A Novel Vesicle Derived Directly from Endoplasmic Reticulum is Involved in the Transport of Vacuolar Storage Proteins in Rice Endosperm

Takahashi, Hideyuki; Saito, Yuhi; Kitagawa, Tomoya; Morita, Shigeto; Masumura, Takehiro; Tanaka, Kunisuke

doi:10.1093/pcp/pci019

Cited by 75 publications

(57 citation statements)

References 22 publications

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“…Golgi-associated dense vesicles containing glutelin and globulin are readily evident in developing rice endosperm cells supporting a role for the Golgi apparatus in routing these storage proteins to the PSV (Krishnan et al 1990(Krishnan et al , 1992). An alternative direct ER to PSV pathway bypassing the Golgi (Hara-Nishimura et al 1998) has also been proposed in rice (Takahashi et al 2005). However, other than this single study, PAC-like vesicles similar to that observed in pumpkin have not been seen in other microscopic studies on rice protein body biogenesis (Krishnan et al 1990, 1992, Ogawa et al 1989.…”

Section: Introductionmentioning

confidence: 72%

Gene-gene interactions between mutants that accumulate abnormally high amounts of proglutelin in rice seed

et al. 2010

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We had previously identified eight mutants, esp2 and g(G)lups1 to 7, which accumulated abnormally high amounts of proglutelin, the major storage protein in rice seeds. Analysis of their seed proteins by SDS-PAGE, their levels of the luminal chaperone BiP and gene-gene interactions indicated that these mutants fell into four classes. The most epistatic class consisted of esp2, which encodes a defective protein disulfide isomerase (PDI). A second class consisting of Glup1, glup2 and glup7 was hypostatic to esp2, and showed abnormally high levels of BiP, suggesting that maturation and export of proglutelins from the ER are inhibited in this class of mutants. The third class containing glup4, Glup5 and glup6 mutations was hypostatic to esp2, Glup1, glup2 and glup7. Since the glup4 allele encodes the small GTPase Rab5a, which participates in the trafficking of proglutelin from Golgi apparatus to the protein storage vacuole (PSV), this third class of mutants is likely affected in this process. Lastly, glup3, which encodes a vacuolar processing enzyme, which proteolytically processes proglutelin into acidic and basic subunits within the PSV, was hypostatic to the other mutants. Overall, these gene relationships are consistent with the sequential intracellular transport and processing of proglutelin and provide novel insights on the trafficking of proglutelin to the PSV.

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Section: Introductionmentioning

confidence: 72%

Gene-gene interactions between mutants that accumulate abnormally high amounts of proglutelin in rice seed

et al. 2010

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“…Electron microscopy was conducted as described by Takahashi et al (12). Samples of RR, CR, and feces were fixed in 4% paraformaldehyde in 0.1 m phosphate buffer (pH 7.2) for 1 h at room temperature.…”

Section: Inmentioning

confidence: 99%

In Vivo Digestibility of Rice Prolamin/Protein Body-I Particle Is Decreased by Cooking

Kubota

Saito

Masumura

et al. 2014

J Nutr Sci Vitaminol

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Rice is a staple cereal and a major source of both protein and energy in most Asian countries. Thus, the true digestibility of cooked rice protein is very important for human nutrition. The proteins in rice endosperm consist mainly of storage proteins, e.g., glutelin, prolamin and globulin. Two major proteins, glutelin and prolamin, can be separated into several protein bands by sodium dodecyl sulfate polyacrylamide gel electrophoresis (SDS-PAGE). Glutelin separates into three bands: proglutelin (57 kDa), an acidic subunit (37-39 kDa), and a basic subunit (22-23 kDa) (1). Prolamin also separates into three bands: 16, 13 and 10 kDa prolamin (2). These storage proteins accumulate in organelles called protein bodies (PBs). Rice endosperm has two different types of PBs; prolamin accumulates in type-I protein bodies (PB-I), while glutelin and globulin accumulate in type-II protein bodies (PB-II) (3). Tanaka et al. (4) reported that fecal protein particles (FPP), such as PBs, were excreted in the feces of humans who had ingested cooked rice (CR). Ogawa et al. (2) demonstrated that the 13 kDa prolamin band in raw rice (RR) remained after pepsin digestion, although the glutelin subunit bands (37-39 and 22-23 kDa) disappeared. These results imply that prolamin is an indigestible protein. However, we recently reported that structural changes induced by alkali extraction can improve the in vivo digestibility of prolamin (5, 6). A study by Eggum et al. showed that cooking decreased the true protein digestibility (TD) of rice from 99.7 to 88.6% (7). However, no reports have directly demonstrated whether rice prolamin is rendered indigestible in vivo by cooking.In the present study, we monitored the gastrointestinal (GI) transit and fecal excretion of rice glutelin and prolamin in rats by using anti-23 kDa glutelin (23G) and anti-13 kDa prolamin (13P) antibodies to estimate their digestibility in CR and RR. Additionally, morphological observations of PBs in the feces of rats fed the CR or RR diets were conducted using electron microscopy to confirm the effects of cooking on PB structure. Although the digestibility of 23G was not affected by cooking, the digestibility of 13P was clearly reduced. Almost intact PB-Is were observed in the feces of rats fed the CR diet. Our results clearly indicate that rice prolamin is not indigestible in its raw form, but is rendered indigestible by cooking. Materials and MethodsMaterials and animal experiment. Rice (Koshihikari, 10% polished fraction) was purchased from Niigata Seifun Co., Ltd. (Tainai, Japan). RR flour was prepared using a jet mill (KV-3-4S, Yakushinkikai Seisakusho, Japan). CR flour was prepared by rinsing the rice first and then cooking it in twice its volume of water in an electric rice cooker (JAG-A100 TM, Tiger Co., Ltd., Osaka, Japan). Summary Rice has storage proteins, e.g., glutelin, globulin and prolamin, in the seeds, which are used as nitrogen sources during germination. Rice prolamin has been reported to be an indigestible protein that decreases the nutritional ...

