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

Onda, Yayoi; Nagamine, Ai; Sakurai, Mutsumi; Kumamaru, Toshihiro; Ogawa, Masahiro; Kawagoe, Yasuhiro

doi:10.1105/tpc.110.079509

Cited by 76 publications

(100 citation statements)

References 44 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…As reported earlier, BiP and PDI are asymmetrically distributed on the cortical ER, where BiP is enriched on the ER around the protein bodies (PB-I) containing the prolamin while PDIL1-1 is not readily detected in PB-I and appears restricted to the cisternal ER (Muench et al, 1997;Satoh-Cruz et al, 2010a;Onda et al, 2011;Supplemental Fig. S7F).…”

Section: Distribution Of Er Chaperonessupporting

confidence: 78%

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 Endosperm

et al. 2011

Self Cite

View full text Add to dashboard Cite

Rice (Oryza sativa) glutelins are synthesized on the endoplasmic reticulum as larger precursors, which are then transported via the Golgi to the protein storage vacuole (PSV), where they are processed into acidic and basic subunits. Three independent glutelin precursor mutant4 (glup4) rice lines, which accumulated elevated levels of proglutelin over the wild type, were identified as loss-of-function mutants of Rab5a, the small GTPase involved in vesicular membrane transport. In addition to the plasma membrane, Rab5a colocalizes with glutelins on the Golgi apparatus, Golgi-derived dense vesicles, and the PSV, suggesting that Rab5a participates in the transport of the proglutelin from the Golgi to the PSV. This spatial distribution pattern was dramatically altered in the glup4 mutants. Numerous smaller protein bodies containing glutelin and a-globulin were evident, and the proteins were secreted extracellularly. Moreover, all three independent glup4 allelic lines displayed the novel appearance of a large dilated, structurally complex paramural body containing proglutelins, a-globulins, membrane biomarkers for the Golgi apparatus, prevacuolar compartment, PSV, and the endoplasmic reticulum luminal chaperones BiP and protein disulfide isomerase as well as b-glucan. These results indicate that the formation of the paramural bodies in glup4 endosperm was due to a significant disruption of endocytosis and membrane vesicular transport by Rab5a loss of function. Overall, Rab5a is required not only for the intracellular transport of proglutelins from the Golgi to the PSV in rice endosperm but also in the maintenance of the general structural organization of the endomembrane system in developing rice seeds.Developing plant seeds accumulate large quantities of storage proteins that are coded by two superfamilies of genes, globulins and prolamins (Shewry et al., 1995). Rice (Oryza sativa) is unique in that it accumulates major quantities of both storage protein types in the form of glutelins and prolamins as well as a third minor species, a-globulins (Tanaka et al., 1980;Krishnan and White, 1995). Glutelin, the dominant storage protein in rice, is homologous to leguminous 11S globulins and is packaged in a protein storage vacuole (PSV;Zhao et al., 1983). Unlike the saline-soluble 11S globulins, however, rice glutelins are only soluble in dilute acid and alkali solutions. During seed development, rice glutelin polypeptides are initially synthesized on the endoplasmic reticulum (ER) membrane as 57-kD proglutelin (Yamagata et al., 1982), which is then transported to the PSVs (Krishnan et al., 1986;Yamagata and Tanaka, 1986), where the precursors are cleaved to acidic and basic subunits (Yamagata et al., 1982). The rice a-globulin, a member of the prolamin superfamily, is also packaged in the PSV, where to-

show abstract

Section: Distribution Of Er Chaperonessupporting

confidence: 78%

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 Endosperm

et al. 2011

Self Cite

View full text Add to dashboard Cite

show abstract

“…It has been reported that PDI5 (At1g21750) chaperones and inhibits cysteine proteases during trafficking to vacuoles prior to programmed cell death of the endothelium in developing seeds (86), and this protein is oxidized during Arabidopsis seed germination (50). In rice seeds, a PDI protein (LOC_Os11g09280) prevents proglutelin and prolamin from aggregating by chaperoning their segregation in the ER lumen (87,88). In addition, PDI2 is highly expressed in Arabidopsis seeds; PDI2 accumulation is localized to both ER and nucleus, and a slight decrease in the germination rate of pdi2 mutant seeds relative to wild-type seeds has been observed (89).…”

Section: Discussionmentioning

confidence: 99%

Dynamic Proteomics Emphasizes the Importance of Selective mRNA Translation and Protein Turnover during Arabidopsis Seed Germination

