Home LiteratureArticle Details
PMID: 31956021 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Salicylic Acid Targets Protein Phosphatase 2A to Attenuate Growth in Plants.

Current biology : CB ·Vol. 30 ·No. 3 ·2020-00-03 ·Pages 381-395.e8

Tan S, Abas M, Verstraeten I, Glanc M, Molnár G, Hajný J, Lasák P, Petřík I, Russinova E, Petrášek J, Novák O, Pospíšil J, Friml J

Abstract

Plants, like other multicellular organisms, survive through a delicate balance between growth and defense against pathogens. Salicylic acid (SA) is a major defense signal in plants, and the perception mechanism as well as downstream signaling activating the immune response are known. Here, we identify a parallel SA signaling that mediates growth attenuation. SA directly binds to A subunits of protein phosphatase 2A (PP2A), inhibiting activity of this complex. Among PP2A targets, the PIN2 auxin transporter is hyperphosphorylated in response to SA, leading to changed activity of this important growth regulator. Accordingly, auxin transport and auxin-mediated root development, including growth, gravitropic response, and lateral root organogenesis, are inhibited. This study reveals how SA, besides activating immunity, concomitantly attenuates growth through crosstalk with the auxin distribution network. Further analysis of this dual role of SA and characterization of additional SA-regulated PP2A targets will provide further insights into mechanisms maintaining a balance between growth and defense.

Keywords
NPR1 PIN PP2A auxin auxin transport gravitropism immunity phosphorylation protein phosphatase 2A salicylic acid
MeSH Terms
Arabidopsis/growth & development,physiology Arabidopsis Proteins/metabolism Indoleacetic Acids/metabolism Plant Immunity Plant Roots/growth & development,metabolism Protein Phosphatase 2/metabolism Salicylic Acid/metabolism Signal Transduction
Chemicals
Arabidopsis Proteins Indoleacetic Acids PIN2 protein, Arabidopsis PP2A protein, Arabidopsis Protein Phosphatase 2 Salicylic Acid
Authors & Affiliations
13 authors, click to expand affiliations / ORCID
Tan Shutang
Institute of Science and Technology Austria (IST Austria), Am Campus 1, 3400 Klosterneuburg, Austria.
Abas Melinda
Institute of Science and Technology Austria (IST Austria), Am Campus 1, 3400 Klosterneuburg, Austria; Department of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences (BOKU), Muthgasse 18, 1190 Vienna, Austria.
Verstraeten Inge
Institute of Science and Technology Austria (IST Austria), Am Campus 1, 3400 Klosterneuburg, Austria.
Glanc Matouš
Institute of Science and Technology Austria (IST Austria), Am Campus 1, 3400 Klosterneuburg, Austria; Department of Experimental Plant Biology, Faculty of Science, Charles University, Viničná 5, 128 44 Prague 2, Czech Republic.
Molnár Gergely
Institute of Science and Technology Austria (IST Austria), Am Campus 1, 3400 Klosterneuburg, Austria; Department of Applied Genetics and Cell Biology, University of Natural Resources and Life Sciences (BOKU), Muthgasse 18, 1190 Vienna, Austria.
Hajný Jakub
Institute of Science and Technology Austria (IST Austria), Am Campus 1, 3400 Klosterneuburg, Austria; Laboratory of Growth Regulators, The Czech Academy of Sciences, Institute of Experimental Botany & Palacký University, Faculty of Science, Šlechtitelů 27, 783 71 Olomouc, Czech Republic.
Lasák Pavel
Laboratory of Growth Regulators, The Czech Academy of Sciences, Institute of Experimental Botany & Palacký University, Faculty of Science, Šlechtitelů 27, 783 71 Olomouc, Czech Republic.
Petřík Ivan
Laboratory of Growth Regulators, The Czech Academy of Sciences, Institute of Experimental Botany & Palacký University, Faculty of Science, Šlechtitelů 27, 783 71 Olomouc, Czech Republic.
Russinova Eugenia
Department of Plant Biotechnology and Bioinformatics, Ghent University, 9052 Ghent, Belgium; Center for Plant Systems Biology, VIB, 9052 Ghent, Belgium.
Petrášek Jan
Department of Experimental Plant Biology, Faculty of Science, Charles University, Viničná 5, 128 44 Prague 2, Czech Republic; Institute of Experimental Botany, The Czech Academy of Sciences, Rozvojová 263, 165 02 Prague 6, Czech Republic.
Novák Ondřej
Laboratory of Growth Regulators, The Czech Academy of Sciences, Institute of Experimental Botany & Palacký University, Faculty of Science, Šlechtitelů 27, 783 71 Olomouc, Czech Republic.
Pospíšil Jiří
Laboratory of Growth Regulators, The Czech Academy of Sciences, Institute of Experimental Botany & Palacký University, Faculty of Science, Šlechtitelů 27, 783 71 Olomouc, Czech Republic; Department of Organic Chemistry, Faculty of Science, Palacký University, tř. 17. listopadu 1192/12, CZ-771 46 Olomouc, Czech Republic.
Friml Jiří
Institute of Science and Technology Austria (IST Austria), Am Campus 1, 3400 Klosterneuburg, Austria. Electronic address: [email protected].
Conflict of Interest

