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

Journal of Experimental Botany

Volumn 63, Issue 1, 2012, Pages 121-130

  Han, Xiaohua ^a   Wang, Yihua ^a   Liu, Xi ^a   Jiang, Ling ^a   Ren, Yulong ^a   Liu, Feng ^a   Peng, Cheng ^a   Li, Jingjing ^a   Jin, Ximing ^a   Wu, Fuqing ^b   Wang, Jiulin ^b   Guo, Xiuping ^b   Zhang, Xin ^b   Cheng, Zhijun ^b   Wan, Jianmin ^a,b  

^a NANJING AGRICULTURAL UNIVERSITY   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

ER stress; floury endosperm; protein disulphide isomerase like 1 1; starch synthesis

Indexed keywords

PROTEIN DISULFIDE ISOMERASE;

ARTICLE; ENDOPLASMIC RETICULUM; ENDOSPERM; METABOLISM; POLYMERASE CHAIN REACTION; RICE;

ENDOPLASMIC RETICULUM; ENDOSPERM; ORYZA SATIVA; POLYMERASE CHAIN REACTION; PROTEIN DISULFIDE-ISOMERASES;

EID: 84555188539     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/err262     Document Type: Article

References (51)

1. Boyce M, Yuan J. 2006. Cellular response to endoplasmic reticulum stress: a matter of life or death. Cell Death and Differentiation 13, 363-373.
2. Bresolin NS, Li Z, Kosar-Hasgemi B, Tetlow IJ, Chatterjee M, Rahman S, Morell MK, Howitt CA. 2006. Characterisation of disproportionating enzyme from wheat endosperm. Planta 224, 20-31.
3. Cacas JL. 2010. Devil inside: does plant programmed cell death involve the endomembrane system? Plant, Cell and Environment 33, 1453-1473.
4. Colleoni C, Dauvillee D, Mouille G, et al. 1999a. Genetic and biochemical evidence for the involvement of a-1,4 glucanotransferases in amylopectin synthesis. Plant Physiology 120, 993-1003.
5. Colleoni C, Dauvillee D, Mouille G, Morell MK, Samuel M, Slomiany MC, Lienard L, Wattebled F, d'Hulst C, Ball S. 1999b. Biochemical characterisation of the Chlamydomonas reinhardtii a-1,4 glucanotransferase supports a direct function in amylopectin biosynthesis. Plant Physiology 120, 1005-1014.
6. Doehlert DC, Kuo TM, Felker FC. 1988. Enzymes of sucrose and hexose metabolism in developing kernels of two inbreds of maize. Plant Physiology 86, 1013-1019.
7. Fujita N, Toyosawa Y, Utsumi Y, et al. 2009. Characterization of pullulanase (PUL)-deficient mutants of rice (Oryza sativa L.) and the function of PUL on starch biosynthesis in the developing rice endosperm. Journal of Experimental Botany 60, 1009-1023.
8. Fujita N, Yoshida M, Kondo T, et al. 2007. Characterization of SSIIIa-deficient mutants of rice: the function of SSIIIa and pleiotropic effects by SSIIIa deficiency in the rice endosperm. Plant Physiology 144, 2009-2023.
9. Fuse T, Sasaki T, Yano M. 2001. Ti-plasmid vectors useful for functional analysis of rice genes. Plant Biotechnology 18, 219-222.
10. Giroux MJ, Hannah LC. 1994. ADP-glucose pyrophosphorylase in shrunken-2 and brittle-2 mutants of maize. Molecular and General Genetics 243, 400-408.
11. Gruber CW, Cemazar M, Heras B, Martin JL, Craik DJ. 2006. Protein disulfide isomerase: the structure of oxidative folding. Trends in Biochemical Sciences 31, 455-464.
12. Hennen-Bierwagen TA, Lin Q, Grimaud F, Planchot V, Keeling PL, James MG, Myers AM. 2009. Proteins from multiple metabolic pathways associate with starch biosynthetic enzymes in high molecular weight complexes: a model for regulation of carbon allocation in maize amyloplasts. Plant Physiology 149, 1541-1559.
13. Hennen-Bierwagen TA, Liu F, Marsh RS, Kim S, Gan Q, Tetlow IJ, Emes MJ, James MG, Myers AM. 2008. Starch biosynthetic enzymes from developing maize endosperm associate in multisubunit complexes. Plant Physiology 146, 1892-1908.
