First published online January 28, 2005; 10.1104/pp.104.056507
Plant Physiology 137:762-778 (2005)
© 2005 American Society of Plant Biologists
GENETICS, GENOMICS, AND MOLECULAR EVOLUTION
Phylogenetic Analyses Identify 10 Classes of the Protein Disulfide Isomerase Family in Plants, Including Single-Domain Protein Disulfide Isomerase-Related Proteins1,[w]
Norma L. Houston,
Chuanzhu Fan2,
(Jenny) Qiu-Yun Xiang,
Jan-Michael Schulze,
Rudolf Jung and
Rebecca S. Boston*
Department of Botany, North Carolina State University, Raleigh, North Carolina 27695–7612 (N.L.H., C.F., Q.-Y.X., R.S.B.); and Pioneer Hi-Bred International, Inc., a DuPont Company, Johnston, Iowa 50131 (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.
1 This work was supported by the U.S. Department of Energy (grant no. DE–FG02–00ER150065 to R.S.B.), the National Science Foundation (grant no. DEB–0129069 to Q.-Y.X.), the North Carolina Agricultural Research Service (R.S.B. and Q.-Y.X.), and a fellowship (to N.L.H.) in the North Carolina State University Functional Genomics graduate program from National Science Foundation Integrative Graduate Education and Research Traineeship (grant no. 9987555).
2 Present address: Department of Ecology and Evolution, University of Chicago, Chicago, IL 60637.
[w] The online version of this article contains Web-only data.
Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.104.056507.
* Corresponding author; e-mail boston{at}unity.ncsu.edu; fax 919–515–3436.
Received November 12, 2004;
returned for revision December 2, 2004;
accepted December 2, 2004.
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