Summary
Plant genetic engineering has contributed substantially to the understanding of gene regulation and plant development, in the generation of transgenic organisms for widespread usage in agriculture, and has increased the potential uses of crops for industrial and pharmaceutical purposes. As the application of geneticallly engineered plants has widened, so has the need to develop methods to fine-tune control of transgene expression. The availability of a broad spectrum of promoters that differ in their ability to regulate the temporal and spatial expression patterns of the transgene can dramatically increase the successful application of transgenic technology. Indeed, a variety of promoters in necessary at all levels of genetic engineering in plants, from basic research discoveries, concepts and question to development of economically viable crops and plant commodities, to addressing legitimate concerns raised about the safety and containment of transgenic plants in the environment. This review covers the characterization and usage of a broad range of promoters employed in plant genetic engineering, including the widespread use of plant promoters with viral and plant origin that drive constitutive expression. Also covered are selected tissue-specific promoters from fruit, seed and grain, tubers, flowers, pistils, anther and pollen, roots and root nodules, and leaves and green tissue. Topics also include organellar promoters, and those found in specific cell types, as well as the development and evaluation of inducible (endogenous and exogenous origin) and synthetic plant promoter systems. Discussions on the relevance and potential pitfalls within specific applications are included.
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References
Alberts, B.; Johnson, A.; Lewis, J.; Baff, M.; Roberts, K.; Walter, P. Molecular biology of the cell. 4th edn. New York: Garland Science: 2003.
Aleman, L. Isolation and characterization of leaf-specific promoters from alfalfa (Medicago sativa). Masters thesis, New Mexico State University, Las Cruces, NM, 2001.
Altschul, S. F.; Madden, T. L.; Schäffer, A. A.; Zhang, J.; Zhang, Z.; Miller, W.; Lipman, D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389–3402; 1997.
An, Y.-Q.; McDowell, J. M.; Huang, S.; McKinney, E. C.; Chambliss, S.; Meagher, R. B. Strong, constitutive expression of the Arabidopsis ACT2/ACT8 actin subclass in vegetative tissues. Plant J. 10:107–121; 1996.
Anderson, S. L.; Kay, S. A. Functional dissection of circadian clock-and phytochorome-regulated transcription of the Arabidopsis CAB2 gene. Proc. Natl Acad. Sci. USA 92:1500–1504; 1995.
Annadama, S.; Beekwilder, M. J.; Kuipers, G.; Visser, P. B.; Outchkourov, N.; Pereira, A.; Udayakumar, M.; De Jong, J.; Jongsma, M. A. Cloning of the chrysanthenum UEP1 promoter and comparative expression in florest and leaves of Dendranthema grandiflora. Transgenic Res. 11:437–445; 2002.
Aoyama, T.; Chua, N.-H. A glucoconticoid-mediated transcriptional induction system in transgenic plants. Plant J. 11:605–612; 1997.
Arguello-Astorga, C. R.; Herrera-Estrella, L. R. Ancestral multipartite units in light-responsive plant promoters have structural features correlating with specific phototransduction pathways. Plant Physiol. 112:1151–1166; 1996.
Atkinson, R. G.; Bolitho, K. M.; Wright, M. A.; Iturriagagoitia-Bueno, T.; Reid, S. J.; Ross, G. S. Apple ACC-oxidase and polygalacturonase: transgenic tomato. Plant Mol. Biol. 38:449–460; 1998.
Barro, F.; Rooke, L.; Bekes, F.; Gras, P.; Tatham, A. S.; Fido, R.; Lazzeri, P. A.; Shewry, P. R.; Barcelo, P. Transformation of wheat with high molecular weight subunit genes results in improved functional properties. Nature Biotechnol. 15:1295–1299; 1997.
Battraw, M. J.; Hall, T. C. Histochemical analysis of CaMV 35S promoter-β-glucuronidase gene expression in transgenic rice plants. Plant Mol. Biol. 15:527–538; 1990.
Benfey, P. N.; Chua, N.-H. Regulated genes in transgenic plants. Science 244:174–181; 1989.
Benfey, P. N.; Ren, L.; Chua, N.-H. Tissue-specific expression from CaMV 35S enhancer subdomains in early stages of plant development. EMBO J. 9:1677–1684; 1990a.
Benfey, P. N.; Takatsuji, H.; Ren, L.; Shah, D.; Chua, N.-H. Sequence requirements of the 5-enolpyruvylshikimate-3-phosphate synthase 5′-upstream region for tissue-specific expression in flowers and seedlings. Plant Cell 2:849–856; 1990b.
Berrocal-Lobo, M.; Molina, A.; Solano, R. Constitutive expression of ETHYLENE-RESPONSE-FACTOR1 in Arabidopsis confers resistance to several necrotrophic fungi. Plant J. 29:23–32; 2002.
Beyer, P.; Al-Babili, S.; Ye, X.; Lucca, P.; Schaub, P.; Welsch, R.; Potrykus, I. Golden rice: introducing the β-carotene biosynthesis pathway into rice endosperm by genetic engineering to defeat vitamin A deficiency. J. Nutr. 132:506S-510S; 2002.
Bohner, S.; Lenk, L.; Rieping, M.; Herold, M.; Gatz, C. Transcriptional activator TGV mediates dexamethasone-inducible and tetracycline-inactivatable gene expression. Plant J. 19:87–95; 1999.
Bonetta, D.; McCourt, P. Genetic analysis of ABA signal transduction pathways. Trends Plant Sci. 3:231–235; 1998.
Bowling, S. A.; Clarke, J. D.; Liu, Y.; Klessig, D. F.; Dong, X. The cpr5 mutant of Arabidopsis expresses both NPR1-dependent and NPR1-independent resistance. Plant Cell 9:1573–1584; 1997.
Bowling, S. A.; Guo, A.; Cao, H.; Gordon, A. S.; Klessig, D. F.; Dong, X. A mutation in Arabidopsis that leads to constitutive expression of systemic acquired resistance. Plant Cell 6:1845–1857; 1994.
Boynton, J. E.; Gillhan, N. W.; Harris, E. H.; Hosler, J. P.; Johnson, A. M.; Jones, A. R.; Randolph-Anderson, R. L.; Robertson, D.; Klein, T. M.; Shark, K. B.; Sanford, J. C. Chloroplast transformation in Chlamydomonas with high velocity microprojectiles. Science 240:1534–1537; 1988.
Bruce, W.; Folkerts, O.; Garnaat, C.; Crasta, O.; Roth, B.; Bowen, B. Expression profiling of the maize flavonoid pathway genes controlled by estradiol-inducible transcription factors CRC and P. Plant Cell 12:65–79; 2000.
Bucchini, I.; Goldman, L. R. Starlink corn: a risk analysis. Environ. Health Perspect. 110:5–13; 2002.
Buchanan, B. B.; Gruissem, W.; Jones, R. L., eds. Biochemistry and molecular biology of plants. Vockville, MD: American Society of Plant Physiologists; 2000:340–342.
Buchner, P.; Rochat, C.; Wuilleme, S.; Boutin, J.-P. Characterization of a tissue-specific and developmentally regulated β-1,3-glucanase gene in pea (Pisum sativum). Plant Mol. Biol. 49:171–186; 2002.
