The highly buffered Arabidopsis immune signaling network conceals the functions of its components

Abstract

Plant immunity protects plants from numerous potentially pathogenic microbes. The biological network that controls plant inducible immunity must function effectively even when network components are targeted and disabled by pathogen effectors. Network buffering could confer this resilience by allowing different parts of the network to compensate for loss of one another’s functions. Networks rich in buffering rely on interactions within the network, but these mechanisms are difficult to study by simple genetic means. Through a network reconstitution strategy, in which we disassemble and stepwise reassemble the plant immune network that mediates Pattern-Triggered-Immunity, we have resolved systems-level regulatory mechanisms underlying the Arabidopsis transcriptome response to the immune stimulant flagellin-22 (flg22). These mechanisms show widespread evidence of interactions among major sub-networks—we call these sectors—in the flg22-responsive transcriptome. Many of these interactions result in network buffering. Resolved regulatory mechanisms show unexpected patterns for how the jasmonate (JA), ethylene (ET), phytoalexin-deficient 4 (PAD4), and salicylate (SA) signaling sectors control the transcriptional response to flg22. We demonstrate that many of the regulatory mechanisms we resolved are not detectable by the traditional genetic approach of single-gene null-mutant analysis. Similar to potential pathogenic perturbations, null-mutant effects on immune signaling can be buffered by the network.

The Receptor-like Cytoplasmic Kinase BIK1 Localizes to the Nucleus and Regulates Defense Hormone Expression during Plant Innate Immunity

“…The plant hormones JA, ET, and SA play important roles during immune signaling post-pathogen recognition (Hillmer et al, 2017; Pieterse et al, 2012; Robert-Seilaniantz et al, 2011; Tsuda et al, 2009). However, a direct mechanistic link connecting PRR signaling to hormone activation is missing.…”

“…Until recently, it was generally accepted that SA and JA have mutually exclusive roles in defense against biotrophic versus necrotrophic pathogens (Glaze-brook, 2005; Spoel et al, 2007). Recent systems biology approaches and network analysis have revealed a previously unrecognized collaborative role between JA and SA during biotrophic and hemibiotrophic pathogen defense (Hillmer et al, 2017; Kim et al, 2014; Tsuda et al, 2009). Direct hormone measurement with higher-order mutations of JA, SA, ET, and phytoalexin deficient 4 (PAD4) signaling networks has revealed that the JA subnetwork positively regulates both SA- and PAD4-mediated signaling, which is important for defense against biotrophic pathogens (Hillmer et al, 2017).…”

“…Jasmonic acid (JA) and ethylene (ET) are mostly involved in resistance against necrotrophic pathogens, while salicylic acid (SA) is involved in providing resistance against biotrophic and hemibiotrophic pathogens (Glazebrook, 2005; Robert-Seilaniantz et al, 2011). Interestingly, SA, JA, and ET levels are increased upon flg22 perception (Felix et al, 1999; Flury et al, 2013; Mishina and Zeier, 2007) and play positive roles in PTI (Hillmer et al, 2017; Kim et al, 2014; Tsuda et al, 2009; Zipfel et al, 2004). However, the mechanism through which PAMP perception at the plasma membrane leads to activation of hormone responses remains unclear.…”

Reactive oxygen species metabolism and plant-fungal interactions

“…Plants have developed finely-tuned innate immune responses to detect the presence of pathogens via pathogen associated molecular patterns (PAMP) triggered Immunity (PTI) and effector triggered immunity (ETI) (Chisholm et al, 2006;Jones and Dangl, 2006;Hillmer et al, 2017). Innate immune responses include callose deposition, increased pathogenesis related (PR) gene expression and oxidative bursts producing ROS.…”

“…Due to the unwanted effects of ETI-especially PCD which would hinder biotrophic survival-pathogens have evolved effector proteins to bypass detection from R proteins. This co-evolution between plant and pathogens serves as the basis of the zig-zag model of plant pathology (Hillmer et al, 2017;Jones and Dangl, 2006). However, oxidative bursts are not effective in preventing proliferation of the necrotrophic fungi B. cinerea and Sclerotinia sclerotiorum, and can be tolerated by the hemibiotrophs, Septoria tritici and M. oryzae (Govrin and Levine, 2000;Shetty et al, 2007;Samalova et al, 2014;Marroquin-Guzman et al, 2017).…”