Declaration of Interests The authors declare no competing interests.

References (79)
79 references, click to expand
  1. Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex.
    Genes Dev. 2001 Oct 15;15(20):2648-53 PMID: 11641271
  2. Structure-function analysis of the presumptive Arabidopsis auxin permease AUX1.
    Plant Cell. 2004 Nov;16(11):3069-83 PMID: 15486104
  3. Negative regulation of defense responses in Arabidopsis by two NPR1 paralogs.
    Plant J. 2006 Dec;48(5):647-56 PMID: 17076807
  4. PIN auxin efflux carrier polarity is regulated by PINOID kinase-mediated recruitment into GNOM-independent trafficking in Arabidopsis.
    Plant Cell. 2009 Dec;21(12):3839-49 PMID: 20040538
  5. ROTUNDA3 function in plant development by phosphatase 2A-mediated regulation of auxin transporter recycling.
    Proc Natl Acad Sci U S A. 2016 Mar 8;113(10):2768-73 PMID: 26888284
  6. Characterization of an Arabidopsis Mutant That Is Nonresponsive to Inducers of Systemic Acquired Resistance.
    Plant Cell. 1994 Nov;6(11):1583-1592 PMID: 12244227
  7. Effect of aspirin on the Wnt/beta-catenin pathway is mediated via protein phosphatase 2A.
    Oncogene. 2006 Oct 19;25(49):6447-56 PMID: 16878161
  8. Nonselective Chemical Inhibition of Sec7 Domain-Containing ARF GTPase Exchange Factors.
    Plant Cell. 2018 Oct;30(10):2573-2593 PMID: 30018157
  9. Opposite Roles of Salicylic Acid Receptors NPR1 and NPR3/NPR4 in Transcriptional Regulation of Plant Immunity.
    Cell. 2018 May 31;173(6):1454-1467.e15 PMID: 29656896
  10. NITRIC OXIDE-ASSOCIATED PROTEIN1 (AtNOA1) is essential for salicylic acid-induced root waving in Arabidopsis thaliana.
    New Phytol. 2015 Jul;207(1):211-24 PMID: 25690466
  11. Activation of Plant Innate Immunity by Extracellular High Mobility Group Box 3 and Its Inhibition by Salicylic Acid.
    PLoS Pathog. 2016 Mar 23;12(3):e1005518 PMID: 27007252
  12. Dissection of Arabidopsis ADP-RIBOSYLATION FACTOR 1 function in epidermal cell polarity.
    Plant Cell. 2005 Feb;17(2):525-36 PMID: 15659621
  13. PLANT MICROBIOME. Salicylic acid modulates colonization of the root microbiome by specific bacterial taxa.
    Science. 2015 Aug 21;349(6250):860-4 PMID: 26184915
  14. Polar transport in plants mediated by membrane transporters: focus on mechanisms of polar auxin transport.
    Curr Opin Plant Biol. 2017 Dec;40:8-14 PMID: 28686910
  15. PIN-driven polar auxin transport in plant developmental plasticity: a key target for environmental and endogenous signals.
    New Phytol. 2014 Jul;203(2):362-77 PMID: 24863651
  16. UHPLC-MS/MS based target profiling of stress-induced phytohormones.
    Phytochemistry. 2014 Sep;105:147-57 PMID: 24947339
  17. Arabidopsis seedling flood-inoculation technique: a rapid and reliable assay for studying plant-bacterial interactions.
    Plant Methods. 2011 Oct 06;7:32 PMID: 21978451
  18. Inducers of plant systemic acquired resistance regulate NPR1 function through redox changes.
    Cell. 2003 Jun 27;113(7):935-44 PMID: 12837250
  19. Specificity of RCN1-mediated protein phosphatase 2A regulation in meristem organization and stress response in roots.
    Plant Physiol. 2008 Feb;146(2):539-53 PMID: 18162590
  20. The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance.