Bustos, M. M.; Guiltinan, M. J.; Jordano, J.; Begum, D.; Kalkan, F. A.; Hall, T. C. Regulation of beta-glucuronidase expression in transgenic tobacco plants by an A/T-rich, cis-acting sequence found upstream of a French bean beta-phascolin gene. Plant Cell 1:839–853; 1989.
Caddick, M. X.; Greenland, A. J.; Jepson, I.; Krause K.-P.; Qu, N.; Riddell, K. V.; Salter, M. G.; Schuch, W.; Sonnewald, U.; Tonsett, A. B. An ethanol inducible gene switch for plants used to manipulate carbon metabolism. Nature Biotechnol. 16:177–180; 1998.
Cahoon, E. B.; Shanklin, J. Substrate-dependent mutant complementation to select fatty acid desaturase variants for metabolic engineering of plant seed oils. Proc. Natl Acad. Sci. USA 97:12350–12355; 2000.
Cao, H.; Li, X.; Dong, X. Generation of broad-spectrum disease resistance by overexpression of an essential regulatory gene in systemic required resistance. Proc. Natl. Acad. Sci. USA 95:6531–6536; 1998.
Carre, I. A.; Kay, S. A. Multiple DNA-protein complexes at a circadian-regulated promoter element. Plant Cell 7:2039–2051; 1995.
Carsolio, C.; Campos, F.; Sanchez, F.; Rocha-Sosa, M. The expression of a chimeric Phaseolus vulgaris nodulin 30-GUS gene is restricted to the rhizobially infected cells in transgenic Lotus corniculatus nodules. Plant Mol. Biol. 26:1995–2001; 1994.
Catiora, R.; Timmers, A. C.; Maillet, F.; Galera, C.; Penmetsa, R. V.; Cook, D.; Denarie, J.; Gough, C. The HCL gene of Medicago truncatula controls the Rhizobium-induced root hair curling. Development 128:1507–1518; 2001.
Chakraborty, S.; Chakraborty, N.; Datta, A. Increased nutritive value of transgenic potato by expressing a nonallergenic seed albumin gene from Amaranthus hypochondriacus. Proc. Natl. Acad. Sci. USA 97:3724–3729; 2000.
Chamberland, S.; Daigle, N.; Bernier, F. The legumin boxes and the 3′ part of a soybean beta-conglycinin promoter are involved in seed gene expression in transgenic tobacco plants. Plant Mol. Biol. 19:937–949; 1992.
Chandrasekharan, M. B.; Bishop, K. J.; Hall, T. C. Module-specific regulation of the β-phascolin promoter during embryogenesis. Plant J. 33:853–866; 2003.
Chen, Z. L.; Naito, S.; Nakamura, I.; Beachy, R. N. Regulated expression of genes encoding soybean beta-conglycinins in transgenic plants. Dev. Genet. 10:112–122; 1989.
Christensen, A. H.; Sharrock, R. A.; Quail, P. H. Maize polyubiquitin genes: structure, thermal perturbation of expression and transcript splicing, and promotes activity following transfer to protoplast by electroporation. Plant Mol. Biol. 18:675–689; 1992.
Christon, P. No credible scientific evidence is presented to support claims that transgenic DNA was introgressed into traditional maize landraces in Oaxaca, Mexico Transgenic Res. 11:iii-v; 2002.
Clark, I. M.; Forde, B. G.; Hallahan, D. L. Spatially distinct expression of two new cytochrome P450s in leaves of Nepeta racemosa: identification of a trichome-specific isoform. Plant Mol. Biol. 33:875–885; 1997.
Conkling, M. A.; Cheng C.-L.; Yamamoto, Y. T.; Goodman, H. M. Isolation of transcriptionally regulated root-specific genes from tobacco. Plant Physiol. 93:1203–1211; 1990.
Cornejo, M.-J.; Luth, D.; Blankenship, K. M.; Anderson, O. D.; Blechl, A. E. Activity of a maize ubiquitin promoter in transgenic rice. Plant Mol. Biol. 23:567–581; 1993.
Corona, V.; Aracri, B.; Kosturkova, G.; Bartley, G. E.; Pitto, L.; Giorgetti, L.; Scolnik, P. A.; Giuliano, G. Regulation of a carotenoid biosynthesis gene promoter during plant development. Plant J. 9:505–512; 1996.
Corriveau, J. L.; Coleman, A. W. Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 angiosperm species. Am. J. Bot. 75:1443–1458; 1988.
Cosgrove, D. J.; Li, L. C.; Cho, H. T.; Hoffmann-Benning, S.; Moore, R. C.; Blecker, D. The growing world of expansins. Plant Cell Physiol. 43:1436–1444; 2002.
Dale, P. J.; Clarke, B.; Fontes, E. M. G. Potential for the environmental impact of transgenic crops. Nature Biotechnol. 20:567–574; 2002.
Daniell, H. Molecular strategies for gene containment in transgenic crops. Nature Biotechnol. 20:581–586; 2002.
Daniell, H.; Datta, R.; Varma, S.; Gray, S.; Lee, S.-L. Containment of herbicide resistance through genetic engineering of the chloroplast genome. Nature Biotechnol. 16:345–348; 1998.
Daniell, H.; Parkinson, C. L. Jumping genes and containment. Nature Biotechnol. 21:374–375; 2003.
de Vetten, N.; ter Horst, J.; van Schaik, H.-P.; de Boer, A.; Mol, J.; Koes, R. A cytochrome b5 is required for full activity of flavonoid 3′, 5′-hydroxylase, a cytochrome P450 involved in the formation of blue flower colors. Proc. Natl. Acad. Sci. USA 96:778–783; 1999.
De Veylder, L.; Van Montagu, M.; Inze, D. Herbicide safener-inducible gene expression in Arabidopsis thaliana Plant Cell Physiol. 38:568–577; 1997.
Deikman, J.; Fischer, R. L. Interaction of a DNA binding factor with the 5′-flanking region of an ethylene-responsive fruit ripening gene from tomato. EMBO J. 7:3315–3320; 1988.
DeRidder, B. P.; Dixon, D. P.; Beussman, D. J.; Edwards, R.; Goldsbrough, P. B. Induction of glutathione S-transferase in Arabidopsis by herbicide safeners. Plant Physiol. 130:1497–1505; 2002.
Dey, N.; Maiti, I. B. Structure and promoter/leader deletion analysis of mirabilis mosaic virus (MMV) full-length transcript promoter in transgenic plants. Plant Mol. Biol. 40:771–782; 1999.
Dhankher, O. P.; Li, Y.; Rosen, B. P.; Shi, J.; Salt, D.; Senecoff, J. F.; Sashti, N. A.; Meagher, R. B. Engineering tolerance and hyperacumulation of arsenic in plants by combining arsenate reductase and γ-glutamylcysteine synthetase expression. Nature Biotechnol. 20:1–6; 2002.
Dixon, R. A.; Steele, C. L. Flavonoids and isoflavonoids—a gold mine for metabolic engineering. Trends Plant Sci. 4:394–400; 1999.