Galland¹,

Huguet²,

Arc³

et al. 2014

Molecular & Cellular Proteomics

140

155

View full text Add to dashboard Cite

During seed germination, the transition from a quiescent metabolic state in a dry mature seed to a proliferative metabolic state in a vigorous seedling is crucial for plant propagation as well as for optimizing crop yield. This work provides a detailed description of the dynamics of protein synthesis during the time course of germination, demonstrating that mRNA translation is both sequential and selective during this process. The complete inhibition of the germination process in the presence of the translation inhibitor cycloheximide established that mRNA translation is critical for Arabidopsis seed germination. However, the dynamics of protein turnover and the selectivity of protein synthesis (mRNA translation) during Arabidopsis seed germination have not been addressed yet. Based on our detailed knowledge of the Arabidopsis seed proteome, we have deepened our understanding of seed mRNA translation during germination by combining twodimensional gel-based proteomics with dynamic radiolabeled proteomics using a radiolabeled amino acid precursor, namely [35 S]-methionine, in order to highlight de novo protein synthesis, stability, and turnover. Our data confirm that during early imbibition, the Arabidopsis translatome keeps reflecting an embryonic maturation program until a certain developmental checkpoint. Furthermore, by dividing the seed germination time lapse into discrete time windows, we highlight precise and specific patterns of protein synthesis. These data refine and deepen our knowledge of the three classical phases of seed germination based on seed water uptake during imbibition and reveal that selective mRNA translation is a key feature of seed germination. Beyond the quantitative control of translational activity, both the selectivity of mRNA translation and protein turnover appear as specific regulatory systems, critical for timing the molecular events leading to successful germination and seedling establishment. Molecular & Cellular Proteomics 13: 10.1074/mcp.M113.032227, 252-268, 2014.Seed germination is a vital stage in the plant life cycle during which embryo cells experience a programmed transition from a quiescent to a highly active metabolic state. Accordingly, seed quality in terms of germination vigor is of paramount importance for both ecological aspects and practical applications, as it influences the level, timing, and uniformity of seedling emergence in a wide range of environmental conditions (1, 2). In efforts to decipher the complex molecular mechanisms that control seed germination, genetic, genomic, and postgenomic analyses have been developed on the model plant Arabidopsis thaliana (3-6). Germination is classically described as a sequential time course divided into three major phases of seed water uptake (7). Phase I is characterized by rapid seed imbibition, which is crucial for the transition from the quiescent metabolic state of the dry seed to the high metabolic activity of the hydrated seed. Phase II corresponds to a period during which the seed imbibition level remains const...

show abstract

“…In rice seeds, a PDI prevents proglutelin and prolamin from aggregating by chaperoning their segregation in the ER lumen (Takemoto et al, 2002). The rice PDIL1-1 localizes to the ER lumen, and facilitates the oxidative folding of vacuole-targeted storage proteins, such as proglutelins and a-globulin (Onda et al, 2011). Other PDIs have been found in chloroplasts of plants (Lu and Christopher, 2006;Shimada et al, 2007) and unicellular algae (Kim and Mayfield, 1997), where they play roles in starch biogenesis (Lu and Christopher, 2006), chaperone and foldase (Shimada et al, 2007), and light-regulated translation of the psbA mRNA (Kim and Mayfield, 1997).…”

Section: Introductionmentioning

confidence: 99%

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

Cho

Yuen

Kang

et al. 2011

Molecules and Cells

View full text Add to dashboard Cite

Protein disulfide isomerase (PDI) is a thiodisulfide oxidoreductase that catalyzes the formation, reduction and rearrangement of disulfide bonds in proteins of eukaryotes. The classical PDI has a signal peptide, two CXXCcontaining thioredoxin catalytic sites (a,a′), two noncatalytic thioredoxin fold domains (b,b′), an acidic domain (c) and a C-terminal endoplasmic reticulum (ER) retention signal. Although PDI resides in the ER where it mediates the folding of nascent polypeptides of the secretory pathway, we recently showed that PDI5 of Arabidopsis thaliana chaperones and inhibits cysteine proteases during trafficking to vacuoles prior to programmed cell death of the endothelium in developing seeds. Here we describe Arabidopsis PDI2, which shares a primary structure similar to that of classical PDI. Recombinant PDI2 is imported into ER-derived microsomes and complements the E. coli protein-folding mutant, dsbA. PDI2 interacted with proteins in both the ER and nucleus, including ER-resident protein folding chaperone, BiP1, and nuclear embryo transcription factor, MEE8. The PDI2-MEE8 interaction was confirmed to occur in vitro and in vivo. Transient expression of PDI2-GFP fusions in mesophyll protoplasts resulted in labeling of the ER, nucleus and vacuole. PDI2 is expressed in multiple tissues, with relatively high expression in seeds and root tips. Immunoelectron microscopy with GFP-and PDI2-specific antisera on transgenic seeds (PDI2-GFP) and wild type roots demonstrated that PDI2 was found in the secretory pathway (ER, Golgi, vacuole, cell wall) and the nuclei. Our results indicate that PDI2 mediates protein folding in the ER and has new functional roles in the nucleus.

show abstract

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

Cited by 76 publications

References 44 publications

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 Endosperm

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 Endosperm

Dynamic Proteomics Emphasizes the Importance of Selective mRNA Translation and Protein Turnover during Arabidopsis Seed Germination

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

Contact Info

Product

Resources

About