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

Plant Journal

Volumn 70, Issue 6, 2012, Pages 1043-1055

  Saito, Yuhi ^a   Shigemitsu, Takanari ^a   Yamasaki, Ryuichi ^a   Sasou, Ai ^a   Goto, Futami ^a   Kishida, Koichi ^a   Kuroda, Masaharu ^b   Tanaka, Kunisuke ^a   Morita, Shigeto ^a,c   Satoh, Shigeru ^a,c   Masumura, Takehiro ^a,c  

^a KYOTO PREFECTURAL UNIVERSITY   (Japan)

^b FOOD RESEARCH INSTITUTE   (Japan)

^c Forestry and Fisheries Technology Center   (Japan)

Author keywords

endoplasmic reticulum; prolamin; protein body; rice (Oryza sativa); seed; storage protein

Indexed keywords

CONSTITUTIVE PROMOTERS; CONTROL OF GENE EXPRESSION; DEVELOPING SEED; ENDOPLASMIC RETICULUM; ENDOSPERM CELLS; FORMATION MECHANISM; FUSION PROTEINS; IMMUNOELECTRON MICROSCOPY; INNER LAYER; INTERNAL STRUCTURE; MECHANISM OF FORMATION; MICROSCOPIC ANALYSIS; MIDDLE LAYER; MRNA EXPRESSION; MULTIGENE FAMILIES; PROLAMIN; REAL TIME RT-PCR; RICE (ORYZA SATIVA); RICE ENDOSPERM; ROUGH ENDOPLASMIC RETICULUMS; SEED STORAGE PROTEINS; STORAGE PROTEINS; TEMPORAL EXPRESSIONS; TRANSGENIC RICE SEEDS;

BIOSYNTHESIS; CELL MEMBRANES; PLANTS (BOTANY); PROTEINS; SEED;

GENE EXPRESSION;

PROLAMIN;

ARTICLE; CLASSIFICATION; CYTOLOGY; ENDOSPERM; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MULTIGENE FAMILY; PLANT SEED; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RICE; TRANSGENIC PLANT;

ENDOSPERM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; MULTIGENE FAMILY; ORYZA SATIVA; PLANTS, GENETICALLY MODIFIED; PROLAMINS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEEDS;

ORYZA SATIVA;

EID: 84862179912     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2012.04947.x     Document Type: Article

References (45)