Dolgov, S. V.; Mityshkina, T. U.; Rukavtsova, E. B.; Buryanov, Y. L.; Vainstein, A.; Weiss, D. Production of transgenic plants of Chrysanthemum morifolium Ramat with the Bacillus thuringiensis delta endotoxin. Acta Hort. 420:46–47; 1995.
Downey, P.; Szabo, I.; Ivashikina, N.; Negro, A.; Guzzo, F.; Ache, P.; Hedrich, R.; Terzi, M.; Lo Schiavo, F. KDC1, a novel carrot root hair K+ channel, Cloning, characterization, and expression in mammalian cells. J. Biol. Chem. 275:39420–39426; 2000.
Du, L.; Chen, Z. Identification of genes encoding receptor-like protein kinases as possible targets of pathogen- and salicylic acid-induced WRKY DNA-binding proteins in Arabidopsis. Plant J. 24:837–847; 2000.
Eaglesham, A.; Pueppke, S. G.; Hacly, R. W. F. eds. Gentically modified food and the consumer. NABC Report 13. New York: National Agricultural Biotechnology Council; 2001.
Elmayan, T.; Tepfer, M. Evaluation in tobacco of the organ specificity and strength of the rolD promoter, domain A of the 35S promoter and the 35S2 promoter. Transgenic Res. 4:388–396; 1995.
Elmayan, T.; Vaucheret, H. Expression of single copies of a strongly expressed 35S transgene can be silenced post-transcriptionally. Plant J. 9:787–797; 1996.
Evans, I. M.; Swinhoe, R.; Gatehouse, L. N.; Gatehouse, J. A.; Boulter, D. Distribution of root mRNA species in other vegetative organs of pea (Pisum sativum L.). Mol. Gen. Genet. 214:153–157; 1988.
Faktor, O.; Kooter, J. M.; Dixon, R. A.; Lamb, C. J. Functional dissection of a bean chalcone synthase gene promoter in transgenic tobacco plants. Plant Mol. Biol. 32:849–859; 1996.
Faktor, O.; Loake, G.; Dixon, R. A.; Lamb, C. J. The G-box and H-box in a 39 bp region of a French bean chalcone synthase promoter constitutes a tissue-specific regulatory element. Plant J. 11:1105–1113; 1997.
Fang, R. X.; Nagy, F.; Sivasubramaniam, S.; Chua, N.-H. Multiple cis regulatory elements for maximal expression of the cauliflower mosaic virus 35S promoter in transgenic plants. Plant Cell 1:141–150; 1989.
Fang, Y.; Hirsch, A. M. Studying early nodulin gene ENOD40 expression and induction by nodulation factor and cytokinin in transgenic alfalfa. Plant Physiol. 116:53–68; 1998.
Fei, H.; Chaillou, S.; Hirel, B.; Mahon, J. D.; Vessey, J. K. Overexpression of a soybean cytosolic glutamine synthetase gene linked to organ-specific promoters in pea plants grown in different concentrations of nitrate. Planta 216:467–474; 2003.
Felenbok, B.; Sequeval, D.; Mathieu, M.; Sibley, S.; Gwynne, D. I.; Davies, R. W. The ethanol regulon in A. nidulans: characterization and sequence of the positive regulatory gene alcR. Gene 73:385–396; 1988.
Ficker, M.; Wemmer, T.; Thompson, R. D. A promoter directing high level expression in pistils of transgenic plants. Plant Mol. Biol. 35:425–431; 1997.
Forde, B. G.; Heyworth, A.; Pywell, J.; Kreis, M. Nucleotide sequence of a B1 hordein gene and the identification of possible upstream regulatory elements in endosperm storage protein genes from barley, wheat and maize. Nucleic Acids Res. 13:7327–7339; 1985.
Fraisier, V.; Gojon, A.; Tillard, P.; Daniel-Vedele, F. Constitutive expression of a putative high-affinity nitrate transporter in Nicotiana plumbaginifolia: evidence for post-transcriptional regulation by a reduced nitrogen source. Plant J. 23:489–496; 2000.
Fraser, P. D.; Romer, S.; Shipton, C. A.; Mills, P. B.; Kiano, J. W.; Misawa, N.; Drake, R. G.; Schuch, W.; Bramley, P. M. Evaluation of transgenic tomato plants expressing an additional phytoene synthase in a fruitspecific manner. Proc. Natl. Acad Sci. USA 99:1092–1097; 2002.
Fraysse, N.; Couderc, F.; Poinsot, V., Surface polysaccharide involvement in establishing the Rhizobium-legume symbiosis. Eur. J. Biochem. 270:1365–1380; 2003.
Fruhling, M.; Schroder, G.; Hohnjec, N.; Puhler, A.; Perlick, A. M.; Kuster, H. The promoter of the Vicia faba L. gene VfEnod 12 encoding an early nodulin is active in cortical cells and nodule primordia of transgenic hairy roots of Vicia hirsuta as well as in the prefixing zone II of mature transgenic V. hirsuta root nodules. Plant Sci. 160:67–75; 2000.
Gahrtz, M.; Stolz, J.; Sauer, N. A phloem specific sucrose-II symporter from Plantago major L. supports the model of apoplastic phloem loading. Plant J. 6:697–706; 1994.
Galili, G.; Hofgen, R. Metabolic engineering of amino acids and storage proteins in plants. Metab. Engng. 4:3–11; 2002.
Gallic, D. R.; Walbot, V. Identification of the motifs within the tobacco mosaic virus 5′-leader responsible for enhancing translation. Nucleic Acids Res. 11:4631–4638; 1992.
Garbarino, J. E.; Oosumi, T.; Belknap, W. R. Isolation of a polyubiquitin promoter and its expression in transgenic potato plants. Plant Physiol. 109:1371–1378; 1995.
Gasser, C. S.; Winter, J. A.; Hironaka, C. M.; Shah, D. M. Structure, expression, and evolution of the 5-enolpyruvylshikimate-3-phosphate synthase genes of petuma and tomato. J. Biol. Chem. 263:4280–4287; 1988.
Gatz, C.; Lenk, I. Promoters that respond to chemical inducers. Trends Plant Sci. 3:352–358; 1998.
Gilmartin, P. M.; Chua, N. H. Spacing between GT-1 binding sites within a light-responsive element is critical for transcriptional activity. Plant Cell 2:447–455; 1990.
Giuliano, G.; Bartley, G. E.; Scolnik, P. A. Regulation of carotenoid biosynthesis during tomato development. Plant Cell 5:379–387; 1993.
Goddijn, O. J. M.; Lindsey, K.; van der Lee, F. M.; Klap, J. C.; Sijmons, P. C. Differential gene expression in nematode induced feeding structures of transgenic plant harbouring promoter-gusA fusion constructs. Plant J. 4:863–873; 1993.
Goldberg, R. B.; Beals, T. P.; Sanders, P. M. Anther development: basic principles and practical applications. Plant Cell 5:1217–1229; 1993.
Goto, F.; Yoshihara, T.; Shigemoto, N.; Toki, S.; Takaiwa, F. Iron fortification of rice seed by the soybean ferritin gene. Nature Biotechnol. 17:282–286; 1999.
Goulding, S. E.; Olmstead R. G.; Morden, C. W.; Wolfe, K. H. Ebb and flow of the chloroplast inverted repeat. Mol. Gen. Genet. 252:195–206; 1996.
