Disruption of the vacuolar calcium-ATPases in arabidopsis results in the activation of a salicylic acid-dependent programmed cell death pathway

Plant Physiology

Volumn 154, Issue 3, 2010, Pages 1158-1171

  Boursiac, Yann ^a,b   Lee, Sang Min ^a   Romanowsky, Shawn ^a   Blank, Robert ^a   Sladek, Chris ^a   Chung, Woo Sik ^a   Harper, Jeffrey F ^a  

^a UNIVERSITY OF NEVADA   (United States)

^b Gyeongsang National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 78249289916     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.110.159038     Document Type: Article

References (78)

1. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ, Chen H, Shinn P, Stevenson DK, Zimmerman J, Barajas P, Cheuk R, et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657
2. Baxter I, Tchieu J, Sussman MR, Boutry M, Palmgren MG, Gribskov M, Harper JF, Axelsen KB (2003) Genomic comparison of P-type ATPase ion pumps in Arabidopsis and rice. Plant Physiol 132: 618-628
3. 2+-ATPase of the endoplasmic reticulum. Am J Physiol Cell Physiol 290: C1503-C1511
4. Bonaventure G, Gfeller A, Rodríguez VM, Armand F, Farmer EE (2007) The fou2 gain-of-function allele and the wild-type allele of Two Pore Channel 1 contribute to different extents or by different mechanisms to defense gene expression in Arabidopsis. Plant Cell Physiol 48: 1775-1789
5. Bosch M, Franklin-Tong VE (2008) Self-incompatibility in Papaver: signaling to trigger PCD in incompatible pollen. J Exp Bot 59: 481-490
6. 2+ signals coordinate zygotic polarization and cell cycle progression in the brown alga Fucus serratus. Development 135: 2173-2181
7. 2+ pumps in plants. J Bioenerg Biomembr 39: 409-414
8. Chomczynski P, Sacchi N (2006) The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: twentysomething years on. Nat Protoc 1: 581-585
9. Clapham DE (2007) Calcium signaling. Cell 131: 1047-1058
10. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium- mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
11. Clough SJ, Fengler KA, Yu IC, Lippok B, Smith RK Jr, Bent AF (2000) The Arabidopsis dnd1 "defense, no death" gene encodes a mutated cyclic nucleotide-gated ion channel. Proc Natl Acad Sci USA 97: 9323-9328
12. Delaney TP, Uknes S, Vernooij B, Friedrich L, Weymann K, Negrotto D, Gaffney T, Gut-Rella M, Kessmann H, Ward E, et al (1994) A central role of salicylic acid in plant disease resistance. Science 266: 1247-1250
13. Dietrich RA, Delaney TP, Uknes SJ, Ward ER, Ryals JA, Dangl JL (1994) Arabidopsis mutants simulating disease resistance response. Cell 77: 565-577
14. Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annu Rev Plant Biol 61: 593-620
15. Du L, Ali GS, Simons KA, Hou J, Yang T, Reddy ASN, Poovaiah BW (2009) Ca(2+)/calmodulin regulates salicylic-acid-mediated plant immunity. Nature 457: 1154-1158
16. 2+ influx is a prerequisite to thaxtomin A-induced cell death in Arabidopsis thaliana cells. J Exp Bot 59: 4259-4270
17. Errakhi R, Meimoun P, Lehner A, Vidal G, Briand J, Corbineau F, Rona JP, Bouteau F (2008b) Anion channel activity is necessary to induce ethylene synthesis and programmed cell death in response to oxalic acid. J Exp Bot 59: 3121-3129
18. Frietsch S, Wang YF, Sladek C, Poulsen LR, Romanowsky SM, Schroeder JI, Harper JF (2007) A cyclic nucleotide-gated channel is essential for polarized tip growth of pollen. Proc Natl Acad Sci USA 104: 14531-14536
19. Gadjev I, Stone JM, Gechev TS (2008) Programmed cell death in plants: new insights into redox regulation and the role of hydrogen peroxide. Int Rev Cell Mol Biol 270: 87-144
20. Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Kessmann H, Ryals J (1993) Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261: 754-756
21. Geisler M, Frangne N, Gomès E, Martinoia E, Palmgren MG (2000) The ACA4 gene of Arabidopsis encodes a vacuolar membrane calcium pump that improves salt tolerance in yeast. Plant Physiol 124: 1814-1827
22. 2+-ATPase regulates adult vegetative development and inflorescence architecture in Arabidopsis. Plant Physiol 146: 716-728
