Biologia plantarum 2017, 61:275-283 | DOI: 10.1007/s10535-017-0745-4

The analysis of mutant phenotypes and tissue expression reveals a role of SNAREs VAMP721 and VAMP722 in seedling growth

L. Zhang1,2, H. Y. Zhao3, W. C. Qi1, F. X. Zheng1, T. Q. Wang1, J. Y. Li1,2,*
1 College of Life Science, Henan Normal University, Xinxiang, P.R. China
2 Engineering Laboratory of Green Medicinal Material Biotechnology, Xinxiang, P.R. China
3 College of Life Sciences and Technology, Xinxiang University, Xinxiang, P.R. China

Membrane traffic mediated by a soluble N-ethylmaleimide sensitive factor attachment protein receptor (SNARE) complex contributes to plant growth and development. However, the functional significance of SNAREs involved in cell wall deposition and seedling development has not been sufficiently explored. In this study, we explored the roles of R-SNAREs VAMP721 (At1g04750) and VAMP722 (At2g33120) in seedling growth of Arabidopsis thaliana by histochemical staining, fluorescence labeling, and analyzing mutant phenotypes. Our results show a massive intracellular accumulation of cellulose and callose, and an abnormal deposition of callose at the expanding cell plate in vamp721vamp722 root cells compared with the wild type. Particularly, ectopic lignin accumulation was also observed in vamp721vamp722 root cells. The alteration of cell wall components was confirmed using Fourier transform infrared analysis. Plasma membrane integrity and cell viability were disturbed in the vamp721vamp722 seedling. Morphological observation shows that vamp721vamp722 mutations impaired development of roots, hypocotyl, cotyledon, and true leaf, and inhibited lateral root formation. Confocal images reveal that green fluorescent protein-tagged VAMP721 and VAMP722 showed a similar expression pattern and were expressed throughout all cells and tissues examined, including root and shoot apical meristems and cells of hypocotyls, cotyledons, and true leaves. Taken together, our results suggest that membrane traffic mediated by VAMP721 and VAMP722 is involved in seedling growth in A. thaliana.

Keywords: Arabidopsis thaliana; callose; cellulose; gene expression; lignin; membrane traffic
Subjects: mutants; callose; cellulose; lignin; gene expression; thylakoid membranes; SNARE
Species: Arabidopsis thaliana

Received: July 10, 2015; Revised: January 30, 2016; Accepted: February 17, 2016; Published: June 1, 2017Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Zhang, L., Zhao, H.Y., Qi, W.C., Zheng, F.X., Wang, T.Q., & Li, J.Y. (2017). The analysis of mutant phenotypes and tissue expression reveals a role of SNAREs VAMP721 and VAMP722 in seedling growth. Biologia plantarum, 61(2), 275-283. doi: 10.1007/s10535-017-0745-4.
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)

