Home LiteratureArticle Details
PMID: 12509529 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense.

The Plant cell ·Vol. 15 ·No. 1 ·2003-01-00 ·Pages 165-78

Lorenzo O, Piqueras R, Sánchez-Serrano JJ, Solano R

Abstract

Cross-talk between ethylene and jasmonate signaling pathways determines the activation of a set of defense responses against pathogens and herbivores. However, the molecular mechanisms that underlie this cross-talk are poorly understood. Here, we show that ethylene and jasmonate pathways converge in the transcriptional activation of ETHYLENE RESPONSE FACTOR1 (ERF1), which encodes a transcription factor that regulates the expression of pathogen response genes that prevent disease progression. The expression of ERF1 can be activated rapidly by ethylene or jasmonate and can be activated synergistically by both hormones. In addition, both signaling pathways are required simultaneously to activate ERF1, because mutations that block any of them prevent ERF1 induction by any of these hormones either alone or in combination. Furthermore, 35S:ERF1 expression can rescue the defense response defects of coi1 (coronative insensitive1) and ein2 (ethylene insensitive2); therefore, it is a likely downstream component of both ethylene and jasmonate signaling pathways. Transcriptome analysis in Col;35S:ERF1 transgenic plants and ethylene/jasmonate-treated wild-type plants further supports the notion that ERF1 regulates in vivo the expression of a large number of genes responsive to both ethylene and jasmonate. These results suggest that ERF1 acts downstream of the intersection between ethylene and jasmonate pathways and suggest that this transcription factor is a key element in the integration of both signals for the regulation of defense response genes.

