Signaling from the Endoplasmic Reticulum Activates Brassinosteroid Signaling and Promotes Acclimation to Stress in Arabidopsis

Abstract

The ability to acclimate to stresses enables plants to grow and develop under adverse environmental conditions. Regulated intramembrane proteolysis (RIP) triggered by endoplasmic reticulum (ER) stress mediates some forms of stress signaling. Brassinosteroids (BRs) have been implicated in plant adaptation to stress, but no mechanisms for activation have been discovered. Here, we reveal a connection between ER stress signaling and BR-mediated growth and stress acclimation. Arabidopsis transcription factors bZIP17 and bZIP28 were translocated from the ER through the Golgi, where they were proteolytically cleaved by site 2 protease and released to translocate into the nucleus. Stresses, including heat and inhibition of protein glycosylation, increased translocation of these two bZIPs to the nucleus. These nuclear-localized bZIPs not only activated ER chaperone genes but also activated BR signaling, which was required for stress acclimation and growth. Thus, these bZIPs link ER stress and BR signaling, which may be a mechanism by which plant growth and stress responses can be integrated.

Heat induces the splicing by IRE1 of a mRNA encoding a transcription factor involved in the unfolded protein response in Arabidopsis

“…Since the discovery of bZIP60, two other stress-induced, membrane-associated TFs have been described in Arabidopsis, AtbZIP17, which responds to UPR agents, heat, and salt stress (20,22) and AtbZIP28 that is activated by UPR agents and heat (21,22,31). Both of these factors are activated conventionally in a manner similar to the activation of ATF6.…”

“…In response to stress, bZIP60 appears in an active, truncated form seemingly to have undergone proteolytic processing similar to AtbZIP17 and AtbZIP28 (20)(21)(22). However, the mechanism for the presumed proteolysis event is not understood, because the C-terminal tail of bZIP60 does not have a canonical S1P cleavage site and its activation does not require S1P or S2P (23).…”

“…ER stress activates bZIP transcription factors, AtbZIP17 and -28, members of a small family of membrane-associated bZIP factors in Arabidopsis (20,21). AtbZIP17 and -28 are activated by mechanisms similar to the activation of ATF6 in mammalian cells (20)(21)(22). Mammalian ATF6 is activated by liberation from the ER and migration to the Golgi apparatus where its C-terminal, lumen-facing domain is cleaved by S1P and S2P proteases, releasing its N-terminal, cytosol-facing component, which enters the nucleus and up-regulates target genes.…”

Arabidopsis thaliana intramembrane proteases

“…The precise chloroplast localization of EGY1 and S2P2 still remains unknown (Zybailov et al 2008;Chen et al 2005). The protein encoded by the AT4G20310 gene has been demonstrated to be directed to the Golgi membrane (Che et al 2010). The localization of EGY3 proteins remains unconfirmed, but AramLocCon predicts localization of this protein in the chloroplast (Schwacke et al 2007).…”

Membrane-tethered transcription factors provide a connection between stress response and developmental pathways

“…Specifically, it was demonstrated that activated forms of AtbZIP17 and AtbZIP28 can also regulate genes involved in the brassinosteroid signaling pathway, thereby identifying a point of integration between ER stress response and growth and development pathways. 14 Previously characterized MTTFs that belong to the NAC family have also been shown to be involved in stress response but also regulate developmental processes in Arabidopsis. NTM1 was one of the first MTTFs to be characterized in Arabidopsis and was shown to mainly regulate genes involved in cell division through interactions with cytokinins.…”