Phylogenetic Analyses Identify 10 Classes of the Protein Disulfide Isomerase Family in Plants, Including Single-Domain Protein Disulfide Isomerase-Related Proteins  

Abstract

(J.-M.S., R.J.)Protein disulfide isomerases (PDIs) are molecular chaperones that contain thioredoxin (TRX) domains and aid in the formation of proper disulfide bonds during protein folding. To identify plant PDI-like (PDIL) proteins, a genome-wide search of Arabidopsis (Arabidopsis thaliana) was carried out to produce a comprehensive list of 104 genes encoding proteins with TRX domains. Phylogenetic analysis was conducted for these sequences using Bayesian and maximum-likelihood methods. The resulting phylogenetic tree showed that evolutionary relationships of TRX domains alone were correlated with conserved enzymatic activities. From this tree, we identified a set of 22 PDIL proteins that constitute a well-supported clade containing orthologs of known PDIs. Using the Arabidopsis PDIL sequences in iterative BLAST searches of public and proprietary sequence databases, we further identified orthologous sets of 19 PDIL sequences in rice (Oryza sativa) and 22 PDIL sequences in maize (Zea mays), and resolved the PDIL phylogeny into 10 groups. Five groups (I-V) had two TRX domains and showed structural similarities to the PDIL proteins in other higher eukaryotes. The remaining five groups had a single TRX domain. Two of these (quiescin-sulfhydryl oxidase-like and adenosine 5#-phosphosulfate reductase-like) had putative nonisomerase enzymatic activities encoded by an additional domain. Two others (VI and VIII) resembled small single-domain PDIs from Giardia lamblia, a basal eukaryote, and from yeast. Mining of maize expressed sequence tag and RNA-profiling databases indicated that members of all of the single-domain PDIL groups were expressed throughout the plant. The group VI maize PDIL ZmPDIL5-1 accumulated during endoplasmic reticulum stress but was not found within the intracellular membrane fractions and may represent a new member of the molecular chaperone complement in the cell.Proper folding of nascent polypeptides into functional proteins relies on a number of molecular chaperones and protein-folding catalysts that act to shield nonnative structures from aggregation until they fold into a native, stable state. One group of these folding catalysts, the protein disulfide isomerases (PDIs), interacts with nascent polypeptides to catalyze the formation, isomerization, and reduction/oxidation of disulfide bonds (for review, see Freedman et al., 1994;Wilkinson and Gilbert, 2004). Multiple PDI-related genes have been identified in each eukaryotic genome surveyed by whole-genome sequencing. For most of the corresponding proteins, a demonstrated biochemical function is lacking; therefore, we refer to them as PDI-like (PDIL) proteins. PDIL proteins are members of a multigene family within the thioredoxin (TRX) superfamily, which includes, in addition, glutaredoxins, TRXs, ferredoxins, and peroxidoxins (Jacquot et al., 2002). All proteins in this ancient superfamily have at least one structural domain that functions through Cys residues in a CXXC tetrapeptide sequence (for review, see Ellgaard, 2004;Wilkinson and Gilbert...

A Relaxed Specificity in Interchain Disulfide Bond Formation Characterizes the Assembly of a Low-Molecular-Weight Glutenin Subunit in the Endoplasmic Reticulum

“…While the donor(s) of oxidizing equivalents for interchain disulfide bond formation remain to be identified, ER-located oxidoreductases (Houston et al, 2005) and plant homologs of the yeast and mammalian Ero proteins (Dixon et al, 2003) are possible players in the pathway leading to the covalent assembly of glutenin subunits.…”

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

“…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).…”

The physiological role of the unfolded protein response in plants

“…Houston et al (2005) showed that BiP and ZmPDIL5-1 proteins accumulate differentially in fl oury-2 maize following the onset of zein protein accumulation 15 days after pollination (DAP) and Shank et al (2001) reported an increase in CCT enzyme activity 16 days after pollination in this mutant. Unfortunately, wild-type maize shows no differential accumulation of BiP or ZmPDIL5-1 and CCT activity appears to drop off 10 to 16 days after pollination.…”