Abstract
The protein disulphide isomerases (PDI) typically catalyse the formation and isomerization of disulphide bonds during the folding of nascent proteins. Some PDI isoforms may also have chaperone roles under house-keeping and/or stress conditions. Human PDIs and PDI-like (PDIL) proteins show a diverse array of catalytic and chaperone roles. However, understanding of the diversity and roles of plant PDILs is limited. This work aimed to identify the PDIL superfamilies in the two main cereals, rice and wheat, to identify candidates with potential roles in seed storage protein deposition and stress response processes. Searches of the rice genomic and wheat transcript assembly databases, with the Arabidopsis PDILs as queries, led to the identification of twenty two genomic loci in rice, encoding up to thirty two putative coding sequences, as well as twenty expressed sequence tags in wheat. The gene structures in rice ranged from 3 to 15 exons, the exon lengths ranging from 22 to 1,054 base pairs (bp) and the intron lengths from 74 to 1345 bp. The wheat TAs ranged from 584-2,444 bp and many sequences appeared to be orthologous to some of the rice loci. The putative proteins of both plants exhibited the characteristic thioredoxin active-site motif WCXXC, but significant diversity in the lengths of putative proteins and the composition or positions of functional domains therein. The PDILs thus fell into five major groups: PDIL1 (7 in rice; 4 in wheat); PDIL2 (9 rice; 4 wheat); PDIL5 (7 rice; 10 wheat); QSOXL (2 rice; 1 wheat); APRL (7 rice; 1 wheat). The analysis of the gene and putative protein sequences, the functional domains of the latter, and comparisons to literature have led to identification of a number of sequences with potential enzymatic and/or chaperone roles. Several of these appear to be candidates for key roles in seed storage protein folding, plant development and stress response processes in these important crops.
Similar content being viewed by others
Abbreviations
- APRL:
-
adenosine 5′-phosphosulfate reductase-like
- BiP:
-
binding protein
- CDS:
-
coding sequence
- ER:
-
endoplasmic reticulum
- ERAD:
-
ER-associated degradation
- EST:
-
expressed sequence tag
- FRX:
-
ferredoxin
- GRX:
-
glutaredoxins
- GSDS:
-
Gene Structure Display Server
- Hsp:
-
heat-shock protein
- PB:
-
protein body
- PDI:
-
protein disulphide isomerase
- PDIL:
-
protein disulphide isomerase-like proteins
- PPIases:
-
peptidyl prolyl cis-trans isomerase
- PRXs:
-
peroxiredoxin
- PSV:
-
protein storage vacuole
- QSOXL:
-
quiescin-sulfhydryl oxidase-like
- QTL:
-
quantitative trait locus
- TA:
-
transcript assembly
- TRX:
-
thioredoxin
- UPR:
-
unfolded protein response
References
Appenzeller-Herzog C. & Ellgaard L. 2008. The human PDI family: versatility packed into a single fold. Biochim. Biophys. Acta 1738: 535–548.
Bhave M., Wu H. & Kamboj A. 2011. Protein disulphide isomerases: diversity and roles in plants, pp. 1–40. In: Walters E. (ed.), Protein Folding, Nova Publishers, New York, USA.
Boden G., Duan X., Homko C., Molina E., Song W., Perez O., Cheung P. & Merali S. 2008. Increase in endoplasmic reticulum stress-related proteins and genes in adipose tissue of obese, insulin-resistant individuals. Diabetes 57: 2438–2444.
Bulleid N. & Freedman R. 1988. Defective co-translational formation of disulphide bonds in protein disulphide-isomerasedeficient microsomes. Nature 335: 649–651.
Cai H., Wang C. & Tsou C. 1994. Chaperone-like activity of protein disulfide isomerase in the refolding of a protein with no disulfide bonds. J. Biol. Chem. 269: 24550–24552.
Ciaffi M., Paolacci A., d’Aloisio E., Tanzarella O. & Porceddu E. 2006. Cloning and characterization of wheat PDI (protein disulfide isomerase) homoeologous genes and promoter sequences. Gene 366: 209–218.
Coughlan J., Hastings C. & Winfrey R. 1996. Molecular characterisation of plant endoplasmic reticulum identification of protein disulfide-isomerase as the major reticuloplasmin. Eur. J. Biochem. 235: 215–224.