    • Open full article

    Supplementary files

    Download filebpl-201702-0009_S1.pdf

    File size: 468.49 kB

    References

    1. Alonso-Simon, A., Garcia-Angulo, P., Melida, H., Encina, A., Alvarez, J.M., Acebes, J.L.: The use of FTIR spectroscopy to monitor modifications in plant cell wall architecture caused by cellulose biosynthesis inhibitors. - Plant Signal Behav. 6: 1104-1110, 2011. Go to original source...
    2. Amano, T., Hirasawa, K., O'Donohue, M.J., Pernolle, J.C., Shioi, Y.: A versatile assay for the accurate, time-resolved determination of cellular viability. - Anal. Biochem. 314: 1-7, 2003. Go to original source...
    3. Bischoff, V., Cookson, S.J., Wu, S., Scheible, W.R., Thaxtomin, A.: affects CESA-complex density, expression of cell wall genes, cell wall composition, and causes ectopic lignification in Arabidopsis thaliana seedlings. - J. exp. Bot. 60: 955-965, 2009. Go to original source...
    4. Bolte, S., Talbot, C., Boutte, Y., Catrice, O., Read, N.D., Satiat-Jeunemaitre, B.: FM-dyes as experimental probes for dissecting vesicle trafficking in living plant cells. - J. Microscopy 214: 159-173, 2004. Go to original source...
    5. Chow, C.M., Neto, H., Foucart, C., Moore, I.: Rab-A2 and Rab-A3 GTPases define a trans-Golgi endosomal membrane domain in Arabidopsis that contributes substantially to the cell plate. - Plant Cell 20: 101-123, 2008. Go to original source...
    6. Crowell, E.F., Bischoff, V., Desprez, T., Rolland, A., Stierhof, Y.D., Schumacher, K., Gonneau, M., Hofte, H., Vernhettes, S.: Pausing of Golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis. - Plant Cell 21: 1141-1154, 2009. Go to original source...
    7. Denness, L., McKenna, J.F., Segonzac, C., Wormit, A., Madhou, P., Bennett, M., Mansfield, J., Zipfel, C., Hamann, T.: Cell wall damage-induced lignin biosynthesis is regulated by a reactive oxygen species-and jasmonic aciddependent process in Arabidopsis. - Plant Physiol. 156: 1364-1374, 2011. Go to original source...
    8. Derby, M.C., Gleeson, P.A.: New insights into membrane trafficking and protein sorting. - Int. Rev. Cytol. 261: 47-116, 2007. Go to original source...
    9. El-Kasmi, F., Krause, C., Hiller, U., Stierhof, Y.D., Mayer, U., Conner, L., Kong, L., Reichardt, I., Sanderfoot, A.A., Jurgens, G.: SNARE complexes of different composition jointly mediate membrane fusion in Arabidopsis cytokinesis. - Mol. Biol. Cell 24: 1593-1601, 2013. Go to original source...
    10. Falbel, T.G., Koch, L.M., Nadeau, J.A., Segui-Simarro, J.M., Sack, F.D., Bednarek, S.Y.: SCD1 is required for cytokinesis and polarized cell expansion in Arabidopsis thaliana. - Development 130: 4011-4024, 2003. Go to original source...
    11. Guseman, J.M., Lee, J.S., Bogenschutz, N.L., Peterson, K.M., Virata, R.E., Xie, B., Kanaoka, M.M., Hong, Z., Torii, K.U.: Dysregulation of cell-to-cell connectivity and stomatal patterning by loss-of-function mutation in Arabidopsis CHORUS (GLUCAN SYNTHASE-LIKE 8). - Development 137: 1731-1741, 2010. Go to original source...
    12. Hematy, K., Sado, P.E., Van Tuinen, A., Rochange, S., Desnos, T., Balzergue, S., Pelletier, S., Renou, J.P., Hofte, H.: A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. - Curr. Biol. 17: 922-931, 2007. Go to original source...
    13. Hong, W.: SNAREs and traffic. - Biochim. biophys. Acta 1744: 120-144, 2005. Go to original source...
    14. Hong, Z., Delauney, A.J., Verma, D.P.: A cell plate-specific callose synthase and its interaction with phragmoplastin. - Plant Cell 13: 755-768, 2001. Go to original source...
    15. Jiang, B., Shen, Z., Shen, J., Yu, D., Sheng, X., Lu, H.: Germination and growth of sponge gourd (Luffa cylindrica) pollen tubes and FTIR analysis of the pollen tube wall. - Scientia Hort. 122: 638-644, 2009. Go to original source...
