Abstract
Expression of α-amylase genes during seedling development plays a key role in production of sugar from the starch stored in the cereal seed. Rice α-amylase Amy3D promoter/GUS constructs in transgenic rice cell lines were studied to identify cis elements in the promoter of this metabolite-regulated gene. Three sequences having the greatest effects on Amy3D gene expression included the amylase element (TATCCAT), the CGACG element, and a G box-related element (CTACGTGGCCA). These promoter cis elements are needed for high-level expression of Amy3D under conditions of sugar starvation. The involvement of G box cis-elements in environmental stress responses suggest a link between the nutrient stress and the environmental stress responses of the plant.
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Beck E, Ziegler P: Biosynthesis and degradation of starch in higher plants. Annu Rev Plant Physiol Plant Mol Biol 40: 95–117 (1989).
Bronstein I, Fortin JJ, Voyta JC, Juo R, Edwards B, Olsen CEM, Lijam N, Kricka LJ: Chemiluminescent reporter gene assays: Sensitive detection of the GUS and SEAP gene products. Bio-Techniques 17: 172–178 (1994).
Chandler PM, Robertson M: Gene expression regulated by abscisic acid and its relation to stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 45: 113–141 (1994).
DeVetten NC, Ferl RJ: Transcriptional regulation of environmentally inducible genes in plants by an evolutionary conserved family of G-box binding factors. Int J Biochem 26: 1055–1068 (1994).
deWet JR, Wood KV, DeLuca M, Helinski DR, Subramani S: Firefly luciferase gene: structure and expression inmammalian cells. Mol Cell Biol 7: 725–737 (1987).
Fromm ME, Morrish F, Armstrong C, Williams R, Thomas J, Klein TM: Inheritance and expression of chimeric genes in the progeny of transgenic maize plants. Bio/technology 8: 833–839 (1990).
Huang N, Chandler J, Thomas BR, Rodriguez RL: Metabolic regulation of α-amylase gene expression in rice cell cultures. Plant Mol Biol 23: 737–747 (1993).
Huang N, Koizumi N, Reinl S, Rodriguez RL: Structural organization and differential expression of rice α-amylase genes. Nucl Acids Res 18: 7007–7014 (1990).
Huang N, Sutliff TD, Litts JC, Rodriguez RL: Classification and characterization of the rice α-amylase multigene family. Plant Mol Biol 14: 655–668 (1990).
Huttly AK, Baulcombe DC: A wheat α-Amy2 promoter is regulated by gibberellin in transformed oat aleurone protoplasts. EMBO J 8: 1907–1913 (1989).
Huttly AK, Martienssen RA, Baulcombe DC: Sequence heterogeneity and differential expression of the α-Amy2 gene family in wheat. Mol Gen Genet 214: 232–240 (1988).
Itoh K, Yamaguchi J, Huang N, Rodriguez RL, Akazawa T, Shimamoto K: Developmental and hormonal regulation of rice α-amylase (RAmy1A)-gusA fusion genes in transgenic rice seeds. Plant Physiol 107: 25–31 (1995).
Izawa T, Foster R, Chua NH: Plant bZIP protein DNA binding specificity. J Mol Biol 230: 1131–1144 (1993).
Jacobsen JV, Gubler F, Chandler PM: Gibberellin action in germinated cereal grains. In: Davies PJ (ed) Plant Hormones, pp. 246–271. Kluwer Academic Publishers, Dordrecht, Netherlands (1995).
Jang J-C, Leon P, Zhou L, Sheen J: Hexokinase as a sugar sensor in higher plants. Plant Cell 9: 5–19 (1997).
Jang J-C, Sheen J: Sugar sensing in higher plants. Plant Cell 6: 1665–1679 (1994).
Jefferson RA, Kavanagh TA, Bevan MW: GUS fusions: α-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901–3907 (1987).
Kao KN: Chromosomal behaviour in somatic hybrids of soybean-Nicotiana glauca. Mol Gen Genet 150: 225–230 (1977).
