The Lifecycle of the Plant Immune System

Abstract

Throughout their life span, plants confront an endless barrage of pathogens and pests. To successfully defend against biotic threats, plants have evolved a complex immune system responsible for surveillance, perception, and the activation of defense. Plant immunity requires multiple signaling processes, the outcome of which vary according to the lifestyle of the invading pathogen(s). In short, these processes require the activation of host perception, the regulation of numerous signaling cascades, and transcriptome reprograming, all of which are highly dynamic in terms of temporal and spatial scales. At the same time, the development of a single immune event is subjective to the development of plant immune system, which is co-regulated by numerous processes, including plant ontogenesis and the host microbiome. In total, insight into each of these processes provides a fuller understanding of the mechanisms that govern plant-pathogen interactions. In this review, we will discuss the "lifecycle" of plant immunity: the development of individual events of defense, including both local and distal processes, as well as the development and regulation of the overall immune system by ontogenesis regulatory genes and environmental microbiota. In total, we will integrate the output of recent discoveries and theories, together with several hypothetical models, to present a dynamic portrait of plant immunity.

Keywords: Defense; development; environment; pathogens; plant immunity; signaling; system; virulence.

Figure 1.

Invasion strategies by phytopathogens. To promote infection, both phyllospheric and rhizospheric pathogens must overcome physical barriers on the plant surface. Filamentous pathogens typically infect their host using the appressorium to invade living cells. During infection, the germinating spore (S) forms an extended tube-like structure (i.e., germination tube, GT), which then develops into an appressoria (A) that promotes the entry into plant. Appressorium can either directly penetrate into epidermis cells by breaking through the cuticle surface and cell wall, or enter through the apoplast, the space between cells. Additionally, wounds or natural openings (i.e., stomata) on the plant surface provide easy entry into the intercellular space. Once inside the host, filamentous pathogens use a root-like structure (i.e., haustoria, H) to obtain host-derived nutrients, resulting in the establishment of the pathogen-host interface. The invasion of bacterial phytopathogens, unlike filamentous pathogen, highly depends on natural openings to enter the plant host.

Figure 2.

A schematic map of plant local immunity. Invasive pathogens are recognized by plant PRR (pattern recognition receptor) proteins, which results in the activation of broad spectrum of downstream signaling, such as Ca²⁺ influx, the accumulation of H₂O₂ generated by RbohD (respiratory burst oxidase homolog protein D), and kinase cascading, which includes signaling pathways mediated by MAPKs, CPKs, and other additional kinases. As depicted, various kinases may also engage in a highly coordinated cross-talk during signal amplification and attenuation. These immune signals, amplified by kinase cascades, trigger a variety of defense responses, including cytoskeletal remodeling, activation of defense function in organelles, and transcriptional reprograming through the activity of pro-immune transcription factors (TF). In total, the sum of this highly coordinated signaling functions to promote plant defense signaling and pathogen resistance. Concomitant with the activation of defense signaling, the attenuation of key immune pathways occurs, a process hypothesized to function in rebalancing of immunity and growth pathways occurs. To cope with plant immunity, pathogens have evolved mechanisms to deliver effector proteins into plant cell, which target and inhibits immune signaling, as well as to subvert immunity through targeting of critical host cellular processes. In response, plants utilize NLR (nucleotide-binding leucine-rich-repeat proteins) proteins to recognize certain effectors through sensing pathogen modification of surveilled host processes (i.e., guardee), resulting the activation of robust immune signaling and cell death (i.e., ETI; effector-triggered immunity). As a potential mechanism to activate ETI, cell membrane (PM)-associated NLRs (in most instances, possessing a coiled-coil domain, i.e, C-NLR), can form a channel-like structure following activation, which presumably functions to mobilize additional defense signaling molecules. NLRs containing a Toll/interleukin-1 receptor-like domain (T-NLRs) at the C-terminus are typically associated with a nuclear subcellular localization, and in large part, function as sensors (i.e., sNLR) that activate helper NLRs (hNLR) to form channels within the PM. As an additional hypothesized mechanism, activated nuclear NLRs may regulate specific defense genes functioning in ETI, by interacting with TFs. Dashed in indicate putative/hypothesized processes.

Figure 3.

