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Do rice suspension-cultured cells treated with abscisic acid mimic developing seeds?

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Abstract

Starch synthesis is activated in the endosperm during seed development and also in rice suspension cells cultured with abscisic acid. In the anticipation that the mechanisms of starch synthesis are similar between the endosperm and the suspension cells cultured with abscisic acid, expression of genes involved in starch synthesis was evaluated in the suspension cells after abscisic acid treatment. However, it was found that the regulatory mechanism of starch synthesis in the suspension cells cultured with abscisic acid was different from that in developing seeds. Expression analyses of genes involved in oil bodies, which accumulate in the embryo and aleurone layer, and seed storage proteins, which accumulate mainly in the endosperm, showed that the former were activated in the suspension cells cultured with abscisic acid, but the latter were not. Master regulators for embryogenesis, OsVP1 (homologue of AtABI3) and OsLFL1 (homologue of AtFUS3 or AtLFL2), were expressed in the suspension cells at levels comparable to those in the embryo. From these results, it is suggested that interactions between regulators and abscisic acid control the synthesis of phytic acid and oil bodies in the cultured cells and embryo. We suggest that the system of suspension cells cultured with abscisic acid helps to reveal the mechanisms of phytic acid and oil body synthesis in embryo.

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References

  • Agboola S, Ng D, Mills D (2005) Characterisation and functional properties of Australian rice protein isolates. J Cereal Sci 41:283–290

    Article  CAS  Google Scholar 

  • Akihiro T, Mizuno K, Fujimura T (2005) Gene expression of ADP-glucose pyrophosphorylase and starch contents in rice cultured cells are cooperatively regulated by sucrose and ABA. Plant Cell Physiol 46:937–946

    Article  CAS  PubMed  Google Scholar 

  • Akihiro T, Umezawa T, Ueki C, Lobna BM, Mizuno K, Ohta M, Fujimura T (2006) Genome wide cDNA-AFLP analysis of genes rapidly induced by combined sucrose and ABA treatment in rice cultured cells. FEBS Lett 580:5947–5952

    Article  CAS  PubMed  Google Scholar 

  • Baud S, Mendoza MS, To A, Harscoët E, Lepiniec L, Dubreucq B (2007) WRINKLED1 specifies the regulatory action of LEAFY COTYLEDON2 towards fatty acid metabolism during seed maturation in Arabidopsis. Plant J 50:825–838

    Article  CAS  PubMed  Google Scholar 

  • Cagampang GB, Cruz LJ, Espiritu SG, Santiage RG, Juliano BO (1966) Studies on the extraction and composition of rice proteins. Cereal Chem 43:145–155

    CAS  Google Scholar 

  • Cernac A, Benning C (2004) WRINKLED1 encodes an AP2/EREB domain protein involved in the control of storage compound biosynthesis in Arabidopsis. Plant J 40:575–585

    Article  CAS  PubMed  Google Scholar 

  • Chen DH, Chyan CL, Jiang PL, Chen CS, Tzen JTC (2012) The same oleosin isoforms are present in oil bodies of rice embryo and aleurone layer while caleosin exists only in those of the embryo. Plant Physiol Biochem 60:18–24

    Article  CAS  PubMed  Google Scholar 

  • Choudhury NH, Juliano BO (1980) Lipids in developing and mature rice grain. Phytochem 19:1063–1069

    Article  CAS  Google Scholar 

  • Chu CC, Wang CC, Sun CS, Hsu C, Yin KC, Chu CY, Bi FY (1975) Establishment of an efficient medium for anther culture of rice through comparative experiments on the nitrogen sources. Sci China Math 18:659–668

    Google Scholar 

  • Chuang RL, Chen JC, Chu J, Tzen JT (1996) Characterization of seed oil bodies and their surface oleosin isoforms from rice embryos. J Biochem 120:74–81

    Article  CAS  PubMed  Google Scholar 

  • Crowe AJ, Abenes M, Plant A, Moloney MM (2000) The seed-specific transactivator, ABI3, induces oleosin gene expression. Plant Sci 151:171–181

