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HIGH IMPACT

Ethylene Response Factors in Jasmonate Signaling and Defense Response

University of Illinois
Urbana, IL 61801

Plants are continually exposed to potential pathogens and herbivores and have evolved defenses to counter such opportunistic invasions, including both physical (i.e. waxy cuticles, cell walls) and biochemical (i.e. defense compounds) barriers (for review, see Grennan, 2006). A key component to mounting an effective response, which may involve a change in gene expression, is an efficient signaling pathway. The identification and characterization of some members of the jasmonate and ethylene (ETH) signaling pathways is the focus of this month's High Impact and the topic of an article by McGrath et al. (2005), "Repressor- and activator-type ethylene response factors functioning in jasmonate signaling and disease resistance identified via a genome-wide screen of Arabidopsis transcription factor gene expression," which as of February 2008 had received 38 citations (Thompson Scientific).

	THE BACKGROUND

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Plants are in constant interaction with other organisms. These interactions can be benign, beneficial, or detrimental for a plant. Plants need to not only distinguish between these interactions but also must have the ability to respond in a timely manner to an opportunistic invasion. This may include the synthesis of defense-related compounds, requiring a change in gene expression.

Several defense signaling pathways have been demonstrated to be regulated by low-M_r signal molecules, such as salicylic acid (SA), abscisic acid, jasmonic acid (JA), and ETH. Major aspects of these pathways have been genetically defined, revealing a linkage between the signaling pathways.

Jasmonates mediate responses to insect and arthropod herbivores, some necrotrophic fungal pathogens, and nonpathogenic fungi as well as being involved in root growth (for review, see Farmer et al., 2003). ETH can act synergistically or antagonistically with JA in the regulation of both stress and developmental responses. The connection between these two signaling pathways has been demonstrated genetically to be the transcription factor (TF) ETHYLENE RESPONSE FACTOR1 (ERF1; Lorenzo et al., 2003).

ERF TFs are a subfamily of the APETELA2 (AP2) TF family and contain a single DNA-binding domain. The target sequence for ERF TFs is the GCC box that is found in several promoters of pathogenesis-related genes as well as ETH- and JA-inducible genes (for review, see Gutterson and Reuber, 2004). SA also induces certain members of the ERF family. Isolation of these TFs would aid in the understanding of this important plant defense pathway.

	WHAT WAS SHOWN

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McGrath et al. (2005) were interested in identifying TFs involved in jasmonate signaling and plant defense. To achieve this, 1,534 TFs from Arabidopsis (Arabidopsis thaliana) were screened using real-time quantitative PCR for a change in transcript level following inoculation with the incompatible necrotrophic pathogen Alternaria brassicicola or exposure to the signaling compound methyl jasmonate (MeJA). This approach identified 134 TFs exhibiting a significant change in transcript levels following treatment, 20 of which were induced by both treatments. Included among these, 20 genes were members of the AP2/ERF family. Functional analysis of two of these gene products, AtERF4 and AtERF2, revealed an antagonistic relationship where AtERF4 acts as a negative regulator of JA-responsive defense gene expression and resistance to the necrotrophic fungal pathogen Fusarium oxysporum while AtERF2 is a positive regulator. The role of these two gene products was determined in Arabidopsis plants either overexpressing the TFs or with a T-DNA insertion in the gene.

In the case of AtERF2, its role as a positive regulator of MeJA response was confirmed, as had previously been suggested in plants overexpressing AtERF2 (Brown et al., 2003). Additionally, a reduction in disease symptoms relative to wild type after inoculation with F. oxysporum was observed, supporting a role for AtERF2 as a positive regulator of disease resistance.

AtERF4 involvement in defense gene regulation was examined in Arabidopsis plants overexpressing AtERF4 as well as T-DNA insertion lines. In the overexpressing plants, the induction of two genes (PDF1.2 and CHIB) known to be regulated by the JA pathway was lower than wild-type plants when treated with MeJA, while a increase in basal transcript levels was observed in the T-DNA lines that did not express AtERF4. Overexpressing plants, when challenged with F. oxysporum, exhibited greater disease symptoms than the wild type. Together, these results strongly suggested the role of AtERF4 as a negative regulator of both JA-dependent response and resistance to necrotrophic pathogens.

A question that still remains open concerns the coordination of the expression and regulation of these two opposing regulators during plant defense. However, the coordinated activation of negative and positive regulators could be a strategy that plants use to mount a defense response that is detrimental to an invading pathogen while avoiding potentially self-inflicted damage (Kazan, 2006).