Granger, C. L.; Cyr, R. J. Characterization of the yeast copper-inducible promoter system in Arabidopsis thaliana. Plant Cell Rep. 20:227–234; 2001.
Green, P. J.; Kay, S. A.; Chua, N.-H. Sequence-specific interactions of a pea nuclear factor with light-responsive elements upstream of the rbeS-3A gene. EMBO J. 6:2543–2549; 1987.
Grenier, J.; Potvin, C.; Trundel, J.; Asselin, A. Some thaumatin-like proteins hydrolyse polymeric β-1,3-glucaus. Plant J. 19:473–480; 1999.
Guo, H.; Moose, S. Conserved noncoding sequences among cultivated cereal genomes identify candidate regulatory sequence elements and patterns of promoter evolution. Plant Cell 15:1143–1158; 2003.
Guo, H.-S.; Fei, J.-F.; Xic, Q.; Chua, N.-H. A chemical-regulated inducible RNAi system in plants. Plant J. 34:383–392; 2003.
Gupta, P.; Raghuvanshi, S.; Tyagi, A. K. Assessment of the efficiency of various gene promoters via biolistics in leaf and regenerating seed callus of millets, Eleusine coracana and Echinochloa crusgalli Plant Biotechnol 18:275–282; 2001.
Ha, S. B.; An, G. Identification of upstream regulatory elements involved in the developmental expression of the Arabidopsis thaliana cab1 gene. Proc. Natl. Acad. Sci. USA 85:8017–8021; 1988.
Hadley, C. W.; Miller, E. C.; Schwartz, S. J.; Clinton, S. K. Tomatoes, lycopene and prostate cancer: progress and promise. Exp. Biol. Med. (Maywood) 227:869–880; 2002.
Hajdukiewicz, P. T. J.; Allison, L.; Maliga, P. The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids. EMBO J. 16:4041–4048; 1997.
Hannoufa, A.; Negruk, V.; Eisner, G.; Lemicux, B. The CER3 gene of Arabidopsis thaliana is expressed in leaves, stems, roots, flowers and apical meristems. Plant J. 10:459–467; 1996.
Hattori, T.; Nakagawa, S.; Nakamura, K. High-level of tuberous roots storage protein genes of sweet potato in stems of plantlets grown in vitro on sucrose medium. Plant Mol. Biol. 14:595–604; 1990.
Hershey, H. P.; Stoner, T. D. Isolation and characterization of cDNA clones for RNA species induced by substituted benzenesulfonamides in corn. Plant Mol. Biol. 17:679–690; 1991.
Ho, M.-W.; Ryan, A.; Cummins, J. Cauliflower mosaic virus promoter—a recipe for disaster? Microb. Ecol. Health Dis. 11:194–197; 1999.
Hodgson, J. Scientists avert new GMO crisis. Nature Biotechnol. 18:13; 2000.
Hohnjec, N.; Kuster, H.; Albus, U.; Frosch, S. C.; Becker, J. D.; Puhler, A.; Perlick, A. M.; Fruhling, M. The broad bean nodulin VIENOD18 is a member of a novel family of plant proteins with homologies to the bacterial MJ0577 superfamily. Mol. Gen. Genet. 264:241–250; 2000.
Holton, T. A. Modification of flower colour via manipulation of P450 gene expression in transgenic plants. Drug Metabol. Drug Interact. 12:359–368; 1995.
Holton, T. A.; Brugliera, F.; Lester, D. R.; Tanaka, Y.; Hyland, C. D.; Menting, K. G.; Lu, C. Y.; Farcy, E.; Stevenson, T. W.; Cormish, E. C. Cloning and expression of cytochrome P450 genes controlling flower colour. Nature 366:276–279; 1993.
Holtorf, A.; Apel, K.; Bohlmann, H. Comparison of different constitutive and inducible promoters for the overexpression of transgene in Arabidopsis thaliana Plant Mol. Biol. 29:637–646; 1995.
Huang, C. Y.; Ayliffe, M. A.; Timmis, J. N. Direct measurement of the chloroplast DNA into the nucleus. Nature 422:72–76; 2003a.
Huang, C. Y.; Ayliffe, M. A.; Timmis, J. N. Organelle evolution meets biotechnology. Nature Biotechnol. 21:489–490; 2003b.
Huang, F.; Buschman, L. L.; Higgins R. A.; McGaughey, W. H. Inheritance to Bacillus thuringiensis toxin (Dispel ES) in European corn borer. Science 284:965–967; 1999.
Hull, R.; Covey, S. N.; Dale, P. Genetically modified plants and the 35S promoter: assessing the risks and enhancing the debate. Microb. Ecol. Health Dis. 12:1–5; 2000.
Husebye, H.; Chadchawan, S.; Winge, P.; Thangstad, O. P.; Bones, A. M. Guard cell-phloem idioblast-specific expression of thioglucoside glucohydrolase 1 (myrosinase) in Arabidopsis. Plant Physiol. 128:1180–1188; 2002.
Imlau, A.; Truernit, E.; Sauer, N. Cell-to-cell and long-distance trafficking of the green fluorescent protein in the phloem and symplastic unloading of the protein into sink tissues. Plant Cell 11:309–322; 1999.
Inaba, T.; Nagano, Y.; Reid, J. B.; Sasaki, Y. DE1, A 12-base pair cis-regulatory element sufficient to confer dark-inducible and light down-regulated expression to a minimal promoter in pea. J. Biol. Chem. 275:19723–19727; 2000.
Jefferson, R.; Goldsbrough, A.; Bevan, M. Transcriptional regulation of a patatin-1 gene in potato. Plant Mol. Biol. 14:995–1006; 1990.
Jeon, J.-S.; Chung, Y.-Y.; Lee, S.; Yi, G.-H.; Oh, B.-G.; An, G. Isolation and characterization of an anther-specific gene, RA8, from rice (Oryza sativa. L.). Plant Mol. Biol. 39:35–44; 1999.
Jones, M. A.; Grierson, C. S. A simple method for obtaining cell-specific cDNA from small numbers of growing root-hair cells in Arabidopsis thaliana J. Exp. Bot. 54:1373–1378; 2003.
Juergensen, K.; Scholz-Starke, J.; Sauer, N.; Hess, P.; van Bel, A. J. E.; Grundler, F. M. W. The companion cell-specific Arabidopsis disaccharide carrier AtSUC2 is expressed in nematode-induced syncytia. Plant Physiol. 131:61–69; 2003.
Kaiser, J. Panel urges further study of biotech corn. Science 290:1867; 2000.
Kaplinsky, N.; Braun, D.; Lisch, D.; Hay, A.; Hake, S.; Freeling, M. Maize transgene results in Mexico are artefacts. Nature 416:601; 2002.
Katz, S. L. Future vaccines and a global perspective. Lancet 350:1767–1770; 1997.
Kawalleck, P.; Somssich, I. E.; Feldbrugge, M.; Hahlbrock, K.; Weisshaar, B. Polyubiquitin gene expression and structural properties of the ubi 2–4 gene in Petrosclinum crispum Plant Mol. Biol. 21:673–684; 1993.