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“…PAC vesicles are between 200 and 400 nm in diameter and consist of an electron-lucent outer region with internal vesicles and an inner core of storage protein aggregates. Rice contains compartments similar to PAC vesicles with a central core of storage proteins (glutelins and a-globulins in this case) and an outer translucent layer with vesicles, but they differ from PAC vesicles in being larger (;1 mm in diameter) and having ribosomes decorating their surface (Takahashi et al, 2005). In addition, physical connections between these compartments and the ER have been suggested based on EM images (Takahashi et al, 2005).…”

Section: Autophagy In Cereal Endosperm Cellsmentioning

confidence: 99%

Delivery of Prolamins to the Protein Storage Vacuole in Maize Aleurone Cells

et al. 2011

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Zeins, the prolamin storage proteins found in maize (Zea mays), accumulate in accretions called protein bodies inside the endoplasmic reticulum (ER) of starchy endosperm cells. We found that genes encoding zeins, a-globulin, and legumin-1 are transcribed not only in the starchy endosperm but also in aleurone cells. Unlike the starchy endosperm, aleurone cells accumulate these storage proteins inside protein storage vacuoles (PSVs) instead of the ER. Aleurone PSVs contain zeinrich protein inclusions, a matrix, and a large system of intravacuolar membranes. After being assembled in the ER, zeins are delivered to the aleurone PSVs in atypical prevacuolar compartments that seem to arise at least partially by autophagy and consist of multilayered membranes and engulfed cytoplasmic material. The zein-containing prevacuolar compartments are neither surrounded by a double membrane nor decorated by AUTOPHAGY RELATED8 protein, suggesting that they are not typical autophagosomes. The PSV matrix contains glycoproteins that are trafficked through a Golgi-multivesicular body (MVB) pathway. MVBs likely fuse with the multilayered, autophagic compartments before merging with the PSV. The presence of similar PSVs also containing prolamins and large systems of intravacuolar membranes in wheat (Triticum aestivum) and barley (Hordeum vulgare) starchy endosperm suggests that this trafficking mechanism may be common among cereals.The cereal endosperm consists of three main cell types: an inner mass of starchy endosperm cells, one to three layers of epidermal aleurone cells, and the transfer cells that contact the maternal vascular tissue (Olsen, 2004). The starchy endosperm accounts for 80 to 90% of the grain weight and contains large amounts of storage proteins and starch. These cells undergo programmed cell death during maturation. Aleurone cells are rich in protein storage vacuoles (PSVs), minerals, and lipid bodies and remain alive during seed development. It is assumed that the breakdown of proteins localized to PSVs in aleurone cells provides an essential source of the amino acids necessary for the synthesis of hydrolytic enzymes required for mobilizing food stored in the starchy endosperm (Filner and Varner, 1967;Jacobsen et al., 1988;Bethke et al., 1998).Besides its biological relevance as a model to study plant development, cell differentiation, and programmed cell death, the cereal endosperm is very important in terms of its nutritional value. Cereal grains contain less protein than do legume seeds, but because cereals are produced and consumed in much larger quantities, they are the main source of protein for the nutrition of humans and livestock (Shewry and Halford, 2002). The major storage proteins in maize (Zea mays) kernels are the alcoholsoluble prolamins, a type of storage proteins present only in grasses. Maize prolamins, referred to as zeins, are divided into different types: a-, b-, g-, and d-zeins (Coleman and Larkins, 1999) that differ in amino acid composition and structural properties (Shewry and Halford, 2002)...

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A Novel Vesicle Derived Directly from Endoplasmic Reticulum is Involved in the Transport of Vacuolar Storage Proteins in Rice Endosperm

Cited by 75 publications

References 22 publications

Gene-gene interactions between mutants that accumulate abnormally high amounts of proglutelin in rice seed

Gene-gene interactions between mutants that accumulate abnormally high amounts of proglutelin in rice seed

In Vivo Digestibility of Rice Prolamin/Protein Body-I Particle Is Decreased by Cooking

Delivery of Prolamins to the Protein Storage Vacuole in Maize Aleurone Cells

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