Creighton T., Hillson D. & Freedman R. 1980. Catalysis by protein-disulphide isomerase of the unfolding and refolding of proteins with disulphide bonds. J. Mol. Biol. 142: 43–62.
d’Aloisio E., Paolacci A.R., Dhanapal A.P., Tanzarella O.A., Porceddu E. & Ciaffi M. 2010. The protein disulfide isomerase gene family in bread wheat (T. aestivum L.). BMC Plant Biol. 10: 101.
Darby N., Penkaa E. & Vincentelli R. 1998. The multi-domain structure of protein disulfide isomerase is essential for high catalytic efficiency. J. Mol. Biol. 276: 239–247.
DuPont F., Hurkman W., Vensel W., Chan R., Lopez R., Tanaka C. & Altenbach S. 2006. Differential accumulation of sulfurrich and sulfur-poor wheat flour proteins is affected by temperature and mineral nutrition during grain development. J. Cereal Sci. 44: 101–112.
DuPont F., William J., Charlene K. & Ronald C. 1998. BiP, HSP70, NDK and PDI in wheat endosperm. I. Accumulation of mRNA and protein during grain development. Physiol. Plantarum 103: 70–79.
Ellgaard L. & Ruddock L. 2005. The human protein disulphide isomerase family: substrate interactions and functional properties. EMBO Rep. 6: 28–32.
Ferrari D. & Soling H. 1999. The protein disulphide-isomerase family: unravelling a string of folds. Biochem. J. 339: 1–10.
Fonseca C., Soiffer R., Ho V., Vanneman M., Jinushi M., Ritz J., Neuberg D., Stone R., DeAngelo D. & Dranoff G. 2009. Protein disulfide isomerases are antibody targets during immunemediated tumor destruction. Blood 113: 1681–1688.
Freedman R., Klappa P. & Ruddock L. 2002. Protein disulfide isomerases exploit synergy between catalytic and specific binding domains. EMBO J. 3: 136–140.
Fu X., Wang P. & Zhu B. 2008. Protein disulfide isomerase is a multifunctional regulator of estrogenic status in target cells. J. Steroid Biochem. Mol. Biol. 112: 127–137.
Gao F., Zhou Y., Zhu W., Li X., Fan L. & Zhang G. 2009. Proteomic analysis of cold stress responsive proteins in Thellungiella rosette leaves. Planta 230: 1033–1046.
Gavel Y. & von Heijne G. 1990. A conserved cleavage-site motif in chloroplast transit peptides. FEBS Lett. 261: 455–458.
Grimwade B., Tatham A.S., Freedman R.B., Shewry P.R. & Napier J.A. 1996. Comparison of the expression patterns of genes coding for wheat gluten proteins and proteins involved in the secretory pathway in developing caryopses of wheat. Plant Mol. Biol. 30: 1067–1073.
Gruber C., Cemazar M., Mechler A., Martin L. & Craik D. 2009. Biochemical and biophysical characterization of a novel plant protein disulfide isomerase. Biopolymers 92: 35–43.
Grynberg A., Nicolas J. & Drapron R. 1977. Presence of a protein disulfide isomerase (EC 5.3.4.1) in wheat germ. C. R. Acad. Sci. Hebd. Seances Acad. Sci. D Sci. Nat. 284: 235–238.
Gutierrez-Marcos J., Roberts M., Campbell E. & Wray J. 1996. Three members of a novel small gene-family from Arabidopsis thaliana able to complement functionally an Escherichia coli mutant defective in PAPS reductase activity encode proteins with a thioredoxin-like domain and “APS reductase” activity. Proc. Natl. Acad. Sci. USA 93: 13377–13382.
Hayano T. & Kikuchi M. 1995 Cloning and sequencing of the cDNA encoding human P5. Gene 164: 377–378.
He Z., Li L. & Luan S. 2004. Immunophilins and parvulins. Superfamily of peptidyl prolyl isomerases in Arabidopsis. Plant Physiol. 134: 1248–1267.
Herman E. & Schmidt M. 2004. Endoplasmic reticulum to vacuole trafficking of endoplasmic reticulum bodies provides an alternate pathway for protein transfer to the vacuole. Plant Physiol. 136: 3440–3446.
Holmgren A. 1985. Thioredoxin. Annu. Rev. Biochem. 54: 237–271.
