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Fine mapping and candidate gene analysis of the floury endosperm gene, FLO(a), in rice

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Molecules and Cells

Abstract

In addition to its role as an energy source for plants, animals and humans, starch is also an environmentally friendly alternative to fossil fuels. In rice, the eating and cooking quality of the grain is determined by its starch properties. The floury endosperm of rice has been explored as an agronomical trait in breeding and genetics studies. In the present study, we characterized a floury endosperm mutant, flo(a), derived from treatment of Oryza sativa ssp. japonica cultivar Hwacheong with MNU. The innermost endosperm of the flo(a) mutant exhibited floury characteristics while the outer layer of the endosperm appeared normal. Starch granules in the flo(a) mutant formed a loosely-packed crystalline structure and X-ray diffraction revealed that the overall crystallinity of the starch was decreased compared to wild-type. The FLO(a) gene was isolated via a map-based cloning approach and predicted to encode the tetratricopeptide repeat domaincontaining protein, OsTPR. Three mutant alleles contain a nucleotide substitution that generated one stop codon or one splice site, respectively, which presumably disrupts the interaction of the functionally conserved TPR motifs. Taken together, our map-based cloning approach pinpointed an OsTPR as a strong candidate of FLO(a), and the proteins that contain TPR motifs might play a significant role in rice starch biosynthetic pathways.

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References

  • Bae, J.M., Giroux, M., and Hannah, L.C. (1990). Cloning and characterization of the brittle-2 gene of maize. Maydica 35, 317–322.

    Google Scholar 

  • Ball, S.G., and Morell, M.K. (2003). From bacterial glycogen to starch, understanding the biogenesis of the plant starch granule. Annu. Rev. Plant Biol. 54, 207–233.

    Article  CAS  PubMed  Google Scholar 

  • Bao, J., Kong, X., Xie, J., and Xu, L. (2004). Analysis of genotypic and environmental effects on rice starch. 1. Apparent amylase content, pasting viscosity, and gel texture. J. Agric. Food Chem. 52, 6010–6016.

    Article  CAS  PubMed  Google Scholar 

  • Bhave, M.R., Lawrence, S., Barton, C., and Hannah, L.C. (1990). Identification and molecular characterization of shrunken-2 cDNA clones of maize. Plant Cell 2, 581–588.

    Article  CAS  PubMed  Google Scholar 

  • Blatch, G.L., and Lassle, M. (1999). The tetratricopeptide repeat, a structural motif mediating protein-protein interactions. Bioessays 21, 932–939.

    Article  CAS  PubMed  Google Scholar 

  • Cao, H., and Shannon, J.C. (1997). BT1, a possible adenylate translocator, is developmentally expressed in maize endosperm but not detected in starchy tissues from several other species. Physiol. Plant 100, 400–406.

    Article  CAS  Google Scholar 

  • Causse, M.A., Fulto, T.M., Cho, Y.G., Ahn, S.N., Chuncongse, J., Wu, K., Xiao, J., Yu, Z,, Ronald, P.C., Harrington, S.E., et al. (1994). Saturated molecular map of the rice genome based on an interspecific backcross population. Genetics 138, 1251–1274.

    CAS  PubMed  Google Scholar 

  • Colleoni, C., Dauvillee, D., Mouille, G., Morell, M., Samuel, M., Slomiany, M.C., Lienard, L., Wattebled, F., d’Hulst, C., and Ball, S. (1999). Biochemical characterization of the Chlamydomonas reinhardtii a-1,4 glucanotransferase supports a direct function in amylopectin biosynthesis. Plant Physiol. 120, 1005–1014.

    Article  CAS  PubMed  Google Scholar 

  • D’Andrea, L., and Regan, L. (2003). TPR proteins, the versatile helix. Trends Biochem. Sci. 28, 655–661.

    Article  PubMed  Google Scholar 

  • Dauvillee, D., Chochois, V., Setup, M., Haebel, S., Eckermann, N., Ritte, G., Ral, J.P., Colleni, C., Hicks, G., Wattebled, F., et al. (2006). Plastidial phosphorylase is required for normal starch synthesis in Chlamydomonas reinhardtii. Plant J. 48, 274–285.

    Article  CAS  PubMed  Google Scholar 

  • Fedoroff, N.V. (2002). RNA-binding proteins in plants, the tip of an iceberg? Curr. Opin. Plant Biol. 5, 452–459.

    Article  CAS  PubMed  Google Scholar 

  • Fisher, D.K., Boyer, C.D., and Hannah, L.C. (1993). Starch branching enzyme II from maize endosperm. Plant Physiol. 102, 1045–1046.

    Article  CAS  PubMed  Google Scholar 

  • Gao, M., Wanat, J., Stinard, P.S., James, M.G., and Myers, A.M. (1998). Characterization of dull1, a maize gene coding for a novel starch synthase. Plant Cell 10, 399–412.