Kay, R.; Chan, A.; Daly, M.; McPherson J. Duplication of CaMV 35S promoter sequences creates a strong enhancer for plant genes. Science 236:1299–1302; 1937.
Keeler, S. J.; Maloney, C. L.; Webber, P. Y.; Patterson, C.; Hirata, L. T.; Falco, S. C.; Rice, J. A. Expression of de novo high-lysine α-helical coiled-coil proteins may significantly increase the accumulated levels of lysine in mature seeds of transgenic tobacco plants. Plant Mol. Biol. 34:15–29; 1997.
Keil, M.; Sanchez-Serrano, J.; Schell, J.; Willmitzer, L. Localization of elements important for the wound-inducible expression of a chimeric potato proteinase inhibitor II-CAT gene in transgenic tobacco plants. Plant Cell 2:61–70; 1990.
Keller, B.; Baumgartner, C. Vascular-specific expression of the bean Grp-1.8 gene is negatively regulated. Plant Cell 3:1639–1646; 1991.
Kidwell, M. G.; Lisch, D. Transposable elements as sources of variation in animals and plants. Proc. Natl Acad. Sci. USA 94:7704–7711; 1997.
Kirsch, C.; Takamiya-Wik, M.; Schmeilzer, E.; Hahlbrock K.; Somssich, I. E. A novel regulatory element involved in rapid activation of parsley EL17 gene family members by fungal elicitor or pathogen infection. Mol. Plant Pathol. 1:243–251; 2000.
Kloti, A.; He, X.; Potrykus, I.; Hohn, T.; Futterer, J. Tissue-specific silencing of a transgene in rice. Proc. Natl. Acad. Sci. USA 99:10881–10886; 2002.
Klotz, K. L.; Lagrimini, L. M. Phytohormone control of the tobacco anionic peroxidase promoter. Plant Mol. Biol. 31:565–573; 1996.
Kluth, A.; Sprunck, S.; Becker, D.; Lorz, H.; Lutticke, S. 5′ deletion of a gbssl promoter region leads to changes in tissue and developmental specificities. Plant Mol. Biol. 49:669–682; 2002.
Kneissl, M. L.; Deikman, J. The toinato E8 gene influences ethylene biosynthesis in fruit but not in flowers. Plant Physiol. 112:537–547; 1996.
Kohli, A.; Griffiths, S.; Palacios, N.; Twyman, R. M.; Vain, P.; Laurie, D. A.; Christou, P. Molecular characterization of transforming plasmid rearrangements in transgenic rice reveals a recombination hotspot in the CaMV 35S promoter and confirms the predominance of microhomology mediated recombination. Plant J. 17:591–601; 1999.
Koltunow, A. M.; Truettner, J.; Cox, K. H.; Walroth, M.; Goldberg, R. B. Different temporal and spatial gene expression patterns occur during anther development. Plant Cell 2:1201–1224; 1990.
Kota, M.; Daniell, H.; Varma, S.; Garczynski, S. F.; Gould, F.; Moar, W. J. Overexpression of the Bacillus thuringiensis (Bt) Cry2Aa2 protein in chloroplasts confers resistance to plants against susceptible and Bt-resistant insects. Proc. Natl Acad. Sci. USA 96:1840–1845; 1999.
Krizek, B. A.; Prost, V.; Joshi, R. M.; Stoming, T.; Glenn T. C. Developing transgenic Arabidopsis plants to be metal-specific bioindicators. Environ. Toxicol. Chem. 22:175–181; 2003.
Kuhlemeier, C.; Cuozzo, M.; Green, P.; Goyvaerts, E.; Ward, K.; Chua, N.-H. Localization and conditional redundancy of regulatory elements in rbcS-3A, a pea gene encoding the small subunit of ribulose-bisphosphate carboxylase. Proc. Natl Acad. Sci. USA 85:4662–4666;1988.
Kuhlemeier, C.; Fluhr R.; Green, P. J.; Chua, N.-H. Sequences in the pea rbcS-3A gene have homology to constitutive mammalian enhancers but function as negative regulatory elements. Genes Dev. 1:247–255; 1987.
Kuhn, C.; Hajirezaci, M.-R.; Fernie, A. R.; Roessner-Tunali, U.; Czechowski, T.; Hirner, B.; Frommer, W. B. The sucrose transporter StSUT1 localizes to sieve elements in potato tuber phloem and influences tuber physiology and development. Plant Physiol. 131:102–113; 2003.
Kumpatla, S. P.; Chandrasekharan, M. B.; Iyer, L. M.; Li, G.; Hall, T. C. Genome intruder scanning and modulation systems and transgene silencing. Trends Plant Sci. 3:97–104; 1998.
Lam, E.; Benfey, P. N.; Gilmartin, P. M.; Fang, R. X.; Chua, N.-H. Sitespecific mutations alter in vitro factor and change promoter expression pattern in transgenic plants. Proc. Natl. Acad. Sci. USA 86:7890–7894; 1989.
Lam, E.; Chua, N. H. ASF-2: a factor that binds to the cauliflower mosaic virus 35S promoter and a conserved GATA motif in Cab promoters. Plant Cell 1:1147–1156; 1989.
Lamacchia, C.; Shewry, P. R.; Di Fonzo, N.; Forsyth, J. L.; Harris, N.; Lazzeri, P. A.; Napier, J. A.; Halford, N. G.; Barcelo, P. Endospermspecific activity of a storage protein gene promoter in transgenic wheat seed. J. Exp. But. 52:243–250; 2001.
Lange, B. M.; Croteau, R. Genetic engineering of essential oil production in mint. Curr. Opin. Plant Biol. 2:139–144; 1999.
Lauridsen, P., Franssen, H.; Stougaard, J.; Bisseling, T.; Marcker, K. A. Conserved regulation of the soybean early nodulin ENOD2 gene promoter in determinate and indeterminate transgenic root nodules. Plant J. 3:484–492, 1993.
Leach, F.; Aoyagi, K. Promoter analysis of the highly expressed rolC and rolD root-inducing genes of Agrobacterium rhizogenes: enhancer and tissue-specific DNA determinants are dissociated. Plant Sci. 79:69–76; 1991.
Lescot, M.; Déhais, P.; Thijs, G.; Marchal, K.; Moreau, Y.; Van de Peer, Y.; Rouzé, P.; Rombauts, S. Plant CARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 30:325–327; 2002.
Lessard, P. A.; Allen, R. D.; Fujiwara, T.; Beachy, R. N. Upstream regulatory sequences from two beta-conglycinin genes. Plant Mol. Biol. 5:873–885; 1993.
Lessard, P. A.; Kulaveerasingam, H.; York, G. M.; Strong, A.; Sinskey, A. Manipulating gene expression for the metabolic engineering in plants. Metab. Engng. 4:67–79; 2002.
Lewinsohn, E.; Schalechet, F.; Wilkinson, J.; Matsui, K.; Tadmor, Y.; Nam, K.-H.; Amar, O.; Lastochkin, E.; Larkov, O.; Ravid, U.; Hiatt, W.; Gepstein, S.; Pichersky, E. Enhanced levels of the aroma and flavor compound S-linalool by metabolic engineering of the terpenoid pathway in tomato fruits. Plant Physiol. 127:1256–1265; 2001.
