Home LiteratureArticle Details
PMID: 15722464 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Dissecting the beta-aminobutyric acid-induced priming phenomenon in Arabidopsis.

The Plant cell ·Vol. 17 ·No. 3 ·2005-03-00 ·Pages 987-99

Ton J, Jakab G, Toquin V, Flors V, Iavicoli A, Maeder MN, Métraux JP, Mauch-Mani B

Abstract

Plants treated with the nonprotein amino acid beta-aminobutyric acid (BABA) develop an enhanced capacity to resist biotic and abiotic stresses. This BABA-induced resistance (BABA-IR) is associated with an augmented capacity to express basal defense responses, a phenomenon known as priming. Based on the observation that high amounts of BABA induce sterility in Arabidopsis thaliana, a mutagenesis screen was performed to select mutants impaired in BABA-induced sterility (ibs). Here, we report the isolation and subsequent characterization of three T-DNA-tagged ibs mutants. Mutant ibs1 is affected in a cyclin-dependent kinase-like protein, and ibs2 is defective in AtSAC1b encoding a polyphosphoinositide phosphatase. Mutant ibs3 is affected in the regulation of the ABA1 gene encoding the abscisic acid (ABA) biosynthetic enzyme zeaxanthin epoxidase. To elucidate the function of the three IBS genes in plant resistance, the mutants were tested for BABA-IR against the bacterium Pseudomonas syringae pv tomato, the oomycete Hyaloperonospora parasitica, and BABA-induced tolerance to salt. All three ibs mutants were compromised in BABA-IR against H. parasitica, although to a different extent. Whereas ibs1 was reduced in priming for salicylate (SA)-dependent trailing necrosis, mutants ibs2 and ibs3 were affected in the priming for callose deposition. Only ibs1 failed to express BABA-IR against P. syringae, which coincided with a defect in priming for SA-inducible PR-1 gene expression. By contrast, ibs2 and ibs3 showed reduced BABA-induced tolerance to salt, which correlated with an affected priming for ABA-inducible gene expression. For all three ibs alleles, the defects in BABA-induced sterility and BABA-induced protection against P. syringae, H. parasitica, and salt could be confirmed in independent mutants. The data presented here introduce three novel regulatory genes involved in priming for different defense responses.