    Article  CAS  PubMed  Google Scholar 

  • Gounalaki, N., Tzamarias, D., and Vlassi, M. (2000). Identification of residues in the TPR domain of Ssn6 responsible for interaction with the Tup1 protein. FEBS Lett. 473, 37–41.

    Article  CAS  PubMed  Google Scholar 

  • Hannah, L.C., and James, M. (2008). The complexities of starch biosynthesis in cereal endosperms. Curr. Opin. Biotechnol. 19, 160–165.

    Article  CAS  PubMed  Google Scholar 

  • Hoshikawa, K. (1989). The growing rice plant, an anatomical monograph, (Tokyo, Japan: Nobunkyo).

    Google Scholar 

  • Hunter, B.G., Beatty, M.K., Singletary, G.W., Hamaker, B.R., Dilkes, B.P., Larkins, B.A., and Jung, R. (2002). Maize opaque endosperm mutations create extensive changes in patterns of gene expression. Plant Cell 14, 2591–2612.

    Article  CAS  PubMed  Google Scholar 

  • Isshiki, M., Matsuda, Y., Takasaki, A., Wong, H.L., Satoh, H., and Shimamoto, K. (2008). Du3, a mRNA cap-binding protein gene, regulates amylase content in Japonica rice seeds. Plant Biotechnol. J. 25, 483–487.

    CAS  Google Scholar 

  • James, M.G., Robertson, D.S., and Myers, A.M. (1995). Characterization of the maize gene sugary1, a determinant of starch composition in kernels. Plant Cell 7, 417–429.

    Article  CAS  PubMed  Google Scholar 

  • Kang, H.G., Park, S., Matsuoka, M., and 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.

    Article  CAS  PubMed  Google Scholar 

  • Kaushik, R.P., and Khush, G.S. (1991). Genetic analysis of endosperm mutants in rice Ovyza sativa L. Theor. Appl. Genet. 83, 146–152.

    Article  Google Scholar 

  • Kawasaki, T., Mizuno, K., Shimada, H., Satoh, H., Kishimoto, N., Okumura, S., Ichikawa, N., and Baba, T. (1996). Coordinated regulation of the genes participating in starch biosynthesis by the rice floury-2 locus. Plant Physiol. 110, 89–96.

    CAS  PubMed  Google Scholar 

  • Kim, K.H., Koh, H.J., Lee, J.H., Park, S.Z., and Heu, M.H. (1993). Diversity of rice quality for processing: Physicochemical characteristics and inheritance of floury endosperm mutants. Korean J. Crop Sci. 38, 264–274.

    Google Scholar 

  • Kim, S.R., Yang, J.I., Moon, S.O., Ryu, C.H., An, K.S., Kim, K.M., Yim, J., and An, G.H. (2009). Rice OGR1 encodes a pentatricopeptide repeat-DYW protein and is essential for RNA editing in mitochondria. Plant J. 59, 738–749

    Article  CAS  PubMed  Google Scholar 

  • Klosgen, R.B., Gierl, A., Schwarz-Sommer, Z., and Saedler, H. (1986). Molecular analysis of the Waxy locus of Zea mays. Mol. Gen. Genet. 203, 237–244.

    Article  Google Scholar 

  • Kosambi, D.D. (1944). The estimation of map distances from recombination values. Ann. Eugen. 12, 172–175.

    Google Scholar 

  • Kubo, A., Rahman, S., Utsumi, Y., Li, Z., Mukai, Y., Yamamoto, M., Ugaki, M., Harada, K., Satoh, H., Konik-Rose, C., 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 Physiol. 137, 43–56.

    Article  CAS  PubMed  Google Scholar 

  • Kumamaru, T., Sato, H., and Satoh, H. (1997). High-lysine mutants of rice, Oryza sativa L. Plant Breed. 116, 245–249.

    Article  CAS  Google Scholar 

  • Lander, E.S., Green, P., Abrahamson, J., Barlow, A., Daly, M.J., Lincoln, S.E., and Newburg, L. (1987). MAPMAKER, an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1, 174–181.

    Article  CAS  PubMed  Google Scholar 

  • Nelson, O.E., and Pan, D. (1995). Starch synthesis in maize endosperms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 46, 475–496.

    Article  CAS  Google Scholar 

  • Nishio, T., and Iida, S. (1993). Mutant having a low content of 16-kDa allergenic protein in rice (Oryza sativa L.). Theor. Appl. Genet. 86, 317–321.

    Article  CAS  Google Scholar 

  • Prodromou, C., Siligardi, G., O’Brien, R., Woolfson, D., Regan, L., Panaretou, B., Ladbury, J., Piper, P., and Pearl, L. (1999). Regulation of Hsp90 ATPase activity by tetratricopeptide repeat domain co-chaperones. EMBO J. 18, 754–762.