MeSH Terms
Arabidopsis/drug effects,genetics,metabolism Arabidopsis Proteins/genetics,metabolism Cyclopentanes/pharmacology DNA-Binding Proteins Ethylenes/pharmacology Gene Expression Regulation, Plant/drug effects Immunity, Innate/drug effects,genetics Nuclear Proteins/genetics Oxylipins Plant Diseases/genetics Plant Growth Regulators/pharmacology Plant Proteins/genetics,metabolism Plants, Genetically Modified Receptors, Cell Surface/genetics,metabolism Signal Transduction/drug effects,genetics Transcription Factors/genetics
Chemicals
Arabidopsis Proteins COI1 protein, Arabidopsis Cyclopentanes DNA-Binding Proteins EIN2 protein, Arabidopsis Ethylenes Nuclear Proteins Oxylipins Plant Growth Regulators Plant Proteins Receptors, Cell Surface Transcription Factors ethylene-responsive element binding protein jasmonic acid ethylene
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Lorenzo Oscar
Departamento de Genética Molecular de Plantas, Centro Nacional de Biotecnología-Consejo Superior de Investigaciones Científicas, Campus Universidad Autónoma, 28049 Madrid, Spain.
Piqueras Raquel
Sánchez-Serrano Jose J
Solano Roberto
References (64)
64 references, click to expand
  1. Nucleotide sequence of a new cDNA for peroxidase from Arabidopsis thaliana.
    Plant Physiol. 1994 Jan;104(1):285-6 PMID: 8115548
  2. Jasmonate-dependent induction of indole glucosinolates in Arabidopsis by culture filtrates of the nonspecific pathogen Erwinia carotovora.
    Plant Physiol. 2001 Jun;126(2):849-60 PMID: 11402212
  3. The jasmonate signal pathway.
    Plant Cell. 2002;14 Suppl:S153-64 PMID: 12045275
  4. A harpin binding site in tobacco plasma membranes mediates activation of the pathogenesis-related gene HIN1 independent of extracellular calcium but dependent on mitogen-activated protein kinase activity.
    Plant Cell. 2001 May;13(5):1079-93 PMID: 11340183
  5. Coordinated plant defense responses in Arabidopsis revealed by microarray analysis.
    Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11655-60 PMID: 11027363
  6. Molecular localisation of ferrochelatase in higher plant chloroplasts.
    Eur J Biochem. 1997 May 15;246(1):32-7 PMID: 9210462
  7. Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis.
    Plant Cell. 1998 Dec;10(12):2103-13 PMID: 9836748
  8. Integration of floral inductive signals in Arabidopsis.
    Nature. 2000 Apr 20;404(6780):889-92 PMID: 10786797
  9. Genes controlling expression of defense responses in Arabidopsis--2001 status.
    Curr Opin Plant Biol. 2001 Aug;4(4):301-8 PMID: 11418339
  10. Myrosinase: gene family evolution and herbivore defense in Brassicaceae.
    Plant Mol Biol. 2000 Jan;42(1):93-113 PMID: 10688132
  11. CYP81E1, a cytochrome P450 cDNA of licorice (Glycyrrhiza echinata L.), encodes isoflavone 2'-hydroxylase.
    Biochem Biophys Res Commun. 1998 Oct 9;251(1):67-70 PMID: 9790908
  12. Jasmonic acid signaling modulates ozone-induced hypersensitive cell death.
    Plant Cell. 2000 Sep;12(9):1633-46 PMID: 11006337
  13. Effect of chitinase antisense RNA expression on disease susceptibility of Arabidopsis plants.
    Plant Mol Biol. 1994 Jul;25(4):587-96 PMID: 8061313
  14. Jasmonate is essential for insect defense in Arabidopsis.
    Proc Natl Acad Sci U S A. 1997 May 13;94(10):5473-7 PMID: 11038546
  15. Interacting signal pathways control defense gene expression in Arabidopsis in response to cell wall-degrading enzymes from Erwinia carotovora.
    Mol Plant Microbe Interact. 2000 Apr;13(4):430-8 PMID: 10755306
  16. Ethylene-insensitive tobacco lacks nonhost resistance against soil-borne fungi.
    Proc Natl Acad Sci U S A. 1998 Feb 17;95(4):1933-7 PMID: 9465120
  17. Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis.
    Plant Cell. 2000 May;12(5):707-20 PMID: 10810145
  18. Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis.
    Plant Physiol. 2002 Jun;129(2):661-77 PMID: 12068110
  19. Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi.
    Plant J. 2002 Jan;29(1):23-32 PMID: 12060224
  20. Ozone-induced cell death occurs via two distinct mechanisms in Arabidopsis: the role of salicylic acid.
    Plant J. 1999 Mar;17(6):603-14 PMID: 10230060
  21. Arabidopsis map kinase 4 negatively regulates systemic acquired resistance.
    Cell. 2000 Dec 22;103(7):1111-20 PMID: 11163186
  22. Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway.
    Plant Cell. 1996 Dec;8(12):2309-23 PMID: 8989885
  23. Signal transduction in the plant immune response.
    Trends Biochem Sci. 2000 Feb;25(2):79-82 PMID: 10664588
  24. Purification and characterization of a hydroxamic acid glucoside beta-glucosidase from wheat (Triticum aestivum L.) seedlings.
    Planta. 2000 Feb;210(3):432-8 PMID: 10750901
  25. Molecular cloning, expression, and induction of berberine bridge enzyme, an enzyme essential to the formation of benzophenanthridine alkaloids in the response of plants to pathogenic attack.
    Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):9969-73 PMID: 1946465
  26. Ethylene biosynthesis and signaling networks.
    Plant Cell. 2002;14 Suppl:S131-51 PMID: 12045274
  27. Cloning and characterization of a pathogen-induced chitinase in Brassica napus.
    Plant Mol Biol. 1992 Oct;20(2):277-87 PMID: 1391771
  28. A role for jasmonate in pathogen defense of Arabidopsis.
    Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):7209-14 PMID: 9618564
  29. Isolation of ethylene-insensitive soybean mutants that are altered in pathogen susceptibility and gene-for-gene disease resistance
    Plant Physiol. 1999 Mar;119(3):935-50 PMID: 10069832
  30. Cross-talk between wound signalling pathways determines local versus systemic gene expression in Arabidopsis thaliana.
    Plant J. 1999 Oct;20(2):135-142 PMID: 10571873
  31. A new family of basic cysteine-rich plant antifungal proteins from Brassicaceae species.
