Distinct Roles of Protein Disulfide Isomerase and P5 Sulfhydryl Oxidoreductases in Multiple Pathways for Oxidation of Structurally Diverse Storage Proteins in Rice[W][OA]

This work examines the localization and functions of two protein disulfide isomerase family oxidoreductases in formation of protein storage bodies in rice endosperm, finding that the two have nonoverlapping localizations, activities, and biological functions. In the rice (Oryza sativa) endosperm, storage proteins are synthesized on the rough endoplasmic reticulum (ER), in which prolamins are sorted to protein bodies (PBs) called type-I PB (PB-I). Protein disulfide isomerase (PDI) family oxidoreductase PDIL2;3, an ortholog of human P5, contains a conserved structural disulfide in the redox-inactive thioredoxin-like (TRX) domain and was efficiently targeted to the surface of PB-I in a redox active site–dependent manner, whereas PDIL1;1, an ortholog of human PDI, was localized in the ER lumen. Complementation analyses using PDIL1;1 knockout esp2 mutant indicated that the a and a′ TRX domains of PDIL1;1 exhibited similar redox activities and that PDIL2;3 was unable to perform the PDIL1;1 functions. PDIL2;3 knockdown inhibited the accumulation of Cys-rich 10-kD prolamin (crP10) in the core of PB-I. Conversely, crP10 knockdown dispersed PDIL2;3 into the ER lumen. Glutathione S-transferase-PDIL2;3 formed a stable tetramer when it was expressed in Escherichia coli, and the recombinant PDIL2;3 tetramer facilitated α-globulin(C79F) mutant protein to form nonnative intermolecular disulfide bonds in vitro. These results indicate that PDIL2;3 and PDIL1;1 are not functionally redundant in sulfhydryl oxidations of structurally diverse storage proteins and play distinct roles in PB development. We discuss PDIL2;3-dependent and PDIL2;3-independent oxidation pathways that sustain disulfide bonds of crP10 in PB-I.

• Publication year

  2011

• Venue

  The Plant Cell

• Publication date

  2011-01-01

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1105/tpc.110.079509PMID 21278127PMCID PMC3051231
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• ERO1-β, a pancreas-specific disulfide oxidase, promotes insulin biogenesis and glucose homeostasis

  2010cited by this paper
• New insights into oxidative folding

  2010influential reference
• Oxidative Activity of Yeast Ero1p on Protein Disulfide Isomerase and Related Oxidoreductases of the Endoplasmic Reticulum*

  2010cited by this paper
• RiceXPro: a platform for monitoring gene expression in japonica rice grown under natural field conditions

  2010cited by this paper
• ERO1-β, a pancreas-specific disulfide oxidase, promotes insulin biogenesis and glucose homeostasis

  2010cited by this paper
• Vacuolar processing enzyme plays an essential role in the crystalline structure of glutelin in rice seed.

  2010cited by this paper
• Protein disulfide isomerase like 1-1 participates in the maturation of proglutelin within the endoplasmic reticulum in rice endosperm.

  2010cited by this paper
• Mapping of the ligand-binding site on the b' domain of human PDI: interaction with peptide ligands and the x-linker region.

  2009cited by this paper
• The vacuolar processing enzyme OsVPE1 is required for efficient glutelin processing in rice.

  2009cited by this paper
• Protein Disulfide Isomerase: A Critical Evaluation of Its Function in Disulfide Bond Formation

  2009cited by this paper
• Protein disulphide isomerase family members show distinct substrate specificity: P5 is targeted to BiP client proteins

  2009cited by this paper
• ER membrane-localized oxidoreductase Ero1 is required for disulfide bond formation in the rice endosperm

  2009influential reference
• Reconstitution of human Ero1-Lalpha/protein-disulfide isomerase oxidative folding pathway in vitro. Position-dependent differences in role between the a and a' domains of protein-disulfide isomerase.