1. Bagga, S., Adams, H., Kemp, J.D., and, Sengupta-Gopalan, C., (1995) Accumulation of 15-kilodalton zein in novel protein bodies in transgenic tobacco. Plant Physiol. 107, 13-23.
2. Bagga, S., Adams, H.P., Rodriguez, F.D., Kemp, J.D., and, Sengupta-Gopalan, C., (1997) Coexpression of the maize δ-zein and β-zein genes results in stable accumulation of δ-zein in endoplasmic reticulum-derived protein bodies formed by β-zein. Plant Cell, 9, 1683-1696. (Pubitemid 28174106)
3. Bechtel, D.B., and, Juliano, B.O., (1980) Formation of protein bodies in the starchy endosperm of rice (Oryza sativa L.): a re-investigation. Ann. Bot. 45, 503-509.
4. Chiu, W., Niwa, Y., Zeng, W., Hirano, T., Kobayashi, H., and, Sheen, J., (1996) Engineered GFP as a vital reporter in plants. Curr. Biol. 6, 325-330.
5. Coleman, C.E., Herman, E.M., Takasaki, K., and, Larkins, B.A., (1996) The maize α-zein sequesters α-zein and stabilizes its accumulation in protein bodies of transgenic tobacco endosperm. Plant Cell, 8, 2335-2345. (Pubitemid 126446968)
6. Coleman, C.E., Yoho, P.R., Escobar, S., and, Ogawa, M., (2004) The accumulation of α-zein in transgenic tobacco endosperm is stabilized by co-expression of β-zein. Plant Cell Physiol. 45, 864-871. (Pubitemid 39123399)
7. Crofts, A.J., Washida, H., Okita, T.W., Ogawa, M., Kumamaru, T., and, Satoh, H., (2004) Targeting of proteins to endoplasmic reticulum-derived compartments in plants. The importance of RNA localization. Plant Physiol. 136, 3414-3419. (Pubitemid 41075780)
8. Esen, A., and, Stetler, D.A., (1992) Immunocytochemical localization of δ-zein in protein bodies of maize endosperm cells. Am. J. Bot. 79, 243-248.
9. Furukawa, S., Mizuma, T., Kiyokawa, Y., Masumura, T., Tanaka, K., and, Wakai, Y., (2003) Distribution of storage proteins in low-glutelin rice seed determined using a fluorescent antibody. J. Biosci. Bioeng. 96, 467-473. (Pubitemid 37533390)
10. Geli, M.I., Torrent, M., and, Ludevid, D., (1994) Two structural domains mediate two sequential events in α-zein targeting: protein endoplasmic reticulum retention and protein body formation. Plant Cell, 6, 1911-1922. (Pubitemid 24986963)
11. Hiei, Y., Ohta, S., Komari, T., and, Kumashiro, T., (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J. 6, 271-282.
12. Kawagoe, Y., Suzuki, K., Tasaki, M., Yasuda, H., Akagi, K., Katoh, E., Nishizawa, N.K., Ogawa, M., and, Takaiwa, F., (2005) The critical role of disulfide bond formation in protein sorting in the endosperm of rice. Plant Cell, 17, 1141-1153. (Pubitemid 43142132)
13. Kim, C.S., Woo, Y.m., Clore, A.M., Burnett, R.J., Carneiro, N.P., and, Larkins, B.A., (2002) Zein protein interactions, rather than the asymmetric distribution of zein mRNAs on endoplasmic reticulum membranes, influence protein body formation in maize endosperm. Plant Cell, 14, 655-672. (Pubitemid 34299671)
14. Krishnan, H.B., Franceschi, V.R., and, Okita, T.W., (1986) Immunochemical studies on the role of the Golgi complex in protein-body formation in rice seeds. Planta, 169, 471-480.
15. Krishnan, H.B., White, J.A., and, Pueppke, S.G., (1992) Characterization and localization of rice (Oryza sativa L.) seed globulins. Plant Sci. 81, 1-11.
16. Kuroda, M., Kimizu, M., and, Mikami, C., (2010) A simple set of plasmids for the production of transgenic plants. Biosci. Biotechnol. Biochem. 74, 2348-2351.
17. Lending, C.R., and, Larkins, B.A., (1989) Changes in the zein composition of protein bodies during maize endosperm development. Plant Cell, 1, 1011-1023.
18. Levanony, H., Rubin, R., Altschuler, Y., and, Galili, G., (1992) Evidence for a novel route of wheat storage proteins to vacuoles. J. Cell Biol. 119, 1117-1128.
19. Li, X., Wu, Y., Zhang, D.Z., Gillikin, J.W., Boston, R.S., Franceschi, V.R., and, Okita, T.W., (1993) Rice prolamine protein body biogenesis: a BiP-mediated process. Science, 262, 1054-1056. (Pubitemid 24035044)
20. Masumura, T., Shibata, D., Hibino, T., Kato, T., Kawabe, K., Takeba, G., Tanaka, K., and, Fujii, S., (1989) cDNA cloning of an mRNA encoding a sulfur-rich 10 kDa prolamin polypeptide in rice seeds. Plant Mol. Biol. 12, 123-130.
21. Masumura, T., Hibino, T., Kidzu, K., Mitsukawa, N., Tanaka, K., and, Fujii, S., (1990) Cloning and characterization of a cDNA encoding a rice 13 kDa prolamin. Mol. Gen. Genet., 221, 1-7. (Pubitemid 20099371)
22. Mitsukawa, N., Konishi, R., Kidzu, K., Ohtsuki, K., Masumura, T., and, Tanaka, K., (1999a) Amino acid sequencing and cDNA cloning of rice seed storage proteins, the 13 kDa prolamins, extracted from type I protein bodies. Plant Biotechnol. 16, 103-113.
23. Mitsukawa, N., Konishi, R., Uchiki, M., Masumura, T., and, Tanaka, K., (1999b) Molecular cloning and characterization of a cysteine-rich 16.6-kDa prolamin in rice seeds. Biosci. Biotechnol. Biochem. 63, 1851-1858. (Pubitemid 129548979)
