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PMID: 23370718 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

PYRABACTIN RESISTANCE1-LIKE8 plays an important role for the regulation of abscisic acid signaling in root.

Plant physiology ·Vol. 161 ·No. 2 ·2013-02-00 ·Pages 931-41

Antoni R, Gonzalez-Guzman M, Rodriguez L, Peirats-Llobet M, Pizzio GA, Fernandez MA, De Winne N, De Jaeger G, Dietrich D, Bennett MJ, Rodriguez PL

Abstract

Abscisic acid (ABA) signaling plays a critical role in regulating root growth and root system architecture. ABA-mediated growth promotion and root tropic response under water stress are key responses for plant survival under limiting water conditions. In this work, we have explored the role of Arabidopsis (Arabidopsis thaliana) PYRABACTIN RESISTANCE1 (PYR1)/PYR1-LIKE (PYL)/REGULATORY COMPONENTS OF ABA RECEPTORS for root ABA signaling. As a result, we discovered that PYL8 plays a nonredundant role for the regulation of root ABA sensitivity. Unexpectedly, given the multigenic nature and partial functional redundancy observed in the PYR/PYL family, the single pyl8 mutant showed reduced sensitivity to ABA-mediated root growth inhibition. This effect was due to the lack of PYL8-mediated inhibition of several clade A phosphatases type 2C (PP2Cs), since PYL8 interacted in vivo with at least five PP2Cs, namely HYPERSENSITIVE TO ABA1 (HAB1), HAB2, ABA-INSENSITIVE1 (ABI1), ABI2, and PP2CA/ABA-HYPERSENSITIVE GERMINATION3 as revealed by tandem affinity purification and mass spectrometry proteomic approaches. We also discovered that PYR/PYL receptors and clade A PP2Cs are crucial for the hydrotropic response that takes place to guide root growth far from regions with low water potential. Thus, an ABA-hypersensitive pp2c quadruple mutant showed enhanced hydrotropism, whereas an ABA-insensitive sextuple pyr/pyl mutant showed reduced hydrotropic response, indicating that ABA-dependent inhibition of PP2Cs by PYR/PYLs is required for the proper perception of a moisture gradient.