Horibe T., Kikuchi M. & Kawakami K. 2008. Interaction of human protein disulfide isomerase and human P5 with drug compounds: analysis using biosensor technology. Process Biochem. 43: 1330–1337.
Houston N., Fan C., Xiang Q. & Schulze J. 2005. Phylogenetic analyses identify 10 classes of the protein disulfide isomerase family in plants, including single-domain protein disulfide isomerase-related proteins. Plant Physiol. 137: 762–778.
Irsigler A., Costa M., Zhang P., Reis P., Dewey R., Boston R. & Fontes E. 2007. Expression profiling on soybean leaves reveals integration of ER- and osmotic stress pathways. BMC Genom. 8: 431.
Iwakasi K., Kamauchi S., Wadahama H., Ishimoto M., Kawada T. & Urade R. 2009. Molecular cloning and characterisation of soybean protein disulphide isomerase family proteins with nonclassic active centre motifs. FEBS J. 276: 4130–4141.
Jackson M., Nilsson T. & Peterson P. 1990. Identification of a consensus motif for retention of transmembrane proteins in the endoplasmic reticulum. EMBO J. 9: 3153–3162.
Jacquot J., Gelhaye E., Rouhier N., Corbier C., Didierjean C. & Aubry A. 2002. Thioredoxins and related proteins in photosynthetic organisms: molecular basis for thiol dependent regulation. Biochem. Pharmacol. 64: 1065–1069.
Jeong W., Lee D., Park S. & Rhee S. 2008. ERp16, an endoplasmic reticulum-resident thiol-disulfide oxidoreductase. J. Biol. Chem. 283: 25557–25566.
Johnson J.C., Appels R. & Bhave M. 2006. The PDI genes of wheat and their syntenic relationship to the esp2 locus of rice. Funct. Integr. Genom. 6: 104–121.
Johnson J.C. & Bhave M. 2004. Molecular characterisation of the protein disulphide isomerase genes of wheat. Plant Sci. 167: 397–410.
Johnson J.C., Clark B. & Bhave M. 2001. Isolation and characterisation of cDNAs encoding protein disulphide isomerases and cyclophilins in wheat. J. Cereal Sci. 34: 159–171.
Kamauchi S., Nakatani H., Nakano C. & Urade R. 2005. Gene expression in response to endoplasmic reticulum stress in Arabidopsis thaliana. FEBS J. 272: 3461–3476.
Kamauchi S., Wadahama H., Iwasaki K., Nakamoto Y., Nishizawa K., Ishimoto M., Kawada T. & Urade R. 2008. Molecular cloning and characterization of two soybean protein disulfide isomerases as molecular chaperones for seed storage proteins. FEBS J. 275: 2644–2658.
Kemmink J., Darby N., Dijkstra K., Nilges M. & Creighton T. 1997. The folding catalyst protein disulfide isomerase is constructed of active and inactive thioredoxin modules. Curr. Biol. 7: 239–245.
Kim Y., Kang K., Kim I., Lee Y., Oh C., Ryoo J., Jeong E. & Ahn K. 2009. Molecular mechanisms of MHC class I-antigen processing: redox considerations. Antioxid. Redox. Signal 11: 907–936.
Klappa P., Ruddock L.W., Darby N. & Freedman R.B. 1998. The b’ domain provides the principal peptide-binding site of protein disulfide isomerase but all domains contribute to binding of misfolded proteins. EMBO J. 17: 927–935.
Laudencia C., Stamova B., Lazo G., Cui X. & Anderson O. 2006. Analysis of the wheat endosperm transcriptome. J. Appl. Genet. 47: 287–302.
Lee J.E. & Hofhaus G. & Lisowsky T. 2000. Erv1p from Saccharomyces cerevisiae is a FAD-linked sulfhydryl oxidase. FEBS J. 477: 62–66.
Li C.P. & Larkins B.A. 1996. Expression of protein disulfide isomerase is elevated in the endosperm of the maize floury-2 mutant. Plant Mol. Biol. 30: 873–882.
Liu F., Rong Y., Zeng L., Zhang X. & Han Z. 2003. Isolation and characterization of a novel human thioredoxin-like gene hTLP19 encoding a secretory protein. Gene 315: 71–78.
Lu D. & Christopher D. 2006. Immunolocalization of a protein disulfide isomerase to Arabidopsis thaliana chloroplasts and its association with starch biogenesis. Int. J. Plant Sci. 167: 1–9.