23. Hellens RP, Edwards EA, Leyland NR, Bean S, Mullineaux PM (2000) pGreen: a versatile and flexible binary Ti vector for Agrobacteriummediated plant transformation. Plant Mol Biol 42: 819-832
24. Hetherington AM, Brownlee C (2004) The generation of Ca(2+) signals in plants. Annu Rev Plant Biol 55: 401-427
25. Hirschi KD (1999) Expression of Arabidopsis CAX1 in tobacco: altered calcium homeostasis and increased stress sensitivity. Plant Cell 11: 2113-2122
26. 2+ pump (ACA2) located in the endoplasmic reticulum of Arabidopsis. Proc Natl Acad Sci USA 97: 6224-6229
27. 2+ sensor priming hypothesis. Curr Opin Plant Biol 9: 654-663
28. Jones AM (2001) Programmed cell death in development and defense. Plant Physiol 125: 94-97
29. 2+ transients and defense responses in tobacco BY-2 cells. Biochem Biophys Res Commun 317: 823-830
30. Kim CK, Han JS, Lee HS, Oh JY, Shigaki T, Park SH, Hirschi K (2006) Expression of an Arabidopsis CAX2 variant in potato tubers increases calcium levels with no accumulation of manganese. Plant Cell Rep 25: 1226-1232
31. Kim MC, Panstruga R, Elliott C, Müller J, Devoto A, Yoon HW, Park HC, Cho MJ, Schulze-Lefert P (2002) Calmodulin interacts with MLO protein to regulate defence against mildew in barley. Nature 416: 447-451
32. Kosuta S, Hazledine S, Sun J, Miwa H, Morris RJ, Downie JA, Oldroyd GED (2008) Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes. Proc Natl Acad Sci USA 105: 9823-9828
33. Kudla J, Batistic O, Hashimoto K (2010) Calcium signals: the lead currency of plant information processing. Plant Cell 22: 541-563
34. 2+ channel as a key regulator of elicitor-induced hypersensitive cell death and mitogen-activated protein kinase activation in rice. Plant J 42: 798-809
35. Lam E (2004) Controlled cell death, plant survival and development. Nat Rev Mol Cell Biol 5: 305-315
36. Lecourieux D, Ranjeva R, Pugin A (2006) Calcium in plant defencesignalling pathways. New Phytol 171: 249-269
37. 2+-ATPase (ACA11) that is localized to vacuole membranes in Arabidopsis. FEBS Lett 581: 3943-3949
38. Lee TF, McNellis TW (2009) Evidence that the BONZAI1/COPINE1 protein is a calcium- and pathogen-responsive defense suppressor. Plant Mol Biol 69: 155-166
39. 2+/Mn2+ pump affects root growth through the secretory process. Plant Physiol 147: 1675-1689
40. Liu J, Jambunathan N, McNellis TW (2005) Transgenic expression of the von Willebrand A domain of the BONZAI 1/COPINE 1 protein triggers a lesion-mimic phenotype in Arabidopsis. Planta 221: 85-94
41. Loewus FA, Murthy PPN (2000) Myo-inositol metabolism in plants. Plant Sci 150: 1-19
42. Lorrain S, Lin B, Auriac MC, Kroj T, Saindrenan P, Nicole M, Balagué C, Roby D (2004) Vascular associated death1, a novel GRAM domaincontaining protein, is a regulator of cell death and defense responses in vascular tissues. Plant Cell 16: 2217-2232
43. Lorrain S, Vailleau F, Balagué C, Roby D (2003) Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci 8: 263-271
44. Ma W, Berkowitz GA (2007) The grateful dead: calcium and cell death in plant innate immunity. Cell Microbiol 9: 2571-2585
45. 2+ elevation is linked to downstream nitric oxide generation through the action of calmodulin or a calmodulin-like protein. Plant Physiol 148: 818-828
46. Mahajan S, Pandey GK, Tuteja N (2008) Calcium- and salt-stress signaling in plants: shedding light on SOS pathway. Arch Biochem Biophys 471: 146-158
47. McAinsh MR, Pittman JK (2009) Shaping the calcium signature. New Phytol 181: 275-294
48. McElver J, Tzafrir I, Aux G, Rogers R, Ashby C, Smith K, Thomas C, Schetter A, Zhou Q, Cushman MA, et al (2001) Insertional mutagenesis of genes required for seed development in Arabidopsis thaliana. Genetics 159: 1751-1763
49. Moeder W, Yoshioka K (2008) Lesion mimic mutants: a classical, yet still fundamental approach to study programmed cell death. Plant Signal Behav 3: 764-767
50. Nawrath C, Métraux JP (1999) Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation. Plant Cell 11: 1393-1404
51. Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Morris P, Ribeiro D, Wilson I (2008) Nitric oxide, stomatal closure, and abiotic stress. J Exp Bot 59: 165-176
