Abstract
Key message
FLO15encodes a plastidic glyoxalase I protein, OsGLYI7, which affects compound starch granule formation and starch synthesis in rice endosperm.
Abstract
Starch synthesis in rice (Oryza sativa) endosperm is a sophisticated process, and its underlying molecular machinery still remains to be elucidated. Here, we identified and characterized two allelic rice floury endosperm 15 (flo15) mutants, both with a white-core endosperm. The flo15 grains were characterized by defects in compound starch granule development, along with decreased starch content. Map-based cloning of the flo15 mutants identified mutations in OsGLYI7, which encodes a glyoxalase I (GLYI) involved in methylglyoxal (MG) detoxification. The mutations of FLO15/OsGLYI7 resulted in increased MG content in flo15 developing endosperms. FLO15/OsGLYI7 localizes to the plastids, and the in vitro GLYI activity derived from flo15 was significantly decreased relative to the wild type. Moreover, the expression of starch synthesis-related genes was obviously altered in the flo15 mutants. These findings suggest that FLO15 plays an important role in compound starch granule formation and starch synthesis in rice endosperm.
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References
Ballicora MA, Iglesias AA, Preiss J (2004) ADP-glucose pyrophosphorylase: a regulatory enzyme for plant starch synthesis. Photosynth Res 79:1–24
Cakir B, Shiraishi S, Tuncel A, Matsusaka H, Satoh R, Singh S, Crofts N, Hosaka Y, Fujita N, Hwang SK, Satoh H, Okita TW (2016) Analysis of the rice ADP-glucose transporter (OsBT1) indicates the presence of regulatory processes in the amyloplast stroma that control ADP-glucose flux into starch. Plant Physiol 170:1271–1283
Chen S, Tao L, Zeng L, Vega-Sanchez ME, Umemura K, Wang GL (2006) A highly efficient transient protoplast system for analyzing defence gene expression and protein-protein interactions in rice. Mol Plant Pathol 7:417–427
Crook EM, Law K (1952) Glyoxalase; the role of the components. Biochem J 52:492–499
Duan E, Wang Y, Liu L, Zhu J, Zhong M, Zhang H, Li S, Ding B, Zhang X, Guo X, Jiang L, Wan J (2016) Pyrophosphate: fructose-6-phosphate 1-phosphotransferase (PFP) regulates carbon metabolism during grain filling in rice. Plant Cell Rep 35:1321–1331
Dupont FM (2008) Metabolic pathways of the wheat (Triticum aestivum) endosperm amyloplast revealed by proteomics. BMC Plant Biol 8:39–56
Fujita N, Kubo A, Suh DS, Wong KS, Jane JL, Ozawa K, Takaiwa F, Inaba Y, Nakamura Y (2003) Antisense inhibition of isoamylase alters the structure of amylopectin and the physicochemical properties of starch in rice endosperm. Plant Cell Physiol 44:607–618
Fujita N, Yoshida M, Kondo T, Saito K, Utsumi Y, Tokunaga T, Nishi A, Satoh H, Park JH, Jane JL, Miyao A, Hirochika H, Nakamura Y (2007) Characterization of SSIIIa-deficient mutants of rice: the function of SSIIIa and pleiotropic effects by SSIIIa deficiency in the rice endosperm. Plant Physiol 144:2009–2023
Han X, Wang Y, Liu X, Jiang L, Ren Y, Liu F, Peng C, Li J, Jin X, Wu F, Wang J, Guo X, Zhang X, Cheng Z, Wan J (2012) The failure to express a protein disulphide isomerase-like protein results in a floury endosperm and an endoplasmic reticulum stress response in rice. J Exp Bot 63:121–130
Hanashiro I, Itoh K, Kuratomi Y, Yamazaki M, Igarashi T, Matsugasako J, Takeda Y (2008) Granule-bound starch synthase I is responsible for biosynthesis of extra-long unit chains of amylopectin in rice. Plant Cell Physiol 49:925–933
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. Plant J 6:271–282
Hoque TS, Uraji M, Tuya A, Nakamura Y, Murata Y (2012) Methylglyoxal inhibits seed germination and root elongation and up-regulates transcription of stress-responsive genes in ABA-dependent pathway in Arabidopsis. Plant Biol (Stuttg) 14:854–858