14. Hiei Y, Ohta S, Komari T, Kumashiro T. 1994. Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. The Plant Journal 6, 271-282.
15. Hunter BG, Beatty MK, Singletary GW, Hamaker BR, Dilkes BP, Larkins BA, Jung R. 2002. Maize opaque endosperm mutations create extensive changes in patterns of gene expression. The Plant Cell 14, 2591-2612.
16. Hwang SK, Nishi A, Satoh H, Okita TW. 2010. Rice endosperm-specific plastidial a-glucan phosphorylase is important for synthesis of short-chain malto-oligosaccharides. Archives of Biochemistry and Biophysics 495, 82-92.
17. Iwata Y, Fedoroff NV, Koizumi N. 2008. Arabidopsis bZIP60 is a proteolysis-activated transcription factor involved in the endoplasmic reticulum stress response. The Plant Cell 20, 3107-3121.
18. Kang H, Park S, Matsuoka M, An G. 2005. White-core endosperm floury endosperm-4 in rice is generated by knockout mutations in the C4-type pyruvate orthophosphate dikinase gene (OsPPDKB). The Plant Journal 42, 901-911.
19. Kaufman RJ. 1999. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes and Development 13, 1211-1233.
20. Kawagoe Y, Kubo A, Satoh H, Takaiwa F, Nakamura Y. 2005. Roles of isoamylase and ADP-glucose pyrophosphorylase in starch granule synthesis in rice endosperm. The Plant Journal 42, 164-174.
21. Kim CS, Hunter BG, Kraft J, Boston RS, Yans S, Jung R, Larkins BA. 2004. A defective signal peptide in a 19-kD a-zein protein causes the unfolded protein response and an opaque endosperm phenotype in the maize De*-B30 mutant. Plant Physiology 134, 380-387.
22. Kleffmann T, Russenberger D, von Zychlinski A, Christopher W, Sjolander K, Gruissem W, Baginsky S. 2004. The Arabidopsis thaliana chloroplast proteome reveals pathway abundance and novel protein functions. Current Biology 14, 354-362.
23. Kossmann J, Visser RGF, Muller-Rober B, Willmitzer L, Sonnewald U. 1991. Cloning and expression analysis of a potato cDNA that encodes branching enzyme: evidence for co-expression of starch biosynthetic genes. Molecular and General Genetics 230, 39-44.
24. Kubo A, Fujita N, Harada K, Matsuda T, Satoh H, Nakamura Y. 1999. The starch-debranching enzymes isoamylase and pullulanase are both involved in amylopectin biosynthesis in rice endosperm. Plant Physiology 121, 399-410.
25. Kubo A, Rahman S, Utsumi Y, et al. 2005. Complementation of sugary-1 phenotype in rice endosperm with the wheat isoamylase1 gene supports a direct role for isoamylase1 in amylopectin biosynthesis. Plant Physiology 137, 43-56.
26. Laboissiere MC, Sturley SL, Raines RT. 1995. The essential function of protein-disulfide isomerase is to unscramble non-native disulfide bonds. Journal of Biological Chemistry 270, 28006-28009.
27. Lending CR, Larkins BA. 1992. Effect of the floury-2 locus on protein body formation during maize endosperm development. Protoplasma 171, 123-133.
28. Liu JX, Srivastava R, Che P, Howell SH. 2007a. Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling. The Plant Journal 51, 897-909.
29. Liu JX, Srivastava R, Che P, Howell SH. 2007b. An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28. The Plant Cell 19, 4111-4119.
30. Liu L, Ma X, Liu S, et al. 2009. Identification and characterization of a novel Waxy allele from a Yunnan rice landrace. Plant Molecular Biology 71, 609-626.
31. Lu DP, Christopher DA. 2006. Immunolocalization of a protein disulfide isomerase to Arabidopsis thaliana chloroplasts and its association with starch biogenesis. International Journal of Plant Sciences 167, 1-9.
32. Myers AM, Morell MK, James MG, Ball SG. 2000. Recent progress toward understanding biosynthesis of the amylopectin crystal. Plant Physiology 12, 989-997.