    16. Kwon, C., Neu, C., Pajonk, S., Yun, H.S., Lipka, U., Humphry, M., Bau, S., Straus, M., Kwaaitaal, M., Rampelt, H., El-Kasm, F., Jurgens, G., Parker, J., Panstruga, R., Lipka, V., Schulze-Lefert, P.: Co-option of a default secretory pathway for plant immune responses. - Nature 451: 835-840, 2008. Go to original source...
    17. Lipka, V., Kwon, C., Panstruga, R.: SNARE-ware: the role of SNARE-domain proteins in plant biology. - Annu. Rev. cell. dev. Biol. 23: 147-174, 2007. Go to original source...
    18. McNeil, P.L., Kirchhausen, T.: An emergency response team for membrane repair. - Nature 6: 499-505, 2005. Go to original source...
    19. Mouille, G., Witucka-Wall, H., Bruyant, M.P., Loudet, O., Pelletier, S., Rihouey, C., Lerouxel, O., Lerouge, P., Hofte, H., Pauly, M.: Quantitative trait loci analysis of primary cell wall composition in Arabidopsis. - Plant Physiol. 141: 1035-1044, 2006. Go to original source...
    20. Peng, L., Zhang, L., Cheng, X., Fan, L.S., Hao, H.Q.: Disruption of cellulose synthesis by 2,6-dichlorobenzonitrile affects the structure of the cytoskeleton and cell wall construction in Arabidopsis. - Plant Biol. 15: 405-414, 2013. Go to original source...
    21. Pratelli, R., Sutter, J.U., Blatt, M.R.: A new catch in the SNARE. - Trends Plant Sci. 9: 187-195, 2004. Go to original source...
    22. Qian, P., Hou, S., Guo, G.: Molecular mechanisms controlling pavement cell shape in Arabidopsis leaves. - Plant Cell Rep. 28: 1147-1157, 2009. Go to original source...
    23. Rao, S.K., Huynh, C., Proux-Gillardeaux, V., Galli, T., Andrews, N.W.: Identification of SNAREs involved in synaptotagmin VII-regulated lysosomal exocytosis. - J. biol. Chem. 279: 20471-20479, 2004. Go to original source...
    24. Rossi, V., Banfield, D.K., Vacca, M., Dietrich, L.E., Ungermann, C., D'Esposito, M., Galli, T., Filippini, F.: Longins and their longin domains: regulated SNAREs and multifunctional SNARE regulators. - Trends Biochem. Sci. 29: 682-688, 2004. Go to original source...
    25. Sanderfoot, A.: Increases in the number of SNARE genes parallels the rise of multicellularity among the green plants. - Plant Physiol. 144: 6-17, 2007. Go to original source...
    26. Schapire, A.L., Voigt, B., Jasik, J., Rosado, A., Lopez-Cobollo, R., Menzel, D., Salinas, J., Mancuso, S., Valpuesta, V., Baluska, F., Botella, M.A.: Arabidopsis synaptotagmin 1 is required for the maintenance of plasma membrane integrity and cell viability. - Plant Cell 20: 3374-3388, 2008. Go to original source...
    27. Uemura, T., Sato, M.H., Takeyasu, K.: The longin domain regulates subcellular targeting of VAMP7 in Arabidopsis thaliana. - FEBS Lett. 579: 2842-2846, 2005. Go to original source...
    28. Uemura, T., Ueda, T., Ohniwa, R.L., Nakano, A., Takeyasu, K., Sato, M.H.: Systematic analysis of SNARE molecules in Arabidopsis: dissection of the post-Golgi network in plant cells. - Cell Struct. Funct. 29: 49-65, 2004. Go to original source...
    29. Winter, D., Vinegar, B., Nahal, H., Ammar, R., Wilson, G.V., Provart, N.J.: An "Electronic Fluorescent Pictograph" browser for exploring and analyzing large-scale biological data sets. - PLoS ONE 2: e718, 2007. Go to original source...
    30. Xu, J., Scheres, B.: Dissection of Arabidopsis ADPRIBOSYLATION FACTOR 1 function in epidermal cell polarity. - Plant Cell 17: 525-536, 2005. Go to original source...
    31. Yang, Z., Fu, Y.: ROP/RAC GTPase signaling. - Curr. Opin. Plant Biol. 10: 490-494, 2007. Go to original source...
    32. Yi, C., Park, S., Yun, H.S., Kwon, C.: Vesicle-associated membrane proteins 721 and 722 are required for unimpeded growth of Arabidopsis under ABA application. - J. Plant Physiol. 170: 529-533, 2013. Go to original source...
    33. Zhang, L., Zhang, H., Liu, P., Hao, H., Jin, J.B., Lin, J.: Arabidopsis R-SNARE proteins VAMP721 and VAMP722 are required for cell plate formation. - PLoS ONE 6: e26129, 2011. Go to original source...

    Return to the content