Hossain MA, Fujita M (2009) Purification of glyoxalase I from onion bulbs and molecular cloning of its cDNA. Biosci Biotechnol Biochem 73:2007–2013
Kalapos MP (1999) Methylglyoxal in living organisms: chemistry, biochemistry, toxicology and biological implications. Toxicol Lett 110:145–175
Kang HG, Park S, Matsuoka M, An G (2005) White-core endosperm floury endosperm-4 in rice is generated by knockout mutations in the C-type pyruvate orthophosphate dikinase gene (OsPPDKB). Plant J 42:901–911
Kaur C, Vishnoi A, Ariyadasa TU, Bhattacharya A, Singla-Pareek SL, Sopory SK (2013) Episodes of horizontal gene-transfer and gene-fusion led to co-existence of different metal-ion specific glyoxalase I. Sci Rep 3:3076–3085
Kaur C, Singlapareek SL, Sopory SK (2014) Glyoxalase and methylglyoxal as biomarkers for plant stress tolerance. Crit Rev Plant Sci 33:429–456
Kaur C, Sharma S, Singlapareek SL, Sopory SK (2016) Methylglyoxal detoxification in plants: role of glyoxalase pathway. Ind J Plant Physiol 21(4):377–390
Kaur C, Sharma S, Hasan MR, Pareek A, Singla-Pareek SL, Sopory SK (2017a) Characteristic variations and similarities in biochemical, molecular, and functional properties of glyoxalases across prokaryotes and eukaryotes. Int J Mol Sci 18:250–270
Kaur C, Tripathi AK, Nutan KK, Sharma S, Ghosh A, Tripathi JK, Pareek A, Singla-Pareek SL, Sopory SK (2017b) A nuclear-localized rice glyoxalase I enzyme, OsGLYI-8, functions in the detoxification of methylglyoxal in the nucleus. Plant J 89:565–576
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. Plant J 42:164–174
Li S, Wei X, Ren Y, Qiu J, Jiao G, Guo X, Tang S, Wan J, Hu P (2017) OsBT1 encodes an ADP-glucose transporter involved in starch synthesis and compound granule formation in rice endosperm. Sci Rep 7:40124–40136
Lin J, Nazarenus TJ, Frey JL, Liang X, Wilson MA, Stone JM (2011) A plant DJ-1 homolog is essential for Arabidopsis thaliana chloroplast development. PLoS One 6:e23731–e23738
Liu TT, Shannon JC (1981) Measurement of Metabolites Associated with Nonaqueously Isolated Starch Granules from Immature Zea mays L. endosperm. Plant Physiol 67:525–529
Liu X, Guo T, Wan X, Wang H, Zhu M, Li A, Su N, Shen Y, Mao B, Zhai H, Mao L, Wan J (2010) Transcriptome analysis of grain-filling caryopses reveals involvement of multiple regulatory pathways in chalky grain formation in rice. BMC Genom 11:730–744
Martin C, Smith AM (1995) Starch biosynthesis. Plant Cell 7:971–985
Matsushima R, Maekawa M, Fujita N, Sakamoto W (2010) A rapid, direct observation method to isolate mutants with defects in starch grain morphology in rice. Plant Cell Physiol 51:728–741
Matsushima R, Maekawa M, Kusano M, Kondo H, Fujita N, Kawagoe Y, Sakamoto W (2014) Amyloplast-localized SUBSTANDARD STARCH GRAIN4 protein influences the size of starch grains in rice endosperm. Plant Physiol 164:623–636
Matsushima R, Maekawa M, Kusano M, Tomita K, Kondo H, Nishimura H, Crofts N, Fujita N, Sakamoto W (2016) Amyloplast membrane protein SUBSTANDARD STARCH GRAIN6 controls starch grain size in rice endosperm. Plant Physiol 170:1445–1459
Mustafiz A, Singh AK, Pareek A, Sopory SK, Singla-Pareek SL (2011) Genome-wide analysis of rice and Arabidopsis identifies two glyoxalase genes that are highly expressed in abiotic stresses. Funct Integr Genom 11:293–305
Mustafiz A, Ghosh A, Tripathi AK, Kaur C, Ganguly AK, Bhavesh NS, Tripathi JK, Pareek A, Sopory SK, Singla-Pareek SL (2014) A unique Ni2+-dependent and methylglyoxal-inducible rice glyoxalase I possesses a single active site and functions in abiotic stress response. Plant J 78:951–963
Nishi A, Nakamura Y, Tanaka N, Satoh H (2001) Biochemical and genetic analysis of the effects of amylose-extender mutation in rice endosperm. Plant Physiol 127:459–472
Peng C, Wang Y, Liu F, Ren Y, Zhou K, Lv J, Zheng M, Zhao S, Zhang L, Wang C, Jiang L, Zhang X, Guo X, Bao Y, Wan J (2014) FLOURY ENDOSPERM6 encodes a CBM48 domain-containing protein involved in compound granule formation and starch synthesis in rice endosperm. Plant J 77:917–930
