Membrane "potential-omics": Toward voltage imaging at the cell population level in roots of living plants

Frontiers in Plant Science

Volumn 4, Issue AUG, 2013, Pages

  Matzke, Antonius J M ^a   Matzke, Marjori ^a  

^a INSTITUTE OF PLANT AND MICROBIAL BIOLOGY   (Taiwan)

Author keywords

Ciona intestinalis voltage sensor containing phosphatase; Nuclear electrophysiology; Nuclear membranes; Root cell; Roots; Systems biology; Transmembrane potential; Voltage sensitive fluorescent protein

Indexed keywords

EID: 84900845710     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2013.00311     Document Type: Article

References (37)

1. Akemann, W., Mutoh, H., Perron, A., Rossier, J., and Knoepfel, T. (2010). Imaging brain electric signals with genetically targeted voltage-sensitive fluorescent proteins. Nat. Methods 7, 643-651. doi: 10.1038/nmeth.1479
2. Benfey, P., Ren, L., and Chua, N. H. (1989). The CaMV 35S enhancer contains at least two domains which can confer different developmental and tissue-specific expression patterns. EMBO J. 8, 2195-2202.
3. Capoen, W., Sun, J., Wysham, D., Otegui, M. S., Venkateshwaran, M., Hirsch, S., et al. (2011). Nuclear membranes control symbiotic calcium signaling of legumes. Proc. Natl. Acad. Sci. U.S.A. 108, 14348-14353. doi: 10.1073/pnas.1107912108
4. Charpentier, M., Bredemeier, R., Wanner, G., Takeda, N., Schleiff, E., and Parniske, M. (2008). Lotus japonicus CASTOR and POLLUX are ion channels essential for per-inuclear calcium spiking in legume root endosymbiosis. Plant Cell 20, 3467-3479. doi: 10.1105/tpc.108.063255
5. Charpentier, M., and Oldroyd, G. E. (2013). Nuclear calcium signaling in plants. Plant Physiol. doi: 10.1104/pp.113.220863 [Epub ahead of print].
6. Cutler, S. R., Ehrhardt, D. W., Griffitts, J. S., and Somerville, C. R. (2000). Random GFP::cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proc. Natl. Acad. Sci. U.S.A. 97, 3718-3723. doi: 10.1073/pnas.97.7.3718
7. Deal, R. B., and Henikoff, S. (2011). The INTACT method for cell type-specific gene expression and chromatin profiling in Arabidopsis thaliana. Nat. Protoc. 6, 56-68. doi: 10.1038/nprot.2010.175
8. Fukushima, A., Kusano, M., Redes-tig, H., Arita, M., and Saito, K. (2009). Integrated omics approaches in plant systems biology. Curr. Opin. Chem. Biol. 13, 532-538. doi: 10.1016/j.cbpa.2009.09.022
9. Graumann, K., Runions, J., and Evans, D. E. (2010). Characterization of SUN-domain proteins at the higher plant nuclear envelope. Plant J. 61, 134-144. doi: 10.1111/j.1365-313X.2009.04038.x
10. Grefen, C., Donald, N., Hashimoto, K., Kudla, J., Schumacher, K., and Blatt, M. R. (2010). A ubiquitin-10 promoter-based vector set for fluorescent protein tagging facilitates temporal stability and native protein distribution in transient and stable expression studies. Plant J. 64, 355-365. doi: 10.1111/j.1365-313X.2010.04322.x
11. Heyndrickx, K. S., and Vandepoele, K. (2012). Systematic identification of functional plant modules through the integration of complementary data sources. Plant Physiol. 159, 884-901. doi: 10.1104/pp.112.196725
12. Hofmeister, H., and O'Hare, P. (2005). Analysis of the localization and topology of nurim, a polytopic protein tightly associated with the inner nuclear membrane. J. Biol. Chem. 280, 2512-2521. doi: 10.1074/jbc.M410504200
13. Keurentjes, J. J. B., Molenaar, J., and Zwaan, B. (2013). Predictive modelling of complex agronomic and biological systems. Plant Cell Environ. doi: 10.1111/pce.12156 [Epub ahead of print].
14. Kleessen, S., Klie, S., and Nikoloski, Z. (2013). Data integration through proximity-based networks provides biological principles of organization across scales. Plant Cell doi: 10.1105/tpc.113.111039 [Epub ahead of print].
15. Matzke, A. J. M., and Matzke, M. A. (1991). The electrical properties of the nuclear envelope, and their possible role in the regulation of eukaryotic gene expression. Bioelectrochem. Bioenerg. 25, 357-370. doi: 10.1016/0302-4598(91)80002-K
16. Matzke, A. J. M., Weiger, T. M., and Matzke, M. (2010). Ion channels at the nucleus: electrophysiology meets the genome. Mol. Plant 3, 642-652. doi: 10.1093/mp/ssq013