  2009influential reference
• Arabidopsis Protein Disulfide Isomerase-5 Inhibits Cysteine Proteases during Trafficking to Vacuoles before Programmed Cell Death of the Endothelium in Developing Seeds[W]

  2008cited by this paper
• Yeast Mpd1p reveals the structural diversity of the protein disulfide isomerase family.

  2008cited by this paper
• Endoplasmic reticulum stress activates the expression of a sub-group of protein disulfide isomerase genes and AtbZIP60 modulates the response in Arabidopsis thaliana

  2008cited by this paper
• The Erv family of sulfhydryl oxidases.

  2008influential reference
• Truncation of a Protein Disulfide Isomerase, PDIL2-1, Delays Embryo Sac Maturation and Disrupts Pollen Tube Guidance in Arabidopsis thaliana[W]

  2008cited by this paper
• Oxidative protein folding in vitro: a study of the cooperation between quiescin-sulfhydryl oxidase and protein disulfide isomerase.

  2008cited by this paper
• The human PDI family: versatility packed into a single fold.

  2008cited by this paper
• 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

  2008cited by this paper
• Protein Body Biogenesis in Cereal Endosperms

  2007cited by this paper
• Disulphide-isomerase-enabled shedding of tumour-associated NKG2D ligands

  2007cited by this paper
• S-Nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration

  2006cited by this paper
• The crystal structure of yeast protein disulfide isomerase suggests cooperativity between its active sites.

  2006influential reference
• Phylogenetic Analyses Identify 10 Classes of the Protein Disulfide Isomerase Family in Plants, Including Single-Domain Protein Disulfide Isomerase-Related Proteins1[w]

  2005cited by this paper
• The Critical Role of Disulfide Bond Formation in Protein Sorting in the Endosperm of Rice

  2005influential reference
• A Structural Disulfide of Yeast Protein-disulfide Isomerase Destabilizes the Active Site Disulfide of the N-terminal Thioredoxin Domain*

  2005cited by this paper
• Glutathione Directly Reduces an Oxidoreductase in the Endoplasmic Reticulum of Mammalian Cells*

  2004influential reference
• The Rice Mutant esp 2 Greatly Accumulates the Glutelin Precursor and Deletes the Protein Disulfide Isomerase 1

  2002influential reference
• A subset of chaperones and folding enzymes form multiprotein complexes in endoplasmic reticulum to bind nascent proteins.

  2002cited by this paper
• The Rice Mutant esp2 Greatly Accumulates the Glutelin Precursor and Deletes the Protein Disulfide Isomerase1

  2002influential reference
• Functional analysis of human P5, a protein disulfide isomerase homologue.

  2002influential reference
• Functional Differences in Yeast Protein Disulfide Isomerases

  2001cited by this paper
• The protein disulphide-isomerase family: unravelling a string of folds.

  1999cited by this paper
• The multi-domain structure of protein disulfide isomerase is essential for high catalytic efficiency.

  1998cited by this paper
• The b′ domain provides the principal peptide‐binding site of protein disulfide isomerase but all domains contribute to binding of misfolded proteins

  1998influential reference
• Expression of protein disulfide isomerase is elevated in the endosperm of the maize floury-2 mutant

  1996cited by this paper
• Rice (Oryza sativa L.) α-Amylase Inhibitors of 14−16 kDa Are Potential Allergens and Products of a Multigene Family

  1996cited by this paper
• Isolation and characterization of a yeast gene, MPD1, the overexpression of which suppresses inviability caused by protein disulfide isomerase depletion

  1995cited by this paper
• Seed storage proteins: structures and biosynthesis.

  1995cited by this paper
• Rice prolamine protein body biogenesis: a BiP-mediated process.

  1993cited by this paper
• Characterization and localization of rice (Oryza sativa L.) seed globulins

  1992cited by this paper
• Catalysis of the oxidative folding of ribonuclease A by protein disulfide isomerase: dependence of the rate on the composition of the redox buffer.

  1991influential reference
• Purification of protein body-I of rice seed and its polypeptide composition

  1987cited by this paper
• Biosynthesis of storage proteins in developing rice seeds.