	THE IMPACT

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The transcript profile of canola (Brassica napus) exposed to the fungal pathogen Sclerotinia sclerotiorum also demonstrated an up-regulation of genes orthologous to AtERF2 and AtERF4 (Yang et al., 2007). This finding lends further support to the involvement of ERFs in expression of defense-related genes, as demonstrated by the work by McGrath et al (2005), and other jasmonate-responsive TFs, as shown in earlier studies (Anderson et al., 2004).

A pathogen-induced ERF gene from wheat (Triticum aestivum), TaERF3, was isolated, and although it was found to contain the highly conserved DNA-binding domains, it had low sequence similarity to other known ERF proteins (Zhang et al., 2007), suggesting that it is a new member of the ERF family. TaERF3-GFP fusion constructs demonstrate targeting of the protein to the nucleus. Changes in TaERF3 transcript profile were investigated in pathogen-exposed resistant and susceptible lines of wheat using real-time quantitative PCR. Induction of the gene was found in all lines, but the induction profiles between the resistant and susceptible lines were different. TaERF3 expression was also induced after treatment with SA, JA, or ETH, but earlier than pathogen exposure. Similarly, transgenic expression of another ERF-type TF, HvRAF, from barley (Hordeum vulgare) in Arabidopsis provided increased resistance against the bacterial pathogen Ralstonia solanacearum (Jung et al., 2007). Together, these suggest the involvement of ERFs in defense signaling pathways in diverse plant species.

	CONCLUSION

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The identification and functional characterization of additional members of the plant defense signaling pathway are important in the understanding of how plants respond to biotic stresses. As more is learned about the different defense signaling pathways, the complexity and interconnectedness between them becomes more apparent.

	FOOTNOTES

 
www.plantphysiol.org/cgi/doi/10.1104/pp.104.900254.

	LITERATURE CITED

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Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, Maclean DJ, Ebert PR, Kazan K (2004) Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 16: 3460–3479[Abstract/Free Full Text]

Brown RL, Kazan K, McGrath KC, Maclean DJ, Manners JM (2003) A role for the GCC-box in jasmonate-mediated activation of the PDF1.2 gene of Arabidopsis. Plant Physiol 132: 1020–1032[Abstract/Free Full Text]

Farmer EE, Alméras E, Krishnamurthy V (2003) Jasmonates and related oxylipins in plant responses to pathogenesis and herbivory. Curr Opin Plant Biol 6: 372–378[CrossRef][ISI][Medline]

Grennan AK (2006) Plant response to bacterial pathogens. Overlap between innate and gene-for-gene defense response. Plant Physiol 142: 809–811[Free Full Text]

Gutterson N, Reuber TL (2004) Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol 7: 465–471[CrossRef][ISI][Medline]

Jung J, Won SY, Suh SC, Kim H, Wing R, Jeong Y, Hwang I, Kim M (2007) The barley ERF-type transcription factor HvRAF confers enhanced pathogen resistance and salt tolerance in Arabidopsis. Planta 225: 575–588[CrossRef][ISI][Medline]

Kazan K (2006) Negative regulation of defense and stress genes by EAR-motif-containing repressors. Trends Plant Sci 11: 109–112[CrossRef][ISI][Medline]

Lorenzo O, Piqueras R, Sanchez-Serrano JJ, Solano R (2003) ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell 15: 165–178[Abstract/Free Full Text]

McGrath KC, Dombrecht B, Manners JM, Schenk PM, Edgar CI, Maclean DJ, Scheible W, Udvardi MK, Kazan K (2005) Repressor- and activator-type ethylene response factors functioning in jasmonate signaling and disease resistance identified via a genome-wide screen of Arabidopsis transcription factor gene expression. Plant Physiol 139: 949–959[Abstract/Free Full Text]

Yang B, Srivastava S, Deyholos MK, Kav NNV (2007) Transcriptional profiling of canola (Brassica napus L.) responses to the fungal pathogen Sclerotinia sclerotiorum. Plant Sci 173: 156–171

Zhang Z, Yao W, Dong N, Liang H, Liu H, Huang R (2007) A novel ERF transcription activator in wheat and its induction kinetics after pathogen and hormone treatments. J Exp Bot 58: 2993–3003[Abstract/Free Full Text]

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