FOR 964: Calcium Signalling via Protein Phosphorylation in Plant Model Cell Types during Environmental Stress Adaption
Final Report Abstract
Plants are of essential importance for all life on earth as they convert sunlight, water, and carbon dioxide into chemical energy. Due to their sessile lifestyle plants exhibit a remarkable ability to appropriately sense and signal changes in environmental parameters in order to efficiently mount a suit of coordinated adaptive responses to these. Second messengers – and among these especially the simple ion calcium (Ca2+) – are central to the underlying signaling processes and for the coordination of downstream responses. The major aims of this research group were: (i) To advance and apply high-resolution biosensorics for monitoring the occurrence and dynamics of Ca2+ signals in plant model systems and model cell types. (ii) To identify and characterize the mechanisms and components that bring about the formation of Ca2+ signals. (iii) To investigate the function and regulation of Ca2+-dependent kinases that translate Ca2+ signals into phosphorylation-regulation of target proteins, with a focus on CDPKs and CBL-CIPKs. (iv) To identify and characterize the targets of these kinases and principles of their regulation. (v) To elucidate the interplay of Ca2+ signaling and hormonal regulation with a focus on ABA signaling as model case, and (vi) to enable modeling approaches building on quantitative datasets that reflect these signaling processes and allow further hypotheses generation. In our research, we used Arabidopsis thaliana as model organism and focused on roots as model organ as well as on guard cells, root hairs, and pollen tubes as model cell types for Ca2+ signaling processes. On the molecular scale, the regulation of various ion channels, NADPH oxidases, and transcription factors served as model cases for our studies. The accomplished scientific progress and the conceptual advances for the field of Ca2+ signaling, that were achieved through the implementation of FOR964, were summarized in a joint review publication of all PIs involved in this FOR (Kudla et al., 2018).
Publications
- (2010). ABA perception and signalling. Trends Plant Sci 15, 395–401
Raghavendra, A.S., Gonugunta, V.K., Christmann, A., and Grill, E.
(See online at https://doi.org/10.1016/j.tplants.2010.04.006) - (2011). A Novel Calcium Binding Site in the Slow Vacuolar Cation Channel TPC1 Senses Luminal Calcium Levels. The Plant Cell 23, 2696–2707
Dadacz-Narloch, B., Beyhl, D., Larisch, C., López-Sanjurjo, E.J., Reski, R., Kuchitsu, K., Müller, T.D., Becker, D., Schönknecht, G., and Hedrich, R.
(See online at https://doi.org/10.1105/tpc.111.086751) - (2011). Calcium-Dependent Protein Kinase CPK21 Functions in Abiotic Stress Response in Arabidopsis thaliana. Molecular Plant 4, 83–96
Franz, S., Ehlert, B., Liese, A., Kurth, J., Cazalé, A.-C., and Romeis, T.
(See online at https://doi.org/10.1093/mp/ssq064) - (2012). Calcium-dependent regulation of cyclic photosynthetic electron transfer by a CAS, ANR1, and PGRL1 complex. Proc Natl Acad Sci USA 109, 17717–17722
Terashima, M., Petroutsos, D., Hüdig, M., Tolstygina, I., Trompelt, K., Gäbelein, P., Fufezan, C., Kudla, J., Weinl, S., Finazzi, G., et al.
(See online at https://doi.org/10.1073/pnas.1207118109) - 2012. FRET-based genetically encoded sensors allow high-resolution live cell imaging of Ca2+ dynamics: Improved vectors for Ca2+ imaging in plants. The Plant Journal, Vol. 69. 2012, Issue 1, pp. 181-192.
Krebs, M., Held, K., Binder, A., Hashimoto, K., Den Herder, G., Parniske, M., Kudla, J., Schumacher, K.
(See online at https://doi.org/10.1111/j.1365-313X.2011.04780.x) - (2014). Pollen tube NAD(P)H oxidases act as a speed control to dampen growth rate oscillations during polarized cell growth. The Plant Journal 78, 94–106
Lassig, R., Gutermuth, T., Bey, T.D., Konrad, K.R., and Romeis, T.
(See online at https://doi.org/10.1111/tpj.12452) - (2014). The phosphoinositide PI(3,5)P2 mediates activation of mammalian but not plant TPC proteins: functional expression of endolysosomal channels in yeast and plant cells. Cell. Mol. Life Sci. 71, 4275–4283
Boccaccio, A., Scholz-Starke, J., Hamamoto, S., Larisch, N., Festa, M., Gutla, P.V.K., Costa, A., Dietrich, P., Uozumi, N., and Carpaneto, A.
(See online at https://doi.org/10.1007/s00018-014-1623-2) - (2014). The vacuolar calcium sensors CBL2 and CBL3 affect seed size and embryonic development in Arabidopsis thaliana. The Plant Journal 78, 146–156
Eckert, C., Offenborn, J.N., Heinz, T., Armarego-Marriott, T., Schültke, S., Zhang, C., Hillmer, S., Heilmann, M., Schumacher, K., Bock, R., et al.
