Protein kinase‐mediated signalling in priming: Immune signal initiation, propagation, and establishment of long‐term pathogen resistance in plants

Abstract

"Priming" in plant phytopathology describes a phenomenon where the "experience" of primary infection by microbial pathogens leads to enhanced and beneficial protection of the plant against secondary infection. The plant is able to establish an immune memory, a state of systemic acquired resistance (SAR), in which the information of "having been attacked" is integrated with the action of "being prepared to defend when it happens again." Accordingly, primed plants are often characterized by faster and stronger activation of immune reactions that ultimately result in a reduction of pathogen spread and growth. Prerequisites for SAR are (a) the initiation of immune signalling subsequent to pathogen recognition, (b) a rapid defence signal propagation from a primary infected local site to uninfected distal parts of the plant, and (c) a switch into an immune signal-dependent establishment and subsequent long-lasting maintenance of phytohormone salicylic acid-based systemic immunity. Here, we provide a summary on protein kinases that contribute to these three conceptual aspects of "priming" in plant phytopathology, complemented by data addressing the role of protein kinases crucial for immune signal initiation also for signal propagation and SAR.

Stress priming, memory, and signalling in plants

“…A study by Hake and Romeis () in this issue focusses on the role of CDPKs in stress priming and memory. CDPKs are not only important for the Ca 2+ ‐ and ROS‐mediated initiation of stress signalling (Dubiella et al, ), but they also support the hormone‐regulated systemic signal propagation upon pathogen infection.…”

“…Protein kinases may further control activities of enzymes involved in the biosynthesis of defensive secondary plant metabolites. Hake and Romeis () propose that CDPKs take up a “primed conformation” after their response to a first priming stimulus which facilitates full activation upon repeated stress exposure.…”

Calcium‐dependent protein kinase 5 links calcium signaling with N‐hydroxy‐l‐pipecolic acid‐ and SARD1‐dependent immune memory in systemic acquired resistance

“…However, SA is not considered to be the only signal molecule to be transported through the plant. Thus, the switch to SAR requires an information relay of the 'having been attacked' perception from local to distal plant sites as well as the initiation and maintenance of an SA-accumulation loop that manifests 'being prepared when it happens again' information (Hake & Romeis, 2018). The asterisks indicate statistically significant differences in comparison to Col-0 (one-way ANOVA, Dunnett post-test; **, P < 0.01; ns, not significant).…”

“…PTI and ETI may result in 'priming' of SAR, rendering a plant prepared for repeated infection after a time gap. Primed plants show more rapid and stronger activation of defense responses upon a secondary infection even by unrelated pathogens (Conrath, 2006;Hilker et al, 2015;Hake & Romeis, 2018).…”

N-hydroxypipecolic acid: a general and conserved activator of systemic plant immunity

“…The perception of pathogens in a primary local infection event induces immune signalling that activates local defences and is propagated to distal plant parts to prepare for future threats. In these so-called ‘primed’ leaves, a faster and stronger immune response is mounted when exposed to a subsequent pathogen attack, and leaf infection damage is reduced to a minimum ( Navarova et al , 2012 ; Hake and Romeis, 2019 ).…”