Abstract
ADP-glucose pyrophosphorylase (AGP) catalyzes the first committed step of starch biosynthesis in higher plants. We previously isolated two rice mutants, osagps2 and osagpl2, which have starch-deficient endosperms and lack the AGP small and large subunits, respectively. In this study, we used two-dimensional gel electrophoresis and peptide mass fingerprinting to identify differentially expressed proteins in the osagps2 and osagpl2 endosperms. We found that the osagps2 and osagpl2 endosperms exhibited reduced levels of glutelins and globulins (the major seed storage proteins), protein disulfide isomerases, and the dnaK-type endoplasmic reticulum chaperone BiP. Interestingly, the osagps2 and osagpl2 endosperms had much lower levels of malate dehydrogenase and alanine aminotransferase compared with wild type endosperm, which likely function in maintaining an adequate ATP supply for starch biosynthesis in seed endosperms that are exposed to low oxygen conditions. Furthermore, metabolomics analysis showed that the levels of free amino acids and soluble sugars were significantly increased in the osagps2 and osagpl2 endosperms. These results demonstrate that carbon and nitrogen metabolisms are tightly coordinated to ensure the proper development of rice seed endosperm.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ballicora MA, Iglesias AA, Preiss J (2004) ADP-glucose pyrophosphorylase: a regulatory enzyme for plant starch synthesis. Photosynth Res 79:1–24
Chen R, Zhao X, Shao Z, Wei Z, Wang Y, Zhu L, Zhao J, Sun M, He R, He G (2007) Rice UDP-glucose pyrophosphorylase1 is essential for pollen callose deposition and its cosuppression results in a new type of thermosensitive genic male sterility. The Plant Cell 19:847–861
Fitzgerald MA, McCouch SR, Hall RD (2009) Not just a grain of rice: the quest for quality. Trends Plant Sci 14:133–139
Kaplan F, Kopka J, Haskell DW, Zhao W, Schiller KC, Gatzke N, Sung DY, Guy CL (2004) Exploring the temperature-stress metabolome of Arabidopsis. Plant Physiol 136:4159–4168
Lee SK, Hwang SK, Han M, Eom JS, Kang HG, Han Y, Choi SB, Cho MH, Bhoo SH, An G, Hahn TR, Okita TW, Jeon JS (2007) Identification of the ADP-glucose pyrophosphorylase isoforms essential for starch synthesis in the leaf and seed endosperm of rice (Oryza sativa L.). Plant Mol Biol 65:531–546
Liao JL, Zhou HW, Zhang HY, Zhong PA, Huang YJ (2013) Comparative proteomic analysis of differentially expressed proteins in the early milky stage of rice grains during high temperature stress. J Exp Bot 65:655–671
Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat Protoc 1:387–396
Nelson OE (1982) Genetic control of polysaccharide and storage protein synthesis in endosperms of barley, maize and sorghum. In Y Pomeranz, ed, Advances in cereal science and technology, Vol 3. American Association of Cereal Chemists, St. Paul, pp 41–71
Onda Y, Kumamaru T, Kawagoe Y (2009) ER membrane-localized oxidoreductase Ero1 is required for disulfide bond formation in the rice endosperm. Proc Natl Acad Sci USA 106:14156–14161
Okita TW, Nakata PA, Anderson JM, Sowokinos J, Morell M, Preiss J (1990) The subunit structure of potato tuber ADP glucose pyrophosphorylase. Plant Physiol 93:785–790
Phee BK, Cho JH, Park S, Jung JH, Lee YH, Jeon JS, Bhoo SH, Hahn TR (2004) Proteomic analysis of the response of Arabidopsis chloroplast proteins to high light stress. Proteomics 4:3560–3568
Phee BK, Park S, Cho JH, Jeon JS, Bhoo SH, Hahn TR (2007) Comparative proteomic analysis of blue light signaling components in the Arabidopsis cryptochrome 1 mutant. Mol Cells 23:154–160
Qu le Q, Takaiwa F (2004) Evaluation of tissue specificity and expression strength of rice seed component gene promoters in transgenic rice. Plant Biotechnol J 2:113–125
Rolletschek H, Weschke W, Weber H, Wobus U, Borisjuk L (2004) Energy state and its control on seed development: starch accumulation is associated with high ATP and steep oxygen gradients within barley grains. J Exp Bot 55:1351–1359
Rolletschek H, Melkus G, Grafahrend-Belau E, Fuchs J, Heinzel N, Schreiber F, Jakob PM, Borisjuk L (2011) Combined noninvasive imaging and modeling approaches reveal metabolic compartmentation in the barley endosperm. Plant Cell 23:3041–3054
Takaiwa F, Ogawa M, Okita TW (1999) Rice glutelins, In PR Shewry, R Casey, eds, Seed proteins, pp 401–425
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 Physiol 128:1212–1222
Tanaka K, Sugimoto T, Ogawa M, Kasi Z (1980) Isolation and characterization of two types of protein bodies in the rice endosperm. Agric Biol Chem 44:1633–1639
Ufaz S, Galili G (2008) Improving the content of essential amino acids in crop plants: goals and opportunities. Plant Physiol 147:954–961
Wakasa Y, Yang L, Hirose S, Takaiwa F (2009) Expression of unprocessed glutelin precursor alters polymerization without affecting trafficking and accumulation. J Exp Bot 60:3503–3511
Winter H, Huber SC (2000) Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. Crit Rev Biochem Mol Biol 35:253–289
Xu SB, Li T, Deng ZY, Chong K, Xue Y, Wang T (2008) Dynamic proteomic analysis reveals a switch between central carbon metabolism and alcoholic fermentation in rice filling grains. Plant Physiol 148:908–925
Yamagata H, Tanaka K (1986) The site of synthesis and accumulation of rice storage proteins. Plant Cell Physiol 27:135–145
Yamakawa H, Hirose T, Kuroda M, Yamaguchi T (2007) Comprehensive expression profiling of rice grain filling-related genes under high temperature using DNA microarray. Plant Physiol 144:258–277
Yamakawa H, Hakata M (2010) Atlas of rice grain filling-related metabolism under high temperature: joint analysis of metabolome and transcriptome demonstrated inhibition of starch accumulation and induction of amino acid accumulation. Plant Cell Physiol 51:795–809
Yi J, An G (2013) Utilization of T-DNA tagging lines in rice. J Plant Biol 56:85–90
Author information
Authors and Affiliations
Corresponding author
Additional information
These authors contributed equally to this work.
Rights and permissions
About this article
Cite this article
Lee, DW., Lee, SK., Phee, BK. et al. Proteomic analysis of the rice endosperm starch-deficient mutants osagps2 and osagpl2 . J. Plant Biol. 58, 252–258 (2015). https://doi.org/10.1007/s12374-015-0160-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12374-015-0160-3