Karrer EE, Litts JC, Rodriguez RL: Differential expression of α-amylase genes in germinating rice and barley seeds. Plant Mol Biol 16: 797–805 (1991).
Karrer EE, Rodriguez RL: Metabolic regulation of rice α-amylase and sucrose synthase genes in planta. Plant J 2: 517–523 (1992).
Koch KE: Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 47: 509–540 (1996).
Kunkel TA, Roberts JD, Zakour RA: Rapid and efficient site-specific mutagenesis without phenotypic selection. Meth Enzymol 154: 367–382 (1987).
Lee B, Martin P, Bangerth F: The effect of sucrose on the levels of abscisic acid, indoleacetic acid and zeatin zeatin riboside in wheat ears growing in liquid culture. Physiol Plant 77: 73–80 (1989).
Lee L, Schroll RE, Grimes HD, Hodges TK: Plant regeneration from indica rice (Oryza sativa L.) protoplasts. Planta 178: 325–333 (1989).
Li L, Qu R, deKochko A, Fauquet C, Beachey RN: An improved rice transformation system using the biolistic method. Plant Cell Rep 12: 250–255 (1993).
Magoulas C, Bally-Cuif L, Loverre-Chyurlia A, Benkel B, Hickey D: A short 52032;-flanking region mediates glucose repression of amylase gene expression in Drosophila melanogaster. Genetics 134: 507–515 (1993).
McGarvey P, Kaper JM: Asimple and rapid method for screening transgenic plants using PCR. Biotechniques 11: 428–432 (1991).
McKendreeJr WL, Ferl RL: Functional elements of the Arabidopsis Adh promoter include the G-box. Plant Mol Biol 19: 859–862 (1992).
Mitsunaga S, Rodriguez RL, Yamaguchi J: Sequence-specific interactions of a nuclear protein factor with the promoter region of a rice gene for alpha-amylase, RAmy3D. Nucl Acids Res 22: 1948–1953 (1994).
Nagata O, Takashima T, Tanaka M, Tsukagoshi N: Aspergillus nidulans nuclear proteins bind to a CCAAT element and the adjacent upstream sequence in the promoter region of the starch-inducible Taka-amylase A gene. Mol Gen Genet 237: 251–260 (1993).
Naito S, Hirai MY, Inaba-Higano K, Nambara E, Fujiwara T, Hayashi H, Komeda Y, Chino M: Expression of soybean seed storage protein genes in transgenic plants and their response to sulfur nutritional conditions. J Plant Physiol 145: 614–619 (1995).
O'Neill SD, Kumagai MH, Majumdar A, Huang N, Sutliff TD, Rodriguez RL: The α-amylase genes in Oryza sativa: characterization of cDNAclones andmRNAexpression during seed germination. Mol Gen Genet 221: 235–244 (1990).
Ono A, Izawa T, Chua NH, Shimamoto K: The rab16b promoter of rice contains two distinct abscisic acid-responsive elements. Plant Physiol 112: 483–491 (1996).
Rademacher W, Jung J: Comparative potency of various synthetic plant growth retardants on the elongation of rice seedlings. J Agron Crop Sci 150: 363-371 (1981).
Rao KV, Rathore KS, Hodges TK: Physical, chemical and physiological parameters for electroporation-mediated gene delivery into rice protoplasts. Transgen Res 4: 361–368 (1995).
Rogers JC, Rogers SW: Definition and functional implications of gibberellin and abscisic acid cis-acting hormone response complexes. Plant Cell 4: 1443–1451 (1992).
Rogers SG, Klee HJ, Horsch RB, Fraley RT: Improved vectors for plant transformation: expression cassette vectors and new selectable markers. Meth Enzymol 153: 253–277 (1987).
Ronne H: Glucose repression in fungi. Trends Genet 11: 12–17 (1995).
Salinas J, Oeda K, Chua N-H: Two G-box-related sequences confer different expression patterns in transgenic tobacco. Plant Cell 4: 1485–1493 (1992).
Sheen J: Feedback control of gene expression. Photosynth Res 39: 427–438 (1994).