33. Nishi A, Nakamura Y, Tanaka N, Satoh H. 2001. Biochemical and genetic analysis of the effects of amylose-extender mutation in rice endosperm. Plant Physiology 127, 459-472.
34. Ohdan T, Francisco PB, Sawada T, Hirose T, Terao T, Satoh H, Nakamura Y. 2005. Expression profiling of genes involved in starch synthesis in sink and source organs of rice. Journal of Experimental Botany 56, 3229-3244.
35. Onda Y, Nagamine A, Sakurai M, Kumamaru T, Ogawa M, 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. The Plant Cell 23, 210-223.
36. Oono Y, Wakasa Y, Hirose S, Yang L, Sakuta C, Takaiwa F. 2010. Analysis of ER stress in developing rice endosperm accumulating b-amyloid peptide. Plant Biotechnology 8, 691-718.
37. O'Shea MG, Morell MK. 1996. High resolution slab gel electrophoresis of 8-amino-1,3,6-pyrenetrisulfonic acid (APTS) tagged oligosaccharides using a DNA sequencer. Electrophoresis 17, 681-686.
38. Ozbun JL, Hawker JS, Greenberg E, Lammel C, Preiss J. 1973. Starch synthetase, phosphorylase, ADPglucose pyrophosphorylase, and UDPglucose pyrophosphorylase in developing maize kernels. Plant Physiology 51, 1-5.
39. Satoh H, Shibahara K, Tokunaga T, et al. 2008. Mutation of the plastidial a-glucan phosphorylase gene in rice affects the synthesis and structure of starch in the endosperm. The Plant Cell 20, 1833-1849.
40. Satoh-Cruz M, Crofts AJ, Takemoto-Kuno Y, Sugino A, Washida H, Crofts N, Okita TW, Ogawa M, Satoh H, Kumamaru T. 2010. Protein disulfide isomerase like 1-1 participates in the maturation of proglutelin within the endoplasmic reticulum in rice endosperm. Plant and Cell Physiology 51, 1581-1593.
41. Schupp N, Ziegler P. 2004. The relation of starch phosphorylases to starch metabolism in wheat. Plant and Cell Physiology 45, 1471-1484.
42. She KC, Kusano H, Koizumi K, et al. 2010. A novel factor FLOURY ENDOSPERM 2 is involved in regulation of rice grain size and starch quality. The Plant Cell 22, 3280-3294.
43. St-Pierre B, Brisson N. 1995. Induction of the plastidic starch-phosphorylase gene in potato storage sink tissue. Planta 195, 339-344.
44. Szegezdi E, Logue SE, Gorman AM, Samali A. 2006. Mediators of endoplasmic reticulum stress-induced apoptosis. EMBO Reports 7, 880-885.
45. Takemoto Y, Coughlan SJ, Okita TW, Satoh H, Ogawa M, Kumamaru T. 2002. The rice mutant esp2 greatly accumulates the glutelin precursor and deletes the protein disulfide isomerase. Plant Physiology 128, 1212-1222.
46. Toyota K, Tamura M, Ohdan T, Nakamura Y. 2006. Expression profiling of starch metabolism-related plastidic translocator genes in rice. Planta 223, 248-257.
47. Wakasa Y, Yasuda H, Oono Y, Kawakatsu T, Hirose S, Takahashi H, Hayashi S, Yang L, Takaiwa F. 2011. Expression of ER quality control-related genes in response to changes in BiP1 levels in developing rice endosperm. The Plant Journal 65, 675-689.
48. Wang Y, Ren Y, Liu X, et al. 2010. OsRab5a regulates endomembrane organization and storage protein trafficking in rice endosperm cells. The Plant Journal 64, 812-824.
49. Wang Y, Zhu S, Liu S, et al. 2009. The vacuolar processing enzyme OsVPE1 is required for efficient glutelin processing in rice. The Plant Journal 58, 606-617.
50. Wilkinson B, Gilbert HF. 2004. Protein disulfide isomerase. Biochimica et Biophysica Acta 1699, 35-44.
51. Yasuda H, Hirose S, Kawakatsu T, Wakasa Y, Takaiwa F. 2009. Overexpression of BiP has inhibitory effects on the accumulation of seed storage proteins in endosperm cells of rice. Plant and Cell Physiology 50, 1532-1543.