Mitogen-Activated Protein Kinase 4 Is a Salicylic Acid-Independent Regulator of Growth But Not of Photosynthesis in Arabidopsis

Abstract

Mitogen-activated protein kinase (MAPK) pathways regulate signal transduction from different cellular compartments and from the extracellular environment to the nucleus in all eukaryotes. One of the best-characterized MAPKs in Arabidopsis thaliana is MPK4, which was shown to be a negative regulator of systemic-acquired resistance. The mpk4 mutant accumulates salicylic acid (SA), possesses constitutive expression of pathogenesis-related (PR) genes, and has an extremely dwarf phenotype. We show that suppression of SA and phylloquinone synthesis in chloroplasts by knocking down the ICS1 gene (by crossing it with the ics1 mutant) in the mpk4 mutant background did not revert mpk4-impaired growth. However, it did cause changes in the photosynthetic apparatus and severely impaired the quantum yield of photosystem II. Transmission microscopy analysis revealed that the chloroplasts' structure was strongly altered in the mpk4 and mpk4/ics1 double mutant. Analysis of reactive oxygen species (ROS)-scavenging enzymes expression showed that suppression of SA and phylloquinone synthesis in the chloroplasts of the mpk4 mutant caused imbalances in ROS homeostasis which were more pronounced in mpk4/ics1 than in mpk4. Taken together, the presented results strongly suggest that MPK4 is an ROS/hormonal rheostat hub that negatively, in an SA-dependent manner, regulates immune defenses, but at the same time positively regulates photosynthesis, ROS metabolism, and growth. Therefore, we concluded that MPK4 is a complex regulator of chloroplastic retrograde signaling for photosynthesis, growth, and immune defenses in Arabidopsis.

LSD1‐, EDS1‐ and PAD4‐dependent conditional correlation among salicylic acid, hydrogen peroxide, water use efficiency and seed yield in Arabidopsis thaliana

“…In addition, a remarkably low number of genes deregulated in field‐grown lsd1 , in comparison to laboratory‐grown lsd1 (Wituszyńska et al ), might imply that the LSD1 suppressive role on CD is supported by other yet undetermined regulators. Potential candidates are CYSTEINE‐RICH RECEPTOR‐LIKE KINASE (Burdiak et al ), MITOGEN ACTIVATED PROTEIN KINASE 4 (Gawroński et al , Witoń et al ) and LSD ONE LIKE 1 (Epple et al ) proteins.…”

ROS, Calcium, and Electric Signals: Key Mediators of Rapid Systemic Signaling in Plants

“…Thus, genes such as LESION SIMULATING DISEASE1, ENHANCED DISEASE SUSCEPTIBILITY1, PHYTOALEXIN DEFICIENT4, ETHYLENE INSENSITIVE2, and MITOGEN-ACTIVATED PROTEIN KINASE 4 were shown to play important roles in the simultaneous regulation of SAA via ROSand salicylic acid-dependent pathways Szechy nska-Hebda et al, 2010;Wituszy nska et al, 2013;Gawro nski et al, 2014;for review, see Karpi nski et al, 2013;Mignolet-Spruyt et al, 2016). In addition, PHOTOSYSTEM II SUBUNIT S-dependent local and systemic wave-like regulation of nonphotochemical quenching (NPQ) and chlorophyll fluorescence decay time, important dissipation and quenching mechanisms of light absorbed in excess, were also proposed to be dependent on ROS and salicylic acid signaling during SAA (Szechy nska- Hebda et al, 2010;Gawro nski et al, 2013Gawro nski et al, , 2014Ciszak et al, 2015;Fig. 2).…”

A review of redox signaling and the control of MAP kinase pathway in plants

“…Furthermore, in atmpk4 mutants or atmpk4 / ics1 double mutants, it was shown that most of the analyzed genes encoding ROS scavenging enzymes, e.g. GR2 (encoding glutathione reductase 2), FSDs (encoding Fe-SODs), and APXs , are down-regulated, whereas CSD2 can be up-regulated [69]. The enzyme analysis demonstrated Cu/Zn-SOD and APX activities were increased whereas Fe-SOD activity was decreased in atmpk4 mutants or atmpk4 / ics1 double mutants [69] (Fig.…”