    Plant Cell. 1997 Sep;9(9):1573-84 PMID: 9338960
  21. Salicylic Acid and Jasmonic Acid Pathways are Activated in Spatially Different Domains Around the Infection Site During Effector-Triggered Immunity in Arabidopsis thaliana.
    Plant Cell Physiol. 2018 Jan 1;59(1):8-16 PMID: 29177423
  22. CATALASE2 Coordinates SA-Mediated Repression of Both Auxin Accumulation and JA Biosynthesis in Plant Defenses.
    Cell Host Microbe. 2017 Feb 8;21(2):143-155 PMID: 28182949
  23. Salicylic acid interferes with clathrin-mediated endocytic protein trafficking.
    Proc Natl Acad Sci U S A. 2013 May 7;110(19):7946-51 PMID: 23613581
  24. The anti-inflammatory agents aspirin and salicylate inhibit the activity of I(kappa)B kinase-beta.
    Nature. 1998 Nov 5;396(6706):77-80 PMID: 9817203
  25. EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana.
    Genes Dev. 1998 Jul 15;12(14):2175-87 PMID: 9679062
  26. Specificity of the accumulation of mRNAs and proteins of the plasma membrane and tonoplast aquaporins in radish organs.
    Planta. 2001 Jan;212(2):294-304 PMID: 11216851
  27. Regulation of polar auxin transport by protein and lipid kinases.
    J Exp Bot. 2016 Jul;67(14):4015-4037 PMID: 27242371
  28. The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats.
    Cell. 1997 Jan 10;88(1):57-63 PMID: 9019406
  29. Arabidopsis snc2-1D activates receptor-like protein-mediated immunity transduced through WRKY70.
    Plant Cell. 2010 Sep;22(9):3153-63 PMID: 20841424
  30. Quantification of subnanomolar amounts of phosphate bound to seryl and threonyl residues in phosphoproteins using alkaline hydrolysis and malachite green.
    Anal Biochem. 1993 Oct;214(1):138-41 PMID: 8250216
  31. Multiple Targets of Salicylic Acid and Its Derivatives in Plants and Animals.
    Front Immunol. 2016 May 26;7:206 PMID: 27303403
  32. A plant locus essential for phylloquinone (vitamin K1) biosynthesis originated from a fusion of four eubacterial genes.
    J Biol Chem. 2006 Jun 23;281(25):17189-96 PMID: 16617180
  33. Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism.
    Nat Cell Biol. 2006 Mar;8(3):249-56 PMID: 16489343
  34. A protein phosphatase 2A complex spatially controls plant cell division.
    Nat Commun. 2013;4:1863 PMID: 23673648
  35. Measurement of auxin transport in Arabidopsis thaliana.
    Nat Protoc. 2009;4(4):437-51 PMID: 19282849
  36. Disparate roles for the regulatory A subunit isoforms in Arabidopsis protein phosphatase 2A.
    Plant Cell. 2004 Mar;16(3):709-22 PMID: 14973165
  37. Local Auxin Biosynthesis Is a Key Regulator of Plant Development.
    Dev Cell. 2018 Nov 5;47(3):306-318.e5 PMID: 30415657
  38. Target identification using drug affinity responsive target stability (DARTS).
    Proc Natl Acad Sci U S A. 2009 Dec 22;106(51):21984-9 PMID: 19995983
  39. Linking development to defense: auxin in plant-pathogen interactions.
    Trends Plant Sci. 2009 Jul;14(7):373-82 PMID: 19559643
  40. Fiji: an open-source platform for biological-image analysis.
    Nat Methods. 2012 Jun 28;9(7):676-82 PMID: 22743772
  41. Maximum yields of microsomal-type membranes from small amounts of plant material without requiring ultracentrifugation.
