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Interactions of Auxinic Compounds on Ca2+ Signaling and Root Growth in Arabidopsis thaliana

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DOI: 10.4236/ajps.2015.619294    2,963 Downloads   3,399 Views   Citations

ABSTRACT

Auxinic-like compounds have been widely used as weed control agents. Over the years, the modes of action of auxinic herbicides have been elucidated, but most studies thus far have focused on their effects on later stages of plant growth. Here, we show that some select auxins and auxiniclike herbicides trigger a rapid elevation in root cytosolic calcium levels within seconds of application. Arabidopsis thaliana plants expressing the Yellow-Cameleon (YC) 3.60 calcium reporter were treated with indole-3-acetic acid (IAA), indole-3-butyric acid (IBA), 1-naphthalene acetic acid (NAA), and two synthetic herbicides, 2,4-dichlorophenoxyacetic acid (2,4-D) and mecoprop [2-(4-chloro- 2-methylphenoxy) propanoic acid], followed by monitoring cytosolic calcium changes over a 10 minute time course. Seconds after application of compounds to roots, the Ca2+ signaling-mediated pathway was triggered, initiating the plant response to these compounds as monitored and recorded using Fluorescence Resonance Energy Transfer (FRET)-sensitized emission imaging. Each compound elicited a specific and unique cytosolic calcium signature. Also primary root development and elongation was greatly reduced or altered when exposed at two concentrations (0.10 and 1.0 μM) of each compound. Within 20 to 25 min after triggering of the Ca2+ signal, root growth inhibition could be detected. We speculate that differences in calcium signature among the tested auxins and auxinic herbicides might correlate with their variation and potency with regard to root growth inhibition.

Conflicts of Interest

The authors declare no conflicts of interest.

Cite this paper

Teaster, N. , Sparks, J. , Blancaflor, E. and Hoagland, R. (2015) Interactions of Auxinic Compounds on Ca2+ Signaling and Root Growth in Arabidopsis thaliana. American Journal of Plant Sciences, 6, 2989-3000. doi: 10.4236/ajps.2015.619294.