    Article  CAS  PubMed  Google Scholar 

  • Finkelstein RR, Gampala SSL, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14:S15–S45

    CAS  PubMed Central  PubMed  Google Scholar 

  • Focks N, Benning C (1998) wrinkled1: a novel, low-seed-oil mutant of Arabidopsis with a deficiency in the seed-specific regulation of carbohydrate metabolism. Plant Physiol 118:91–101

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Frandsen GI, Mundy J, Tzen JTC (2001) Oil bodies and their associated proteins, oleosin and caleosin. Physiol Plant 112:301–307

    Article  CAS  PubMed  Google Scholar 

  • Fu FF, Xue HW (2010) Coexpression analysis identifies rice starch Regulator1, a rice AP2/EREBP family transcription factor, as a novel rice starch biosynthesis regulator. Plant Physiol 154:927–938

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gutierrez L, Van Wuytswinkel O, Castelain M, Bellini C (2007) Combined networks regulating seed maturation. Trends Plant Sci 12:294–300

    Article  CAS  PubMed  Google Scholar 

  • Hattori T, Terada T, Hamasuna ST (1994) Sequence and functional analyses of the rice gene homologous to the maize Vp1. Plant Mol Biol 24:805–810

    Article  CAS  PubMed  Google Scholar 

  • Ichihara K, Kobayashi N, Saito K (2003) Lipid synthesis and acyl-CoA synthetase in developing rice seeds. Lipids 38:881–884

    Article  CAS  PubMed  Google Scholar 

  • Iwai T, Takahashi M, Oda K, Terada Y, Yoshida KT (2012) Dynamic changes in the distribution of minerals in relation to phytic acid accumulation during rice seed development. Plant Physiol 160:2007–2014

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jain M, Nijhawan A, Tyagi AK, Khurana JP (2006) Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochem Biophys Res Commun 345:646–651

    Article  CAS  PubMed  Google Scholar 

  • Jeon JS, Ryoo N, Hahn TR, Walia H, Nakamura Y (2010) Starch biosynthesis in cereal endosperm. Plant Physiol Biochem 48:383–392

    Article  CAS  PubMed  Google Scholar 

  • Kagaya Y, Okuda R, Ban A, Toyoshima R, Tsutsumida K, Usui H, Yamamoto A, Hattori T (2005) Indirect ABA-dependent regulation of seed storage protein genes by FUSCA3 transcription factor in Arabidopsis. Plant Cell Physiol 46:300–311

    Article  CAS  PubMed  Google Scholar 

  • Kawakatsu T, Yamamoto MP, Hirose S, Yano M, Takaiwa F (2008) Characterization of a new rice glutelin gene GluD-1 expressed in the starchy endosperm. J Exp Bot 59:4233–4245

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kawakatsu T, Yamamoto MP, Touno SM, Yasuda H, Takaiwa F (2009) Compensation and interaction between RISBZ1 and RPBF during grain filling in rice. Plant J 59:908–920

    Article  CAS  PubMed  Google Scholar 

  • 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 Physiol 121:399–410

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lee SK, Hwang SK, Han M et al (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

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Luthe DS (1983) Storage protein accumulation in developing rice (Oryza sativa L.) seeds. Plant Sci Lett 32:147–158

    Article  CAS  Google Scholar 

  • Matsuno K, Fujimura T (2014) Induction of phytic acid synthesis by abscisic acid in suspension-cultured cells of rice. Plant Sci 217–218:152–157

    Article  PubMed  Google Scholar 

  • Meinke DW, Franzmann LH, Nickle TC, Yeung EC (1994) Leafy cotyledon mutants of Arabidopsis. Plant Cell 6:1049–1064

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nakagawa H, Ohkura E, Ohmiya K, Hattori T (1996) The seed-specific transcription factor VP1 (OSVP1) is expressed in rice suspension-cultured cells. Plant Cell Physiol 37:355–362

    Article  CAS  PubMed  Google Scholar 

  • Nakase M, Hotta H, Adachi T, Aoki N, Nakamura R, Masumura T, Tanaka K, Matsuda T (1996) Cloning of the rice seed α-globulin-encoding gene: sequence similarity of the 5′-flanking region to those of the genes encoding wheat high-molecular-weight glutenin and barley D hordein. Gene 170:223–226

