A Role for the Cysteine-Rich 10 kDa Prolamin in Protein Body I Formation in Rice

The rice prolamins consist of cysteine-rich 10 kDa (CysR10), 14 kDa (CysR14) and 16 kDa (CysR16) molecular species and a cysteine-poor 13 kDa (CysP13) polypeptide. These storage proteins form protein bodies (PBs) composed of single spherical intracisternal inclusions assembled within the lumen of the rough endoplasmic reticulum. Immunofluorescence and immunoelectron microscopy demonstrated that CysR10 and CysP13 were asymmetrically distributed within the PBs, with the former concentrated at the electron-dense center core region and the latter distributed mainly to the electron-lucent peripheral region. These results together with temporal expression data showed that the formation of prolamin-containing PB-I in the wild-type endosperm was initiated by the accumulation of CysR10 to form the center core. In mutants deficient for cysteine-rich prolamins, the typical PB-I structures containing the electron-dense center core were not observed, and instead were replaced by irregularly shaped, electron-lucent, hypertrophied PBs. Similar, deformed PBs were observed in a CysR10 RNA interference plant line. These results suggest that CysR10, through its formation of the central core and its possible interaction with other cysteine-rich prolamins, is required for tight packaging of the proteins into a compact spherical structure.

[1]  M. Ogawa,et al.  Distinct Roles of Protein Disulfide Isomerase and P5 Sulfhydryl Oxidoreductases in Multiple Pathways for Oxidation of Structurally Diverse Storage Proteins in Rice[W][OA] , 2011, Plant Cell.

[2]  H. Yasuda,et al.  Reducing Rice Seed Storage Protein Accumulation Leads to Changes in Nutrient Quality and Storage Organelle Formation1[W][OA] , 2010, Plant Physiology.

[3]  T. Okita,et al.  Protein disulfide isomerase like 1-1 participates in the maturation of proglutelin within the endoplasmic reticulum in rice endosperm. , 2010, Plant & cell physiology.

[4]  T. Okita,et al.  Identification of cis-localization elements of the maize 10-kDa delta-zein and their use in targeting RNAs to specific cortical endoplasmic reticulum subdomains. , 2009, The Plant journal : for cell and molecular biology.

[5]  T. Kumamaru,et al.  ER membrane-localized oxidoreductase Ero1 is required for disulfide bond formation in the rice endosperm , 2009, Proceedings of the National Academy of Sciences.

[6]  T. Okita,et al.  Protein Body Biogenesis in Cereal Endosperms , 2007 .

[7]  T. Okita,et al.  The role of mRNA and protein sorting in seed storage protein synthesis, transport, and deposition. , 2005, Biochemistry and cell biology = Biochimie et biologie cellulaire.

[8]  T. Jomori,et al.  Expression of the Small Peptide GLP-1 in Transgenic Plants , 2005, Transgenic Research.

[9]  E. Katoh,et al.  The Critical Role of Disulfide Bond Formation in Protein Sorting in the Endosperm of Rice , 2005, The Plant Cell Online.

[10]  T. Okita,et al.  The Rice Mutant esp2 Greatly Accumulates the Glutelin Precursor and Deletes the Protein Disulfide Isomerase1 , 2002, Plant Physiology.

[11]  B. Larkins,et al.  Zein Protein Interactions, Rather Than the Asymmetric Distribution of Zein mRNAs on Endoplasmic Reticulum Membranes, Influence Protein Body Formation in Maize Endosperm , 2002, The Plant Cell Online.

[12]  B. Larkins,et al.  Genomics Analysis of Genes Expressed in Maize Endosperm Identifies Novel Seed Proteins and Clarifies Patterns of Zein Gene Expression , 2001, The Plant Cell Online.

[13]  T. Okita,et al.  Messenger RNA targeting of rice seed storage proteins to specific ER subdomains , 2000, Nature.

[14]  S. Toki,et al.  Iron fortification of rice seed by the soybean ferritin gene , 1999, Nature Biotechnology.

[15]  Kunisuke Tanaka,et al.  Amino Acid Sequencing and cDNA Cloning of Rice Seed Storage Proteins, the 13kDa Prolamins, Extracted from Type I Protein Bodies , 1999 .

[16]  A. Suzuki,et al.  Promoters of Rice Seed Storage Protein Genes Direct Endosperm-Specific Gene Expression in Transgenic Rice , 1998 .