References

[1] Kögel, F. and Kostermans, D.G.F.R. (1934) Heteroauxin as a Metabolite of Lower Plant-Like Organisms; Isolation from Yeast. Hoppe-Seyler’s Zeitschrift fur Physiologische Chemie, 228, 113-121.
[2] Went, F.W. and Thimann, K.V. (1937) Phytohormones. The Macmillan Company, New York.
[3] Woodward, A.W. and Bartel, B. (2005) Auxin: Regulation, Action and Interaction. Annals of Botany, 95, 707-735.
http://dx.doi.org/10.1093/aob/mci083
[4] Teale, W.D., Paponov, I.A. and Palme, K. (2006) Auxin in Action: Signaling, Transport and the Control of Plant Growth and Development. Nature Reviews. Molecular Cell Biology, 7, 847-859.
http://dx.doi.org/10.1038/nrm2020
[5] Costacurta, A. and Vanderleyden, J. (1995) Synthesis of Phytohormones by Plant-Associated Bacteria. Critical Reviews in Microbiology, 21, 1-18.
http://dx.doi.org/10.3109/10408419509113531
[6] Maor, R., Haskin, S., Levi-Kedmi, H. and Sharon, A. (2004) In Planta Production of Indole-3-Acetic Acid by Colletotrichum gloeosporioides f. sp. Aeschynomene. Applied Environmental Microbiology, 70, 1852-1854.
http://dx.doi.org/10.1128/AEM.70.3.1852-1854.2004
[7] Zimmerman, P.W. and Wilcoxon, F. (1935) Several Chemical Growth Substances Which Cause Initiation of Roots and Other Responses in Plants. Contributions from Boyce Thompson Institute, 7, 209-229.
[8] Blommaert, K. (1954) Growth- and Inhibiting-Substances in Relation to the Rest Period of the Potato Tuber. Nature, 174, 970-972.
http://dx.doi.org/10.1038/174970b0
[9] Epstein, E. and Ludwig-Miller, J. (1993) Indole-3-Butyric Acid in Plants: Occurrence, Synthesis, Metabolism, and Transport. Physiologia Plantarum, 88, 382-389.
http://dx.doi.org/10.1111/j.1399-3054.1993.tb05513.x
[10] Ludwig-Miller, J. (2000) Indole-3-Butyric Acid in Plant Growth and Development. Plant Growth Regulation, 32, 219-230.
http://dx.doi.org/10.1023/A:1010746806891
[11] Strader, L.C., Culler, A.H., Cohen, J.D. and Bartel, B. (2010) Conversion of Endogenous Indole-3-Butyric Acid to Indole-3-Acetic Acid Drives Cell Expansion in Arabidopsis Seedlings. Plant Physiology, 153, 1577-1586.
http://dx.doi.org/10.1104/pp.110.157461
[12] Bartel, B. (1997) Auxin Biosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology, 48, 51-66.
http://dx.doi.org/10.1146/annurev.arplant.48.1.51
[13] Zolman, B.K., Silva, I.D. and Bartel, B. (2001) The Arabidopsis pxa1 Mutant Is Defective in an ATP-Binding Cassette Transporter-Like Protein Required for Peroxisomal Fatty Acid Beta-Oxidation. Plant Physiology, 127, 1266-1278.
http://dx.doi.org/10.1104/pp.010550
[14] Pokorny, R. (1941) Some Chlorophenoxyacetic Acids. Journal of the American Chemical Society, 63, 1768.
http://dx.doi.org/10.1021/ja01851a601
[15] Zimmerman, P.W. and Hitchcock, A.E. (1942) Substituted Phenoxy and Benzoic Acid Growth Substances and the Relation of Structure to Physiological Activity. Contributions from Boyce Thompson Institute, 12, 321-343.
[16] Marth, P.C. and Mitchell, J.W. (1944) 2,4-Dichlorophenoxyacetic Acid as a Differential Herbicide. Botanical Gazette, 106, 224-232.
http://dx.doi.org/10.1086/335289
[17] Hamner, C.L. and Tukey, H.B. (1944) The Herbicidal Action of 2,4-Dichlorophenoxyacetic Acid and 2,4,5-Trichloro-phenoxyacetic Acid on Bindweed. Science, 100, 154-155.
http://dx.doi.org/10.1126/science.100.2590.154
[18] Hepler, P.K. (2005) Calcium: A Central Regulator of Plant Growth and Development. Plant Cell, 17, 2142-2155.