Lu D. & Christopher D. 2008a. Endoplasmic reticulum stress activates the expression of a sub-group of protein disulfide isomerase genes and AtbZIP60 modulates the response in Arabidopsis thaliana. Mol. Genet. Genom. 280: 199–210.
Lu D. & Christopher D. 2008b. Light enhances the unfolded protein response as measured by BiP2 gene expression and the secretory GFP-2SC marker in Arabidopsis. Physiol. Plant. 134: 360–368.
Lu D. & Christopher D. 2008c. The effect of irradiance and redoxmodifying reagents on the 52 kDa protein disulfide isomerase of Arabidopsis chloroplasts. Biol. Plant. 52: 42–48.
Manukyan D., Bruehl M., Massberg S. & Engelmann B. 2008. Protein disulfide isomerase as a trigger for tissue factordependent fibrin generation. Thromb. Res. 122: 19–22.
Martinez I. & Chrispeels M. 2003. Genomic analysis of the unfolded protein response in Arabidopsis shows its connection to important cellular processes. Plant Cell 15: 561–576.
Mogelsvang S. & Simpson D.J. 1998. Changes in the levels of seven proteins involved in polypeptide folding and transport during endosperm development of two barley genotypes differing in storage protein localisation. Plant Mol. Biol. 36: 541–552.
Monnat J., Neuhaus E., Pop M., Ferrari D., Kramer B. & Soldati T. 2000. Identification of a novel saturable endoplasmic reticulum localisation mechanism mediated by the C-terminus of a Dictyostelium protein disulphide isomerase. Mol. Biol. Cell. 11: 3469–3484.
Nakamura T. & Lipton S. 2009. Cell death: protein misfolding and neurodegenerative diseases. Apoptosis 14: 455–468.
Nguyen Van D., Wallis K., Howard M., Haapalainen A., Salo K., Saaranen M., Sidhu A., Wierenga R., Freedman R., Ruddock L. & Williamson R. 2008. Alternative conformations of the x region of human protein disulphide-isomerase modulate exposure of the substrate binding b’ domain. J. Mol. Biol. 383: 1144–1155.
Noiva R. 1999. Protein disulfide isomerase: the multifunctional redox chaperone of the endoplasmic reticulum. Seminars Cell. Dev. Biol. 10: 481–493.
Ondzighi C., Christopher D., Cho E., Chang S. & Staehelin L. 2008. Arabidopsis protein disulfide isomerase-5 inhibits cysteine proteases during trafficking to vacuoles before programmed cell death of the endothelium in developing seeds. Plant Cell 20: 2205–2220.
Price E.R., Zydowsky L.D., Jin M.J., Baker C.H., McKeon F.D. & Walsh C.T. 1991. Human cyclophilin B: a second cyclophilin gene encodes a peptidyl-prolyl isomerase with a signal sequence. Proc. Natl. Acad. Sci. USA 88: 1903–1907.
Prior A., Uhrig J., Heins L., Wiesmann A., Lillig C., Stoltze C., Soll J. & Schwenn J. 1999. Structural and kinetic properties of adenylyl sulfate reductase from Catharanthus roseus cell cultures. Biochim. Biophys. Acta 1430: 25–38.
Ray S., Anderson J., Urmeev F. & Goodwin S. 2003. Rapid induction of a protein disulfide isomerase and defense-related genes in wheat in response to the hemibiotrophic fungal pathogen Mycosphaerella graminicola. Plant Mol. Biol. 53: 701–714.
Roden L.T., Miflin B.J. & Freedman R.B. 1982. Protein disulphide isomerase is located in the endoplasmic reticulum of developing wheat endosperm. FEBS Lett. 138: 121–124.
Serrato A., Guilleminot J., Meyer Y. & Vignols F. 2008. AtCXXS: atypical members of the Arabidopsis thaliana thioredoxin h family with a remarkably high disulfide isomerase activity. Physiol. Plant. 133: 611–622.
Shewry P.R. & Halford N.G. 2002. Cereal seed storage proteins: structures, properties and role in grain utilization. J. Exp. Bot. 53: 947–958.
Shimoni Y., Segal C., Zhu X.Z. & Calili C. 1995a. Nucleotide sequence of a wheat cDNA encoding protein disulfide isomerase. Plant Physiol. 107: 281.
