Home LiteratureArticle Details
PMID: 20837703 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

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

Plant physiology ·Vol. 154 ·No. 3 ·2010-11-00 ·Pages 1158-71

Boursiac Y, Lee SM, Romanowsky S, Blank R, Sladek C, Chung WS, Harper JF

Abstract

Calcium (Ca(2+)) signals regulate many aspects of plant development, including a programmed cell death pathway that protects plants from pathogens (hypersensitive response). Cytosolic Ca(2+) signals result from a combined action of Ca(2+) influx through channels and Ca(2+) efflux through pumps and cotransporters. Plants utilize calmodulin-activated Ca(2+) pumps (autoinhibited Ca(2+)-ATPase [ACA]) at the plasma membrane, endoplasmic reticulum, and vacuole. Here, we show that a double knockout mutation of the vacuolar Ca(2+) pumps ACA4 and ACA11 in Arabidopsis (Arabidopsis thaliana) results in a high frequency of hypersensitive response-like lesions. The appearance of macrolesions could be suppressed by growing plants with increased levels (greater than 15 mm) of various anions, providing a method for conditional suppression. By removing plants from a conditional suppression, lesion initials were found to originate primarily in leaf mesophyll cells, as detected by aniline blue staining. Initiation and spread of lesions could also be suppressed by disrupting the production or accumulation of salicylic acid (SA), as shown by combining aca4/11 mutations with a sid 2 (for salicylic acid induction-deficient2) mutation or expression of the SA degradation enzyme NahG. This indicates that the loss of the vacuolar Ca(2+) pumps by itself does not cause a catastrophic defect in ion homeostasis but rather potentiates the activation of a SA-dependent programmed cell death pathway. Together, these results provide evidence linking the activity of the vacuolar Ca(2+) pumps to the control of a SA-dependent programmed cell death pathway in plants.

MeSH Terms
Apoptosis Arabidopsis/enzymology,genetics Arabidopsis Proteins/genetics,metabolism Calcium Signaling Calcium-Transporting ATPases/genetics,metabolism Gene Expression Regulation, Plant Gene Knockout Techniques Mutation Pseudomonas syringae Salicylic Acid/metabolism Vacuoles/enzymology
Chemicals
Arabidopsis Proteins ACA11 protein, Arabidopsis ACA4 protein, Arabidopsis Calcium-Transporting ATPases Salicylic Acid
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Boursiac Yann
Biochemistry Department, University of Nevada, Reno, Nevada 89557, USA.
Lee Sang Min
Romanowsky Shawn
Blank Robert
Sladek Chris
Chung Woo Sik
Harper Jeffrey F
References (77)
77 references, click to expand
  1. The grateful dead: calcium and cell death in plant innate immunity.
    Cell Microbiol. 2007 Nov;9(11):2571-85 PMID: 17714518
  2. 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. 1997 Nov;9(11):2077-2091 PMID: 12237354
  3. Salicylic acid induction-deficient mutants of Arabidopsis express PR-2 and PR-5 and accumulate high levels of camalexin after pathogen inoculation.
    Plant Cell. 1999 Aug;11(8):1393-404 PMID: 10449575
  4. Identification of putative voltage-dependent Ca2+-permeable channels involved in cryptogein-induced Ca2+ transients and defense responses in tobacco BY-2 cells.
