Annexin 1 regulates the H2O2-induced calcium signature in Arabidopsis thaliana roots

Plant Journal

Volumn 77, Issue 1, 2014, Pages 136-145

  Richards, Siân L ^a   Laohavisit, Anuphon ^a,c   Mortimer, Jennifer C ^a,c   Shabala, Lana ^b   Swarbreck, Stéphanie M ^a   Shabala, Sergey ^b   Davies, Julia M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF TASMANIA   (Australia)

^c RIKEN   (Japan)

Author keywords

annexin; Arabidopsis; calcium; glutathione; peroxide; root

Indexed keywords

ANNEXINS; ARABIDOPSIS; ARABIDOPSIS THALIANA; DIFFERENTIAL REGULATION; GLUTATHIONES; ION-SELECTIVE MICROELECTRODES; REACTIVE OXYGEN SPECIES; ROOT;

ANTIBIOTICS; CELL MEMBRANES; HYDROGEN PEROXIDE; MICROELECTRODES; OXIDATION; PEPTIDES; PEROXIDES;

CALCIUM;

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ANNEXIN; ANNEXIN 1, ARABIDOPSIS; ARABIDOPSIS PROTEIN; CALCIUM; CALCIUM CHANNEL; HYDROGEN PEROXIDE; POTASSIUM;

ARABIDOPSIS; CALCIUM SIGNALING; CELL MEMBRANE; DOWN REGULATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT EPIDERMIS; PLANT ROOT; PROTOPLAST; UPREGULATION;

ANNEXINS; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; CELL MEMBRANE; DOWN-REGULATION; GENE EXPRESSION REGULATION, PLANT; HYDROGEN PEROXIDE; MUTAGENESIS, INSERTIONAL; PLANT EPIDERMIS; PLANT ROOTS; POTASSIUM; PROTOPLASTS; STRESS, PHYSIOLOGICAL; UP-REGULATION;

EID: 84890973346     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/tpj.12372     Document Type: Article

References (51)

