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IN BRIEF

Arabidopsis Synaptotagmin1 Maintains Plasma Membrane Integrity

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The plasma membrane is the selectively permeable lipid bilayer that surrounds living cells. It contains a wide variety of proteins and lipids and is not merely a passive barrier, but a dynamic entity that plays an active role in regulating cellular transport and signaling. As one of the first points of contact for environmental signals impinging upon the cell, the plasma membrane plays an important role in stress responses. This is of particular relevance in plants, which cannot move or take shelter from potentially damaging environmental conditions.

Animal cells undergo frequent disruptions to the plasma membrane (e.g., skeletal and cardiac muscle cells), and the plasma membrane of animal cells can rapidly reseal disrupted sites in a tightly regulated process that is dependent on extracellular Ca²⁺ (McNeil and Kirchhausen, 2005). Synaptotagmins are a family of membrane trafficking proteins that function as Ca²⁺ sensors in a number of SNARE-dependent plasma membrane vesicle fusion processes, such as resealing, exocytosis, and neurotransmitter release (Lynch et al., 2007). Synaptotagmin homologs have been identified in plants (Craxton, 2004), and Arabidopsis SYT1 protein levels have been shown to increase rapidly in parallel with the acquisition of freezing tolerance during cold acclimation (Kawamura and Uemura, 2003). However, direct evidence of a role for synaptotagmin in protection of the plant plasma membrane has not been provided so far.

This issue of The Plant Cell includes two reports that characterize the function of Arabidopsis SYT1 and demonstrate that it plays an important role in maintaining plasma membrane integrity, especially under conditions of high potential for membrane disruption, such as freezing and osmotic stress. Schapire et al. (pages 3374–3388) identified SYT1 from a genetic screen for mutants showing hypersensitivity to osmotic stress, whereas Yamazaki et al. (pages 3389–3404) used RNA interference along with other bioassays to investigate the role of SYT1 in the acquisition of freezing tolerance.

Both groups found that SYT1 is localized predominantly to the plasma membrane, and disruption of SYT1 function leads to decreased tolerance to osmotic stress and freezing (see figure ). Mammalian synaptotagmins contain a transmembrane domain at the N terminus and two conserved calcium binding domains (C2A and C2B) at the C terminus. Schapire et al. show the C2A domain of At SYT1 exhibits Ca²⁺-dependent binding to phospholipid membranes. Meanwhile, Yamazaki et al. used immunoassays with leaf sections and isolated plasma membrane fractions to show that the C2A domain is exposed on the cytosolic side of the plasma membrane and likely participates in the acquisition of Ca²⁺-dependent freezing tolerance. These highly complementary studies suggest that, similar to the situation in animal cells, SYT1-dependent resealing is an important component of maintaining plasma membrane integrity in plants.

View larger version (83K): [in this window] [in a new window] [as a PowerPoint slide]   SYT1 plays a role in acquisition of freezing tolerance. Wild-type (left panel) and syt1 T-DNA mutant seedlings (right panel) after cold acclimation followed by 12 h of freezing at –10°C and recovery at 23°C for 10 d. (Image from Yamazaki et al. [2008].)

www.plantcell.org/cgi/doi/10.1105/tpc.108.201211

REFERENCES

Craxton, M. (2004). Synaptotagmin gene content of the sequenced genomes. BMC Genomics 5: 43.[CrossRef][Medline]

Kawamura, Y., and Uemura, M. (2003). Mass spectrometric approach for identifying putative plasma membrane proteins of Arabidopsis leaves associated with cold acclimation. Plant J. 36: 141–154.[CrossRef][Web of Science][Medline]

Lynch, K.L., Gerona, R.R., Larsen, E.C., Marcia, R.F., Mitchell, J.C., and Martin, T.F. (2007). Synaptotagmin C₂A loop 2 mediates Ca²⁺-dependent SNARE interactions essential for Ca²⁺-triggered vesicle exocytosis. Mol. Biol. Cell 18: 4957–4968.[Abstract/Free Full Text]

McNeil, P.L., and Kirchhausen, T. (2005). An emergency response team for membrane repair. Nat. Rev. Mol. Cell Biol. 6: 499–505.[CrossRef][Web of Science][Medline]

Schapire, A.L., Voigt, B., Jasik, J., Rosado, A., Lopez-Cobollo, R., Menzel, D., Salinas, J., Mancuso, S., Valpuesta, V., Baluska, F., and Botella, M.A. (2008). Arabidopsis SYNAPTOTAGMIN1 is required for the maintenance of plasma membrane integrity and cell viability. Plant Cell 20: 3374–3388.[Abstract/Free Full Text]

Yamazaki, T., Kawamura, Y., Minami, A., and Uemura, M. (2008). Calcium-dependent freezing tolerance in Arabidopsis involves membrane resealing via SYNAPTOTAGMIN1. Plant Cell 20: 3389–3404.[Abstract/Free Full Text]

Related articles in Plant Cell:

Arabidopsis Synaptotagmin 1 Is Required for the Maintenance of Plasma Membrane Integrity and Cell Viability

Arnaldo L. Schapire, Boris Voigt, Jan Jasik, Abel Rosado, Rosa Lopez-Cobollo, Diedrik Menzel, Julio Salinas, Stefano Mancuso, Victoriano Valpuesta, Frantisek Baluska, and Miguel A. Botella
Plant Cell 2008 20: 3374-3388. [Abstract] [Full Text]  

Calcium-Dependent Freezing Tolerance in Arabidopsis Involves Membrane Resealing via Synaptotagmin SYT1

Tomokazu Yamazaki, Yukio Kawamura, Anzu Minami, and Matsuo Uemura
Plant Cell 2008 20: 3389-3404. [Abstract] [Full Text]  

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