  1982influential reference
• Isolation and Characterization of Two Types of Protein Bodies in the Rice Endosperm

  1980influential reference

• Metabolomics and transcriptomics analyses reveal quality differences in forage-grain ratoon rice under varying mowing stages.

  2026cites this paper
• Enhancing quality traits in staple crops: current advances and future perspectives.

  2025cites this paper
• Vacuolar compartments preserved among loosely packed amyloplasts account for heat-induced rice chalky formation under low nitrogen conditions

  2025cites this paper
• OsSPL14 and OsNF-YB9/YC8-12 subunits cooperate to enhance grain appearance quality by promoting Waxy and PDIL1-1 expression in rice

  2025cites this paper
• PDIL2-3 encoding a protein disulfide isomerase-like enzyme is essential for grain yield and appearance quality in rice (Oryza sativa L.)

  2025cites this paper
• Variations in endosperm structure facilitate the formation of high protein quality in tetraploid rice

  2024cites this paper
• Down-Regulation of Rice Glutelin by CRISPR-Cas9 Gene Editing Decreases Carbohydrate Content and Grain Weight and Modulates Synthesis of Seed Storage Proteins during Seed Maturation

  2023cites this paper
• Influence on Accumulation Levels and Subcellular Localization of Prolamins by Fusion with the Functional Peptide in Transgenic Rice Seeds

  2023cites this paper
• Population genetic analysis and scans for adaptation and contemporary selection footprints provide genomic insight into aus, indica and japonica rice cultivars diversification

  2023cites this paper
• Genetic architecture of head rice and rice chalky grain percentages using genome-wide association studies

  2023cites this paper
• Genome-wide differences of alternative splicing between Oryza sativa ssp. indica and Oryza sativa ssp. japonica

  2023cites this paper
• Genetic Background Negates Improvements in Rice Flour Characteristics and Food Processing Properties Caused by a Mutant Allele of the PDIL1-1 Seed Storage Protein Gene

  2022cites this paper
• Thiol‐disulfide oxidoreductase PDI1;1 regulates actin structures in Oryza sativa root cells

  2022cites this paper
• Genetic control of grain appearance quality in rice.

  2022cites this paper
• Endomembrane‐mediated storage protein trafficking in plants: Golgi‐dependent or Golgi‐independent?

  2022cites this paper
• Specialized endoplasmic reticulum‐derived vesicles in plants: Functional diversity, evolution, and biotechnological exploitation

  2022cites this paper
• Two protein disulfide isomerase subgroups work synergistically in catalyzing oxidative protein folding.

  2021cites this paper
• Rice seed storage proteins: Biosynthetic pathways and the effects of environmental factors.

  2021cites this paper
• Unique Glutelin Expression Patterns and Seed Endosperm Structure Facilitate Glutelin Accumulation in Polyploid Rice Seed

  2021cites this paper
• The Arabidopsis Protein Disulfide Isomerase Subfamily M Isoform, PDI9, Localizes to the Endoplasmic Reticulum and Influences Pollen Viability and Proper Formation of the Pollen Exine During Heat Stress

  2020influential citation
• Genome-Wide Characterization of PDI Gene Family in Medicago truncatula and their Roles in Response to ER stress.

  2020cites this paper
• A novel soybean protein disulfide isomerase family protein possesses dithiol oxidation activity: Identification and characterization of GmPDIL6.

  2020cites this paper
• Regulation of intracellular transport of the glutelin in the rice endosperm cell

  2019cites this paper
• Eukaryotic peptide chain release factor 1 participates in translation termination of specific cysteine-poor prolamines in rice endosperm.

  2019cites this paper
• Oxidative protein folding in the plant endoplasmic reticulum

  2019cites this paper
• Towards coeliac‐safe bread

  2019cites this paper
• OsERdj7 is an ER-resident J-protein involved in ER quality control in rice endosperm.