    Anal Biochem. 2010 Jun 15;401(2):217-27 PMID: 20193653
  42. Differential Regulation of Clathrin and Its Adaptor Proteins during Membrane Recruitment for Endocytosis.
    Plant Physiol. 2016 May;171(1):215-29 PMID: 26945051
  43. Members of the abscisic acid co-receptor PP2C protein family mediate salicylic acid-abscisic acid crosstalk.
    Plant Direct. 2017 Nov 06;1(5):e00020 PMID: 31245670
  44. The tobacco salicylic acid-binding protein 3 (SABP3) is the chloroplast carbonic anhydrase, which exhibits antioxidant activity and plays a role in the hypersensitive defense response.
    Proc Natl Acad Sci U S A. 2002 Sep 3;99(18):11640-5 PMID: 12185253
  45. Differential scanning calorimetry techniques: applications in biology and nanoscience.
    J Biomol Tech. 2010 Dec;21(4):167-93 PMID: 21119929
  46. Identification of multiple salicylic acid-binding proteins using two high throughput screens.
    Front Plant Sci. 2015 Jan 12;5:777 PMID: 25628632
  47. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants.
    Nature. 2012 May 16;486(7402):228-32 PMID: 22699612
  48. Direct and Indirect Targeting of PP2A by Conserved Bacterial Type-III Effector Proteins.
    PLoS Pathog. 2016 May 18;12(5):e1005609 PMID: 27191168
  49. The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability.
    Nat Protoc. 2007;2(9):2212-21 PMID: 17853878
  50. Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway.
    Curr Biol. 2007 Oct 23;17(20):1784-90 PMID: 17919906
  51. Salicylic Acid Affects Root Meristem Patterning via Auxin Distribution in a Concentration-Dependent Manner.
    Plant Physiol. 2019 Jul;180(3):1725-1739 PMID: 31036755
  52. PIN-dependent auxin transport: action, regulation, and evolution.
    Plant Cell. 2015 Jan;27(1):20-32 PMID: 25604445
  53. Two inducers of plant defense responses, 2,6-dichloroisonicotinec acid and salicylic acid, inhibit catalase activity in tobacco.
    Proc Natl Acad Sci U S A. 1995 Aug 1;92(16):7143-7 PMID: 11607566
  54. Kinetic analysis of monoclonal antibody-antigen interactions with a new biosensor based analytical system.
    J Immunol Methods. 1991 Dec 15;145(1-2):229-40 PMID: 1765656
  55. A molecular rheostat adjusts auxin flux to promote root protophloem differentiation.
    Nature. 2018 Jun;558(7709):297-300 PMID: 29875411
  56. Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux.
    Cell. 2007 Sep 21;130(6):1044-56 PMID: 17889649
  57. Overexpression of Arabidopsis MAP kinase kinase 7 leads to activation of plant basal and systemic acquired resistance.
    Plant J. 2007 Dec;52(6):1066-79 PMID: 17908155
  58. The Arabidopsis NPR1 protein is a receptor for the plant defense hormone salicylic acid.
    Cell Rep. 2012 Jun 28;1(6):639-47 PMID: 22813739
  59. A mesogenic triphenylene-perylene-triphenylene triad.
    Org Lett. 2011 Feb 18;13(4):764-7 PMID: 21247135
  60. Vectorial information for Arabidopsis planar polarity is mediated by combined AUX1, EIN2, and GNOM activity.
    Curr Biol. 2006 Nov 7;16(21):2143-9 PMID: 17084699
  61. The Inhibitor Endosidin 4 Targets SEC7 Domain-Type ARF GTPase Exchange Factors and Interferes with Subcellular Trafficking in Eukaryotes.
    Plant Cell. 2018 Oct;30(10):2553-2572 PMID: 30018156
