The HSF-like Transcription Factor TBF1 Is a Major Molecular Switch for Plant Growth-to-Defense Transition

Department of Biology, Box 90338, Duke University, Durham, NC 27708, USA.
Current biology: CB (Impact Factor: 9.57). 01/2012; 22(2):103-12. DOI: 10.1016/j.cub.2011.12.015
Source: PubMed


Induction of plant immune responses involves significant transcription reprogramming that prioritizes defense over growth-related cellular functions. Despite intensive forward genetic screens and genome-wide expression-profiling studies, a limited number of transcription factors have been found that regulate this transition.
Using the endoplasmic-reticulum-resident genes required for antimicrobial protein secretion as markers, we identified a heat-shock factor-like transcription factor that specifically binds to the TL1 (GAAGAAGAA) cis element required for the induction of these genes. Surprisingly, plants lacking this TL1-binding factor, TBF1, respond normally to heat stress but are compromised in immune responses induced by salicylic acid and by microbe-associated molecular pattern, elf18. Genome-wide expression profiling indicates that TBF1 plays a key role in the growth-to-defense transition. Moreover, the expression of TBF1 itself is tightly regulated at both the transcriptional and translational levels. Two upstream open reading frames encoding multiple aromatic amino acids were found 5' of the translation initiation codon of TBF1 and shown to affect its translation.
Through this unique regulatory mechanism, TBF1 can sense the metabolic changes upon pathogen invasion and trigger the specific transcriptional reprogramming through its target genes expression.

