 10,000 was used to study cellular free Ca2+, and carboxyfluorescein was used to monitor plasmodesmatal closure. When Mas-7 was microinjected into the cytoplasm of cell 1 (the tip cell of a chain of cells), a rapid increase in calcium green dextran-10,000 fluorescence was observed in the cytoplasmic areas on both sides of the plasmodesmata connecting cells 1 and 2 during the same time that the diffusion of carboxyfluorescein through them was blocked. The inhibition of cell-to-cell diffusion was transient, and the closed plasmodesmata reopened within 30 s. The elevated Ca2+ level near plasmodesmata was also transient and returned to base level in about 1.5 min. The transient increase in Ca2+, once initiated in cell 1, repeated with an oscillatory period of 3 min. Elevated Ca2+ and oscillations of Ca2+ were also observed near interconnecting cell walls throughout the chain of cells, indicating that the signal had been transmitted. Previously, we reported that IP3 closed plasmodesmata; now we report that it stimulated Ca2+ and oscillations similar to Mas-7. The effect was specific for similar concentrations of Mas-7 over Mas-17 and active IP3 over inactive IP3. It is important that the Ca2+ channel blocker La3+ eliminated the responses from Mas-7 and IP3, indicating that an influx of Ca2+ was required. These results support the contention that plasmodesmata functioning is regulated via Ca2+ and that IP3 may be an intermediary between the stimulus and Ca2+ elevations.