    FEBS Lett. 1993 Feb 1;316(3):233-40 PMID: 8422949
  32. The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens.
    Plant Cell. 2001 May;13(5):1025-33 PMID: 11340179
  33. Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENE-INSENSITIVE3 and ETHYLENE-RESPONSE-FACTOR1.
    Genes Dev. 1998 Dec 1;12(23):3703-14 PMID: 9851977
  34. Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens.
    Proc Natl Acad Sci U S A. 1998 Dec 8;95(25):15107-11 PMID: 9844023
  35. Jasmonate signaling mutants of Arabidopsis are susceptible to the soil fungus Pythium irregulare.
    Plant J. 1998 Sep;15(6):747-54 PMID: 9807813
  36. Rapid activation of a novel plant defense gene is strictly dependent on the Arabidopsis RPM1 disease resistance locus.
    EMBO J. 1992 Dec;11(13):4677-84 PMID: 1464303
  37. Salicylic acid induces the expression of a number of receptor-like kinase genes in Arabidopsis thaliana.
    Plant Cell Physiol. 2000 Sep;41(9):1038-44 PMID: 11100776
  38. cDNA cloning of carrot extracellular beta-fructosidase and its expression in response to wounding and bacterial infection.
    Plant Cell. 1990 Nov;2(11):1107-19 PMID: 2152110
  39. Isolation of pathogen/stress-inducible cDNAs from alfalfa by mRNA differential display.
    Plant Mol Biol. 1997 Mar;33(4):737-43 PMID: 9132065
  40. Induced plant responses to pathogen attack. Analysis and heterologous expression of the key enzyme in the biosynthesis of phytoalexins in soybean (Glycine max L. Merr. cv. Harosoy 63).
    Eur J Biochem. 1991 Mar 14;196(2):423-30 PMID: 1840523
  41. Acquired resistance in Arabidopsis.
    Plant Cell. 1992 Jun;4(6):645-56 PMID: 1392589
  42. Requirement of functional ethylene-insensitive 2 gene for efficient resistance of Arabidopsis to infection by Botrytis cinerea.
    Plant Physiol. 1999 Dec;121(4):1093-102 PMID: 10594097
  43. Analysis of two incompletely spliced Arabidopsis cDNAs encoding novel types of peroxidase.
    Biochim Biophys Acta. 1998 Nov 26;1443(1-2):149-54 PMID: 9838086
  44. Monoterpene synthases from grand fir (Abies grandis). cDNA isolation, characterization, and functional expression of myrcene synthase, (-)-(4S)-limonene synthase, and (-)-(1S,5S)-pinene synthase.
    J Biol Chem. 1997 Aug 29;272(35):21784-92 PMID: 9268308
  45. The jasmonate-inducible AP2/ERF-domain transcription factor ORCA3 activates gene expression via interaction with a jasmonate-responsive promoter element.
    Plant J. 2001 Jan;25(1):43-53 PMID: 11169181
  46. Isolation and characterization of a cDNA clone encoding an osmotin-like protein from Arabidopsis thaliana.
    Gene. 1997 May 20;191(1):51-6 PMID: 9210588
  47. Identification of Arabidopsis ethylene-responsive element binding factors with distinct induction kinetics after pathogen infection.
    Plant Physiol. 2002 Apr;128(4):1313-22 PMID: 11950980
  48. Sequence of a poplar bark storage protein gene.
    Plant Physiol. 1993 Aug;102(4):1347-8 PMID: 8278552
  49. ORCA3, a jasmonate-responsive transcriptional regulator of plant primary and secondary metabolism.
    Science. 2000 Jul 14;289(5477):295-7 PMID: 10894776
  50. Ethylene as a Signal Mediating the Wound Response of Tomato Plants
    Science. 1996 Dec 13;274(5294):1914-7 PMID: 8943205
  51. Characterization and expression of caffeoyl-coenzyme A 3-O-methyltransferase proposed for the induced resistance response of Vitis vinifera L.
    Plant Physiol. 1997 Nov;115(3):1039-48 PMID: 9390437
  52. Interplay of signaling pathways in plant disease resistance.
    Trends Genet. 2000 Oct;16(10):449-55 PMID: 11050331
  53. Differential accumulation of mRNAs encoding extracellular and intracellular PR proteins in tomato induced by virulent and avirulent races of Cladosporium fulvum.
    Plant Mol Biol. 1992 Nov;20(3):513-27 PMID: 1421154
  54. Plant Defense Genes Are Synergistically Induced by Ethylene and Methyl Jasmonate.
    Plant Cell. 1994 Aug;6(8):1077-1085 PMID: 12244267
  55. Differential regulation of an auxin-producing nitrilase gene family in Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 1994 Jul 5;91(14):6649-53 PMID: 8022831
  56. Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression.
    Plant Cell. 1996 Aug;8(8):1225-37 PMID: 8776893
  57. Arabidopsis thaliana contains a large family of germin-like proteins: characterization of cDNA and genomic sequences encoding 12 unique family members.
    Plant Mol Biol. 1998 Dec;38(6):929-43 PMID: 9869400
  58. beta-1,3-Glucanase is highly-expressed in laticifers of Hevea brasiliensis.
    Plant Mol Biol. 1995 Oct;29(2):397-402 PMID: 7579190
  59. A novel signaling pathway controlling induced systemic resistance in Arabidopsis.
    Plant Cell. 1998 Sep;10(9):1571-80 PMID: 9724702
  60. Ozone-sensitive arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death.
    Plant Cell. 2000 Oct;12(10):1849-62 PMID: 11041881
  61. The complexity of disease signaling in Arabidopsis.
    Curr Opin Immunol. 2001 Feb;13(1):63-8 PMID: 11154919
  62. Involvement of the Arabidopsis alpha-DOX1 fatty acid dioxygenase in protection against oxidative stress and cell death.
    Plant J. 2002 Jan;29(1):61-2 PMID: 12060227
  63. Primary structure and expression of plant homologues of animal and fungal thioredoxin-dependent peroxide reductases and bacterial alkyl hydroperoxide reductases.
    Plant Mol Biol. 1996 Jun;31(3):553-64 PMID: 8790288
  64. Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses.
    Plant Cell. 2002 Mar;14(3):559-74 PMID: 11910004
Article Info
Journal
The Plant cell
Abbr.
Plant Cell
ISSN
1040-4651
DOI
10.1105/tpc.007468
Published
2003-01-00
Pages
165-78
Language
English
Region
England
NLM ID
9208688
PMCID
PMC143489
Subset
IM
External Links
PubMed source DOI: 10.1105/tpc.007468 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