Shimoni Y., Zhu X., Levanony H., Segal G. & Galili G. 1995b. Purification, characterization, and intracellular localization of glycosylated protein disulfide isomerase from wheat grains. Plant Physiol. 108: 327–335.
Shorrosh B. & Dixon R. 1992. Molecular characterisation and expression of an alfalfa protein with sequence similarity to mammalian ERp72, a glucose-regulated endoplasmic reticulum protein containing active site sequences of protein disulphide isomerase. Plant J. 2: 51–58.
Sliskovic I., Raturi A. & Mutus B. 2005. Characterization of the S-denitrosation activity of protein disulfide isomerase. J. Biol. Chem. 280: 8733–8741.
Takemoto Y., Coughlan S.J., Okita T.W., Satoh H., Ogawa M. & Kumamaru T. 2002. The rice mutant esp2 greatly accumulates the glutelin precursor and deletes the protein disulfide isomerase. Plant Physiol. 128: 1212–1222.
Thorpe C., Hoober K., Raje S., Glynn N., Burnside J., Turi G. & Coppock D. 2002. Sulfhydryl oxidases: emerging catalysts of protein disulfide bond formation in eukaryotes. Arch. Biochem. Biophys. 405: 1–12.
Tosi P., Parker M., Gritsch C., Carzaniga R., Martin B. & Shewry S. 2009. Trafficking of storage proteins in developing grain of wheat. J. Exp. Bot. 60: 979–991.
Urade R. 2007. Cellular response to unfolded proteins in the endoplasmic reticulum of plants. FEBS J. 274: 1152–1171.
Ushioda R., Hoseki J., Araki K., Jansen G., Thomas D. & Nagata K. 2008. ERdj5 is required as a disulfide reductase for degradation of misfolded proteins in the ER. Science 321: 569–572.
Vitale A. & Ceriotti A. 2004. Protein quality control mechanisms and protein storage in the endoplasmic reticulum. A conflict of interests? Plant Physiol. 136: 3420–3426.
Wadahama H., Kamauchi S., Ishimoto M., Kawada T. & Urade R. 2007. Protein disulfide isomerase family proteins involved in soybean protein biogenesis. FEBS J. 274: 687–703.
Wadahama H., Kamauchi S., Nakamoto Y., Nishizawa K., Ishimoto M., Kawada T. & Urade R. 2008. A novel plant protein disulfide isomerase family homologous to animal P5 — molecular cloning and characterization as a functional protein for folding of soybean seed-storage proteins. FEBS J. 275: 399–410.
Wang H., Boavida L., Ron M. & McCormick S. 2008. Truncation of a protein disulfide isomerase, PDIL2-1, delays embryo sac maturation and disrupts pollen tube guidance in Arabidopsis thaliana. Plant Cell 20: 3300–3311.
Wells W., Xu D., Yang Y. & Rocque P. 1990. Mammalian thioltransferase (glutaredoxin) and protein disulfide isomerase have dehydroascorbate reductase activity. J. Biol. Chem. 265: 15361–15364.
Wilkinson B. & Gilbert H. 2004. Protein disulfide isomerase. Biochim. Biophys. Acta 1699: 35–44.
Woycechowsky K, Raines R. 2000. Native disulfide bond formation in proteins. Curr. Opin. Chem. Biol. 4: 533–539.
Xu Z., Ueda K., Masuda K., Ono M. & Inoue M. 2002. Molecular characterisation of a novel protein disulphide isomerase in carrot. Gene 284: 225–231.
Yang K., Xia C., Liu X., Dou X., Wang W., Chen L., Zhang X., Xie L., He L., Ma X. & Ye D. 2009. A mutation in the Thermosensitive Male Sterile 1, encoding a heat shock protein with DnaJ and PDI domains, leads to thermosensitive gametophyte male sterility in Arabidopsis. Plant J. 57: 870–882.
Author information
Authors and Affiliations
Corresponding author
Additional information
Electronic supplementary material. The online version of this article (DOI: 10.2478/s11756-011-0164-5) contains supplementary material, which is available to authorized users.
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Wu, H., Dorse, S. & Bhave, M. In silico identification and analysis of the protein disulphide isomerases in wheat and rice. Biologia 67, 48–60 (2012). https://doi.org/10.2478/s11756-011-0164-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2478/s11756-011-0164-5