The fog of war: How network buffering protects plants’ defense secrets from pathogens

Plants lack the mechanisms needed for adaptive immunity and thus rely entirely on innate immunity to protect themselves from pathogens and pests [1]. Their innate immune systems must protect against innumerable, highly adaptable viruses bacteria, fungi, oomycetes, nematodes, and insects. Two important components of the plant immune system are induced by the presence of pathogen molecules [1]. One of these is triggered by molecules common to multiple microbes (pathogen-associated molecular patterns [PAMPs]), such as bacterial flagellin, fungal, or arthropod chitin fragments. PAMP-triggered immunity (PTI) is mediated by a diversity of cell surface receptors, some of which carry intracellular kinase domains. The second inducible component of defense is triggered as a result of plants’ recognition of specific virulence proteins (effectors) produced by pathogens—known as effector-triggered immunity (ETI). Complex and overlapping networks of signal transduction events mediate and integrate the induction of the defense responses that comprise PTI and ETI [2]. Signaling networks that mediate plants’ responses to the abiotic environment must also be integrated [3]. These signaling networks involve phosphorylation cascades as well as the release of chemical signals, such as reactive oxygen species, lipid and inositol derivatives, and plant hormones, such as salicylic acid (SA), jasmonic acid (JA), ethylene (ET), and abscisic acid [4]. The defense responses themselves include thousands of gene expression changes involving genes encoding antimicrobial proteins and peptides, secondary metabolite biosynthetic genes, and many genes of currently unknown function [4]. Molecular dissections of successful plant pathogens have revealed that a common strategy for overcoming plant defenses is the production of chemicals and/or effector proteins that can enter inside host cells and interfere with the signaling events responsible for PTI and ETI [5]. A major challenge for plants therefore is to protect these signaling events from pathogen interference. In this issue of PLOS Genetics, Hillmer et al. [6] describe a highly detailed, systems-level dissection of the signaling network that mediates PTI responses in the model plant Arabidopsis. The study, which integrates mutational analysis, transcript and hormone profiling, and statistical modeling, reveals that the PTI signaling network is highly buffered against interference. In other words, overall transmission of signaling through the network persists even when major components are interrupted, for example by mutations or by the actions of pathogen effectors (Fig 1). Buffering of the immune signaling network can also influence pathogen evolution as it obscures the contributions of individual pathogen proteins to virulence.