  2019cites this paper
• OP-PCPJ180241 626..642

  2019cites this paper
• Multiple strategies for heat adaptation to prevent chalkiness in the rice endosperm

  2018cites this paper
• A conserved motif is essential for the correct assembly of proglutelins and for their export from the endoplasmic reticulum in rice endosperm

  2018cites this paper
• Title Expression and characterization of protein disulfide isomerasefamily proteins in bread wheat

  2018cites this paper
• Laser Microdissection-Based Tissue-Specific Transcriptome Analysis Reveals a Novel Regulatory Network of Genes Involved in Heat-Induced Grain Chalk in Rice Endosperm

  2018cites this paper
• Arabidopsis Aspartic Protease ASPG1 Affects Seed Dormancy, Seed Longevity and Seed Germination

  2018cites this paper
• Buried treasure: biosynthesis, structures and applications of cyclic peptides hidden in seed storage albumins.

  2018cites this paper
• Formation of Protein Disulfide Bonds Catalyzed by OsPDIL1;1 is Mediated by MicroRNA5144-3p in Rice

  2018cites this paper
• Atypical protein disulfide isomerases (PDI): Comparison of the molecular and catalytic properties of poplar PDI-A and PDI-M with PDI-L1A

  2017cites this paper
• Multiple strategies for heat adaptation in rice endosperms revealed by on-site cell-specific analysis

  2017cites this paper
• Novel Soybean Enzymes Involved in the Oxidative Protein Folding in the Endoplasmic Reticulum

  2017cites this paper
• Identification and characterization of GmPDIL7, a soybean ER membrane‐bound protein disulfide isomerase family protein

  2017cites this paper
• A Quantitative Acetylomic Analysis of Early Seed Development in Rice (Oryza sativa L.)

  2017cites this paper
• Compensatory rebalancing of rice prolamins by production of recombinant prolamin/bioactive peptide fusion proteins within ER-derived protein bodies

  2017cites this paper
• Retarded germination of Nicotiana tabacum seeds following insertion of exogenous DNA mimics the seed persistent behavior

  2017influential citation
• Tailoring Grain Storage Reserves for a Healthier Rice Diet and its Comparative Status with Other Cereals.

  2016cites this paper
• Mature forms of the major seed storage albumins in sunflower: A mass spectrometric approach.

  2016cites this paper
• Deposition mode of transforming growth factor-β expressed in transgenic rice seed

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• Comprehensive proteomic analysis of developing protein bodies in maize (Zea mays) endosperm provides novel insights into its biogenesis

  2016cites this paper
• Molecular physiological aspects of chalking mechanism in rice grains under high-temperature stress

  2016cites this paper
• A Molecular Physiological Mechanism of Rice Grain Chalking by High Temperature Stress

  2016cites this paper
• Golgi/plastid‐type manganese superoxide dismutase involved in heat‐stress tolerance during grain filling of rice

  2015cites this paper
• Proteomic Analysis of Cold Stress Responses in Banana Leaves

  2015cites this paper
• Cooperative Protein Folding by Two Protein Thiol Disulfide Oxidoreductases and ERO1 in Soybean1[OPEN]

  2015cites this paper
• Proteome analysis of wheat embryo (Triticum aestivum) Sensu stricto germination under osmotic stress.

  2015cites this paper
• Conserved C272/278 in b domain regulate the function of PDI-P5 to make lysozymes trypsin-resistant forms via significant intermolecular disulfide cross-linking.

  2015cites this paper
• Cassava root membrane proteome reveals activities during storage root maturation

  2015cites this paper
• Expression and characterization of protein disulfide isomerase family proteins in bread wheat

  2015cites this paper
• Lack of Globulin Synthesis during Seed Development Alters Accumulation of Seed Storage Proteins in Rice

  2015cites this paper
• Cooperation of Soybean PDI Family Members and ERO1

  2015cites this paper
• Phylogenetic characterization and promoter expression analysis of a novel hybrid protein disulfide isomerase/cargo receptor subfamily unique to plants and chromalveolates

  2015cites this paper
• Rice seed for delivery of vaccines to gut mucosal immune tissues.