http://dx.doi.org/10.1105/tpc.105.032508
[19] Dodd, A.N., Kudla, J. and Sanders, D. (2010) The Language of Calcium Signaling. Annual Review of Plant Biology, 61, 593-620.
http://dx.doi.org/10.1146/annurev-arplant-070109-104628
[20] Kudla, J., Batistic, O. and Hashimoto, K. (2010) Calcium Signals: The Lead Currency of Plant Information Processing. Plant Cell, 22, 563-641.
http://dx.doi.org/10.1105/tpc.109.072686
[21] Shishova, M. and Lindberg, S. (2004) Auxin Induces an Increase of Ca2+ Concentration in the Cytosol of Wheat Leaf Protoplasts. Journal of Plant Physiology, 16, 937-945.
http://dx.doi.org/10.1016/j.jplph.2003.12.005
[22] Gehring, C.A., Irving, H.R. and Parish, R.W.(1990) Effects of Auxin and Abscisic Acid on Cytosolic Calcium and pH in Plant Cells. Proceedings of the National Academy of Sciences of the United States of America, 87, 9645-9649.
http://dx.doi.org/10.1073/pnas.87.24.9645
[23] Shishova, M., Yemelyanov, V., Kirpichnikova, A. and Lindberg, S. (2007) A Shift in Sensitivity to Auxin within Development of Maize Seedlings. Journal of Plant Physiology, 164, 1323-1330.
http://dx.doi.org/10.1016/j.jplph.2006.09.005
[24] Monshausen, G.B., Miller, N.D., Murphy, A.S. and Gilroy, S.(2011) Dynamics of Auxin-Dependent Ca2+ and pH Signaling in Root Growth Revealed by Integrating High-Resolution Imaging with Automated Computer Vision-Based Analysis. Plant Journal, 65, 309-318.
http://dx.doi.org/10.1111/j.1365-313X.2010.04423.x
[25] Verret, F., Wheeler, G., Taylor, A.R., Farnham, G. and Brownlee, C. (2010) Calcium Channels in Photosynthetic Eukaryotes: Implications for Evolution of Calcium-Based Signaling. New Phytologist, 187, 23-43.
http://dx.doi.org/10.1111/j.1469-8137.2010.03271.x
[26] Wheeler, G.L. and Brownlee, C. (2008) Ca2+ Signaling in Plants and Green Algae—Changing Channels. Trends in Plant Science, 13, 506-514.
http://dx.doi.org/10.1016/j.tplants.2008.06.004
[27] McAinsh, M.R. and Pittman, J.K. (2009) Shaping the Calcium Signature. New Phytologist, 181, 275-294.
http://dx.doi.org/10.1111/j.1469-8137.2008.02682.x
[28] McCormack, E., Tsai, Y.-C. and Braam, J. (2005) Handling Calcium Signaling: Arabidopsis CaMs and CMLs. Trends in Plant Science, 10, 1360-1365.
http://dx.doi.org/10.1016/j.tplants.2005.07.001
[29] Wang, Y.S., Motes, C.M., Mohamalawari, D.R. and Blancaflor, E.B. (2004) Green Fluorescent Protein Fusions to Arabidopsis Fimbrin 1 for Spatio-Temporal Imaging of F-Actin Dynamics in Roots. Cell Motility and the Cytoskeleton, 59, 79-93.
http://dx.doi.org/10.1002/cm.20024
[30] Rincón-Zachary, M., Teaster, N.D., Sparks, J.A., Valster, A.H., Motes, C.M. and Blancaflor, E.B. (2010) Fluorescence Resonance Energy Transfer-Sensitized Emission of Yellow Cameleon 3.60 Reveals Root Zone-Specific Calcium Signatures in Arabidopsis in Response to Aluminum and Other Trivalent Cations. Plant Physiology, 152, 1-17.
http://dx.doi.org/10.1104/pp.109.147256
[31] Miyawaki, A. (2003) Visualization of the Spatial and Temporal Dynamics of Intracellular Signaling. Developmental Cell, 4, 296-305. http://dx.doi.org/10.1016/S1534-5807(03)00060-1
[32] van Rheenen, J., Langeslag, M. and Jalink, K. (2004) Correcting Confocal Acquisition to Optimize Imaging of Fluorescence Resonance Energy Transfer by Sensitized Emission. Biophysical Journal, 86, 2517-2529.
http://dx.doi.org/10.1016/S0006-3495(04)74307-6