    Biochem Biophys Res Commun. 2004 May 7;317(3):823-30 PMID: 15081414
  5. A cyclic nucleotide-gated channel is essential for polarized tip growth of pollen.
    Proc Natl Acad Sci U S A. 2007 Sep 4;104(36):14531-6 PMID: 17726111
  6. Programmed cell death in plants: distinguishing between different modes.
    J Exp Bot. 2008;59(3):435-44 PMID: 18256053
  7. A plant plasma membrane Ca2+ pump is required for normal pollen tube growth and fertilization.
    Proc Natl Acad Sci U S A. 2004 Jun 22;101(25):9502-7 PMID: 15197266
  8. Acquired resistance in Arabidopsis.
    Plant Cell. 1992 Jun;4(6):645-56 PMID: 1392589
  9. Targeted ablation of plasma membrane Ca2+-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. 2004 Aug 6;279(32):33742-50 PMID: 15178683
  10. Roles of Ion Channels in Initiation of Signal Transduction in Higher Plants.
    Plant Cell. 1995 Jul;7(7):833-844 PMID: 12242389
  11. Genomic comparison of P-type ATPase ion pumps in Arabidopsis and rice.
    Plant Physiol. 2003 Jun;132(2):618-28 PMID: 12805592
  12. Roles of ion channels and transporters in guard cell signal transduction.
    FEBS Lett. 2007 May 25;581(12):2325-36 PMID: 17462636
  13. The chimeric cyclic nucleotide-gated ion channel ATCNGC11/12 constitutively induces programmed cell death in a Ca2+ dependent manner.
    Plant Mol Biol. 2007 Dec;65(6):747-61 PMID: 17885810
  14. The Arabidopsis dnd1 "defense, no death" gene encodes a mutated cyclic nucleotide-gated ion channel.
    Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):9323-8 PMID: 10900264
  15. Vacuolar calcium channels.
    J Exp Bot. 2007;58(7):1559-69 PMID: 17355948
  16. Ca(2+)/calmodulin regulates salicylic-acid-mediated plant immunity.
    Nature. 2009 Feb 26;457(7233):1154-8 PMID: 19122675
  17. Programmed cell death in plants: new insights into redox regulation and the role of hydrogen peroxide.
    Int Rev Cell Mol Biol. 2008;270:87-144 PMID: 19081535
  18. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  19. Relationship between calcium decoding elements and plant abiotic-stress resistance.
    Int J Biol Sci. 2008 Apr 26;4(2):116-25 PMID: 18463716
  20. Calcium signaling.
    Cell. 2007 Dec 14;131(6):1047-58 PMID: 18083096
  21. The role of SERCA2a/PLN complex, Ca(2+) homeostasis, and anti-apoptotic proteins in determining cell fate.
    Pflugers Arch. 2009 Jan;457(3):687-700 PMID: 18415121
  22. Calmodulin interacts with MLO protein to regulate defence against mildew in barley.
    Nature. 2002 Mar 28;416(6879):447-51 PMID: 11919636
  23. Ca2+ signals coordinate zygotic polarization and cell cycle progression in the brown alga Fucus serratus.
    Development. 2008 Jun;135(12):2173-81 PMID: 18480164
  24. Programmed cell death in development and defense.
    Plant Physiol. 2001 Jan;125(1):94-7 PMID: 11154305
  25. A calcium-dependent protein kinase can inhibit a calmodulin-stimulated Ca2+ pump (ACA2) located in the endoplasmic reticulum of Arabidopsis.
    Proc Natl Acad Sci U S A. 2000 May 23;97(11):6224-9 PMID: 10823962
  26. The vacuolar Ca2+-activated channel TPC1 regulates germination and stomatal movement.
    Nature. 2005 Mar 17;434(7031):404-8 PMID: 15772667
  27. Nitrate efflux is an essential component of the cryptogein signaling pathway leading to defense responses and hypersensitive cell death in tobacco.
    Plant Cell. 2002 Aug;14(8):1937-51 PMID: 12172032
  28. Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants?
    Trends Plant Sci. 2003 Jun;8(6):263-71 PMID: 12818660
  29. A distinct endosomal Ca2+/Mn2+ pump affects root growth through the secretory process.
    Plant Physiol. 2008 Aug;147(4):1675-89 PMID: 18567829
  30. Guard cell ABA and CO2 signaling network updates and Ca2+ sensor priming hypothesis.
    Curr Opin Plant Biol. 2006 Dec;9(6):654-63 PMID: 17010657
  31. Calcium, kinases and nodulation signalling in legumes.
    Nat Rev Mol Cell Biol. 2004 Jul;5(7):566-76 PMID: 15232574
  32. Genome-wide insertional mutagenesis of Arabidopsis thaliana.
    Science. 2003 Aug 1;301(5633):653-7 PMID: 12893945
  33. Self-incompatibility in Papaver: signalling to trigger PCD in incompatible pollen.
    J Exp Bot. 2008;59(3):481-90 PMID: 17872920
  34. Insertional mutagenesis of genes required for seed development in Arabidopsis thaliana.
    Genetics. 2001 Dec;159(4):1751-63 PMID: 11779812
  35. A central role of salicylic Acid in plant disease resistance.
    Science. 1994 Nov 18;266(5188):1247-50 PMID: 17810266
  36. An endoplasmic reticulum-bound Ca(2+)/Mn(2+) pump, ECA1, supports plant growth and confers tolerance to Mn(2+) stress.