    Article  CAS  PubMed  Google Scholar 

  • Nakashima K, Yamaguchi-Shinozaki K (2013) ABA signaling in stress-response and seed development. Plant Cell Rep 32:959–970

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • O’Dell BL, De Boland AR, Koirtyohann SR (1972) Distribution of phytate and nutritionally important elements among the morphological components of cereal grains. J Agric Food Chem 20:718–723

    Article  Google Scholar 

  • Ogawa M, Tanaka K, Kasai Z (1979) Accumulation of phosphorus, magnesium and potassium in developing rice grains: followed by electron microprobe X-ray analysis focusing on the aleurone layer. Plant Cell Physiol 20:19–27

    CAS  Google Scholar 

  • Ohdan T, Francisco PB Jr, 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. J Exp Bot 56:3229–3244

    Article  CAS  PubMed  Google Scholar 

  • Peng LT, Shi ZY, Li L, Shen GZ, Zhang JL (2007) Ectopic expression of OsLFL1 in rice represses Ehd1 by binding on its promoter. Biochem Biophys Res Commun 360:251–256

    Article  CAS  PubMed  Google Scholar 

  • Peng LT, Shi ZY, Li L, Shen GZ, Zhang JL (2008) Overexpression of transcription factor OsLFL1 delays flowering time in Oryza sativa. J Plant Physiol 165:876–885

    Article  CAS  PubMed  Google Scholar 

  • Phillips J, Artsaenko O, Fiedler U, Horstmann C, Mock HP, Müntz K, Conrad U (1997) Seed-specific immunomodulation of abscisic acid activity induces a developmental switch. EMBO J 16:4489–4496

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pouvreau B, Baud S, Vernoud V, Morin V, Py C, Gendrot G, Pichon JP, Rouster J, Paul W, Rogowsky PM (2011) Duplicate maize Wrinkled1 transcription factors activate target genes involved in seed oil biosynthesis. Plant Physiol 156:674–686

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Qu LQ, 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

    Article  CAS  Google Scholar 

  • Sano Y, Katsumata M, Okuno K (1986) Genetic studies of speciation in cultivated rice. 5. Inter- and intraspecific differentiation in the waxy gene expression of rice. Euphytica 35:1–9

    Article  Google Scholar 

  • Sato Y, Antonio BA, Namiki N, Takehisa H, Minami H, Kamatsuki K, Sugimoto K, Shimizu Y, Hirochika H, Nagamura Y (2011) RiceXPro: a platform for monitoring gene expression in japonica rice grown under natural field conditions. Nucleic Acids Res 39:D1141–D1148

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sato Y, Takehisa H, Kamatsuki K, Minami H, Namiki N, Ikawa H, Ohyanagi H, Sugimoto K, Antonio BA, Nagamura Y (2013) RiceXPro version 3.0: expanding the informatics resource for rice transcriptome. Nucleic Acids Res 41:D1206–D1213

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Satoh H, Nishi A, Yamashita K, Takemoto Y, Tanaka Y, Hosaka Y, Sakurai A, Fujita N, Nakamura Y (2003) Starch-branching enzyme I-deficient mutation specifically affects the structure and properties of starch in rice endosperm. Plant Physiol 133:1111–1121

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shen B, Allen WB, Zheng P, Li C, Glassman K, Ranch J, Nubel D, Tarczynski MC (2010) Expression of ZmLEC1 and ZmWRI1 increases seed oil production in maize. Plant Physiol 153:980–987

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shewry PR, Halford NG (2002) Cereal seed storage proteins: structures, properties and role in grain utilization. J Exp Bot 53:947–958

    Article  CAS  PubMed  Google Scholar 

  • Suzuki M, Ketterling MG, Li QB, McCarty DR (2003) Viviparous1 alters global gene expression patterns through regulation of abscisic acid signaling. Plant Physiol 132:1664–1677