MeSH Terms
Alleles Amino Acid Sequence Aminobutyrates/pharmacology Arabidopsis/drug effects,genetics,physiology Base Sequence Cyclin-Dependent Kinases/genetics,metabolism DNA, Bacterial/genetics DNA, Plant/genetics Drug Resistance/genetics Genes, Plant Genes, Regulator Models, Biological Molecular Sequence Data Mutation Oomycetes/pathogenicity Osmotic Pressure Oxidoreductases/genetics,metabolism Phosphoric Monoester Hydrolases/genetics,metabolism Plant Diseases/genetics,microbiology Plants, Genetically Modified Pseudomonas syringae/pathogenicity Sequence Homology, Amino Acid Sodium Chloride
Chemicals
Aminobutyrates DNA, Bacterial DNA, Plant T-DNA 3-aminobutyric acid Sodium Chloride Oxidoreductases zeaxanthin epoxidase Cyclin-Dependent Kinases Phosphoric Monoester Hydrolases
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Ton Jurriaan
Department of Science, Laboratory of Biochemistry, University of Neuchâtel, 2007 Neuchâtel, Switzerland.
Jakab Gabor
Toquin Valérie
Flors Victor
Iavicoli Annalisa
Maeder Muriel N
Métraux Jean-Pierre
Mauch-Mani Brigitte
References (49)
49 references, click to expand
  1. Expression of the Phytophthora infestans ipiB and ipiO genes in planta and in vitro.
    Mol Gen Genet. 1994 Aug 2;244(3):269-77 PMID: 8058038
  2. The isolation of abscisic acid (ABA) deficient mutants by selection of induced revertants in non-germinating gibberellin sensitive lines of Arabidopsis thaliana (L.) heynh.
    Theor Appl Genet. 1982 Dec;61(4):385-93 PMID: 24270501
  3. Characterization of a salicylic acid-insensitive mutant (sai1) of Arabidopsis thaliana, identified in a selective screen utilizing the SA-inducible expression of the tms2 gene.
    Mol Plant Microbe Interact. 1997 Jan;10(1):69-78 PMID: 9002272
  4. 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
  5. Genome-wide insertional mutagenesis of Arabidopsis thaliana.
    Science. 2003 Aug 1;301(5633):653-7 PMID: 12893945
  6. Cyclin-dependent kinases: engines, clocks, and microprocessors.
    Annu Rev Cell Dev Biol. 1997;13:261-91 PMID: 9442875
  7. beta-Aminobutyric acid-induced protection of Arabidopsis against the necrotrophic fungus Botrytis cinerea.
    Plant Physiol. 2001 Jun;126(2):517-23 PMID: 11402183
  8. Direct involvement of phosphatidylinositol 4-phosphate in secretion in the yeast Saccharomyces cerevisiae.
    J Biol Chem. 1999 Nov 26;274(48):34294-300 PMID: 10567405
  9. Cytology of induced systemic resistance of tomato to Phytophthora infestans.
    Planta. 1991 Mar;183(4):491-6 PMID: 24193841
  10. Participation of the phosphoinositide metabolism in the hypersensitive response of Citrus limon against Alternaria alternata.
    Biol Res. 2001;34(1):43-50 PMID: 11471522
  11. New EMBO members' review: actin cytoskeleton regulation through modulation of PI(4,5)P(2) rafts.
    EMBO J. 2001 Aug 15;20(16):4332-6 PMID: 11500359
  12. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana.
    Plant J. 1998 Dec;16(6):735-43 PMID: 10069079
  13. Potentiation of pathogen-specific defense mechanisms in Arabidopsis by beta -aminobutyric acid.
    Proc Natl Acad Sci U S A. 2000 Nov 7;97(23):12920-5 PMID: 11058166
  14. The phosphoinositide phosphatase Sac1p controls trafficking of the yeast Chs3p chitin synthase.
    Curr Biol. 2001 Sep 18;11(18):1421-6 PMID: 11566100
  15. A high-throughput Arabidopsis reverse genetics system.
    Plant Cell. 2002 Dec;14(12):2985-94 PMID: 12468722
  16. A benzothiadiazole primes parsley cells for augmented elicitation of defense responses
    Plant Physiol. 1998 Aug;117(4):1333-9 PMID: 9701589
  17. Induction of pathogen resistance in barley by abiotic stress.
    Plant Biol (Stuttg). 2004 Sep;6(5):529-36 PMID: 15375723
  18. Arabidopsis signal transduction mutant defective in chemically and biologically induced disease resistance.
    Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6602-6 PMID: 11607555
  19. Loss of a callose synthase results in salicylic acid-dependent disease resistance.
    Science. 2003 Aug 15;301(5635):969-72 PMID: 12920300
  20. Rapid accumulation of phosphatidylinositol 4,5-bisphosphate and inositol 1,4,5-trisphosphate correlates with calcium mobilization in salt-stressed arabidopsis.
    Plant Physiol. 2001 Jun;126(2):759-69 PMID: 11402204
  21. Methyl jasmonate conditions parsley suspension cells for increased elicitation of phenylpropanoid defense responses.
    Biochem Biophys Res Commun. 1992 Nov 30;189(1):304-8 PMID: 1449484
  22. Beta-amino-butyric acid-induced resistance against necrotrophic pathogens is based on ABA-dependent priming for callose.
