Phytochromes enhance SOS2-mediated PIF1 and PIF3 phosphorylation and degradation to promote Arabidopsis salt tolerance

Abstract

Soil salinity is one of the most detrimental abiotic stresses affecting plant survival, and light is a core environmental signal regulating plant growth and responses to abiotic stress. However, how light modulates the plant’s response to salt stress remains largely obscure. Here, we show that Arabidopsis (Arabidopsis thaliana) seedlings are more tolerant to salt stress in the light than in the dark, and that the photoreceptors phytochrome A (phyA) and phyB are involved in this tolerance mechanism. We further show that phyA and phyB physically interact with the salt tolerance regulator SALT OVERLY SENSITIVE2 (SOS2) in the cytosol and nucleus, and enhance salt-activated SOS2 kinase activity in the light. Moreover, SOS2 directly interacts with and phosphorylates PHYTOCHROME-INTERACTING FACTORS PIF1 and PIF3 in the nucleus. Accordingly, PIFs act as negative regulators of plant salt tolerance, and SOS2 phosphorylation of PIF1 and PIF3 decreases their stability and relieves their repressive effect on plant salt tolerance in both light and dark conditions. Together, our study demonstrates that photo-activated phyA and phyB promote plant salt tolerance by increasing SOS2-mediated phosphorylation and degradation of PIF1 and PIF3, thus broadening our understanding of how plants adapt to salt stress according to their dynamic light environment.

Molecular mechanisms underlying coordinated responses of plants to shade and environmental stresses

“…It was previously shown that heterologous overexpression of a hyperactive mutant of oat phyA (serine 599 mutated to alanine) in turfgrass enhances its tolerance to high salinity and heavy metal toxicity by increasing chlorophyll content, total biomass, and photosynthetic efficiency (Gururani et al., 2016). Consistent with these observations, a recent study reported that Arabidopsis phyA‐211 , phyB‐9 , and phyA‐211 phyB‐9 mutants all displayed salt‐sensitive phenotypes in the light, indicating that both phyA and phyB positively regulate salt tolerance (Ma et al., 2023) (Figure 3). A previous study showed that Arabidopsis seedlings overexpressing PIF4 exhibited a salt‐sensitive phenotype, indicating that PIF4 acts as a negative regulator of salt tolerance (Sakuraba et al., 2017).…”

“…A previous study showed that Arabidopsis seedlings overexpressing PIF4 exhibited a salt‐sensitive phenotype, indicating that PIF4 acts as a negative regulator of salt tolerance (Sakuraba et al., 2017). Consistently, pifq mutant seedlings displayed increased resistance to NaCl treatment in the dark, indicating that PIFs negatively regulate salt stress tolerance (Ma et al., 2023) (Figure 3). Salt‐activated SOS2 directly phosphorylates PIF1/PIF3 to decrease their stability and relieve their repressive effect on plant salt tolerance (Ma et al., 2023).…”

“…Consistently, pifq mutant seedlings displayed increased resistance to NaCl treatment in the dark, indicating that PIFs negatively regulate salt stress tolerance (Ma et al., 2023) (Figure 3). Salt‐activated SOS2 directly phosphorylates PIF1/PIF3 to decrease their stability and relieve their repressive effect on plant salt tolerance (Ma et al., 2023). It should be noted that SOS2‐mediated phosphorylation leads to increased accumulation of PIF4/PIF5 in the shade, but decreased accumulation of PIF1/PIF3 in response to light under salt stress.…”

“…It should be noted that SOS2‐mediated phosphorylation leads to increased accumulation of PIF4/PIF5 in the shade, but decreased accumulation of PIF1/PIF3 in response to light under salt stress. Moreover, photoactivated phyA and phyB interact with SOS2 and positively regulate salt‐induced SOS2 kinase activity (Han et al., 2023; Ma et al., 2023). However, as mentioned above, phyB is deactivated under shade conditions whereas phyA is activated under deep shade.…”

Phytochrome B phosphorylation expanded: site‐specific kinases are identified

“…This idea is supported by the observations on PAPP2C and PAPP5 phosphatases that are active in the nucleus (Ryu et al ., 2005; Phee et al ., 2008; Fig. 2) and that phyB interacts with a kinase in the nucleus that phosphorylates PIFs resulting in modified light signaling (Ma et al ., 2023). Thus on the one hand, nuclear phyB phosphorylation is an important subject to study and, specifically, phosphorylation of nuclear phyB is expected to be detected.…”