[33] Feige, J.N., Sage, D., Wahli, W., Desvergne, B. and Gelman, L. (2005) PixFRET, an ImageJ Plug-in for FRET Calculation That Can Accommodate Variations in Spectral Bleed-Throughs. Microscopy Research and Technique, 68, 51-58.
http://dx.doi.org/10.1002/jemt.20215
[34] Heap, I. (2015) The International Survey of Herbicide Resistant Weeds. Online.
www.weedscience.org
[35] Bush, D.S. (1995) Calcium Regulation in Plant Cells and Its Role in Signaling. Annual Review of Plant Physiology and Plant Molecular Biology, 46, 95-122.
http://dx.doi.org/10.1146/annurev.pp.46.060195.000523
[36] Yang, T. and Poovaiah, B.W. (2000) Molecular and Biochemical Evidence for the Involvement of Calcium/Calmodulin in Auxin Action. Journal of Biological Chemistry, 275, 3137-3143.
http://dx.doi.org/10.1074/jbc.275.5.3137
[37] Gong, M., Van der Luit, A.H., Knight, M.R. and Trewavas, A.J. (1998) Heat-Shock-Induced Changes in Intracellular Ca2+ Level in Tobacco Seedlings in Relation to Thermotolerance. Plant Physiology, 16, 429-437.
http://dx.doi.org/10.1104/pp.116.1.429
[38] Knight, M.R., Campbell, A.K., Smith, S.M. and Trewavas, A.J. (1991) Transgenic Plant Aequorin Reports the Effects of Touch and Cold-Shock and Elicitors on Cytoplasmic Calcium. Nature, 352, 524-526.
http://dx.doi.org/10.1038/352524a0
[39] Knight, M.R., Smith, S.M. and Trewavas, A.J. (1992) Wind-Induced Plant Motion Immediately Increases Cytosolic Calcium. Proceedings of the National Academy of Sciences of the United States of America, 89, 4967-4971.
http://dx.doi.org/10.1073/pnas.89.11.4967
[40] Tavernier, E., Wendehenne, D., Blein, J.-P. and Pugin, A. (1995) Involvement of Free Calcium in Action of Cryptogein, a Proteinaceous Elicitor of Hypersensitive Reaction in Tobacco Cells. Plant Physiology, 109, 1025-1031.
[41] Deshpande, S. and Hall, J.C. (1995) Comparison of Flash-Induced Light Scattering Transients and Proton Efflux from Auxinic-Herbicide Resistant and Susceptible Wild Mustard Protoplasts: A Possible Role for Calcium in Mediating Auxinic Herbicide Resistance. Biochemica Biophysica Acta, 1244, 69-78.
http://dx.doi.org/10.1016/0304-4165(94)00196-5
[42] Deshpande, S. and Hall, J.C. (1996) ATP-Dependent Auxin- and Auxinic-Herbicide Induced Volume Changes in Isolated Protoplast Suspensions from Sinapis arvensis L. Pesticide Biochemistry and Physiology, 56, 26-43.
http://dx.doi.org/10.1006/pest.1996.0056
[43] Wang, Y. and Hall, J.C. (2001) Calcium May Mediate Auxinic Herbicide Resistance in Wild Mustard. Weed Science, 49, 2-7.
http://dx.doi.org/10.1614/0043-1745(2001)049[0002:CMMAHR]2.0.CO;2
[44] Walsh, T.A., Neal, R., Merio, A.O., Honma, M., Hicks, G.R., Wolff, K., Matsumura, W. and Davies, J.P. (2006) Mutation in an Auxin Receptor Homolog AFB5 and in SGT1b Confer Resistance to Synthetic Picolinate Auxins and Not to 2,4-Dichlorophenoxyacetic Acid or Indole-3-Acetic Acid in Arabidopsis. Plant Physiology, 142, 542-552.
http://dx.doi.org/10.1104/pp.106.085969
[45] Pufky, J., Qiu, Y., Rao, M.V., Hurban, P. and Jones, A.M. (2003) The Auxin-Induced Transcriptome for Etiolated Arabidopsis Seedlings Using a Structure/Function Approach. Functional & Integrative Genomics, 3, 135-143.
http://dx.doi.org/10.1007/s10142-003-0093-7
[46] Gleason, C., Foley, R.C. and Singh, K.B. (2011) Mutant Analysis in Arabidopsis Provides Insight into the Molecular Mode of Action of the Auxinic Herbicide Dicamba. PLoS ONE, 6, e17245.