MeSH Terms
Abscisic Acid/metabolism,pharmacology Arabidopsis/drug effects,genetics,metabolism Arabidopsis Proteins/genetics,metabolism Gene Expression Regulation, Plant/drug effects Germination/drug effects Immunoblotting Mass Spectrometry Mutation Phosphoprotein Phosphatases/genetics,metabolism Plant Growth Regulators/metabolism,pharmacology Plant Roots/drug effects,genetics,metabolism Plants, Genetically Modified Protein Binding Proteome/genetics,metabolism Seeds/drug effects,genetics,metabolism Signal Transduction Water/metabolism,pharmacology
Chemicals
Arabidopsis Proteins PYL8 protein, Arabidopsis Plant Growth Regulators Proteome Water Abscisic Acid ABI1 protein, Arabidopsis ABI2 protein, Arabidopsis AHG3 protein, Arabidopsis HAB1 protein, Arabidopsis HAB2 protein, Arabidopsis Phosphoprotein Phosphatases
Authors & Affiliations
11 authors, click to expand affiliations / ORCID
Antoni Regina
Instituto de Biologia Molecular y Celular de Plantas, Consejo Superior de Investigaciones Cientificas-Universidad Politecnica de Valencia, ES-46022 Valencia, Spain.
Gonzalez-Guzman Miguel
Rodriguez Lesia
Peirats-Llobet Marta
Pizzio Gaston A
Fernandez Maria A
De Winne Nancy
De Jaeger Geert
Dietrich Daniela
Bennett Malcom J
Rodriguez Pedro L
References (56)
56 references, click to expand
  1. Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal.
    Nat Cell Biol. 2005 Nov;7(11):1057-65 PMID: 16244669
  2. Generation of active pools of abscisic acid revealed by in vivo imaging of water-stressed Arabidopsis.
    Plant Physiol. 2005 Jan;137(1):209-19 PMID: 15618419
  3. Hydrotropism interacts with gravitropism by degrading amyloplasts in seedling roots of Arabidopsis and radish.
    Plant Physiol. 2003 Jun;132(2):805-10 PMID: 12805610
  4. A gene essential for hydrotropism in roots.
    Proc Natl Acad Sci U S A. 2007 Mar 13;104(11):4724-9 PMID: 17360591
  5. Efficient octopine Ti plasmid-derived vectors for Agrobacterium-mediated gene transfer to plants.
    Nucleic Acids Res. 1985 Jul 11;13(13):4777-88 PMID: 4022773
  6. Activity of guard cell anion channel SLAC1 is controlled by drought-stress signaling kinase-phosphatase pair.
    Proc Natl Acad Sci U S A. 2009 Dec 15;106(50):21425-30 PMID: 19955405
  7. PYR/PYL/RCAR family members are major in-vivo ABI1 protein phosphatase 2C-interacting proteins in Arabidopsis.
    Plant J. 2010 Jan;61(2):290-9 PMID: 19874541
  8. GUS fusions: beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants.
    EMBO J. 1987 Dec 20;6(13):3901-7 PMID: 3327686
  9. Protein phosphatases 2C regulate the activation of the Snf1-related kinase OST1 by abscisic acid in Arabidopsis.
    Plant Cell. 2009 Oct;21(10):3170-84 PMID: 19855047
  10. Hydrotropism in abscisic acid, wavy, and gravitropic mutants of Arabidopsis thaliana.
    Planta. 2002 Dec;216(2):203-11 PMID: 12447533
  11. Type 2C protein phosphatases directly regulate abscisic acid-activated protein kinases in Arabidopsis.
    Proc Natl Acad Sci U S A. 2009 Oct 13;106(41):17588-93 PMID: 19805022
  12. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins.
    Science. 2009 May 22;324(5930):1068-71 PMID: 19407142
  13. Enhancement of abscisic acid sensitivity and reduction of water consumption in Arabidopsis by combined inactivation of the protein phosphatases type 2C ABI1 and HAB1.
    Plant Physiol. 2006 Aug;141(4):1389-99 PMID: 16798945
  14. Identification and disruption of a plant shaker-like outward channel involved in K+ release into the xylem sap.
    Cell. 1998 Sep 4;94(5):647-55 PMID: 9741629
  15. Phospho-site mapping, genetic and in planta activation studies reveal key aspects of the different phosphorylation mechanisms involved in activation of SnRK2s.
    Plant J. 2010 Sep;63(5):778-90 PMID: 20561261
  16. Abscisic acid: emergence of a core signaling network.
    Annu Rev Plant Biol. 2010;61:651-79 PMID: 20192755
  17. Analysis of an activated ABI5 allele using a new selection method for transgenic Arabidopsis seeds.
    FEBS Lett. 2004 Mar 12;561(1-3):127-31 PMID: 15013763
  18. Gain-of-function and loss-of-function phenotypes of the protein phosphatase 2C HAB1 reveal its role as a negative regulator of abscisic acid signalling.
    Plant J. 2004 Feb;37(3):354-69 PMID: 14731256
  19. In vitro reconstitution of an abscisic acid signalling pathway.
    Nature. 2009 Dec 3;462(7273):660-4 PMID: 19924127
  20. A unique short-chain dehydrogenase/reductase in Arabidopsis glucose signaling and abscisic acid biosynthesis and functions.
    Plant Cell. 2002 Nov;14(11):2723-43 PMID: 12417697
  21. Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family.
    Plant J. 2003 Jul;35(1):44-56 PMID: 12834401
  22. A tandem affinity purification-based technology platform to study the cell cycle interactome in Arabidopsis thaliana.
    Mol Cell Proteomics. 2007 Jul;6(7):1226-38 PMID: 17426018
  23. A thermodynamic switch modulates abscisic acid receptor sensitivity.
    EMBO J. 2011 Aug 16;30(20):4171-84 PMID: 21847091
  24. An efficient tandem affinity purification procedure for interaction proteomics in mammalian cells.
    Nat Methods. 2006 Dec;3(12):1013-9 PMID: 17060908
  25. Phosphorylation of the Arabidopsis AtrbohF NADPH oxidase by OST1 protein kinase.
    FEBS Lett. 2009 Sep 17;583(18):2982-6 PMID: 19716822
  26. Arabidopsis lateral root development: an emerging story.