(See online at https://doi.org/10.1111/tpj.12456) - 2014. Site- and kinase-specific phosphorylation-mediated activation of SLAC1, a guard cell anion channel stimulated by abscisic acid. Science Signaling, Vol. 7, No. 342. 2014, ra86–ra86.
Maierhofer, T., Diekmann, M., Offenborn, J.N., Lind, C., Bauer, H., Hashimoto, K., Al-Rasheid, K.A.S., Luan, S., Kudla, J., Geiger, D., Hedrich, R.
(See online at https://doi.org/10.1126/scisignal.2005703) - (2015). Cytosolic Ca2+ Signals Enhance the Vacuolar Ion Conductivity of Bulging Arabidopsis Root Hair Cells. Molecular Plant 8, 1665–1674
Wang, Y., Dindas, J., Rienmüller, F., Krebs, M., Waadt, R., Schumacher, K., Wu, W.-H., Hedrich, R., and Roelfsema, M.R.G.
(See online at https://doi.org/10.1016/j.molp.2015.07.009) - (2015). STATE TRANSITION7-Dependent Phosphorylation Is Modulated by Changing Environmental Conditions, and Its Absence Triggers Remodeling of Photosynthetic Protein Complexes. Plant Physiol. 168, 615–634
Bergner, S.V., Scholz, M., Trompelt, K., Barth, J., Gäbelein, P., Steinbeck, J., Xue, H., Clowez, S., Fucile, G., Goldschmidt-Clermont, M., et al.
(See online at https://doi.org/10.1104/pp.15.00072) - 2015. Vacuolar CBL-CIPK12 Ca2+-Sensor-Kinase Complexes Are Required for Polarized Pollen Tube Growth. Current Biology, Vol. 25. 2015, Issue 11, pp. 1475-1482.
Steinhorst, L., Mähs, A., Ischebeck, T., Zhang, C., Zhang, X., Arendt, S., Schültke, S., Heilmann, I., Kudla, J.
(See online at https://doi.org/10.1016/j.cub.2015.03.053) - (2016). Abscisic acid controlled sex before transpiration in vascular plants. PNAS 113, 12862–12867
McAdam, S.A.M., Brodribb, T.J., Banks, J.A., Hedrich, R., Atallah, N.M., Cai, C., Geringer, M.A., Lind, C., Nichols, D.S., Stachowski, K., et al.
(See online at https://doi.org/10.1073/pnas.1606614113) - (2017). A quantitative hypermorphic CNGC allele confers ectopic calcium flux and impairs cellular development. ELife Sciences 6, e25012
Chiasson, D.M., Haage, K., Sollweck, K., Brachmann, A., Dietrich, P., and Parniske, M.
(See online at https://doi.org/10.7554/eLife.25012) - (2017). Multiparameter imaging of calcium and abscisic acid and high-resolution quantitative calcium measurements using R-GECO1-mTurquoise in Arabidopsis. New Phytologist 216, 303–320
Waadt, R., Krebs, M., Kudla, J., and Schumacher, K.
(See online at https://doi.org/10.1111/nph.14706) - (2017). Two spatially and temporally distinct Ca2+ signals convey Arabidopsis thaliana responses to K+ deficiency. New Phytologist 213, 739–750
Behera, S., Long, Y., Schmitz‐Thom, I., Wang, X.-P., Zhang, C., Li, H., Steinhorst, L., Manishankar, P., Ren, X.- L., Offenborn, J.N., et al.
(See online at https://doi.org/10.1111/nph.14145) - (2018). Advances and current challenges in calcium signaling. New Phytologist 218, 414–431
Kudla, J., Becker, D., Grill, E., Hedrich, R., Hippler, M., Kummer, U., Parniske, M., Romeis, T., and Schumacher, K.
(See online at https://doi.org/10.1111/nph.14966) - (2018). Advances and current challenges in calcium signaling. New Phytologist 218, 414–431
Kudla, J., Becker, D., Grill, E., Hedrich, R., Hippler, M., Kummer, U., Parniske, M., Romeis, T., and Schumacher, K.
(See online at https://doi.org/10.1111/nph.14966) - (2018). Symbiosis-related genes sustain the development of a downy mildew pathogen on Arabidopsis thaliana
Ried, M.K., Banhara, A., Binder, A., Hwu, F.-H., Gust, A.A., Höfle, C., Hückelhoven, R., Nürnberger, T., and Parniske, M.
(See online at https://doi.org/10.1101/286872) - 2018. Fine-tuning of RBOHF activity is achieved by differential phosphorylation and Ca2+ binding. New Phytologist, Vol. 221. 2019, Issue 4, pp. 1935-1949.
Han, J.-P., Köster, P., Drerup, M.M., Scholz, M., Li, S., Edel, K.H., Hashimoto, K., Kuchitsu, K., Hippler, M., Kudla, J.
(See online at https://doi.org/10.1111/nph.15543)