24. Muench, D.G., Wu, Y., Zhang, Y., Li, X., Boston, R.S., and, Okita, T.W., (1997) Molecular cloning, expression and subcellular localization of a BiP homolog from rice endosperm tissue. Plant Cell Physiol. 38, 404-412. (Pubitemid 127467255)
25. Nagamine, A., Matsusaka, H., Ushijima, T., Kawagoe, Y., Ogawa, M., Okita, T.W., and, Kumamaru, T., (2011) A role for the cysteine-rich 10 kDa prolamin in protein body I formation in rice. Plant Cell Physiol. 52, 1003-1016.
26. Ogawa, M., Kumamaru, T., Satoh, H., Iwata, N., Omura, T., Kasai, Z., and, Tanaka, K., (1987) Purification of protein body-I of rice seed and its polypeptide composition. Plant Cell Physiol. 28, 1517-1527.
27. Ohta, S., Mita, S., Hattori, T., and, Nakamura, K., (1990) Construction and expression in tobacco of a β-glucuronidase (GUS) reporter gene containing an intron within the coding sequence. Plant Cell Physiol. 31, 805-813.
28. Onda, Y., Nagamine, A., Sakurai, M., Kumamaru, T., Ogawa, M., and, Kawagoe, Y., (2011) Distinct roles of protein disulfide isomerase and P5 sulfhydryl oxidoreductases in multiple pathways for oxidation of structurally diverse storage proteins in rice. Plant Cell, 23, 210-223.
29. Oparka, K.J., and, Harris, N., (1982) Rice protein-body formation: all types are initiated by dilation of the endoplasmic reticulum. Planta, 154, 184-188.
30. Rechinger, K.B., Simpson, D.J., Svendsen, I., and, Cameron-Mills, V., (1993) A role for α3 hordein in the transport and targeting of prolamin polypeptides to the vacuole of developing barley endosperm. Plant J. 4, 841-853. (Pubitemid 2017556)
31. Reyes, F.C., Chung, T., Holding, T., Jung, R., Vierstra, R., and, Otegui, M.S., (2011) Delivery of prolamins to the protein storage vacuole in maize aleurone cells. Plant Cell, 23, 769-784.
32. Saito, Y., Nakatsuka, N., Shigemitsu, T., Tanaka, K., Morita, S., Satoh, S., and, Masumura, T., (2008) Thin frozen film method for visualization of storage proteins in mature rice grains. Biosci. Biotechnol. Biochem. 72, 2779-2781.
33. Saito, Y., Kishida, K., Takata, K., Takahashi, H., Shimada, T., Tanaka, K., Morita, S., Satoh, S., and, Masumura, T., (2009) A green fluorescent protein fused to rice prolamin forms protein body-like structures in transgenic rice. J. Exp. Bot. 60, 615-627.
34. Saito, Y., Shigemitsu, T., Tanaka, K., Morita, S., Satoh, S., and, Masumura, T., (2010) Ultrastructure of mature protein body in the starchy endosperm of dry cereal grain. Biosci. Biotechnol. Biochem. 74, 1485-1487.
35. Shotwell, M.A., and, Larkins, B.A., (1989) The biochemistry and molecular biology of seed storage proteins. In The Biochemistry of Plants: A Comprehensive Treatise, Vol. 15 (, Marcus, A., ed). New York: Academic Press, pp. 297-345.
36. Shull, J.M., Watterson, J.J., and, Kirleis, A.W., (1992) Purification and immunocytochemical localization of kafirins in Sorghum bicolor (L. Moench) endosperm. Protoplasma, 171, 64-74.
37. Takahashi, H., Morita, S., Masumura, T., and, Tanaka, K., (2004) Preparation of an endosperm protoplasts from a dwarf rice variety and transient expression of green-fluorescent protein. Plant Biotechnol. 21, 109-112. (Pubitemid 39033481)
38. Takahashi, H., Saito, Y., Kitagawa, T., Morita, S., Masumura, T., and, Tanaka, K., (2005) A novel vesicle derived directly from endoplasmic reticulum is involved in the transport of vacuolar storage proteins in rice endosperm. Plant Cell Physiol. 46, 245-249. (Pubitemid 40307220)
39. Takemoto, Y., Coughlan, S.J., Okita, T.W., Satoh, H., Ogawa, M., and, Kumamaru, T., (2002) The rice mutant esp2 greatly accumulates the glutelin precursor and deletes the protein disulfide isomerase. Plant Physiol. 128, 1212-1222. (Pubitemid 34305775)
40. Tanaka, K., Sugimoto, T., Ogawa, M., and, Kasai, Z., (1980) Isolation and characterization of two types of protein bodies in the rice endosperm. Agric. Biol. Chem. 44, 1633-1639.
41. Xu, J.H., and, Messing, J., (2009) Amplification of prolamin storage protein genes in different subfamilies of the Poaceae. Theor. Appl. Genet. 119, 1397-1412.
42. Yamagata, H., and, Tanaka, K., (1986) The site of synthesis and accumulation of rice storage proteins. Plant Physiol. 27, 135-145.
43. Yamagata, H., Sugimoto, T., Tanaka, K., and, Kasai, Z., (1982) Biosynthesis of storage proteins in developing rice seeds. Plant Physiol. 70, 1094-1100.
44. Yamagata, H., Nomura, T., Arai, S., Tanaka, K., and, Iwasaki, T., (1992) Nucleotide sequence of a cDNA that encodes a rice prolamin. Biosci. Biotechnol. Biochem. 56, 537.
45. Yasuda, H., Hirose, S., Kawakatsu, T., Wakasa, Y., and, Takaiwa, F., (2009) Overexpression of BiP has inhibitory effects on the accumulation of seed storage proteins in endosperm cells of rice. Plant Cell Physiol. 50, 1532-1543.