CAMTA-Mediated Regulation of Salicylic Acid Immunity Pathway Genes in Arabidopsis Exposed to Low Temperature and Pathogen Infection

Abstract

Arabidopsis thaliana calmodulin binding transcription activator (CAMTA) factors repress the expression of genes involved in salicylic acid (SA) biosynthesis and SA-mediated immunity in healthy plants grown at warm temperature (22°C). This repression is overcome in plants exposed to low temperature (4°C) for more than a week and in plants infected by biotrophic and hemibiotrophic pathogens. Here, we present evidence that CAMTA3-mediated repression of SA pathway genes in nonstressed plants involves the action of an N-terminal repression module (NRM) that acts independently of calmodulin (CaM) binding to the IQ and CaM binding (CaMB) domains, a finding that is contrary to current thinking that CAMTA3 repression activity requires binding of CaM to the CaMB domain. Induction of SA pathway genes in response to low temperature did not occur in plants expressing only the CAMTA3-NRM region of the protein. Mutational analysis provided evidence that the repression activity of the NRM was suppressed by action of the IQ and CaMB domains responding to signals generated in response to low temperature. Plants expressing the CAMTA3-NRM region were also impaired in defense against the bacterial hemibiotrophic pathogen Pseudomonas syringae pv tomato DC3000. Our results indicate that the regulation of CAMTA3 repression activity by low temperature and pathogen infection involves related mechanisms, but with distinct differences.

Plant immunity in signal integration between biotic and abiotic stress responses

“…Salicylic acid immunity is repressed by CAMTA1–CAMTA3 at moderate temperatures, but derepressed under prolonged coldness or pathogen challenge (Du et al ., ; Kim et al ., ). An N‐terminal domain of CAMTA3 alone is sufficient to repress SA‐related genes, but its repression is relieved through intramolecular interaction with the C‐terminal CaM‐binding domain during cold‐induced immunity (Kim et al ., ). Massive immune activation in camta3‐ knockout plants (at 19–21°C) led to the notion that CAMTAs act as negative regulators of immunity (Du et al ., ; Nie et al ., ).…”

“…NPR1 independence of salt/drought tolerance, despite HSFA1 requirement therein, points to cold-specific engagement of the NPR1-HSFA1 module, which does not require SA, defense-related TGAs, NPR1 sumoylation, ABA or CBF1. Further studies will be required for the mechanisms underlying NPR1/HSFA1-mediated freezing tolerance and their possible involvement in cold-induced immunity (Kuwabara & Imai, 2009;Kim et al, 2017).…”

Pst DC3000 infection alleviates subsequent freezing and heat injury to host plants via a salicylic acid‐dependent pathway in Arabidopsis

“…Therefore, pathogen‐induced SA accumulation plays a key role in mediating the establishment of cold and heat tolerance induced by pathogen infection. In our previous work, SA was evidenced to be required for cold‐activated defense response (Kim et al, ; Wu et al, ). Taken together, SA is suggested to be a phytohormone underlying the interaction between defense response and abiotic stress such as cold and heat in plants.…”

“…In overwintering grasses, some pathogenesis‐related proteins, including endochitinases, β‐1,3‐glucanases, and thaumatin‐like proteins, were synthesized after exposed to low temperatures (Seo et al, ), and it was evidenced that cold acclimation induced the accumulation of SA, a classical disease resistance phytohormone, in Arabidopsis , wheat, and grape berry (Kim, Park, Gilmour, & Thomashow, ; Miura & Furumoto, ). Furthermore, Kim et al () detected increased disease resistance in cold acclimated Arabidopsis plants. Their work indicated that the activation of disease resistance is associated with the release of CAMTA transcription factors‐mediated repression of SA biosynthesis (Kim et al, ).…”

“…Furthermore, Kim et al () detected increased disease resistance in cold acclimated Arabidopsis plants. Their work indicated that the activation of disease resistance is associated with the release of CAMTA transcription factors‐mediated repression of SA biosynthesis (Kim et al, ). Recently Wu et al () reported that a cold stress as short as 8 hr is also able to activate the immunity to Pseudomonas syringae pv.…”