Endoplasmic reticulum stress activates the expression of a sub-group of protein disulfide isomerase genes and AtbZIP60 modulates the response in Arabidopsis thaliana

Abstract

Proteins entering the secretory pathway of eukaryotic cells are folded into their native structures in the endoplasmic reticulum (ER). Disruption of protein folding causes ER stress and activates signaling cascades, designated the unfolded protein response (UPR), that restore folding capacity. In mammals and yeast, the protein disulfide isomerases (PDIs) are key protein folding catalysts activated during UPR. However, little is known about the response of PDI genes to UPR in plants. In Arabidopsis thaliana, we identified 12 PDI genes that differed in polypeptide length, presence of signal peptide and ER retention signal, and the number and positions of thioredoxin and transmembrane domains. AtPDI gene expression was investigated in different tissues, in response to chemically induced UPR, and in null mutants of UPR signaling mediators (AtIRE1-2 and AtbZIP60). The expression of six AtPDI genes was significantly up-regulated by UPR and sharply attenuated by the transcription inhibitor, actinomycin D, indicating UPR induced AtPDI gene transcription. AtPDI and BIP2 (Binding protein) gene expression was not affected in the Atire1-2 mutant exposed to UPR, however, the expression of four AtPDI genes was decreased in the Atbzip60 mutant. We proposed that additional UPR signaling factors complement AtbZIP60 in the activation of AtPDI gene expression during ER stress in plants.

Protein Disulfide Isomerase-2 of Arabidopsis Mediates Protein Folding and Localizes to Both the Secretory Pathway and Nucleus, Where It Interacts with Maternal Effect Embryo Arrest Factor

“…1A). PDI2 resides in a distinct phylogenetic subgroup of six members of the PDI family characterized by an a-b-b′-a′ domain configuration (Lu and Christopher, 2008), similar to that of classical PDIs from Homo sapiens (HsPDI; 32% sequence identity to PDI2) and Saccharomyces cerevisiae (ScPDI1; 24% identity) (Supplementary Fig. 1).…”

“…Protein disulfide isomerase-2, PDI2 (EC 5.3.4.1), is the largest of the 12 PDIs encoded in Arabidopsis genome (Lu and Christopher, 2008). The PDI2 gene (accession No.…”

“…PDI utilizes the thioredoxin domains for catalysis, which places them in the superfamily of thioredoxin-like proteins (Motohashi et al, 2001). However, PDIs are several-fold larger than thioredoxins (Ferrari and Soling, 1999;Lu and Christopher, 2008) and have other functions in addition to protein folding.…”

“…In the Arabidopsis thaliana genome, there are either 22 (Houston et al, 2005) or 12 PDI-like genes (Lu and Christopher, 2008), depending on whether the more distantly related adeno-sine 5′-phosphosulfate-like and quiescin-sulfhydryl oxidase gene families are included. In plants, PDIs have been implicated in several biological processes, including the unfolded protein response (Lu and Christopher, 2008) and folding storage proteins during the biogenesis of protein bodies from the ER in the seed endosperm (Li and Larkins, 1996;Okita and Rogers, 1996;Shimoni et al, 1995).…”

“…In plants, PDIs have been implicated in several biological processes, including the unfolded protein response (Lu and Christopher, 2008) and folding storage proteins during the biogenesis of protein bodies from the ER in the seed endosperm (Li and Larkins, 1996;Okita and Rogers, 1996;Shimoni et al, 1995). In rice seeds, a PDI prevents proglutelin and prolamin from aggregating by chaperoning their segregation in the ER lumen (Takemoto et al, 2002).…”