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

Abstract

Summary Systemic acquired resistance (SAR) prepares infected plants for faster and stronger defense activation upon subsequent attacks. SAR requires an information relay from primary infection to distal tissue and the initiation and maintenance of a self‐maintaining phytohormone salicylic acid (SA)‐defense loop. In spatial and temporal resolution, we show that calcium‐dependent protein kinase CPK5 contributes to immunity and SAR. In local basal resistance, CPK5 functions upstream of SA synthesis, perception, and signaling. In systemic tissue, CPK5 signaling leads to accumulation of SAR‐inducing metabolite N‐hydroxy‐L‐pipecolic acid (NHP) and SAR marker genes, including Systemic Acquired Resistance Deficient 1 (SARD1) Plants of increased CPK5, but not CPK6, signaling display an ‘enhanced SAR’ phenotype towards a secondary bacterial infection. In the sard1‐1 background, CPK5‐mediated basal resistance is still mounted, but NHP concentration is reduced and enhanced SAR is lost. The biochemical analysis estimated CPK5 half maximal kinase activity for calcium, K50 [Ca2+], to be c. 100 nM, close to the cytoplasmic resting level. This low threshold uniquely qualifies CPK5 to decode subtle changes in calcium, a prerequisite to signal relay and onset and maintenance of priming at later time points in distal tissue. Our data explain why CPK5 functions as a hub in basal and systemic plant immunity.

Inducible biosynthesis and immune function of the systemic acquired resistance inducer N-hydroxypipecolic acid in monocotyledonous and dicotyledonous plants

“…Thus, in the absence of biotic challenge, plants apparently keep NHP at very low basal levels. Two recent studies have reported that Arabidopsis lines or mutant plants with constitutively elevated levels of NHP show permanently activated defenses and dwarfed phenotypes: specifically, lines overexpressing the calcium-dependent protein kinase CPK5 and mutants in which CAMTA3 , a negative immune-regulatory gene, is defective ( Guerra et al , 2020 ; Sun et al , 2020 ). When crossed with the fmo1 mutant, both lines lose their dwarfism and their ability to synthesize NHP, indicating that the growth retardation is caused by constitutively elevated levels of NHP.…”

Systemic propagation of immunity in plants

“…Notably, SARD1‐dependent defense responses through SA and Pip/NHP are further activated by CALCIUM‐DEPENDENT PROTEIN KINASE 5 (CPK5) (Dubiella et al ., 2013; Guerra et al ., 2020). After infection the CPK5 kinase is presumably activated by changes in intracellular Ca 2+ levels, and phosphorylates the reactive oxygen species (ROS)‐producing enzyme RESPIRATORY BURST HOMOLOG D (RBOHD) (Dubiella et al ., 2013).…”

Rapid systemic signaling during abiotic and biotic stresses: is the ROS wave master of all trades?

“…Systemic signaling from local to systemic tissues was demonstrated for many types of stresses including abiotic conditions, such as light stress, mechanical stress and temperature stress, as well as biotic stresses, such as bacterial, fungal and viral infections (e.g. Guerra et al , ; Choi et al , ; Katano et al , ; Lai et al , ; Chen et al , ). The faster the systemic response is, the better chance the plant has to acclimate and defend itself against the upcoming abiotic or biotic challenge (Kollist et al , ).…”