Plaxton WC (1996) The organization and regulation of plant glycolysis. Annu Rev Plant Physiol Plant Mol Biol 47:185–214
Racker E (1951) The mechanism of action of glyoxalase. J Biol Chem 190:685–696
Richard JP (1993) Mechanism for the formation of methylglyoxal from triosephosphates. Biochem Soc Trans 21:549–553
Rolletschek H, Borisjuk L, Koschorreck M, Wobus U, Weber H (2002) Legume embryos develop in a hypoxic environment. J Exp Bot 53:1099–1107
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
Ryoo N, Yu C, Park CS, Baik MY, Park IM, Cho MH, Bhoo SH, An G, Hahn TR, Jeon JS (2007) Knockout of a starch synthase gene OsSSIIIa/Flo5 causes white-core floury endosperm in rice (Oryza sativa L.). Plant Cell Rep 26:1083–1095
Sankaranarayanan S, Jamshed M, Kumar A, Skori L, Scandola S, Wang T, Spiegel D, Samuel MA (2017) Glyoxalase goes green: the expanding roles of glyoxalase in plants. Int J Mol Sci 18:898–912
Shan QW, Wang YP, Li J, Zhang Y, Chen KL, Liang Z, Zhang K, Liu JX, Xi JZJ, Qiu JL, Gao CX (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 31:686–688
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739
Tang XJ, Peng C, Zhang J, Cai Y, You XM, Kong F, Yan HG, Wang GX, Wang L, Jin J, Chen WW, Chen XG, Ma J, Wang P, Jiang L, Zhang WW, Wan JM (2016) ADP-glucose pyrophosphorylase large subunit 2 is essential for storage substance accumulation and subunit interactions in rice endosperm. Plant Sci 249:70–83
Thornalley PJ (1990) The glyoxalase system: new developments towards functional characterization of a metabolic pathway fundamental to biological life. Biochem J 269:1–11
Wei X, Jiao G, Lin H, Sheng Z, Shao G, Xie L, Tang S, Xu Q, Hu P (2017) GRAIN INCOMPLETE FILLING 2 regulates grain filling and starch synthesis during rice caryopsis development. J Integr Plant Biol 59:134–153
Zeng Z, Xiong F, Yu X, Gong X, Luo J, Jiang Y, Kuang H, Gao B, Niu X, Liu Y (2016) Overexpression of a glyoxalase gene, OsGly I, improves abiotic stress tolerance and grain yield in rice (Oryza sativa L.). Plant Physiol Biochem 109:62–71
Zhang MZ, Fang JH, Yan X, Liu J, Bao JS, Fransson G, Andersson R, Jansson C, Aman P, Sun C (2012) Molecular insights into how a deficiency of amylose affects carbon allocation–carbohydrate and oil analyses and gene expression profiling in the seeds of a rice waxy mutant. BMC Plant Biol 12:230–247
Zhang XQ, Hou P, Zhu HT, Li GD, Liu XG, Xie XM (2013) Knockout of the VPS22 component of the ESCRT-II complex in rice (Oryza sativa L.) causes chalky endosperm and early seedling lethality. Mol Biol Rep 40:3475–3481
Zhang L, Ren Y, Lu B, Yang C, Feng Z, Liu Z, Chen J, Ma W, Wang Y, Yu X, Wang Y, Zhang W, Wang Y, Liu S, Wu F, Zhang X, Guo X, Bao Y, Jiang L, Wan J (2016) FLOURY ENDOSPERM7 encodes a regulator of starch synthesis and amyloplast development essential for peripheral endosperm development in rice. J Exp Bot 67:633–647
Acknowledgements
This research was supported by the Key Laboratory of Biology, Genetics and Breeding of Japonica Rice in Mid-lower Yangtze River, Ministry of Agriculture, P. R. China, and Jiangsu Collaborative Innovation Center for Modern Crop Production, and grants from The National Key Research and Development Program of China (2017YFD0100404), Jiangsu Science and Technology Development Program (BE2015355-1, BE2017368), and Agricultural Science and Technology Innovation Fund project of Jiangsu Province (CX(16)1029).
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You, X., Zhang, W., Hu, J. et al. FLOURY ENDOSPERM15 encodes a glyoxalase I involved in compound granule formation and starch synthesis in rice endosperm. Plant Cell Rep 38, 345–359 (2019). https://doi.org/10.1007/s00299-019-02370-9
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DOI: https://doi.org/10.1007/s00299-019-02370-9