A Genomic Approach to Identify Regulatory Nodes in the Transcriptional Network of Systemic Acquired Resistance in Plants

By Dong Wang, N. Amornsiripanitch, Xinnian Dong. PLoS Pathogens, 2006

759 citations recorded by the source corpus.

Many biological processes are controlled by intricate networks of transcriptional regulators. With the development of microarray technology, transcriptional changes can be examined at the whole-genome level. However, such analysis often lacks information on the hierarchical relationship between components of a given system. Systemic acquired resistance (SAR) is an inducible plant defense response involving a cascade of transcriptional events induced by salicylic acid through the transcription cofactor NPR1. To identify additional regulatory nodes in the SAR network, we performed microarray analysis on Arabidopsis plants expressing the NPR1-GR (glucocorticoid receptor) fusion protein. Since nuclear translocation of NPR1-GR requires dexamethasone, we were able to control NPR1-dependent transcription and identify direct transcriptional targets of NPR1. We show that NPR1 directly upregulates the expression of eight WRKY transcription factor genes. This large family of 74 transcription factors has been implicated in various defense responses, but no specific WRKY factor has been placed in the SAR network. Identification of NPR1-regulated WRKY factors allowed us to perform in-depth genetic analysis on a small number of WRKY factors and test well-defined phenotypes of single and double mutants associated with NPR1. Among these WRKY factors we found both positive and negative regulators of SAR. This genomics-directed approach unambiguously positioned five WRKY factors in the complex transcriptional regulatory network of SAR. Our work not only discovered new transcription regulatory components in the signaling network of SAR but also demonstrated that functional studies of large gene families have to take into consideration sequence similarity as well as the expression patterns of the candidates.

Subfields: Plant Science

View Paper: https://www.semanticscholar.org/paper/fc35d9e56c7e90d91d1a98deab854fa8e7b2f8e8

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Citations in the corpus

How do plants achieve immunity? Defence without specialized immune cells (2012, background): “thaliana plants with these compounds results in marked transcriptional changes in more than 2,000 genes, including those that encode pathogenesis-related (PR) proteins with antimicrobial activit”
Role of plant hormones in plant defence responses (2009, background): “These genes included an auxin importer AUX1, an auxin exporter PIN7, auxin receptors TIR1 and AFB1, and genes belonging to auxin inducible SAUR and Aux/IAA family (Wang et al. 2007).”
Regulation of water, salinity, and cold stress responses by salicylic acid (2014, background): “Furthermore, the transcriptome analysis of wild-type and npr1 plants following treatment with BTH, a functional analog of SA, revealed that almost all BTH-responsive genes are under NPR1 control (Wang et al., 2006).”
Systemic acquired resistance: turning local infection into global defense. (2013, neutral): “(137) showed that WRKY54 and WRKY70 are important suppressors of SA biosynthesis: In the wrky54 wrky70 double mutant, ICS1 was expressed and SA accumulated at much higher levels than it did in the wild type.”
Hormonal modulation of plant immunity. (2012, background): “The regulatory protein NPR1 is an important transducer of SA-induced redox changes and a crucial transcriptional coactivator of many SA-responsive genes (Wang et al. 2006).”
Signaling mechanisms in pattern-triggered immunity (PTI). (2015, background): “NPR1, although not clearly itself an SA receptor, is a master regulator of SAmediated responses controlling gene expression (Mou et al., 2003; Wang et al., 2006), but some evidences also suggest that there are SA receptors other than NPR3 and NPR4 to mediate NPR1-”
Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. (2007, methodology): “To investigate whether SA treatment affects auxin levels, we measured free auxin (indole-3-acetic acid; IAA) in SA-treated plants under conditions similar to those of the microarray experiment [12].”
Impact of root exudates and plant defense signaling on bacterial communities in the rhizosphere. A review (2011, background): “such as PR-1 (Zhang et al. 1999; Pieterse and Van Loon 2004; Wang et al. 2006).”
Salicylic Acid, a multifaceted hormone to combat disease. (2009, background): “WRKY70 is required for SA-mediated resistance in various plantpathogen interactions (49, 100, 101), although expression of ICS1 and SA accumulation were upregulated in wrky70/wrky54 double mutants (205).”
Growth-defense tradeoffs in plants: a balancing act to optimize fitness. (2014, positive): “WRKYs are involved in both NPR1-dependent and NPR1-independent SA signaling and, as in the case of PTI, include both positive and negative regulators of SA-mediated defense (Yu et al., 2001; Wang et al., 2006; Rushton et al., 2010; Fu and Dong, 2013).”
Networks of WRKY transcription factors in defense signaling. (2007, background): “Loss-ofAtWRKY70 function rendered plants susceptible to the bacteria Erwinia carotovora and Pseudomonas syringae as well as the fungi Erysiphe cichoracearum and Botrytis cinerea [13,15,16 ].”
The Role of WRKY Transcription Factors in Plant Immunity[W] (2009, background): “Expression of at least nine WRKY genes, AtWRKY18, -38, -53, -54, -58, -59, -62, -66, and -70, is dependent on NPR1, suggesting that they may be under TGA factor control (Wang et al., 2006; Mao et al., 2007).”
The WRKY Gene Family in Rice (Oryza sativa) (2007, background): “The latest microarray analysis on Arabidopsis plants expressing the NPR1-glucocorticoid receptor (GR) fusion protein indicates that NPR1 directly upregulates the expression of eight WRKY transcription factor genes (Wang et al. 2006).”
Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. (2010, background): “For instance, WRKY54 and WRKY70 positively regulate SA-response gene expression but also negatively regulate SA accumulation (Wang et al., 2006).”