17. Matzke, M. A., and Matzke, A. J. M. (1986). Visualization of mitochondria and nuclei in living plant cells by the use of a potential-sensitive fluorescent dye. Plant Cell Environ. 9, 73-77. doi: 10.1111/1365-3040.ep11614344
18. Matzke, M. A., Matzke, A. J. M., and Neuhaus, G. (1988). Cell age-related differences in the interaction of a potential-sensitive fluorescent dye with nuclear envelopes of Acetabularia mediterranea. Plant Cell Environ. 11, 157-163. doi: 10.1111/j.1365-3040.1988.tb01132.x
19. Merzlyak, E. M., Goedhart, J., Shcherbo, D., Bulina, M. E., Shcheglov, A. S., Fradkov, A. F., et al. (2007). Bright monomeric red fluorescent protein with an extended fluorescence lifetime. Nat. Methods 4, 555-557. doi: 10.1038/nmeth1062
20. Murata, Y., Iwasaki, H., Sasaki, M., Inaba, K., and Okamura, Y. (2005). Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature 435, 1239-1243. doi: 10.1038/nature03650
21. Musheev, M. U., Filiptsev, Y., Okhonin, V., and Krylov, S. N. (2010). Electric field destabilizes noncova-lent protein-DNA complexes. J. Am. Chem. Soc. 132, 13639-13641. doi: 10.1021/ja105754h
22. Musheev, M. U., Kanoatov, M., and Krylov, S. N. (2013). Non-uniform velocity of homogeneous DNA in a uniform electric field: consequence of electric field induced slow dissociation of highly stable DNA-counter-ion complexes. J. Am. Chem. Soc. 135, 8041-8046. doi: 10.1021/ja402257x
23. Mutoh, H., and Knoepfel, T. (2013). Probing neuronal activities with genetically-encoded optical indicators: from a historical to a forward-looking perspective. Pflugers Arch. 465, 361-371. doi: 10.1007/s00424-012-1202-z
24. Mutoh, H., Perron, A., Akemann, W., Iwamoto, Y., and Knoepfel, T. (2011). Optogenetic monitoring of membrane potentials. Exp. Physiol. 96, 13-18. doi: 10.1113/expphys-iol.2010.053942
25. Noble, D. (2013). A biological relativity view of the relationships between genomes and phenotypes. Prog. Biophys. Mol. Biol. 111, 59-65. doi: 10.1016/j.pbiomolbio.2012.09.004
26. Oda, Y., and Fukuda, H. (2011). Dynamics of Arabidopsis SUN proteins during mitosis and their involvement in nuclear shaping. Plant J. 66, 629-641. doi: 10.1111/j.1365-313X.2011.04523.x
27. Pastrana, E. (2012). Light-based electro-physiology. Nat. Methods 9, 38. doi: 10.1038/nmeth.1825
28. Perron, A., Akemann, W., Mutoh, H., and Knopfel, T. (2012). Genetically encoded probes for optical imaging of brain electrical activity. Prog. Brain Res. 196, 63-77. doi: 10.1016/B978-0-444-59426-6.00004-5
29. Perron, A., Mutoh, H., Akemann, W., Gautam, S. G., Dimitrov, D., Iwamoto, Y., et al. (2009a). Second and third generation voltage-sensitive fluorescent proteins for monitoring membrane potential. Front. Mol. Neurosci. 2:5. doi: 10.3389/neuro.02.005.2009
30. Perron, A., Mutoh, H., Launey, T., and Knöpfel, T. (2009b). Red-shifted voltage-sensitive fluorescent proteins. Chem. Biol. 16, 1268-1277. doi: 10.1016/j.chembiol.2009.11.014
31. Peterka, D. S., Takahashi, H., and Yuste, R. (2011). Imaging voltage in neurons. Neuron 69, 9-21. doi: 10.1016/j.neuron.2010.12.010
32. Riely, B. K., Lougnon, G., Ane, J.-M., and Cook, D. R. (2007). The symbiotic ion channel homolog DMI1 is localized in the nuclear membrane of Medicago truncatula roots. Plant J. 49, 208-216. doi: 10.1111/j.1365-313X.2006.02957.x
33. Rose, A., and Meier, I. (2001). A domain unique to plant RanGAP is responsible for its targeting to the plant nuclear rim. Proc. Natl. Acad. Sci. U.S.A. 98, 15377-15382. doi: 10.1073/pnas.261459698
34. Shcherbo, D., Murphy, C. S., Ermakova, G. V., Solovieva, E. A., Chep-urnykh, T. V., Shcheglov, A. S., et al. (2009). Far-red fluorescent tags for protein imaging in living tissues. Biochem. J. 418, 567-574. doi: 10.1042/BJ20081949
35. Shemer, I., Brinne, B., Tegner, J., and Grillner, S. (2008). Electro-tonic signals along intercellular membranes may interconnect dendritic spines and nucleus. PLoS Comput. Biol. 4:e1000036. doi: 10.1371/jour-nal.pcbi.1000036
36. Weijers, D., van Dijk, M. F., Venecken, R.-J., Quint, A., Hooykaas, P., and Offringa, R. (2001). An Arabidopsis Minute-like pheno-type caused by a semi-dominant mutation in RIBOSOMAL PROTEIN S5 gene. Development 128, 4289-4299.
37. Zhang, W., Li, F., and Ni, L. (2010). Integrating multiple 'omics' analysis for microbial biology: applications and methodologies. Microbiology 156, 287-301. doi: 10.1099/mic.0.034793-0