52. Okunade GW, Miller ML, Azhar M, Andringa A, Sanford LP, Doetschman T, Prasad V, Shull GE (2007) Loss of the Atp2c1 secretory pathway Ca(2+)-ATPase (SPCA1) in mice causes Golgi stress, apoptosis, and midgestational death in homozygous embryos and squamous cell tumors in adult heterozygotes. J Biol Chem 282: 26517-26527
53. 2+-ATPase (PMCA) 1 and 4 indicates a major housekeeping function for PMCA1 and a critical role in hyperactivated sperm motility and male fertility for PMCA4. J Biol Chem 279: 33742-33750
54. Oldroyd GED, Downie JA (2004) Calcium, kinases and nodulation signaling in legumes. Nat Rev Mol Cell Biol 5: 566-576
55. Pandey S, Zhang W, Assmann SM (2007) Roles of ion channels and transporters in guard cell signal transduction. FEBS Lett 581: 2325-2336
56. 2+-activated channel TPC1 regulates germination and stomatal movement. Nature 434: 404-408
57. Piffanelli P, Zhou F, Casais C, Orme J, Jarosch B, Schaffrath U, Collins NC, Panstruga R, Schulze-Lefert P (2002) The barleyMLOmodulator of defense and cell death is responsive to biotic and abiotic stress stimuli. Plant Physiol 129: 1076-1085
58. Pottosin II, Schönknecht G (2007) Vacuolar calcium channels. J Exp Bot 58: 1559-1569
59. 2+-ATPase knockout mice. Ann N Y Acad Sci 1099: 276-286
60. Pugin A, Frachisse JM, Tavernier E, Bligny R, Gout E, Douce R, Guern J (1997) Early events induced by the elicitor cryptogein in tobacco cells: involvement of a plasma membrane NADPH oxidase and activation of glycolysis and the pentose phosphate pathway. Plant Cell 9: 2077-2091
61. 2+-ATPase is essential for stress adaptation in Physcomitrella patens. Proc Natl Acad Sci USA 105: 19555-19560
62. 2+ signals induced by abiotic and biotic stresses. Plant J 53: 287-299
63. Reape TJ, Molony EM, McCabe PF (2008) Programmed cell death in plants: distinguishing between different modes. J Exp Bot 59: 435-444
64. 2+ pump is required for normal pollen tube growth and fertilization. Proc Natl Acad Sci USA 101: 9502-9507
65. Sirichandra C, Wasilewska A, Vlad F, Valon C, Leung J (2009) The guard cell as a single-cellmodel towards understanding drought tolerance and abscisic acid action. J Exp Bot 60: 1439-1463
66. Song WY, Zhang ZB, Shao HB, Guo XL, Cao HX, Zhao HB, Fu ZY, Hu XJ (2008) Relationship between calcium decoding elements and plant abiotic-stress resistance. Int J Biol Sci 4: 116-125
67. Sussman MR, Amasino RM, Young JC, Krysan PJ, Austin-Phillips S (2000) The Arabidopsis knockout facility at the University ofWisconsin- Madison. Plant Physiol 124: 1465-1467
68. Talke IN, Blaudez D, Maathuis FJM, Sanders D (2003) CNGCs: prime targets of plant cyclic nucleotide signalling? Trends Plant Sci 8: 286-293
69. Uknes S, Mauch-Mani B, Moyer M, Potter S, Williams S, Dincher S, Chandler D, Slusarenko A, Ward E, Ryals J (1992) Acquired resistance in Arabidopsis. Plant Cell 4: 645-656
70. 2+ dependent manner. Plant Mol Biol 65: 747-761
71. Vafiadaki E, Papalouka V, Arvanitis DA, Kranias EG, Sanoudou D (2009) The role of SERCA2a/PLN complex, Ca(2+) homeostasis, and antiapoptotic proteins in determining cell fate. Pflugers Arch 457: 687-700
72. Verkhratsky A (2007) Calcium and cell death. Subcell Biochem 45: 465-480
73. Ward JM, Mäser P, Schroeder JI (2009) Plant ion channels: gene families, physiology, and functional genomics analyses. Annu Rev Physiol 71: 59-82
74. Ward JM, Pei ZM, Schroeder JI (1995) Roles of ion channels in initiation of signal transduction in higher plants. Plant Cell 7: 833-844
75. Wendehenne D, Lamotte O, Frachisse JM, Barbier-Brygoo H, Pugin A (2002) Nitrate efflux is an essential component of the cryptogein signaling pathway leading to defense responses and hypersensitive cell death in tobacco. Plant Cell 14: 1937-1951
76. Wildermuth MC, Dewdney J, Wu G, Ausubel FM (2001) Isochorismate synthase is required to synthesize salicylic acid for plant defence. Nature 414: 562-565
77. 2+/Mn2+ pump, ECA1, supports plant growth and confers tolerance to Mn2+ stress. Plant Physiol 130: 128-137
78. Zhu X, Caplan J, Mamillapalli P, Czymmek K, Dinesh-Kumar SP (2010) Function of endoplasmic reticulum calcium ATPase in innate immunitymediated programmed cell death. EMBO J 29: 1007-1018