1. Allen, G.A., Chu, S.P., Schumacher, K., et al. (2000) Alteration of stimulus-specific guard cell oscillations and stomatal closing in Arabidopsis det3 mutant. Science, 289, 2338-2342.
2. 2. Plant Physiol. 135, 1685-1696.
3. 2-responsive NAC transcription factor, controls senescence in Arabidopsis thaliana. Mol. Plant, 4, 346-360.
4. Cantero, A., Barthakur, S., Bushart, T.J., Chou, S., Morgan, R.O., Fernandez, M.P., Clark, G.B., and, Roux, S.J., (2006) Expression profiling of the Arabidopsis annexin gene family during germination, de-etiolation and abiotic stress. Plant Physiol. Biochem. 44, 13-24.
5. Clark, G.B., Morgan, R.O., Fernandez, M.-P., and, Roux, S.J., (2012) Evolutionary adaptation of plant annexins has diversified their molecular structures, interactions and functional roles. New Phytol. 196, 695-712.
6. 2+-interdependent, reactive oxygen species gradient is associated with polarized growth in Fucus serratus zygotes. Planta, 227, 1037-1046.
7. Cõrdoba-Pedregosa, M.D., Cõrdoba, F., Villaba, J.M., and, González-Reyes, J.A., (2003) Zonal changes in ascorbate and hydrogen peroxide contents and ascorbate-related enzyme activities in onion roots. Plant Physiol., 131, 697-706.
8. +-permeable channels in plant root cells. J. Cell Sci. 116, 81-88.
9. 2+ channels. Plant J. 49, 377-386.
10. 2+ channels. Plant J. 58, 903-913.
11. +-efflux conductance activated by hydroxyl radicals: single-channel properties, genetic basis and involvement in stress-induced cell death. J. Cell Sci. 123, 1468-1479.
12. Dinneny, J.R., Long, T.A., Wang, J.Y., et al. (2008) Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science, 320, 942-945.
13. Foreman, J., Demidchik, V., Bothwell, J.H., et al. (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature, 422, 442-446.
14. Foyer, C.H., and, Noctor, G., (2011) Ascorbate and glutathione: the heart of the redox. Plant Physiol. 155, 2-18.
15. Gadjev, I., Vanderauwera, S., Gechev, T.S., Laloi, C., Minkov, I.N., Shulaev, V., Apel, K., Inze, D., Mittler, R., and, Van Breusegem, F., (2006) Transcriptomic footprints disclose specificity of reactive oxygen species signaling in Arabidopsis. Plant Physiol. 141, 436-445.
16. 2. J. Biol. Chem. 285, 29286-29294.
17. + release into the xylem sap. Cell, 94, 647-655.
18. Gorecka, K.M., Konopka-Postupolska, D., Hennig, J., Buchet, R., and, Pikula, S., (2005) Peroxidase activity of annexin 1 from Arabidopsis thaliana. Biochem. Biophys. Res. Commun. 336, 868-875.
19. Hooijmaijers, C., Rhee, J.Y., Kwak, K.J., Chung, G.C., Horie, T., Katsuhara, M., and, Kang, H., (2012) Hydrogen peroxide permeability of plasma membrane aquaporins of Arabidopsis thaliana. J. Plant. Res. 125, 147-153.
20. Hua, D., Wang, C., He, J., He, J.N., Liao, H., Duan, Y., Zhu, Z.Q., Guo, Y., Chen, Z.Z., and, Gong, Z.Z., (2012) A plasma membrane receptor kinase, GHR1, mediates abscisic acid- and hydrogen peroxide-regulated stomatal movement in Arabidopsis. Plant Cell, 24, 2546-2561.
21. Huh, S.M., Noh, E.Y., Kim, H.G., Jeon, B.W., Bae, K., Hu, H.C., Kwak, J.M., and, Park, O.K., (2010) Arabidopsis annexins AnnAt1 and AnnAt4 interact with each other and regulate drought and salt-stress responses. Plant Cell Physiol. 59, 1499-1514.
22. Konopka-Postupolska, D., Clark, G., Goch, G., Debski, J., Floras, K., Cantero, A., Fijolek, B., Roux, S., and, Hennig, J., (2009) The role of annexin 1 in drought stress in Arabidopsis. Plant Physiol. 150, 1394-1410.
23. 2+-influx in B-cells. Curr. Biol. 9, 1403-1406.
24. Kung, C.-C.S., Huang, W.-N., Huang, Y.C., and, Yeh, K.C., (2006) Proteomic survey of copper-binding proteins in Arabidopsis roots by immobilized metal affinity chromatography and mass spectrometry. Proteomics, 6, 2746-2758.
25. Laohavisit, A., and, Davies, J.M., (2009) Multifunctional annexins. Plant Sci. 177, 532-539.
26. Laohavisit, A., and, Davies, J.M., (2011) Annexins. New Phytol. 189, 40-53.
27. 2+- permeable conductance. Plant Cell, 21, 479-493.
28. Laohavisit, A., Brown, A.T., Cicuta, P., and, Davies, J.M., (2010) Annexins: components of the calcium and reactive oxygen signaling network. Plant Physiol. 152, 1824-1829.
29. +-permeable conductance in root cells. Plant Cell, 24, 1522-1533.
30. Li, S.W., Xue, L.G., Xu, S.J., Feng, H.Y., and, An, L.Z., (2009) Hydrogen peroxide acts as a signal molecule in the adventitious root formation of mung bean seedlings. Environ. Exp. Bot. 65, 63-71.
31. Li, S., Wang, X., Zhang, Y., Zhang, Y.L., Jia, H.L., and, Bi, Y.R., (2011) cGMP regulates hydrogen peroxide accumulation in calcium-dependent salt resistance pathway in Arabidopsis thaliana roots. Planta, 234, 709-722.
32. â- by maize roots and their role in wall loosening and elongation growth. Plant Physiol. 136, 3114-3123.
33. Marino, D., Dunand, C., Puppo, A., and, Pauly, N., (2012) A burst of plant NADPH oxidases. Trends Plant Sci. 17, 9-15.
34. McAinsh, M.R., and, Pitman, J.K., (2009) Shaping the calcium signature. New Phytol. 181, 275-294.
35. Miller, G., Schlauch, K., Tam, R., Cortes, D., Torres, M.A., Shulaev, V., Dangl, J.L., and, Mittler, R., (2009) The plant NADPH oxidase RBOHD mediates rapid systemic signaling in response to diverse stimuli. Sci. Signal. 2, ra45.
36. Miller, G., Suzuki, N., Ciftci-Yilmaz, S., and, Mittler, R., (2010) Reactive oxygen species homeostasis and signaling during drought and salinity stresses. Plant, Cell Environ. 33, 453-467.
37. Mittler, R., Vanderauwera, S., Suzuki, N., Miller, G., Tognetti, V.B., Vandepoele, K., Gollery, M., Shulaev, V., and, Van Breusegem, F., (2011) ROS signaling: the new wave? Trends Plant Sci. 16, 300-309.
38. Nasution, O., Srinivasa, K., Kim, M., Kim, Y.J., Kim, W., Jeong, W., and, Choi, W., (2008) Hydrogen peroxide induces hyphal differentiation in Candida albicans. Eukaryot. Cell, 7, 2008-2011.
39. Pfaffl, M.W., (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29 (9), e45.
40. Ramakers, C., Ruijter, J.M., Deprez, R.H.L., and, Moorman, A.F.M., (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci. Lett. 339, 60-62.
41. Rentel, M.C., and, Knight, M.R., (2004) Oxidative stress-induced calcium signaling in Arabidopsis. Plant Physiol. 135, 1471-1479.
42. Rodrigo-Moreno, A., Andrés-Colás, N., Poschenrieder, C., Gunsé, B., Peñarrubia, L., and, Shabala, S., (2013) Calcium- and potassium-permeable plasma membrane transporters are activated by copper in Arabidopsis root tips: linking copper transport with cytosolic hydroxyl radical production. Plant, Cell Environ. 36, 844-855.
43. Scheuring, D., Viotti, C., Kruger, F., et al. (2011) Multivesicular bodies mature from the trans-golgi network/early endosome in Arabidopsis. Plant Cell, 23, 3463-3481.
44. - fluxes associated with post-chilling recovery of plasma membrane transporters in Zea mays leaf and root tissues. Physiol. Plant. 114, 47-56.
45. Short, E.F., North, K.A., Roberts, M.R., Hetherington, A.M., Shirras, A.D., and, McAinsh, M.R., (2012) A stress-specific calcium signature regulating an ozone-responsive gene expression network in Arabidopsis. Plant J. 71, 948-961.
46. Swanson, S., and, Gilroy, S., (2010) ROS in plant development. Physiol. Plant. 138, 384-392.
47. Tsukagoshi, H., Busch, W., and, Benfey, P.N., (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell, 143, 606-616.
48. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., and, Speleman, F., (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3 (7), 00341.
49. Whalley, H.J., and, Knight, M.R., (2013) Calcium signatures are decoded by plants to give specific gene responses. New Phytol. 197, 690-693.
50. 2 increased catalase and peroxidase activities and proline content in Nitraria tangutorum callus. Biol. Plant. 56, 330-336.
51. Zhang, W., Jeon, B.W., and, Assmann, S.M., (2011) Heterotrimeric G-protein regulation of ROS signaling and calcium currents in Arabidopsis guard cells. J. Exp. Bot. 62, 2371-2379.