    Article  CAS  PubMed  Google Scholar 

  • Qiao, Y.L., Jiang, W.Z., Rahman, L., Chu, S.H., Piao, R.H., Han, L.Z., and Koh, H.J. (2008). Comparison of molecular linkage maps and QTLs for morphological traits in two reciprocal backcross populations of rice. Mol. Cells 25, 417–427.

    CAS  PubMed  Google Scholar 

  • Rosado, A., Schapire, A.L., Bressan, R.A., Harfouche, A.L., Hasegawa, P.M., Valpuesta, V., and Botella, M.A. (2006). The Arabidopsis tetratricopeptide repeat-containing protein TTL1 is required for osmotic stress responses and abscisic acid sensitivity. Plant Physiol. 142, 1113–1126.

    Article  CAS  PubMed  Google Scholar 

  • Ryoo, N.Y., Yu, C., Park, C.S., Baik, M.Y., Park, I.M., Cho, M.H., Bhoo, S.H., An, G.H., Hahn, T.R., and Jeon, J.S. (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.

    Article  CAS  PubMed  Google Scholar 

  • Satoh, H., and Omura, T. (1981). New endosperm mutations induced by chemical mutagen in rice, Oryza sativa L. Jpn. J. Breed. 31, 316–326.

    CAS  Google Scholar 

  • Satoh, H., Shibahara, K., Tokunaga, T., Nishi, A., Tasaki, M., Hwang, S.K., Okita, T.W., Kaneko, N., Fujita, N., Yoshida, M., et al. (2008). Mutation of the plastidial a-glucan phosphorylase gene in rice affects the synthesis and structure of starch in the endosperm. Plant Cell 20, 1833–1849.

    Article  CAS  PubMed  Google Scholar 

  • Schupp, N., and Ziegler, P. (2004). The relation of starch phosphorylases to starch metabolism in wheat. Plant Cell Physiol. 45, 1471–1484.

    Article  CAS  PubMed  Google Scholar 

  • Shannon, J.C., Pien, F.M., and Liu, K.C. (1996). Nucleotides and nucleotide sugars in developing maize (Zea mays L.) endosperms. Synthesis of ADP-glucose in brittle-1. Plant Physiol. 110, 835–843.

    CAS  PubMed  Google Scholar 

  • Shure, M., Wessler, S., and Fedoroff, N. (1983). Molecular identification and isolation of the Waxy locus in maize. Cell 35, 225–233.

    Article  CAS  PubMed  Google Scholar 

  • Smith, A.M., Denyer, K., and Martin, C. (1997). The synthesis of the starch granule. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48, 67–87.

    Article  CAS  PubMed  Google Scholar 

  • Stinard, P.S., Robertson, D.S., and Schnable, P.S. (1993). Genetic isolation, cloning, and analysis of a Mutator-induced, dominant antimorph of the maize amylose extender1 locus. Plant Cell 5, 1555–1566.

    Article  CAS  PubMed  Google Scholar 

  • Sullivan, T.D., Strelow, L.I., Illingworth, C.A., Phillips, R.L., and Nelson, O.E.J. (1991). Analysis of maize Brittle-1 alleles and a defective suppressor-mutator-induced mutable allele. Plant Cell 3, 1337–1348.

    Article  CAS  PubMed  Google Scholar 

  • Tseng, T.S., Swain, S.M., and Olszewski, N.E. (2001). Ectopic expression of the tetratricopeptide repeat domain of SPINDLY causes defects in gibberellins response. Plant Physiol. 126, 1250–1258.

    Article  CAS  PubMed  Google Scholar 

  • Wang, K.L., Yoshida, H., Lurin, C., and Ecker, J.R. (2004). Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein. Nature 428, 945–950.

    Article  CAS  PubMed  Google Scholar 

  • Yang, J., Roe, S.M., Cliff, M.J., Williams, M.A., Ladbury, J.E., Cohen, P.T., and Barford, D. (2005). Molecular basis for TPR domain-mediated regulation of protein phosphatase 5. EMBO J. 24, 1–10.

    Article  PubMed  Google Scholar 

  • Zeng, D.L., Yan, M.X., Wang, Y.H., Liu, X.F., Qian, Q., and Li, J.Y. (2007). Du1, encoding a novel Prp1 protein, regulates starch biosynthesis through affecting the splicing of Wxb pre-mRNAs in rice (Oryza sativa L.). Plant Mol. Biol. 65, 501–509.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, Q.F., Shen, B.Z., Dai, X.K., Mei, M.H., Maroof, M.A.S., and Li, Z.B. (1994). Using bulked extremes and recessive class to map genes for photoperiod-sensitive genic male sterility in rice. Proc. Natl. Acad. Sci. USA 91, 8675–8679.

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Hee-Jong Koh.

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Qiao, Y., Lee, SI., Piao, R. et al. Fine mapping and candidate gene analysis of the floury endosperm gene, FLO(a), in rice. Mol Cells 29, 167–174 (2010). https://doi.org/10.1007/s10059-010-0010-6

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  • DOI: https://doi.org/10.1007/s10059-010-0010-6

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