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tang T, Xie H, Wang Y, Lü B, Liang J (2009) The effect of sucrose and abscisic acid interaction on sucrose synthase and its relationship to grain filling of rice (Oryza sativa L.). J Exp Bot 60:2641–2652

    Article  CAS  PubMed  Google Scholar 

  • To A, Joubès J, Barthole G, Lécureuil A, Scagnelli A, Jasinski S, Lepiniec L, Baud S (2012) WRINKLED transcription factors orchestrate tissue-specific regulation of fatty acid biosynthesis in Arabidopsis. Plant Cell 24:5007–5023

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Umemoto T, Yano M, Satoh H, Shomura A, Nakamura Y (2002) Mapping of a gene responsible for the difference in amylopectin structure between japonica-type and indica-type rice varieties. Theor Appl Genet 104:1–8

    Article  CAS  PubMed  Google Scholar 

  • Villareal RM, Juliano BO (1978) Properties of glutelin from mature and developing rice grain. Phytochem 17:177–182

    Article  CAS  Google Scholar 

  • Wang F, Perry SE (2013) Identification of direct targets of FUSCA3, a key regulator of Arabidopsis seed development. Plant Physiol 161:1251–1264

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang JC, Xu H, Zhu Y, Liu QQ, Cai XL (2013) OsbZIP58, a basic leucine zipper transcription factor, regulates starch biosynthesis in rice endosperm. J Exp Bot 64:3453–3466

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wu C, Adachi T, Hatano T, Washida H, Suzuki A, Takaiwa F (1998) Promoters of rice seed storage protein genes direct endosperm-specific gene expression in transgenic rice. Plant Cell Physiol 39:885–889

    Article  CAS  Google Scholar 

  • Xie Z, Li X, Glover BJ, Bai S, Rao GY, Luo J, Yang J (2008) Duplication and functional diversification of HAP3 genes leading to the origin of the seed-developmental regulatory gene, LEAFY COTYLEDON1 (LEC1), in nonseed plant genomes. Mol Biol Evol 25:1581–1592

    Article  CAS  PubMed  Google Scholar 

  • Yamagata H, Sugimoto T, Tanaka K, Kasai Z (1982) Biosynthesis of storage proteins in developing rice seeds. Plant Physiol 70:1094–1100

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yamamoto MP, Onodera Y, Touno SM, Takaiwa F (2006) Synergism between RPBF Dof and RISBZ1 bZIP activators in the regulation of rice seed expression genes. Plant Physiol 141:1694–1707

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yamamoto A, Kagaya Y, Usui H, Hobo T, Takeda S, Hattori T (2010) Diverse roles and mechanisms of gene regulation by the Arabidopsis seed maturation master regulator FUS3 revealed by microarray analysis. Plant Cell Physiol 51:2031–2046

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Zhang J, Wang Z, Liu K, Wang P (2006) Post-anthesis development of inferior and superior spikelets in rice in relation to abscisic acid and ethylene. J Exp Bot 57:149–160

    Article  CAS  PubMed  Google Scholar 

  • Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Routine procedure for growing rice plants in culture solution. Laboratory manual for physiological studies of rice, 3rd edn. International Rice Research Institute, Los Baños, pp 61–66

    Google Scholar 

  • Zhu G, Ye N, Yang J, Peng X, Zhang J (2011) Regulation of expression of starch synthesis genes by ethylene and ABA in relation to the development of rice inferior and superior spikelets. J Exp Bot 62:3907–3916

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

We thank Morio Kato for providing the developing rice seeds from Agricultural and Forestry Research Center.

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  1. Graduate School of Life and Environmental Sciences, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki, 305-8577, Japan

    Koya Matsuno & Tatsuhito Fujimura

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  1. Koya Matsuno
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  2. Tatsuhito Fujimura
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Correspondence to Koya Matsuno.

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Communicated by A. K. Tyagi.

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Matsuno, K., Fujimura, T. Do rice suspension-cultured cells treated with abscisic acid mimic developing seeds?. Mol Genet Genomics 290, 1551–1562 (2015). https://doi.org/10.1007/s00438-015-1018-6

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