Li, Z.; Jayasankar, S.; Gray, D. J. Expression of a bifunctional green fluorescent protein (GFP) fusion marker under the control of three constitutive promoters and enhanced derivatives in transgenic grape (Vitis vinifera). Plant Sci. 160:877–887; 2001.
Liu, X.-J.; Prat, S.; Willmitzer, L.; Frommer, W. B. Cis regulatory elements directing tuber-specific and sucrose-inducible expression of a chimeric class I patatin promoter/GUS-gene fusion. Mol. Gen. Genet. 223:401–406; 1990.
Liu, X.-J.; Rocha-Sosa, M.; Hummel, S.; Willmitzer, L.; Frommer, W. B. A detailed study of the regulation and evolution of the two classes of patatin genes in Solanum tuberosum L. Plant Mol. Biol. 17:1139–1154; 1991.
Logemann, J.; Lipphardt, S.; Lorz, H.; Hauser, I.; Willmitzer, L.; Schell, J. 5′ upstrean, sequences from the wun1 gene are responsible for gene activation by wounding in transgenic plants. Plant Cell 1:151–158; 1989.
Losey, J. E.; Raynor, L. S.; Carter, M. C. Transgenic pollen harms monarch larvae. Nature 399:214; 1999.
MacKnight, R. C.; Reynolds, P. H. S.; Farnden, K. J. F. Analysis of the lupin Nodulin-45 promoter: conserved regulatory sequences are important for promoter activity. Plant Mol. Biol. 27:457–466; 1995.
Maeo, K.; Tomiya, T.; Hayashi, K.; Akaiki, M.; Morikama, A.; Ishiguro, S.; Nakamura, K. Sugar-responsible elements in the promoter of a gene for β-amylase of sweet potato. Plant Mol. Biol. 46:627–637; 2001.
Maeshima, M.; Sasaki, T.; Asahi, T. Characterization of major proteins in sweet potato tubcrous roots. Phytochemistry 24:1899–1902; 1985.
Maiti, I. B.; Ghosh, S. K.; Gowda, S.; Kiernan, J.; Shepherd, R. J. Promoter/leader deletion analysis and plant expression vectors with the figwort mosaic virus (FMV) full length transcript (FLt) promoter containing single or double enhancer domains. Transgenic Res. 6:143–156; 1997.
Maliga, P. Engineering the plastid genome of higher plants.Curr. Opin. Plant Biol. 5:164–172; 2002.
Mann, C. C. Has CM corn invaded Mexico? Science 295:1617–1618; 2002.
Mariani, C.; DeBeuckeleer, M.; Truettnet, J.; Leemans, J.; Goldberg, R. Induction of male sterility in plants by a chimacric ribonuclease gene. Nature 347:737–741; 1990.
Martinez, A.; Sparks, C.; Hart, C. A.; Thompson, J.; Jepson, I. Ecdysone agonist inducible transcription in transgenic tobacco plants. Plant J. 19:97–106; 1999.
Marzabal, P.; Busk, P. K.; Ludevid, M. D.; Torrent, M. The bifactorial endosperm box of gamma-zein gene: characterisation and function of the Pb3 and GZM cis-acting elements. Plant J. 16:41–52; 1998.
McBride, K. E.; Schaaf, D. J.; Daley, M.; Stalker, D. M. Controlled expression of plastid transgenes in plants based on a nuclear DNA-encoded and plastid targeted T7 RNA polymerase. Proc. Natl Acad. Sci. USA 91:7301–7305; 1994.
McBride, K. E.; Svab, Z.; Schaaf, D. J.; Hogan, P. S.; Stalker D. M.; Maliga, P. Amplification of a chimeric Bacillus gene in chloroplasts leads to an extraordinary level of an insecticidal protein in tobacco. Bio/Technology 13:362–365; 1995.
McCaskill D.; Croteau, R. Strategies for bioengineering the development and metabolism of glandular tissues in plants Nature Biotechnol. 17:31–36; 1999.
McDonald, J. F. Macroevolution and retroviral elements: insertion of viral-like DNA segments may bring about rapid and dramatic changes in gene regulation and development. Bioscience 40:183–191; 1999.
McElroy, D.; Blowers, A. D.; Jenes, B.; Wu, R. Construction of expression vectors based on the rice actin 1 (Actl) 5′ region for use in monocot transformation. Mol. Gen. Genet. 231:150–160; 1991.
Mett, V. L.; Lochhead, L. P.; Reynolds, P H. S. Copper-controllable gene expression system for whole plants. Proc. Natl Acad Sci. USA 90:4567–4571; 1993.
Mett, V. L.; Podivinsky, E.; Tennant, A. M.; Lochhead, L. P.; Jones, W. T.; Reynolds, P. H. S. A system for tissue-specific copper-controllable gene expression in transgenic plants: nodule-specific antisense of aspartate aminotransferase-P2. Transgenic Res. 5:105–113; 1996.
Metz, M.; Fütterer, J. Suspect evidence of transgenic contamination. Nature Advance (online publication) 416:600–601; 2002.
Meyer, P.; Saedler, H. Homology-dependent gene silencing in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:23–48; 1996.
Mohammed, A.; Douches, D. S.; Pett, W.; Grafius E.; Coombs, J.; Liswidowati, Li. W.; Madkour, M. A. Evaluation of potato tuber moth (Lepidoptera: Gelechiidue) resistance in tubers of Bt-cry5 transgenic potato lines. J. Econ. Entomol. 93:472–476; 2000.
Mol, J.; Cornish, E.; Mason, J.; Koes, R. Novel coloured flowers. Curr. Opin. Biotechnol. 10:198–201; 1999.
Montgomery, J.; Pollard, V.; Deikman, J.; Fischer, R. L. Positive and negative regulatory regions control the spatial distribution of polygalacturonse transcription in tomato fruit pericarp. Plant Cell 5:1049–1062; 1993.
Morel, J.-B.; Tepfer, M. Pour une èvaluation scientifique des risques: le cas du promoteur 35S. Biofutur 201:32–35; 2000.
Nagata, N.; Saito, C.; Sakai, A.; Kuroiwa, H.; Kuroiwa, T. The selective increase or decrease of organellar DNA in generative cells just after pollen mitosis one controls cytoplasmic inheritance. Planta 209:53–65; 1999.
Narusaka, Y.; Nakashima, K.; Shinwari, Z.K.; Sakuma, Y.; Furihata, T.; Abe, H.; Narusaka, M.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant J 34:137–148; 2003.
Nelson, G. C., ed. Genetically modified organisms in agriculture. Economics and politics. San Diego, CA: Academic Press; 2001.
Nicholass, F. J.; Smith, C. J. S.; Schuch, W.; Bird, C. R.; Grierson, D. High levels of ripening-specific reporter gene expression directed by tomato fruit polygalacturonase gene-flanking regions. Plant Mol. Biol. 28:423–435; 1995.
Nomura, M.; Katayama, K.; Nishimura, A.; Ishida, Y.; Ohta, S.; Komari, T.; Miyao-Tokutomi, M.; Tajima, S.; Matsuoka, M. The promoter of rbcS in a C3 plant (rice) directs organ-specific, light-dependent expression in a C4 plant (maize), but does not confer bundle sheath cell-specific expression. Plant Mol. Biol. 44:99–106; 2000.