    Plant Physiol. 2002 Sep;130(1):128-37 PMID: 12226493
  37. pGreen: a versatile and flexible binary Ti vector for Agrobacterium-mediated plant transformation.
    Plant Mol Biol. 2000 Apr;42(6):819-32 PMID: 10890530
  38. The ACA10 Ca2+-ATPase regulates adult vegetative development and inflorescence architecture in Arabidopsis.
    Plant Physiol. 2008 Feb;146(2):716-28 PMID: 18065565
  39. The guard cell as a single-cell model towards understanding drought tolerance and abscisic acid action.
    J Exp Bot. 2009;60(5):1439-63 PMID: 19181866
  40. Distinct phenotypes among plasma membrane Ca2+-ATPase knockout mice.
    Ann N Y Acad Sci. 2007 Mar;1099:276-86 PMID: 17446468
  41. Calcium in plant defence-signalling pathways.
    New Phytol. 2006;171(2):249-69 PMID: 16866934
  42. Expression of an Arabidopsis CAX2 variant in potato tubers increases calcium levels with no accumulation of manganese.
    Plant Cell Rep. 2006 Nov;25(11):1226-32 PMID: 17024452
  43. 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. 2007 Dec;48(12):1775-89 PMID: 17981874
  44. Nitric oxide, stomatal closure, and abiotic stress.
    J Exp Bot. 2008;59(2):165-76 PMID: 18332225
  45. The generation of Ca(2+) signals in plants.
    Annu Rev Plant Biol. 2004;55:401-27 PMID: 15377226
  46. The origin and function of calmodulin regulated Ca2+ pumps in plants.
    J Bioenerg Biomembr. 2007 Dec;39(5-6):409-14 PMID: 18000746
  47. Calcium- and salt-stress signaling in plants: shedding light on SOS pathway.
    Arch Biochem Biophys. 2008 Mar 15;471(2):146-58 PMID: 18241665
  48. The barley MLO modulator of defense and cell death is responsive to biotic and abiotic stress stimuli.
    Plant Physiol. 2002 Jul;129(3):1076-85 PMID: 12114562
  49. Identification of a calmodulin-regulated autoinhibited Ca2+-ATPase (ACA11) that is localized to vacuole membranes in Arabidopsis.
    FEBS Lett. 2007 Aug 21;581(21):3943-9 PMID: 17662727
  50. CNGCs: prime targets of plant cyclic nucleotide signalling?
    Trends Plant Sci. 2003 Jun;8(6):286-93 PMID: 12818663
  51. The language of calcium signaling.
    Annu Rev Plant Biol. 2010;61:593-620 PMID: 20192754
  52. Differential and chaotic calcium signatures in the symbiosis signaling pathway of legumes.
    Proc Natl Acad Sci U S A. 2008 Jul 15;105(28):9823-8 PMID: 18606999
  53. Glucose-induced mixed [Ca2+]c oscillations in mouse beta-cells are controlled by the membrane potential and the SERCA3 Ca2+-ATPase of the endoplasmic reticulum.
    Am J Physiol Cell Physiol. 2006 Jun;290(6):C1503-11 PMID: 16381799
  54. Isochorismate synthase is required to synthesize salicylic acid for plant defence.
    Nature. 2001 Nov 29;414(6863):562-5 PMID: 11734859
  55. Plant ion channels: gene families, physiology, and functional genomics analyses.
    Annu Rev Physiol. 2009;71:59-82 PMID: 18842100
  56. Vascular associated death1, a novel GRAM domain-containing protein, is a regulator of cell death and defense responses in vascular tissues.
