From Chaos to Harmony: Responses and Signaling upon Microbial Pattern Recognition

Abstract

Pathogen- or microbe-associated molecular patterns (PAMPs/MAMPs) are detected as nonself by host pattern recognition receptors (PRRs) and activate pattern-triggered immunity (PTI). Microbial invasions often trigger the production of host-derived endogenous signals referred to as danger- or damage-associated molecular patterns (DAMPs), which are also perceived by PRRs to modulate PTI responses. Collectively, PTI contributes to host defense against infections by a broad range of pathogens. Remarkable progress has been made toward demonstrating the cellular and physiological responses upon pattern recognition, elucidating the molecular, biochemical, and genetic mechanisms of PRR activation, and dissecting the complex signaling networks that orchestrate PTI responses. In this review, we present an update on the current understanding of how plants recognize and respond to nonself patterns, a process from which the seemingly chaotic responses form into a harmonic defense.

Keywords: damage-associated molecular patterns (DAMPs); microbial elicitors; pathogen- or microbe-associated molecular patterns (PAMPs or MAMPs); pattern recognition receptors (PRRs); pattern-triggered immunity (PTI); plant defense.

Figure 1

Cellular and physiological responses triggered by patterns in plants. Plant cell surface–resident pattern recognition receptors (PRRs) perceive microbe-associated molecular patterns (MAMPs) or damage-associated molecular patterns (DAMPs) and recruit the coreceptors, leading to a series of intertwined cellular and physiological responses. PRR complex formation is accompanied by rapid transphosphorylation in the complex and phosphorylation of receptor-like cytoplasmic kinases (RLCKs). Activation of PRR complexes activates mitogen-activated protein kinase (MAPK) cascades and calcium-dependent protein kinases (CDPKs), which regulate gene transcriptional changes and other cellular responses. The hallmarks of pattern-triggered immunity (PTI) responses include calcium influx, ion efflux, actin filament remodeling, plasmodesmata (PD) and stomatal closure, callose deposition, and production of reactive oxygen species (ROS), nitride oxide (NO), phosphatidic acid (PA), phytoalexins, and phytohormones. Collectively, these responses contribute to plant resistance against a variety of pathogens. The potential connections among different responses, which were mainly derived from the studies using inhibitors, are indicated with an arrowed line for positive regulation and a T-shaped line for negative regulation. Abbreviations: DGK, diacylglycerol kinase; ET, ethylene; JA, jasmonic acid; PLC, phospholipase C; PLD, phospholipase D; SA, salicylic acid; TF, transcription factor.

Figure 2

Temporal dynamics of hallmark responses upon pattern perception. Pattern perception by pattern recognition receptors (PRRs) activates complex signaling events, culminating in a series of cellular and physiological responses with spatial and temporal dynamics. Some of the responses occur as early as seconds to minutes or as long as hours to days. Some responses are temporarily induced, whereas some are long lasting. The exemplary hallmark responses are shown with a timescale on the top. Images modified with permission from References (extracellular alkalization) and 53 (stomatal closure), and adapted by permission from Macmillan Publishers Ltd: Reference , copyright 2015 (ethylene production), Reference , copyright 2007 (growth inhibition), and Reference , copyright 2015 (Ca²⁺ influx). Abbreviations: Co-IP, co-immunoprecipitation; LPS, lipopolysaccharide; MAPK, mitogen-activated protein kinase; PGN, peptidoglycan; RLCK, receptor-like cytoplasmic kinase; RLU, relative light unit; ROS, reactive oxygen species; WB, Western blot.

Figure 3

Elicitation of early pattern recognition receptor (PRR) signaling in Arabidopsis and rice. (a) flg22-induced early signaling in Arabidopsis. (i) In the resting state, FLS2 does not form a stable complex with BAK1 but interacts with several receptor-like cytoplasmic kinases (RLCKs) (including BIK1, PCRK1/2, and BSK1), NADPH oxidase RBOHD, and heterotrimeric G proteins (XLG2/Gβ/Gγ). BAK1 interacts with the pseudokinase BIR2 to block the interaction between BAK1 and FLS2, the phosphatase PP2A to reduce its kinase activity, and the E3 ligases PUB12 and PUB13. BIK1 also associates with BAK1, the heterotrimeric G proteins, the phosphatase PP2C38, and CPK28. CPK28 phosphorylates BIK1, likely promoting BIK1 degradation through the 26S proteasome, whereas the heterotrimeric G proteins may suppress BIK1 degradation. (ii) Upon flg22 perception, FLS2 associates and transphosphorylates with BAK1, subsequently releasing BIK1, BSK1, BIR2, and the heterotrimeric G proteins from the FLS2-BAK1 complex. BIK1 phosphorylates RBOHD to regulate reactive oxygen species (ROS) production. RBOHD activity is also regulated by CDPKs and XLG2. The activated PRR complex further activates two mitogen-activated protein kinase (MAPK) cascades (MEKK1-MKK1/2-MPK4 and MEKK-MKK4/5-MPK3/6) and CPK4/5/6/11, which regulate gene transcriptional changes through phosphoregulation of transcription factors and the general transcription machinery. The FLS2 signaling is also positively regulated by PCRK1/2 and negatively regulated by MKKK7. (iii) To attenuate the activated PRRs, the plant E3 ubiquitin ligases PUB12 and PUB13 are phosphorylated by BAK1 and recruited to FLS2 for FLS2 ubiquitination and degradation in the vacuole or 26S proteasome. flg22 perception also induces FLS2 endocytosis and intracellular trafficking, which may lead to FLS2 degradation or full activation of defense responses. Other PRR complex components, such as BAK1 and BIK1, may also undergo endocytosis and degradation. Similar signaling mechanisms also apply to other PRRs, in particular, leucine-rich repeat (LRR)–receptor-like kinase (RLK)-encoded PRRs. Abbreviations: LE/MVB, late endosome/multivesicular body; TGN/EE, trans-Golgi network/early endosome. (b) Chitin-induced early signaling in Arabidopsis and rice. (i) In Arabidopsis, LYK5 heterodimerizes with CERK1 upon chitin perception. Phosphorylation of CERK1 further phosphorylates and activates PBL27, which directly interacts with MAPKKK5 and phosphorylates and activates the MAPK cascade (MAPKKK5-MKK4/5-MPK3/6). CERK1, to a lesser extent, also phosphorylates BIK1, which contributes to a ROS burst. (ii) In rice, OsCERK1 is recruited to chitin elicitor-binding protein (CEBiP) upon chitin perception. Activated OsCERK1 phosphorylates OsRLCK185 and likely OsRLCK176, which are required for the activation of chitin-induced MAPK cascades consisting of OsMAPKKK-OsMKK4-OsMPK3/6. OsCERK1 also phosphorylates OsRacGEF1, leading to the activation of OsRac1. OsRac1 is required for the chitin-induced MAPK activation and regulates ROS burst by interacting with OsRBOH.