  2015cites this paper
• Erratum to: Phylogenetic characterization and promoter expression analysis of a novel hybrid protein disulfide isomerase/cargo receptor subfamily unique to plants and chromalveolates

  2015cites this paper
• Seed storage albumins: biosynthesis, trafficking and structures.

  2014cites this paper
• Differential activity of rice protein disulfide isomerase family members for disulfide bond formation and reduction

  2014influential citation
• Cis-element of the rice PDIL2-3 promoter is responsible for inducing the endoplasmic reticulum stress response.

  2014cites this paper
• Oxidative Protein-Folding Systems in Plant Cells

  2013influential citation
• Variation in the Subcellular Localization and Protein Folding Activity among Arabidopsis thaliana Homologs of Protein Disulfide Isomerase

  2013cites this paper
• Two traditional maize inbred lines of contrasting technological abilities are discriminated by the seed flour proteome.

  2013cites this paper
• Accumulation of rice prolamin–GFP fusion proteins induces ER-derived protein bodies in transgenic rice calli

  2013cites this paper
• ER stress response induced by the production of human IL-7 in rice endosperm cells

  2013influential citation
• Functional and Evolutionary Genomics of Protein Disulphide Isomerase (PDI) Gene Family in Wheat and ItsWild relatives: A Review

  2013influential citation
• Dynamic Proteomics Emphasizes the Importance of Selective mRNA Translation and Protein Turnover during Arabidopsis Seed Germination*

  2013cites this paper
• Wheat Protein Disulfide Isomerase (PDI) Promoter Sequence Analysis in Triticum aestivum cv Chinese Spring and its Wild Relatives

  2013cites this paper
• P5-type sulfhydryl oxidoreductase promotes the sorting of proteins to protein body I in rice endosperm cells

  2013cites this paper
• Seed Storage Proteins

  2013cites this paper
• Evolution, Structure, and Function of Prolamin Storage Proteins

  2013cites this paper
• The Characteristic Polyhedral, Sharp-edged Shape of Compound-type Starch Granules in Rice Endosperm is Achieved via the Septum-like Structure of the Amyloplast

  2013cites this paper
• Overexpression of a protein disulfide isomerase-like protein from Methanothermobacter thermoautotrophicum enhances mercury tolerance in transgenic rice.

  2012cites this paper
• RNA targeting to a specific ER sub-domain is required for efficient transport and packaging of α-globulins to the protein storage vacuole in developing rice endosperm.

  2012cites this paper
• Redox regulation of glutenin subunit assembly in the plant endoplasmic reticulum.

  2012cites this paper
• Formation mechanism of the internal structure of type I protein bodies in rice endosperm: relationship between the localization of prolamin species and the expression of individual genes.

  2012cites this paper
• Protein Disulfide Isomerase-Like Protein 1-1 Controls Endosperm Development through Regulation of the Amount and Composition of Seed Proteins in Rice

  2012influential citation
• The oxidative protein folding machinery in plant cells

  2012cites this paper
• The Small GTPase Rab 5 a Is Essential for Intracellular Transport of Proglutelin from the Golgi Apparatus to the Protein Storage Vacuole and Endosomal Membrane Organization in Developing Rice Endosperm 1 [ C ] [ W ] [ OA ]

  2011cites this paper
• Generation of transgenic rice lines with reduced contents of multiple potential allergens using a null mutant in combination with an RNA silencing method.

  2011cites this paper
• Oxidative protein folding

  2011influential citation
• The failure to express a protein disulphide isomerase-like protein results in a floury endosperm and an endoplasmic reticulum stress response in rice

  2011cites this paper
• A Role for the Cysteine-Rich 10 kDa Prolamin in Protein Body I Formation in Rice

  2011cites this paper
• 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

  2011cites this paper
• The formation, function and fate of protein storage compartments in seeds

  2011cites this paper
• The Small GTPase Rab5a Is Essential for Intracellular Transport of Proglutelin from the Golgi Apparatus to the Protein Storage Vacuole and Endosomal Membrane Organization in Developing Rice Endosperm1[C][W][OA]

  2011cites this paper