Nunberg, A. N.; Li, Z., Bogue, M. A.; Vivekananda, J.; Reddy, A. S.; Thomas, T. L. Developmental and hormonal regulation of sunflower helianthinin genes: proximal promoter sequences confer regionalized seed expression. Plant Cell 6:473–486; 1994.
Odell, J. T.; Nagy, F.; Chua, N.-H. Identification of DNA sequences required for activity of the cauliflower mosaic virus 35S promoter. Nature 313:810–812; 1985.
Ohme-Takagi, M.; Shinshi, H. Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell 7:173–182; 1995.
Ohta, S.; Hattori, T.; Morikami, A.; Nakamura, K. High-level expression of a sweet potato sporamin gene promoter; β-glucuronidase (GUS) fusion gene in the stems of transgenic tobacco plants is conferred by multiple cell type-specific regulatory elements. Mol. Gen. Genet. 225:369–378; 1991.
Opperman, C. H.; Taylor, C. G.; Conkling, M. A. Root-knot nematode-directed expression of a plant root-specific gene. Science 263:221–223; 1994.
Orozco, B. M.; Ogren, W. L. Localization of light-inducible and tissue-specific regions of the spinach ribulose bisphophate carboxylase/oxygenase (rubisco) activase promoter in transgenic tobacco plants. Plant Mol. Biol. 23:1129–1138; 1993.
Paiva, E.; Lister, R. M.; Park, W. D. Induction and accumulation of major tuber proteins of potato in stems and petioles. Plant Physiol. 71:161–168; 1983.
Persans, M. W.; Wang, J.; Schuler, M. A.. Characterization of maize cytochrome P450 monooxygenases induced in response to safeners and bacterial pathogens. Plant Physiol. 125:1126–1138; 2001.
Picchulla, B.; Merforth, N.; Rudolph, B. Identification of tomato Lhc promoter regions necessary for circadian expression. Plant Mol. Biol. 38:655–662; 1998.
Plesch, G.; Ehrhardt, T.; Mucller-Rocber, B. Involvement of TAAAG elements suggests a role for Dof transcription factors in guard cell-specific gene expression. Plant J. 28:455–464; 2001.
Plesse, B.; Criqui, M.-C.; Durr, A.; Parmentier, Y.; Fleck, J.; Genschik, P. Effects of the polyubiquitin gene Ubi.U4 leader intron and first ubiquitin monomer on reporter gene expression in Nicotiana tabacum. Plant Mol. Biol. 45:655–667; 2001.
Portis, A. R. Regulation of ribulose-1,5-bisphosphate carboxylase/oxygenase activity. Annu. Rev. Plant Physiol. Plant Mol. Biol. 43:415–437; 1992.
Poulsen, C.; Chua, N.-H. Dissection of 5′ upstream sequences for selective expression of Nicotiana plumbaginfolia rbcS-8B gene. Mol. Gen. Genet. 214:13–23; 1983.
Quist, D.; Chapela, I. H. Transgenic DNA introgressed into traditional maize landraces in Oaxaca. Mexico. Nature 414:541–543; 2001.
Ramlov, K. B.; Laursen, N. B.; Stougaard, J.; Marcker, K. A. Site-directed mutagenesis of the organ-specific element in the soybean leghemoglobin lbc3 gene promoter. Plant J. 4:577–580; 1993.
Rao, A. V. Lycopene, tomatoes and the prevention of coronary heart disease. Exp. Biol. Med. (Maywood) 227:908–913; 2002.
Ricsmcier, J. W.; Willmitzer, L.; Frommer, W. B. Evidence for an essential role of the sucrose transporter in phloem loading and assimilate partitioning. EMBO J. 13:1–7; 1994.
Roslan, H. A.; Salter, M. G.; Wood, C. D.; White, M. R. H.; Croft, K. P.; Robson, F.; Coupland, G.; Doonan, J.; Laufs, P.; Tomsett, A. B.; Caddick, M. X. Characterization of the ethanol-inducible alc gene-expression system in Arabidopsis thaliana. Plant J 28:225–235; 2001.
Ruf, S.; Hermann, M.; Berger, I. J.; Carrer, H.; Bock, R. Stable genetic transformation of tomato plastids and expression of a foreign protein in fruit. Nature Biotechnol 19:870–875; 2001.
Rushton, P. J.; Reinstadler, A.; Lipka, V.; Lippok, B.; Somssich, I. E. Synthetic plant promoters containing defined regulatory elements provide novel insights into pathogen-and wound-induced signaling. Plant Cell 14:749–762; 2002.
Rushton, P. J.; Torres, J. T.; Parniske, M.; Wernert, P.; Hahlbrock, K.; Somssich, I. E. Interaction of elicitor-induced DNA binding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO J. 15:5690–5700; 1996.
Russell, P. J. Genetics. 4th edn. New York: Harper Collins College; 1996.
Salter, M. G.; Paine, J. A.; Riddell, K. V.; Jepson, I.; Greenland, A. J.; Caddick, M. X.; Tomsett, A. B. Characterisation of the ethanol-inducible alc gene expression system for transgenic plants. Plant J. 16:127–132; 1998.
Sandal, N. N.; Bojsen, K.; Marcker, K. A. A small family of nodule-specific genes from soybean. Nucleic Acids Res. 15:1507–1519; 1987.
Sandhu, J. S.; Krasnyanski, S. E.; Domier, L. L.; Korban, S. S.; Osadjan, M. D.; Buetow, D. E. Oral immunization of mice with transgenic tomato fruit expressing respiratory syncytial virus-F protein induces a systemic immune response. Transgenic Res. 9:127–135; 2000.
Sanger, M.; Daubert, S.; Goodman, R. M. Characteristics of a strong promoter from the figwort mosaic virus: comparison with the analogous 35S promoter from cauliflower mosaic virus and the regulated mannopine synthase promoter. Plant Mol. Biol. 14:433–443; 1990.
Sassa, H.; Ushijima, K.; Hirano, H. A pistil-speeific thaumatin/PR5-like protein gene of Japanese pear (Pyrus serotina): sequence and promoter activity of the 5′ region in transgenic tobacco. Plant Mol. Biol. 50:371–377; 2002.
Schaffner, A. R.; Sheen, J. Maize rheS promoter activity depends on sequence elements not found in dicot rbeS promoters. Plant Cell 3:997–1012; 1991.
Scheid, O. M.; Probst, A. V.; Afsar, K.; Pazkowski, J. Two regulatory levels of transcriptional gene silencing in Arabidopsis. Proc. Natl. Acad. Sci. USA 99:13659–13662; 2002.
Schenk, P. M.; Remans, T.; Sagi, L.; Elliott, A. R.; Dietzgen, R. G.; Swennen, R.; Ebert, P. R.; Grof, C. P. L.; Manners, J. M. Promoters for pregenomic RNA of banana streak badnavirus are active for transgene expression in monocot and dicot plants. Plant Mol. Biol. 47:399–412; 2001.
