The mitogen-activated protein kinase 4-phosphorylated heat shock factor A4A regulates responses to combined salt and heat stresses

Abstract

Heat shock factors regulate responses to high temperature, salinity, water deprivation, or heavy metals. Their function in combinations of stresses is, however, not known. Arabidopsis HEAT SHOCK FACTOR A4A (HSFA4A) was previously reported to regulate responses to salt and oxidative stresses. Here we show, that the HSFA4A gene is induced by salt, elevated temperature, and a combination of these conditions. Fast translocation of HSFA4A tagged with yellow fluorescent protein from cytosol to nuclei takes place in salt-treated cells. HSFA4A can be phosphorylated not only by mitogen-activated protein (MAP) kinases MPK3 and MPK6 but also by MPK4, and Ser309 is the dominant MAP kinase phosphorylation site. In vivo data suggest that HSFA4A can be the substrate of other kinases as well. Changing Ser309 to Asp or Ala alters intramolecular multimerization. Chromatin immunoprecipitation assays confirmed binding of HSFA4A to promoters of target genes encoding the small heat shock protein HSP17.6A and transcription factors WRKY30 and ZAT12. HSFA4A overexpression enhanced tolerance to individually and simultaneously applied heat and salt stresses through reduction of oxidative damage. Our results suggest that this heat shock factor is a component of a complex stress regulatory pathway, connecting upstream signals mediated by MAP kinases MPK3/6 and MPK4 with transcription regulation of a set of stress-induced target genes.

Unusual DNA-binding properties of the Arabidopsis thaliana WRKY50 transcription factor at target gene promoters

“…In wheat, overexpression of WRKY30 leads to enhanced heat and drought stress tolerance (El-Esawi et al 2019 ). Enhanced heat stress tolerance is conceivable in the light of WRKY30 transcriptional induction by the heat shock factor A4A which itself is a target for mitogen-activated protein kinase 4 phosphorylation (Perez-Salamo et al 2014 ; Andrasi et al 2019 ). WRKY50 may be a second TF regulating WRKY30 gene expression during abiotic stress.…”

Protein kinases in plant responses to drought, salt, and cold stress

“…Oxidation stress is a common output feature of abiotic stress. The stress‐activated MAP kinases MPK3/6 and MPK4 also phosphorylate HEAT SHOCK FACTOR A4A (HSFA4A), which enhances the expression of its direct downstream target HSP17.6A under salt stress, thus increasing tolerance to salt, heat, and oxidative stress (Perez‐Salamo et al, 2014; Andrasi et al, 2019). SALT TOLERANCE RECEPTOR‐LIKE CYTOPLASMIC KINASE1 (STRK1) also phosphorylates and activates CATALASE C to regulate H 2 O 2 homeostasis and improve rice salt tolerance (Zhou et al, 2018).…”

“…In contrast to OST1, MPK3, MPK6, and BIN2 negatively regulate the stability and DNA binding activity of ICE1 in Arabidopsis (Zhao et al, 2017; Li et al, 2017a; Andrasi et al, 2019). MPK3 and MPK6 interact with and phosphorylate ICE1 under cold stress conditions, thus promoting ICE1 degradation and the attenuation of ICE1 binding to CBF promoters (Zhao et al, 2017; Li et al, 2017a).…”

Genomics-assisted prediction of salt and alkali tolerances and functional marker development in apple rootstocks

“…We detected a salt stress specific co-expression network including a series of heat shock protein genes. Plant heat stress TFs regulate responses not only to high temperatures but also to diverse environmental stresses [ 52 – 54 ]. HSFA4A of Arabidopsis promotes the expression of a wide range of defense genes and regulates tolerance to salinity [ 55 ].…”