    Plant J. 2004 Apr;38(1):119-30 PMID: 15053765
  23. Sac1 lipid phosphatase and Stt4 phosphatidylinositol 4-kinase regulate a pool of phosphatidylinositol 4-phosphate that functions in the control of the actin cytoskeleton and vacuole morphology.
    Mol Biol Cell. 2001 Aug;12(8):2396-411 PMID: 11514624
  24. Salt and drought stress signal transduction in plants.
    Annu Rev Plant Biol. 2002;53:247-73 PMID: 12221975
  25. Differential effectiveness of salicylate-dependent and jasmonate/ethylene-dependent induced resistance in Arabidopsis.
    Mol Plant Microbe Interact. 2002 Jan;15(1):27-34 PMID: 11858171
  26. Priming in plant-pathogen interactions.
    Trends Plant Sci. 2002 May;7(5):210-6 PMID: 11992826
  27. A gene encoding a phosphatidylinositol-specific phospholipase C is induced by dehydration and salt stress in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 1995 Apr 25;92(9):3903-7 PMID: 7732004
  28. Systemic acquired resistance.
    Annu Rev Phytopathol. 1997;35:235-70 PMID: 15012523
  29. Requirement of salicylic Acid for the induction of systemic acquired resistance.
    Science. 1993 Aug 6;261(5122):754-6 PMID: 17757215
  30. Regulation of interferon production by human monocytes: requirements for priming for lipopolysaccharide-induced production.
    J Leukoc Biol. 1991 Aug;50(2):176-81 PMID: 1649241
  31. Acquired resistance in Arabidopsis.
    Plant Cell. 1992 Jun;4(6):645-56 PMID: 1392589
  32. Unexpected protein families including cell defense components feature in the N-myristoylome of a higher eukaryote.
    J Biol Chem. 2003 Oct 31;278(44):43418-29 PMID: 12912986
  33. Cytology of induced systemic resistance of cucumber to Colletotrichum lagenarium.
    Planta. 1991 Mar;183(4):484-90 PMID: 24193840
  34. Cell signaling during cold, drought, and salt stress.
    Plant Cell. 2002;14 Suppl:S165-83 PMID: 12045276
  35. SAC1-like domains of yeast SAC1, INP52, and INP53 and of human synaptojanin encode polyphosphoinositide phosphatases.
    J Biol Chem. 1999 May 7;274(19):12990-5 PMID: 10224048
  36. Two simple media for the demonstration of pyocyanin and fluorescin.
    J Lab Clin Med. 1954 Aug;44(2):301-7 PMID: 13184240
  37. Salicylic Acid in Rice (Biosynthesis, Conjugation, and Possible Role).
    Plant Physiol. 1995 Jun;108(2):633-639 PMID: 12228500
  38. Abscisic acid determines basal susceptibility of tomato to Botrytis cinerea and suppresses salicylic acid-dependent signaling mechanisms.
    Plant Physiol. 2002 Feb;128(2):491-501 PMID: 11842153
  39. The Arabidopsis CDPK-SnRK superfamily of protein kinases.
    Plant Physiol. 2003 Jun;132(2):666-80 PMID: 12805596
  40. SIGNALING TO THE ACTIN CYTOSKELETON IN PLANTS.
    Annu Rev Plant Physiol Plant Mol Biol. 2000 Jun;51:257-288 PMID: 15012193
  41. Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion.
    Plant Cell. 1998 Jul;10(7):1121-34 PMID: 9668132
  42. Identification of Pseudomonas syringae pathogens of Arabidopsis and a bacterial locus determining avirulence on both Arabidopsis and soybean.
    Plant Cell. 1991 Jan;3(1):49-59 PMID: 1824334
  43. Three SAC1-like genes show overlapping patterns of expression in Arabidopsis but are remarkably silent during embryo development.
    Plant J. 2003 May;34(3):293-306 PMID: 12713536
  44. Characterization of an Arabidopsis Mutant That Is Nonresponsive to Inducers of Systemic Acquired Resistance.
    Plant Cell. 1994 Nov;6(11):1583-1592 PMID: 12244227
  45. Benzothiadiazole-induced priming for potentiated responses to pathogen infection, wounding, and infiltration of water into leaves requires the NPR1/NIM1 gene in Arabidopsis.
    Plant Physiol. 2002 Mar;128(3):1046-56 PMID: 11891259
  46. Molecular cloning of two novel protein kinase genes from Arabidopsis thaliana.
    Biochim Biophys Acta. 1993 Oct 19;1216(1):9-14 PMID: 8218420
  47. Novel complexes of cyclin-dependent kinases and a cyclin-like protein from Arabidopsis thaliana with a function unrelated to cell division.
    Cell Mol Life Sci. 2003 Feb;60(2):401-12 PMID: 12678503
  48. A novel signaling pathway controlling induced systemic resistance in Arabidopsis.
    Plant Cell. 1998 Sep;10(9):1571-80 PMID: 9724702
  49. Arabidopsis is susceptible to infection by a downy mildew fungus.
    Plant Cell. 1990 May;2(5):437-45 PMID: 2152169
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
Published
2005-03-00
Epub
2005-00-18
Pages
987-99
Language
English
Region
England
NLM ID
9208688
PMCID
PMC1069713
Subset
IM
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]