[17]  P. Shewry,et al.  Seed storage proteins: structures and biosynthesis. , 1995, The Plant cell.

[18]  W. Kim,et al.  Expression of Storage Protein Multigene Families in Developing Rice Endosperm , 1993 .

[19]  T. Okita,et al.  Accumulation of Prolamines and Glutelins during Rice Seed Development: a Quantitative Evaluation , 1993 .

[20]  G. Galili,et al.  Evidence for a novel route of wheat storage proteins to vacuoles , 1992, The Journal of cell biology.

[21]  T. Wen,et al.  cDNA cloning and gene expression of the major prolamins of rice , 1992, Plant Molecular Biology.

[22]  A. W. Kirleis,et al.  Purification and immunocytochemical localization of kafirins inSorghum bicolor (L. Moench) endosperm , 1992, Protoplasma.

[23]  A. Esen,et al.  Immunocytochemical localization of δ-zein in the protein bodies of maize endosperm cells , 1992 .

[24]  L. Shyur,et al.  Nucleotide sequence of two rice prolamin cDNAs. , 1990, Nucleic acids research.

[25]  Kunisuke Tanaka,et al.  Cloning and characterization of a cDNA encoding a rice 13 kDa prolamin , 1990, Molecular and General Genetics MGG.

[26]  B. Larkins,et al.  Changes in the zein composition of protein bodies during maize endosperm development. , 1989, The Plant cell.

[27]  H. Satoh,et al.  Mutants for rice storage proteins , 1989, Theoretical and Applied Genetics.

[28]  D. Shibata,et al.  cDNA cloning of an mRNA encoding a sulfur-rich 10 kDa prolamin polypeptide in rice seeds , 1989, Plant Molecular Biology.

[29]  T. Okita,et al.  Structure, expression, and heterogeneity of the rice seed prolamines. , 1988, Plant physiology.

[30]  T. Okita,et al.  Nucleotide and primary sequence of a major rice prolamine , 1988, FEBS letters.

[31]  Kunisuke Tanaka,et al.  Purification of protein body-I of rice seed and its polypeptide composition , 1987 .

[32]  H. Krishnan,et al.  Immunochemical studies on the role of the Golgi complex in protein-body formation in rice seeds , 1986, Planta.

[33]  B. Larkins,et al.  Analysis of sequence microheterogeneity among zein messenger RNAs. , 1982, The Journal of biological chemistry.

[34]  D. Wettstein,et al.  Protein body formation in the developing barley endosperm , 1980 .

[35]  Kunisuke Tanaka,et al.  Isolation and Characterization of Two Types of Protein Bodies in the Rice Endosperm , 1980 .

[36]  D. Bechtel,et al.  Formation of Protein Bodies in the Starchy Endosperm of Rice (Oryza sativa L.): A Re-investigation , 1980 .

[37]  T. Rost.  The ultrastructure and physiology of protein bodies and lipids from hydrated dormant and nondormant embryos of Setaria lutescens (Gramineae) , 1972 .

[38]  S. U. Siddiqui,et al.  Vacuolar processing enzyme plays an essential role in the crystalline structure of glutelin in rice seed. , 2010, Plant & cell physiology.

[39]  P. Shewry,et al.  The Characteristics, Structures and Evolutionary Relationships of Prolamins , 1999 .

[40]  T. Okita,et al.  The Prolamins of Rice , 1999 .

[41]  H. Gilbert,et al.  Protein disulfide isomerase. , 1998, Methods in enzymology.

[42]  T. Okita,et al.  The Storage Proteins of Rice and Oat , 1997 .

[43]  B. Larkins,et al.  Cellular and Molecular Biology of Plant Seed Development , 1997, Advances in Cellular and Molecular Biology of Plants.

[44]  H. Satoh,et al.  Mutants for rice storage proteins. IV. Maternally inherited mutants for storage proteins of protein bodies in the starchy endosperm , 1990, Heredity.

[45]  H. Satoh,et al.  Mutants for rice storage proteins. III. Genetic analysis of mutants for storage proteins of protein bodies in the starchy endosperm.:III. Genetic analysis of mutants for storage proteins of protein bodies in the starchy endosperm , 1987 .

[46]  Kunisuke Tanaka,et al.  The Site of Synthesis and Accumulation of Rice Storage Proteins , 1986 .