Post-translational modification of host proteins in pathogen-triggered defence signalling in plants

Abstract

Microbial plant pathogens impose a continuous threat to global food production. Similar to animals, an innate immune system allows plants to recognize pathogens and swiftly activate defence. To activate a rapid response, receptor-mediated pathogen perception and subsequent downstream signalling depends on post-translational modification (PTM) of components essential for defence signalling. We discuss different types of PTMs that play a role in mounting plant immunity, which include phosphorylation, glycosylation, ubiquitination, sumoylation, nitrosylation, myristoylation, palmitoylation and glycosylphosphatidylinositol (GPI)-anchoring. PTMs are rapid, reversible, controlled and highly specific, and provide a tool to regulate protein stability, activity and localization. Here, we give an overview of PTMs that modify components essential for defence signalling at the site of signal perception, during secondary messenger production and during signalling in the cytoplasm. In addition, we discuss effectors from pathogens that suppress plant defence responses by interfering with host PTMs.

Figure 1

Defence‐related signal transduction cascades that depend on post‐translational modifications. Receptors mediate recognition of microbe‐associated molecular patterns (MAMPs) and race‐specific elicitors (elicitor), but they require additional proteins for their function. Proteins with nucleotide‐binding and leucine‐rich repeat domains (NB‐LRR) recognize their cognate elicitors intracellularly, while receptor‐like proteins (RLP) and receptor‐like kinases (RLK) are probably activated outside the cell. RLPs require additional proteins that bind the cytoplasmically localized part of the protein to mediate downstream signalling, while RLKs require their kinase domain to autophosphorylate and form complexes with additional proteins. RLKs might become ubiquitinated, after which they are internalized and targeted for proteasome‐mediated degradation. Signalling downstream from the receptor eventually leads to the formation of secondary messengers such as phosphatidic acid (PA), possibly via phospholipase C (PLC) phosphorylation, and nitric oxide (NO). The concentrations of ions such as H⁺, K⁺ and Ca²⁺ are controlled by (de)phosphorylation of the respective ATPase while the production of ROS is stimulated upon phosphorylation of the NADPH oxidases (RBOH). The secondary messengers also mediate phosphorylation of proteins such as calcium‐dependent protein kinases (CDPK), or syntaxins, which might promote the release of pathogenesis‐related (PR) proteins into the apoplast. Mitogen‐activated protein kinase (MAPK) cascades are activated by phosphorylation of the individual components, which eventually leads to the phosphorylation of, amongst others WRKY transcription factors, 1‐aminocyclopropane‐1‐carboxylic acid synthase (ACS) and MAP kinase substrate 1 (MKS1), which influence the production of ethylene (Et) and salicylic acid (SA), respectively. Also, E3‐ligases are activated, which might result in the ubiquitination and subsequent degradation of negative regulators of the signalling cascades, thereby providing a positive feedback loop. In addition, negative feedback loops are required to prevent an uncontrolled hypersensitive response (HR). For example, MAPK (MPK)‐mediated ethylene production negatively regulates MAPK activation. The secondary messengers influence each other and fine‐tune the downstream signal while proteins modified by secondary messengers might inhibit receptor‐mediated signals. Eventually, a balanced signal will lead to increased (basal) resistance and possibly a HR. Phosphorylation states as presented in this figure represent the active state of the protein. Protein names indicated in grey might be specific for a particular plant–pathogen interaction. ACIK1, Avr9/Cf‐9‐induced kinase 1; CITRX, Cf‐9‐interacting thioredoxin; RIN4, RPM1‐interacting protein 4; BAK1, BRASSINOSTEROID‐INSENSITIVE 1; XB3, Xa21‐binding protein 3; Adi3, AvrPto‐dependent Pto‐interacting protein 3; PDK1, 3‐phosphoinositide‐dependent protein kinase‐1; AGC‐kinase, protein kinase A, G and C family; OXI1, oxidative signal‐inducible 1.