Dynamics of signaling processes associated with local immunity. The signaling processes associated with local immune signaling can largely be described in a temporal fashion; for the sake of comparison, we suppose “Time 0” = PRR activation. To estimate the signaling dynamics (i.e., timing of initiation, sustained saturation, peak of increasing speed, and termination), pub lished data recording the development of immune processes following elicitor treatment or pathogen infection are collected, analyzed, and translated into this figure. Dashed lines in indicate estimation without direct evidence.

Figure 4.

The mechanism of distal immune signal transmission. (A) Biotic stresses trigger systemic immune signaling. Local immunity is induced following local pathogen perception, which results not only in the activation of local signaling, but also the induction of distal signaling within the root parenchyma and/or mesophyll. When the signal(s) reach the vasculature, signal transmission is substantially accelerated until it arrives at the site of distal parenchyma tissues in the leaf and/or root, after which time signal transmission decelerates. (B) Generation of distal signal molecules in local cells. Following immune activation, Ca²⁺ influx is initiated through an unknown Ca²⁺ channel(s) that are directly activated by PRR and/or RBOHD-synthesized H₂O₂. This initial influx activates Ca²⁺-dependent signaling nodules as CPKs and CaM, which further activates additional Ca²⁺ channels such as CGNC2/4, rendering robust secondary Ca²⁺ influxes. Local defense response also leads to biosynthesis of immune hormones such as SA and JA, a partial of which will spread to distal tissues. (C) Transmission of distal signals in parenchyma cells (including mesophyll). Ca²⁺ influx at a given location can activate RbohD via CPKs and presumably CIPKs, a process that results in the generation of H₂O₂ and the further activation of unknown H₂O₂-activated Ca²⁺ channels. Simultaneously, Ca²⁺ influx triggers an unknown glutamate (Glu) efflux pathway that activate glutamate-gated Ca²⁺ channel GRL3.3/3.6. Tonoplast membrane localized TPC1, a Ca²⁺ channel, gated by both Ca²⁺ and the resultant electrical potential may serve to amplify the Ca²⁺ signal. The transmission of signaling molecules is slowed at intercellular junctions as a result of the cell wall. (D) Transmission of distal signals within the vasculature. The mechanisms are the same as those in parenchyma (C), yet the gap of the intercellular junction is relieved via the action of the sieve plate, resulting in a faster speed of signal transmission.

Figure 5.

Phenotypic example of age-related immunity in Arabidopsis. (A) Disease symptom varies in simultaneously inoculated rosette leaves of 5-week-old Arabidopsis Col-0 following dip-inoculation with Pst DC3000 (10⁸ CFU/mL). While early-developed rosette leaves (red arrow) show severe disease symptoms (i.e., shrinking, chlorosis, and water-soaking), late-developed leaves (blue arrow) do not show disease symptoms in response to pathogen inoculation. (B) Immune-associated gene expression gradually changes among leaves in different development order. To illustrate this, we downloaded published RNA-microarray data (Winter et al., 2007) reflecting the transcriptome of Arabidopsis rosette leaves 2, 4, 6, 7, 8, 10, 12, and both healthy and senescent cauline leaves. To screen for immune-associated genes, we selected genes within 10 key immune-associated categories: immune, immunity, resistance, defense, biotic, chitin, fungus, flagellin, peptidoglycan, and bacterium. As an output of this analysis, we identified 3901 genes with potential roles related to plant immunity. Next, we used a Pearson filter (|r| > 0.5 and P-value ≤ 0.05) to select and categorize genes whose expression pattern are corelated to the development order of different samples and determined 2104 immune-associated genes that can be categorized into 4 groups, with differing but significant trends, during development of Arabidopsis. The average pattern of each group of these genes is presented. Bold, tinted line: average. Thin, dark line: average ± se.

Figure 6.

The development of plant immune system is regulated by both autologous genes and commensal microbiota. Plant immune system maturation is correlated with the system development of the plant. In this process, miR156/157-SPLs plays a significant role in regulating the expression of genes functioning in immunity, including JAZ3, N, RPS4, ICS, and FLS2. As a central regulatory module of plant development, miR156/157-SPLs also play a key role in the synchronization of plant aging and organ morphogenesis. Additionally, the development of the plant immune system is indispensable to its commensal microbiota. While they do not necessarily cause disease, these microbes stimulate the development, maturation, and activity of the plant immune system, as well as the general development of the plant. To recruit a healthy microbiota, plants can selectively or nonselectively repel pathogens and attract beneficial microbes. Beneficial microbes can also inhibit the population growth of host associated pathogens, and as such, indirectly influence plant immunity.