  62. Isochorismate synthase is required to synthesize salicylic acid for plant defence.
    Nature. 2001 Nov 29;414(6863):562-5 PMID: 11734859
  63. Uncoupling PR gene expression from NPR1 and bacterial resistance: characterization of the dominant Arabidopsis cpr6-1 mutant.
    Plant Cell. 1998 Apr;10(4):557-69 PMID: 9548982
  64. Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism.
    Science. 1996 Aug 16;273(5277):948-50 PMID: 8688077
  65. Cantharidin-binding protein: identification as protein phosphatase 2A.
    Proc Natl Acad Sci U S A. 1992 Dec 15;89(24):11867-70 PMID: 1334551
  66. Salicylic acid beyond defence: its role in plant growth and development.
    J Exp Bot. 2011 Jun;62(10):3321-38 PMID: 21357767
  67. The growth-defense pivot: crisis management in plants mediated by LRR-RK surface receptors.
    Trends Biochem Sci. 2014 Oct;39(10):447-56 PMID: 25089011
  68. PP2A-3 interacts with ACR4 and regulates formative cell division in the Arabidopsis root.
    Proc Natl Acad Sci U S A. 2016 Feb 2;113(5):1447-52 PMID: 26792519
  69. A mutation in protein phosphatase 2A regulatory subunit A affects auxin transport in Arabidopsis.
    EMBO J. 1996 May 1;15(9):2115-24 PMID: 8641277
  70. Auxin efflux carrier activity and auxin accumulation regulate cell division and polarity in tobacco cells.
    Planta. 2002 Dec;216(2):302-8 PMID: 12447544
  71. DAD2 is an α/β hydrolase likely to be involved in the perception of the plant branching hormone, strigolactone.
    Curr Biol. 2012 Nov 6;22(21):2032-6 PMID: 22959345
  72. PIN proteins perform a rate-limiting function in cellular auxin efflux.
    Science. 2006 May 12;312(5775):914-8 PMID: 16601150
  73. Proteasome-mediated turnover of the transcription coactivator NPR1 plays dual roles in regulating plant immunity.
    Cell. 2009 May 29;137(5):860-72 PMID: 19490895
  74. The Arabidopsis NIM1 protein shows homology to the mammalian transcription factor inhibitor I kappa B.
    Plant Cell. 1997 Mar;9(3):425-39 PMID: 9090885
  75. Reporters for sensitive and quantitative measurement of auxin response.
    Nat Methods. 2015 Mar;12(3):207-10, 2 p following 210 PMID: 25643149
  76. A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance.
    Plant Cell. 1994 Dec;6(12):1845-57 PMID: 7866028
  77. SCF(TIR1/AFB)-auxin signalling regulates PIN vacuolar trafficking and auxin fluxes during root gravitropism.
    EMBO J. 2013 Jan 23;32(2):260-74 PMID: 23211744
  78. A plant miRNA contributes to antibacterial resistance by repressing auxin signaling.
    Science. 2006 Apr 21;312(5772):436-9 PMID: 16627744
  79. Mitogen-Activated Protein Kinase Cascade MKK7-MPK6 Plays Important Roles in Plant Development and Regulates Shoot Branching by Phosphorylating PIN1 in Arabidopsis.
    PLoS Biol. 2016 Sep 12;14(9):e1002550 PMID: 27618482
Full Text / Full Text
PMC full text available locally, click to read

Loading full text...

Article Info
Journal
Current biology : CB
Abbr.
Curr Biol
ISSN
1879-0445
DOI
10.1016/j.cub.2019.11.058
Email
[email protected]
Published
2020-00-03
Epub
2020-00-16
Pages
381-395.e8
Language
English
Region
England
NLM ID
9107782
PMCID
PMC6997888
Subset
IM
External Links
PubMed source DOI: 10.1016/j.cub.2019.11.058 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