Shen QX, Zhang PN, Ho T-HD: Modular nature of abscisic acid (ABA) response complexes: composite promoter units that are necessary and sufficient for ABA induction of gene expression in barley. Plant Cell 8: 1107–1119 (1996).
Sissons MJ, MacGregor AW: Hydrolysis of barley starch granules by α-glucosidases from malt. J Cereal Sci 19: 161–169 (1994).
Sivamani E, Shen P, Opalka N, Beachy RN, Fauquet CM: Selection of large quantities of embryogenic calli from indica rice seeds for production of fertile transgenic plants using the biolistic method. Plant Cell Rep 15: 322–327 (1996).
Skriver K, Olsen FL, Rogers JC, Mundy J: Cis-acting DNA elements responsive to gibberellin and its antagonist abscisic acid. Proc Natl Acad Sci USA 88: 7266–7270 (1991).
Sun Z, Henson CA: A quantitative assessment of the importance of barley seed α-amylase, debranching enzyme, and aglucosidase in starch degradation. Arch Biochem Biophys 284: 298–305 (1991).
Sung HI, Liu LF, Lur HS, Kao CH: Sucrose-starvation-induced changes in polyamine and abscisic acid levels of suspensioncultured rice cells. Bot Bull Acad Sin 36: 47–51 (1995).
Terashima M, Hayashi N, Thomas BR, Rodriguez RL, Katoh S: Kinetic parameters of two rice α-amylase isozymes for oligosaccharide degradation. Plant Sci 116: 9–14 (1996).
Thomas BR, Chandler J, Simmons CR, Huang N, Karrer E, Rodriguez RL: Gene regulation and protein secretion from plant cell cultures: the rice α-amylase system. In: Ryu DDY, Furusaki S (eds) Advances in Plant Biotechnology, pp. 37–55. Elsevier, Amsterdam, (1994).
Thomas BR, Rodriguez RL: Metabolite signals regulate gene expression and source/sink relations in cereal seedlings. Plant Physiol 106: 1235–1239 (1994).
Thomas BR, Terashima M, Katoh S, Stoltz T, Rodriguez RL: Metabolic regulation of source-sink relations in cereal seedlings. In: Madore MA, Lucas WJ (eds) Carbon Partitioning and Source-Sink Interactions in Plants, pp. 78–90. American Society of Plant Physiologists, Rockville, MD, (1995).
Thompson JA, Abdullah R, Cocking EC: Protoplast culture of rice (Oryza sativa L.) using media solidified with agarose. Plant Sci 47: 123–133 (1986).
Vaulont S, Kahn A: Transcriptional control of metabolic regulation genes by carbohydrates. FASEB J 8: 28–35 (1994).
Williams ME, Foster R, Chua N-H: Sequences flanking the hexameric G-box core CACGTG affect the specificity of protein binding. Plant Cell 4: 485–496 (1992).
Witt W, Buchholz A, Sauter JJ: Binding of endoamylase to native starch grains from poplar wood. J Exp Bot 46: 1761–1769 (1995).
Witt W, Sauter JJ: In vitro degradation of starch grains by phosphorylases and amylases from poplar wood. J Plant Physiol 146: 35–40 (1995).
Yu S-M, Tzou W-S, Lo W-S, Kuo Y-H, Lee H-T, Wu R: Regulation of α-amylase-encoding gene expression in germinating seeds and cultured cells of rice. Gene 122: 247–253 (1992).
Yu SM, Lee YC, Fang SC, Chan MT, Hwa SF, Liu LF: Sugars act as signal molecules and osmotica to regulate the expression of α-amylase genes and metabolic activities in germinating cereal grains. Plant Mol Biol 30: 1277–1289 (1996).
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Hwang, YS., Karrer, E., Thomas, B. et al. Three cis-elements required for rice α-amylase Amy3D expression during sugar starvation. Plant Mol Biol 36, 331–341 (1998). https://doi.org/10.1023/A:1005956104636
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DOI: https://doi.org/10.1023/A:1005956104636