Schoenbeek, M. A.; Temple, S. J.; Trepp, G. B.; Rlumenthal, J. M.; Samac, D. A.; Gantt, J. S.; Hernandez, G.; Vance, C. P. Decreased NADH glutamate synthase activity in nodules and flowers of alfalfa (Medicago sativa L.) transformed with an antisense glutamate synthase transgene. J. Exp. Bot. 51:29–39; 2000.
Scott, S. E.; Wilkinson, M. J. Low probability of chloroplast movement from oilsed rape (Brassica napas) into wild Brassica rapa. Nature Biotechnol. 17:390–392; 1999.
Sengupta-Gopalan, C.; Reichert, N. A.; Barker, R. F.; Hall, T. C.; Kemp, J. D. Developmentally regulated expression of the bean β-phaseolin gene in tobacco seed. Proc. Natl Acad. Sci. USA 82:3320–3324, 1985.
Shen, S.; Li, Q.; He, S.-Y.; Barker, K. R.; Li, D.; Hunt, A. G. Conversion of compatible plant-pathogen interactions into incompatible interactions by expression of the Pseudomonas syringae pv. syringae 61 hrmA gene in transgenic tobacco plants. Plant J. 23:205–213; 2000.
Shiba, H.; Takayama, S.; Iwano, M.; Shimosato, H.; Funato, M.; Nakagawa, T.; Che, F.-S.; Suzuki, G.; Watanabe, M.; Hinata, K.; Isogai, A. A pollen coat protein SPII/SCR, determines the pollen S-specificity in the self-incompatibility of Brassica species. Plant Physiol. 125:2095–2103; 2001.
Shiina, T.; Allison, L.; Maliga, P. rbcL transcript levels in tobacco plastids are independent of light: reduced dark transcription rate is compensated by increased mRNA stability. Plant Cell 10:1713–1722; 1998.
Shimkets, R. A.; Lowe, D. G.; Tai, J. T.; Sehl, P.; Jin, H.; Yang, R.; Predki, P. F.; Rothberg, B. E.; Murtha, M. T.; Roth, M. E.; Shenoy, S. G.; Windemuth, A.; Simpson, J. W.; Simons, J. F.; Daley, M. P.; Gold, S. A.; McKenna, M. P.; Hillan, K.; Went, C. T.; Rothberg, J. M. Gene expression analysis by transcript profiling coupled to a gene database query. Nature Biotechnol. 17:798–803; 1999.
Shintani, D.; DellaPenna, D. Elevating the vitamin E content of plants through metabolic engineering. Science 282:2098–2100; 1998.
Shiva, V. Viar against nature and the people of the South. In: Andersen, S., ed. Views from the South. The effects of globalization and the WTO on Third World countrics. Chicago: Food First Books and The International Forum on Globalization; 2000:91–125.
Sidorov, V. A.; Kasten, D.; Pang, S.-Z.; Hajdukiewicz, P. T. J.; Staub, J. M.; Nehra, N. S. Stable chloroplast transformation in potato: use of green fluorescent protein as a plastid marker. Plant J. 19:209–216; 1999.
Siebertz, B.; Logemann, J.; Willmitzer, L.; Schell, J. cis-Analysis of the wound-inducible promoter wunl in transgenic tobacco plants and histochemical localization of its expression. Plant Cell 1:961–968; 1989.
Stadler, R.; Brandner, J.; Schulz, A.; Gahrtz, M.; Sauer, N. Phloem loading by the PmSUC2 sucrose carrier from Plantago major into companion cells. Plant Cell 7:1545–1554; 1995.
Stadler, R.; Sauer, N. The Arabidopsis thaliana atSUC2 gene is specifically expressed in companion cells. Bot. Acta 109:299–306; 1996.
Staub, J. M.; Garcia, B.; Graves, J.; Hajdukiewicz, P. T. J.; Hunter, P.; Nehra, N. S.; Paradkar, V.; Schlitler, M.; Carroll, J. A.; Spatola, L.; Ward, D.; Ye, G.; Russell, D. A. High-yield production of a human therapeutic protein in tobacco chloroplasts. Nature Biotechnol. 18:333–338; 2000.
Staub, J. M.; Maliga, P. Translation of psbA mRNA is regulated by light via the 5′-untranslated region in tobacco plastids. Plant J. 6:547–553; 1994.
Staub, J. M.; Maliga, P. Expression of a chimeric uidA gene indicates that polycistronic mRNAs are efficiently translated in tobacco plastids. Plant J. 7:845–848; 1995.
Stougaard, J.; Marcker, K. A.; Otten, L.; Schell, J. Nodule-specific expression of a chimeric soybean leghaemoglobin gene in transgenic Lotus corniculatus. Nature 321:669–674; 1986.
Stougaard, J.; Sandal, N. N.; Groen, A.; Kuhle, A.; Mareker, K. A. 5′ Analysis of the soybean leghemoglobin lbc 3 gene: regulatory elements required for promoter activity and organ specificity. EMBO J. 6:3565–3569; 1987.
Strozycki, M.; Karlowski, W. M.; Dessaux, Y.; Petit, A.; Legocki, A. B. Lupine beghemoglobin I: expression in transgenic Lotus and tobacco tissues. Mol. Gen. Genet. 263:173–182; 2000.
Stniver, M. H.; Custers, J. H. H. V. Engineering disease resistance in plants. nature 411:865–868; 2001.
Sunilkuman, G.; Connell, J. P.; Smith, C. W.; Reddy, A. S.; Rathore, K. S. Cotton α-globulin promoter: isolation and functional characterization in transgenic cotton, Arabidopsis, and tobacco. Transgenic Res. 11:347–359; 2002.
Svab, Z.; Hajdukiewicz, P. T. J.; Maliga, P. Stable transformation of plastids in higher plants. Proc. Natl Acad. Sci. USA 87:8526–8530; 1990.
Szabados, L.; Ratet, P.; Grunenberg, B.; de Bruijn, F. J. Functional analysis of the Sesbania rostrata leghemoglobin glb3 gene 5′-upstream region in transgenic Lotus corniculatus and Nicotiana tabacum. Plant Cell 2:973–986; 1990.
Szezyglowski, K.; Potter, T.; Stoltzfus, J.; Fujimoto, S. Y.; de Bruijn, F. J. Differential expression of the Sesbania rostrata leghemoglobin glb3 gene promoter in transgenic legume and non-legume plants. Plant Mol. Biol. 31:931–935; 1996.
Szymanski, D. B.; Lloyd, A. M.; Marks, D. Progress in the molecular genetic analysis of trichome initiation and morphogenesis in Arabidopsis. Trends Plant Sci. 5:214–219; 2000.
Takayama, S.; Shiba, H.; Iwano, M.; Shimosato, H.; Che, F.-S.; Kai, N.; Watanabe, M.; Suzuki, G.; Hinata, K.; Isogai, A. The pollen determinant of self-incompatibility in Brassica campestris. Proc. Natl Acad. Sci. USA 97:1920–1925; 2000.
Takeda, S.; Sugimoto, K.; Otsuki, H.; Hirochika, H. A 13-bp cis-regulatory element in the LTR promoter of the tobacco retrotransposon Ttol is involved in responsiveness to tissue culture, wounding, methyl jasmonate and fungal glicitors. Plant J. 18:383–393; 1999.
Taylor, L. P.; Helper, P. K. Pollen germination and tube growth. