The Unfolded Protein Response Supports Plant Development and Defense as well as Responses to Abiotic Stress

Abstract

The unfolded protein response (UPR) is a stress response conserved in eukaryotic organisms and activated by the accumulation of misfolded proteins in the endoplasmic reticulum (ER). Adverse environmental conditions disrupt protein folding in the ER and trigger the UPR. Recently, it was found that the UPR can be elicited in the course of plant development and defense. During vegetative plant development, the UPR is involved in normal root growth and development, the effect of which can be largely attributed to the influence of the UPR on plant hormone biology. The UPR also functions in plant reproductive development by protecting male gametophyte development from heat stress. In terms of defense, the UPR has been implicated in virus and microbial defense. Viral defense represents a double edge sword in that various virus infections activate the UPR, however, in a number of cases, the UPR actually supports viral infections. The UPR also plays a role in plant immunity to bacterial infections, again through the action of plant hormones in regulating basal immunity responses.

Keywords: ER (endoplasmic reticulum) stress; IRE1; auxin; bZIP28; brassinosteroid; plant virus; protein folding; regulated-IRE1 dependent RNA decay (RIDD).

FIGURE 1

Two branches of UPR signaling pathway in plants. One branch involves the dual protein kinase and ribonuclease, IRE1, which splices bZIP60 mRNA when activated. The other branch is mediated by two ER membrane-anchored transcription factors, bZIP17 and bZIP28. Different stresses interfere with protein folding in the ER, leading to an accumulation of unfolded or misfolded proteins in the ER, activating the UPR. The splicing of bZIP60(u) mRNA introduces a frameshift, such that the resultant spliced form bZIP60(s) mRNA is translated into a transcription factor targeted to the nucleus. ER stress also provokes the mobilization of the membrane-anchored transcription factors from ER to Golgi, where they are processed to bZIP17(p) and bZIP28(p) by Golgi resident S1P and S2P proteases, releasing their cytosolic transcription factor domains. The factors from both branches are targeted to the nucleus, and either homodimerize or heterodimerize to bind to the promoters and regulate the expression of stress response genes. Based on Howell (2013b).

FIGURE 2

Structural map of IRE1b and diverse roles for the UPR. (A) IRE1b has a single transmembrane domain (TMD) and localizes in the ER membrane with its N-terminus in the ER lumen and its C-terminus facing the cytosol. Numbers below the diagram represent residues, which when mutated specifically block the following activities: D608N, K610N block the nucleotide binding activity, D628A knocks out the protein kinase catalytic activity and D820A interferes with the RNase activity (Deng et al., 2013). (B) The UPR plays roles beyond stress to include vegetative and reproductive development, microbial immunity, and virus infection.