    Plant Cell. 2004 Aug;16(8):2217-32 PMID: 15269331
  57. Requirement of salicylic Acid for the induction of systemic acquired resistance.
    Science. 1993 Aug 6;261(5122):754-6 PMID: 17757215
  58. Lesion mimic mutants: A classical, yet still fundamental approach to study programmed cell death.
    Plant Signal Behav. 2008 Oct;3(10):764-7 PMID: 19513227
  59. Calcium and cell death.
    Subcell Biochem. 2007;45:465-80 PMID: 18193648
  60. Innate immunity signaling: cytosolic Ca2+ elevation is linked to downstream nitric oxide generation through the action of calmodulin or a calmodulin-like protein.
    Plant Physiol. 2008 Oct;148(2):818-28 PMID: 18689446
  61. 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. 2007 Sep 7;282(36):26517-27 PMID: 17597066
  62. Function of endoplasmic reticulum calcium ATPase in innate immunity-mediated programmed cell death.
    EMBO J. 2010 Mar 3;29(5):1007-18 PMID: 20075858
  63. Identification of a putative voltage-gated Ca2+ channel as a key regulator of elicitor-induced hypersensitive cell death and mitogen-activated protein kinase activation in rice.
    Plant J. 2005 Jun;42(6):798-809 PMID: 15941394
  64. Arabidopsis mutants simulating disease resistance response.
    Cell. 1994 May 20;77(4):565-77 PMID: 8187176
  65. An early Ca2+ influx is a prerequisite to thaxtomin A-induced cell death in Arabidopsis thaliana cells.
    J Exp Bot. 2008;59(15):4259-70 PMID: 19015217
  66. The Arabidopsis knockout facility at the University of Wisconsin-Madison.
    Plant Physiol. 2000 Dec;124(4):1465-7 PMID: 11115860
  67. Transgenic expression of the von Willebrand A domain of the BONZAI 1/COPINE 1 protein triggers a lesion-mimic phenotype in Arabidopsis.
    Planta. 2005 Apr;221(1):85-94 PMID: 15843967
  68. Anion channel activity is necessary to induce ethylene synthesis and programmed cell death in response to oxalic acid.
    J Exp Bot. 2008;59(11):3121-9 PMID: 18612171
  69. Expression of Arabidopsis CAX1 in tobacco: altered calcium homeostasis and increased stress sensitivity.
    Plant Cell. 1999 Nov;11(11):2113-22 PMID: 10559438
  70. Evidence that the BONZAI1/COPINE1 protein is a calcium- and pathogen-responsive defense suppressor.
    Plant Mol Biol. 2009 Jan;69(1-2):155-66 PMID: 18855102
  71. Controlled cell death, plant survival and development.
    Nat Rev Mol Cell Biol. 2004 Apr;5(4):305-15 PMID: 15071555
  72. Calcium signals: the lead currency of plant information processing.
    Plant Cell. 2010 Mar;22(3):541-63 PMID: 20354197
  73. The ACA4 gene of Arabidopsis encodes a vacuolar membrane calcium pump that improves salt tolerance in yeast.
    Plant Physiol. 2000 Dec;124(4):1814-27 PMID: 11115896
  74. A PIIB-type Ca2+-ATPase is essential for stress adaptation in Physcomitrella patens.
    Proc Natl Acad Sci U S A. 2008 Dec 9;105(49):19555-60 PMID: 19050080
  75. Loss of the vacuolar cation channel, AtTPC1, does not impair Ca2+ signals induced by abiotic and biotic stresses.
    Plant J. 2008 Jan;53(2):287-99 PMID: 18028262
  76. The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: twenty-something years on.
    Nat Protoc. 2006;1(2):581-5 PMID: 17406285
  77. Shaping the calcium signature.
    New Phytol. 2009 Jan;181(2):275-294 PMID: 19121028
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
1532-2548
DOI
10.1104/pp.110.159038
Published
2010-11-00
Epub
2010-00-13
Pages
1158-71
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC2971596
Subset
IM
Grants
NIGMS NIH HHS · 1R01 GM070813-01 · United States
NIDCR NIH HHS · DE-FG03-94ER20152 · United States
NCRR NIH HHS · P20 RR-016464 · United States
External Links
PubMed source DOI: 10.1104/pp.110.159038 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2