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Selected References

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  1. Allan A. C., Fricker M. D., Ward J. L., Beale M. H., Trewavas A. J. Two Transduction Pathways Mediate Rapid Effects of Abscisic Acid in Commelina Guard Cells. Plant Cell. 1994 Sep;6(9):1319–1328. doi: 10.1105/tpc.6.9.1319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Allbritton N. L., Meyer T. Localized calcium spikes and propagating calcium waves. Cell Calcium. 1993 Nov;14(10):691–697. doi: 10.1016/0143-4160(93)90095-n. [DOI] [PubMed] [Google Scholar]
  3. Boitano S., Dirksen E. R., Sanderson M. J. Intercellular propagation of calcium waves mediated by inositol trisphosphate. Science. 1992 Oct 9;258(5080):292–295. doi: 10.1126/science.1411526. [DOI] [PubMed] [Google Scholar]
  4. Citovsky V. Probing Plasmodesmal Transport with Plant Viruses. Plant Physiol. 1993 Aug;102(4):1071–1076. doi: 10.1104/pp.102.4.1071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Davies E. Intercellular and intracellular signals and their transduction via the plasma membrane-cytoskeleton interface. Semin Cell Biol. 1993 Apr;4(2):139–147. doi: 10.1006/scel.1993.1017. [DOI] [PubMed] [Google Scholar]
  6. Drøbak B. K., Ferguson I. B. Release of Ca2+ from plant hypocotyl microsomes by inositol-1,4,5-trisphosphate. Biochem Biophys Res Commun. 1985 Aug 15;130(3):1241–1246. doi: 10.1016/0006-291x(85)91747-4. [DOI] [PubMed] [Google Scholar]
  7. Drøbak B. K., Watkins P. A. Inositol(1,4,5)trisphosphate production in plant cells: stimulation by the venom peptides, melittin and mastoparan. Biochem Biophys Res Commun. 1994 Nov 30;205(1):739–745. doi: 10.1006/bbrc.1994.2727. [DOI] [PubMed] [Google Scholar]
  8. Gilroy S., Bethke P. C., Jones R. L. Calcium homeostasis in plants. J Cell Sci. 1993 Oct;106(Pt 2):453–461. doi: 10.1242/jcs.106.2.453. [DOI] [PubMed] [Google Scholar]
  9. Jaffe L. F. Classes and mechanisms of calcium waves. Cell Calcium. 1993 Nov;14(10):736–745. doi: 10.1016/0143-4160(93)90099-r. [DOI] [PubMed] [Google Scholar]
  10. Johnson C. H., Knight M. R., Kondo T., Masson P., Sedbrook J., Haley A., Trewavas A. Circadian oscillations of cytosolic and chloroplastic free calcium in plants. Science. 1995 Sep 29;269(5232):1863–1865. doi: 10.1126/science.7569925. [DOI] [PubMed] [Google Scholar]
  11. Knight M. R., Read N. D., Campbell A. K., Trewavas A. J. Imaging calcium dynamics in living plants using semi-synthetic recombinant aequorins. J Cell Biol. 1993 Apr;121(1):83–90. doi: 10.1083/jcb.121.1.83. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Legendre L., Yueh Y. G., Crain R., Haddock N., Heinstein P. F., Low P. S. Phospholipase C activation during elicitation of the oxidative burst in cultured plant cells. J Biol Chem. 1993 Nov 25;268(33):24559–24563. [PubMed] [Google Scholar]
  13. McAinsh M. R., Brownlee C., Hetherington A. M. Visualizing Changes in Cytosolic-Free Ca2+ during the Response of Stomatal Guard Cells to Abscisic Acid. Plant Cell. 1992 Sep;4(9):1113–1122. doi: 10.1105/tpc.4.9.1113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. McAinsh M. R., Webb AAR., Taylor J. E., Hetherington A. M. Stimulus-Induced Oscillations in Guard Cell Cytosolic Free Calcium. Plant Cell. 1995 Aug;7(8):1207–1219. doi: 10.1105/tpc.7.8.1207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Mushegian A. R., Koonin E. V. The proposed plant connexin is a protein kinase-like protein. Plant Cell. 1993 Sep;5(9):998–999. doi: 10.1105/tpc.5.9.998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Oparka K. J. Signalling via plasmodesmata--the neglected pathway. Semin Cell Biol. 1993 Apr;4(2):131–138. doi: 10.1006/scel.1993.1016. [DOI] [PubMed] [Google Scholar]
  17. Pethig R., Kuhn M., Payne R., Adler E., Chen T. H., Jaffe L. F. On the dissociation constants of BAPTA-type calcium buffers. Cell Calcium. 1989 Oct;10(7):491–498. doi: 10.1016/0143-4160(89)90026-2. [DOI] [PubMed] [Google Scholar]
  18. Quarmby L. M., Hartzell H. C. Two distinct, calcium-mediated, signal transduction pathways can trigger deflagellation in Chlamydomonas reinhardtii. J Cell Biol. 1994 Mar;124(5):807–815. doi: 10.1083/jcb.124.5.807. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Rooney T. A., Thomas A. P. Intracellular calcium waves generated by Ins(1,4,5)P3-dependent mechanisms. Cell Calcium. 1993 Nov;14(10):674–690. doi: 10.1016/0143-4160(93)90094-m. [DOI] [PubMed] [Google Scholar]
  20. Sanderson M. J., Charles A. C., Boitano S., Dirksen E. R. Mechanisms and function of intercellular calcium signaling. Mol Cell Endocrinol. 1994 Jan;98(2):173–187. doi: 10.1016/0303-7207(94)90136-8. [DOI] [PubMed] [Google Scholar]
  21. Sanderson M. J. Intercellular calcium waves mediated by inositol trisphosphate. Ciba Found Symp. 1995;188:175–194. [PubMed] [Google Scholar]
  22. Schumaker K. S., Sze H. Inositol 1,4,5-trisphosphate releases Ca2+ from vacuolar membrane vesicles of oat roots. J Biol Chem. 1987 Mar 25;262(9):3944–3946. [PubMed] [Google Scholar]
  23. Tucker J. E., Mauzerall D., Tucker E. B. Symplastic Transport of Carboxyfluorescein in Staminal Hairs of Setcreasea purpurea Is Diffusive and Includes Loss to the Vacuole. Plant Physiol. 1989 Jul;90(3):1143–1147. doi: 10.1104/pp.90.3.1143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Yueh Y. G., Crain R. C. Deflagellation of Chlamydomonas reinhardtii follows a rapid transitory accumulation of inositol 1,4,5-trisphosphate and requires Ca2+ entry. J Cell Biol. 1993 Nov;123(4):869–875. doi: 10.1083/jcb.123.4.869. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Yule D. I., Williams J. A. Mastoparan induces oscillations of cytosolic Ca2+ in rat pancreatic acinar cells. Biochem Biophys Res Commun. 1991 May 31;177(1):159–165. doi: 10.1016/0006-291x(91)91962-c. [DOI] [PubMed] [Google Scholar]

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