http://dx.doi.org/10.1371/journal.pone.0017245
[47] Lomax, T.L., Mehlhorn, R.J. and Briggs, W.R. (1985) Active Auxin Uptake by Zucchini Membrane Vesicles: Quantitation Using Electron-Spin-Resonance Volume and Delta pH Determinations. Proceedings of the National Academy of Sciences of the United States of America, 82, 6541-6545.
http://dx.doi.org/10.1073/pnas.82.19.6541
[48] Swarup, R. and Bennett, M. (2003) Auxin Transport: The Fountain of Life in Plants? Developmental Cell, 5, 824-826.
http://dx.doi.org/10.1016/S1534-5807(03)00370-8
[49] Swarup, R., Kargul, J., Marchant, A., Zadik, D., Rahman, A., Mills, R., Yemm, A., May, S., Williams, L., Millner, P., Tsurumi, S., Moore, I., Napier, R., Kerr, I.D. and Bennett, M.J. (2004) Structure-Function Analysis of the Presumptive Arabidopsis Auxin Permease AUX1. Plant Cell, 16, 3069-3083.
http://dx.doi.org/10.1105/tpc.104.024737
[50] Sabatini, S., Beis, D., Wolkenfelt, H., Murfett, J., Guilfoyle, T., Malamy, J., Benfey, P., Leyser, O., Bechtold, N., Weisbeek, P. and Scheres, B. (1999) An Auxin-Dependent Distal Organizer of Pattern and Polarity in the Arabidopsis Root. Cell, 99, 463-472.
http://dx.doi.org/10.1016/S0092-8674(00)81535-4
[51] Wang, Y., Deshpande, S. and Hall, J.C. (1997) Calcium Ion Dynamics in Auxinic-Herbicide Resistant and Susceptible Biotypes of Sinapis arvensis. Brighton Crop Protection Conference—Weeds, 2, 765-770.
[52] Heap, I. and Morrison, I.M. (1992) Resistance to Auxin-Type Herbicides in Wild Mustard (S. arvensis L.) Populations in Western Canada. Proceedings of the Weed Science Society of America, 32, 55.
[53] Peniuk, M.G., Romano, M.L. and Hall, J.C. (1993) Physiological Investigations into the Resistance of a Wild Mustard (Sinapis arvensis L.) Biotype to Auxinic Herbicides. Weed Research, 33, 431-440.
http://dx.doi.org/10.1111/j.1365-3180.1993.tb01959.x
[54] Webb, S.R. and Hall, J.C. (1995) Auxinic-Herbicide Resistant and Susceptible Wild Mustard (Sinapis arvensis L.) Biotypes: Effects of Auxinic Herbicides on Seedling Growth and Auxin-Binding Activity. Pesticide Biochemistry and Physiology, 52, 137-148.
http://dx.doi.org/10.1006/pest.1995.1038
[55] Aloni, R., Aloni, E., Langhans, M. and Ullrich, C.I. (2006) Role of Cytokinin and Auxin in Shaping Root Architecture: Regulating Vascular Differentiation, Lateral Root Initiation, Root Apical Dominance and Root Gravitropism. Annals of Botany, 97, 883-893.
http://dx.doi.org/10.1093/aob/mcl027
[56] Overvoorde, P., Fukaki, H. and Beeckman, T. (2010) Auxin Control of Root Development. Cold Spring Harbor Perspectives in Biology, 2, a001537.
http://dx.doi.org/10.1101/cshperspect.a001537
[57] Berridge, M.J., Lipp, P. and Bootman, M.D. (2000) The Versatility and Universality of Calcium Signaling. Nature Reviews. Molecular Cell Biology, 1, 11-21.
http://dx.doi.org/10.1038/35036035
[58] Devine, M.D., Duke, S.O. and Fedtke, C. (1993) Herbicides with Auxin Activity. In: Devine, M.D., Duke, S.O. and Fedtke, C., Eds., Physiology of Herbicide Action, Prentice Hall, Englewood Cliffs, 295-309.
[59] Sterling, T.M. and Hall, J.C. (1997) Mechanism of Action of Natural Auxins and the Auxinic Herbicides. In: Roe, R.M., Burton, J.D. and Kuhr, R.J., Eds., Herbicide Activity: Biochemistry and Molecular Biology, IOS Press, Amsterdam, 111-141.

  
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