Download full-text


Available from: Wei Wang,
62 Reads
  • Source
    • "Interestingly, SA and Pseudomonas infection cause DNA damage, such as DNA double strand breaks, suggesting that DNA damage response is an intrinsic component of SA-mediated transcription during plant immunity (Yan et al., 2013; Song and Bent, 2014). Besides functional regulation of transcription factors by NPR1 through complex formation, NPR1 also controls expression of transcription factors, such as WRKY transcription factors, which are required for SA-mediated transcriptional reprogramming (Wang et al., 2006; Pajerowska-Mukhtar et al., 2012). The Arabidopsis genome encodes 74 WRKY factors which bind the specific DNA sequence (C/TTGACT/C), termed the W-box (Rushton et al., 2010). "
    [Show abstract] [Hide abstract]
    ABSTRACT: The phytohormone salicylic acid (SA) is a small phenolic compound that regulates diverse physiological processes, in particular plant resistance against pathogens. Understanding SA-mediated signaling has been a major focus of plant research. Pathogen-induced SA is mainly synthesized via the isochorismate pathway in chloroplasts, with ICS1 (ISOCHORISMATE SYNTHASE 1) being a critical enzyme. Calcium signaling regulates activities of a subset of transcription factors thereby activating nuclear ICS1 expression. The produced SA triggers extensive transcriptional reprogramming in which NPR1 (NON-EXPRESSOR of PATHOGENESIS-RELATED GENES 1) functions as the central coactivator of TGA transcription factors. Recently, two alternative but not exclusive models for SA perception mechanisms were proposed. The first model is that NPR1 homologs, NPR3 and NPR4, perceive SA thereby regulating NPR1 protein accumulation. The second model describes that NPR1 itself perceives SA, triggering an NPR1 conformational change thereby activating SA-mediated transcription. Besides the direct SA binding, NPR1 is also regulated by SA-mediated redox changes and phosphorylation. Emerging evidence show that pathogen virulence effectors target SA signaling, further strengthening the importance of SA-mediated immunity.
    Frontiers in Plant Science 12/2014; 5:697. DOI:10.3389/fpls.2014.00697 · 3.95 Impact Factor
  • Source
    • "We showed that AED1 transcript accumulation is induced locally and systemically by infection and locally by SA (Figs. 4 and 6). Because the conditional overexpression of AED1-HA repressed both SAR and SA-induced resistance without affecting the growth of Pst in healthy plants (Fig. 5; Supplemental Fig. S7), AED1 might be part of a homeostatic mechanism to limit SAR signaling (Fig. 7) and thus regulate the resource allocation in the tradeoff between defense and plant growth (Heidel and Dong, 2006; van Hulten et al., 2006; Traw et al., 2007; Pajerowska-Mukhtar et al., 2012). In support of this, we found that reduced AED1 transcript levels in Arabidopsis RNAi:AED1/At5g10770 plants caused severe stunting, a phenotype that is often observed in constitutive defense mutants (Shirano et al., 2002; Figure 7. Model integrating EDS1, PAD4, AED1, and LLP1 in SAR signaling. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Systemic acquired resistance (SAR) is an inducible immune response that depends on ENHANCED DISEASE SUSCEPTIBILITY1 (EDS1). Here, we show that Arabidopsis thaliana EDS1 is required for both SAR signal generation in primary infected leaves and SAR signal perception in systemic uninfected tissues. In contrast to SAR signal generation, local resistance remains intact in eds1 mutant plants in response to Pseudomonas syringae delivering the effector protein AvrRpm1. We utilized the SAR-specific phenotype of the eds1 mutant to identify new SAR regulatory proteins in plants conditionally expressing AvrRpm1. Comparative proteomic analysis of apoplast-enriched extracts from AvrRpm1-expressing wild type and eds1 mutant plants led to the identification of 12 APOPLASTIC, EDS1-DEPENDENT (AED) proteins. The genes encoding AED1, a predicted aspartyl protease, and another AED, LEGUME LECTIN-LIKE PROTEIN1 (LLP1), were induced locally and systemically during SAR signaling and locally by salicylic acid (SA) or its functional analog BTH. Because conditional over-accumulation of AED1-HA inhibited SA-induced resistance and SAR but not local resistance, the data suggest that AED1 is part of a homeostatic feedback mechanism regulating systemic immunity. In llp1 mutant plants, SAR was compromised, whereas the local resistance that is normally associated with EDS1 and SA as well as responses to exogenous SA appeared largely unaffected. Together, the data indicate that LLP1 promotes systemic rather than local immunity, possibly in parallel with SA. Our analysis reveals new positive and negative components of SAR and reinforces the notion that SAR represents a distinct phase of plant immunity beyond local resistance.
    Plant physiology 04/2014; 165(2). DOI:10.1104/pp.114.239665 · 6.84 Impact Factor
  • Source
    • "NPR1 upregulates the expression of numerous genes encoding ER-resident proteins involved in protein folding and secretion in anticipation of PR protein production [24]. NPR1-dependent genes encoding ER proteins are enriched in the TL1 cis-element [24] that is recognized by the heat shock factor-like protein TBF1 [28]. Mutation of TBF1 reduces apoplastic accumulation of PR-1 and impairs both SA- and elf18- induced disease resistance. "
    [Show abstract] [Hide abstract]
    ABSTRACT: During the plant immune response, large-scale transcriptional reprogramming is modulated by numerous transcription (co) factors. The Arabidopsis basic leucine zipper transcription factors TGA1 and TGA4, which comprise the clade I TGA factors, have been shown to positively contribute to disease resistance against virulent strains of the bacterial pathogen Pseudomonas syringae. Despite physically interacting with the key immune regulator, NON-EXPRESSOR OF PATHOGENESIS-RELATED GENES 1 (NPR1), following elicitation with salicylic acid (SA), clade I function was shown to be largely independent of NPR1. Unlike mutants in NPR1, tga1-1 tga4-1 plants do not display reductions in steady-state levels of SA-pathway marker genes following treatment with this phenolic signaling metabolite or after challenge with virulent or avirulent P. syringae. By exploiting bacterial strains that have limited capacity to suppress Arabidopsis defence responses, the present study demonstrates that tga1-1 tga4-1 plants are compromised in basal resistance and defective in several apoplastic defence responses, including the oxidative burst of reactive oxygen species, callose deposition, as well as total and apoplastic PATHOGENESIS-RELATED 1 (PR-1) protein accumulation. Furthermore, analysis of npr1-1 and the tga1-1 tga4-1 npr1-1 triple mutant indicates that clade I TGA factors act substantially independent of NPR1 in mediating disease resistance against these strains of P. syringae. Increased sensitivity to the N-glycosylation inhibitor tunicamycin and elevated levels of endoplasmic reticulum (ER) stress marker genes encoding ER-resident chaperones in mutant seedlings suggest that loss of apoplastic defence responses is associated with aberrant protein secretion and implicate clade I TGA factors as positive regulators of one or more ER-related secretion pathways.
    PLoS ONE 09/2013; 8(9):e77378. DOI:10.1371/journal.pone.0077378 · 3.23 Impact Factor
Show more