SALT OVERLY SENSITIVE2 stabilizes phytochrome-interacting factors PIF4 and PIF5 to promoteArabidopsisshade avoidance

Abstract

Sun-loving plants trigger the shade avoidance syndrome (SAS) to compete against their neighbors for sunlight. Phytochromes are plant red (R) and far-red (FR) light photoreceptors that play a major role in perceiving the shading signals and triggering SAS. Shade induces a reduction in the level of active phytochrome B (phyB), thus increasing the abundance of PHYTOCHROME-INTERACTING FACTORS (PIFs), a group of growth-promoting transcription factors. However, whether other factors are involved in modulating PIF activity in the shade remains largely obscure. Here, we show that SALT OVERLY SENSITIVE2 (SOS2), a protein kinase essential for salt tolerance, positively regulates SAS in Arabidopsis thaliana. SOS2 directly phosphorylates PIF4 and PIF5 at a serine residue close to their conserved motif for binding to active phyB. This phosphorylation thus decreases their interaction with phyB and post-translationally promotes PIF4 and PIF5 protein accumulation. Notably, the role of SOS2 in regulating PIF4 and PIF5 protein abundance and SAS is more prominent under salt stress. Moreover, phyA and phyB physically interact with SOS2 and promote SOS2 kinase activity in the light. Collectively, our study uncovers an unexpected role of salt-activated SOS2 in promoting SAS by modulating the phyB-PIF module, providing insight into the coordinated response of plants to salt stress and shade.

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

“…Third, accumulating evidence shows that certain key components may be involved in plant responses to multiple stresses. For example, SOS2 was recently shown to promote both plant tolerance to salt and plant responses to shade (Han et al., 2023). Extensive identification of these key components and elucidation of their action mechanisms in mediating plant responses to multiple stresses will provide candidate genes for the design and breeding of new crop varieties with enhanced tolerance to multiple environmental stresses.…”

“…Interestingly, SALT OVERLY SENSITIVE2 (SOS2), a key protein kinase for promoting salt tolerance, was recently shown to positively regulate SAS (Han et al., 2023). Under shade conditions, SOS2 post‐translationally promotes PIF4/PIF5 protein accumulation by directly phosphorylating a conserved serine residue of PIF4/PIF5 near their APB motifs, thereby decreasing their interactions with phyB (Han et al., 2023) (Figure 3).…”

“…Interestingly, SALT OVERLY SENSITIVE2 (SOS2), a key protein kinase for promoting salt tolerance, was recently shown to positively regulate SAS (Han et al., 2023). Under shade conditions, SOS2 post‐translationally promotes PIF4/PIF5 protein accumulation by directly phosphorylating a conserved serine residue of PIF4/PIF5 near their APB motifs, thereby decreasing their interactions with phyB (Han et al., 2023) (Figure 3). Moreover, salt stress enhances the role of SOS2 in promoting PIF4/PIF5 protein abundance and shade avoidance, but inhibits overall hypocotyl elongation under shade conditions (Han et al., 2023; Hayes et al., 2019), suggesting that salt‐activated SOS2 may prevent exaggerated salt inhibition of shade‐induced hypocotyl elongation.…”

“…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.…”

Designing salt stress‐resilient crops: Current progress and future challenges

“…Light is an important environmental cue that plays a fundamental role in regulating plant growth, development, and salt stress responses (Han et al, 2023;Yang et al, 2023a). Plants sense the low red (R) to far-red (FR) (R:FR) ratio in the shade and rapidly trigger elements of shade avoidance syndrome (SAS), including elongated hypocotyls and petioles, and early flowering (Han et al, 2023). Salt stress strongly inhibits shade-induced hypocotyl elongation through ABA-dependent signaling (Hayes et al, 2019).…”