    Trends Plant Sci. 2009 Jul;14(7):399-408 PMID: 19559642
  27. High-resolution whole-mount imaging of three-dimensional tissue organization and gene expression enables the study of Phloem development and structure in Arabidopsis.
    Plant Cell. 2008 Jun;20(6):1494-503 PMID: 18523061
  28. Root growth maintenance during water deficits: physiology to functional genomics.
    J Exp Bot. 2004 Nov;55(407):2343-51 PMID: 15448181
  29. Molecular mimicry regulates ABA signaling by SnRK2 kinases and PP2C phosphatases.
    Science. 2012 Jan 6;335(6064):85-8 PMID: 22116026
  30. Boosting tandem affinity purification of plant protein complexes.
    Trends Plant Sci. 2008 Oct;13(10):517-20 PMID: 18771946
  31. A no hydrotropic response root mutant that responds positively to gravitropism in Arabidopsis.
    Plant Physiol. 2003 Feb;131(2):536-46 PMID: 12586878
  32. Osmotic regulation of root system architecture.
    Plant J. 2005 Jul;43(1):17-28 PMID: 15960613
  33. Arabidopsis PYR/PYL/RCAR receptors play a major role in quantitative regulation of stomatal aperture and transcriptional response to abscisic acid.
    Plant Cell. 2012 Jun;24(6):2483-96 PMID: 22739828
  34. The sax1 dwarf mutant of Arabidopsis thaliana shows altered sensitivity of growth responses to abscisic acid, auxin, gibberellins and ethylene and is partially rescued by exogenous brassinosteroid.
    Plant J. 1999 May;18(3):303-14 PMID: 10377995
  35. Physiological genomics of response to soil drying in diverse Arabidopsis accessions.
    Plant Cell. 2012 Mar;24(3):893-914 PMID: 22408074
  36. A gateway cloning vector set for high-throughput functional analysis of genes in planta.
    Plant Physiol. 2003 Oct;133(2):462-9 PMID: 14555774
  37. Threonine at position 306 of the KAT1 potassium channel is essential for channel activity and is a target site for ABA-activated SnRK2/OST1/SnRK2.6 protein kinase.
    Biochem J. 2009 Dec 10;424(3):439-48 PMID: 19785574
  38. Different phosphorylation mechanisms are involved in the activation of sucrose non-fermenting 1 related protein kinases 2 by osmotic stresses and abscisic acid.
    Plant Mol Biol. 2007 Mar;63(4):491-503 PMID: 17103012
  39. Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs.
    Plant J. 2009 Nov;60(4):575-88 PMID: 19624469
  40. Targeted interactomics reveals a complex core cell cycle machinery in Arabidopsis thaliana.
    Mol Syst Biol. 2010 Aug 10;6:397 PMID: 20706207
  41. Regulators of PP2C phosphatase activity function as abscisic acid sensors.
    Science. 2009 May 22;324(5930):1064-8 PMID: 19407143
  42. Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors.
    Plant J. 2005 Dec;44(6):939-49 PMID: 16359387
  43. Gibberellin signaling in the endodermis controls Arabidopsis root meristem size.
    Curr Biol. 2009 Jul 28;19(14):1194-9 PMID: 19576770
  44. Roles of amyloplasts and water deficit in root tropisms.
    Plant Cell Environ. 2008 Feb;31(2):205-17 PMID: 18047572
  45. Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco.
    Proc Natl Acad Sci U S A. 2011 Apr 5;108(14):5891-6 PMID: 21436041
  46. Root Growth Maintenance at Low Water Potentials (Increased Activity of Xyloglucan Endotransglycosylase and Its Possible Regulation by Abscisic Acid).
    Plant Physiol. 1994 Oct;106(2):607-615 PMID: 12232354
  47. A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells.
    Proc Natl Acad Sci U S A. 2009 Dec 15;106(50):21419-24 PMID: 19955427
  48. The short-rooted phenotype of the brevis radix mutant partly reflects root abscisic acid hypersensitivity.
    Plant Physiol. 2009 Apr;149(4):1917-28 PMID: 19201913
  49. Triple loss of function of protein phosphatases type 2C leads to partial constitutive response to endogenous abscisic acid.
    Plant Physiol. 2009 Jul;150(3):1345-55 PMID: 19458118
  50. Identification of two protein kinases required for abscisic acid regulation of seed germination, root growth, and gene expression in Arabidopsis.
    Plant Cell. 2007 Feb;19(2):485-94 PMID: 17307925
  51. Use of the glucosyltransferase UGT71B6 to disturb abscisic acid homeostasis in Arabidopsis thaliana.
    Plant J. 2006 May;46(3):492-502 PMID: 16623908
  52. Both abscisic acid (ABA)-dependent and ABA-independent pathways govern the induction of NCED3, AAO3 and ABA1 in response to salt stress.
    Plant Cell Environ. 2006 Oct;29(10):2000-8 PMID: 16930325
  53. Closely related receptor complexes differ in their ABA selectivity and sensitivity.
    Plant J. 2010 Jan;61(1):25-35 PMID: 19769575
  54. Selective inhibition of clade A phosphatases type 2C by PYR/PYL/RCAR abscisic acid receptors.
    Plant Physiol. 2012 Feb;158(2):970-80 PMID: 22198272
  55. Hormonal regulation of root growth: integrating local activities into global behaviour.
    Trends Plant Sci. 2012 Jun;17(6):326-31 PMID: 22401844
  56. Brassinosteroid perception in the epidermis controls root meristem size.
    Development. 2011 Mar;138(5):839-48 PMID: 21270053
Article Info
Journal
Plant physiology
Abbr.
Plant Physiol
ISSN
1532-2548
Published
2013-02-00
Epub
2012-00-14
Pages
931-41
Language
English
Region
United States
NLM ID
0401224
PMCID
PMC3561030
Subset
IM
Grants
Biotechnology and Biological Sciences Research Council · BB/D019613/1 · United Kingdom
Biotechnology and Biological Sciences Research Council · BB/G023972/1 · United Kingdom
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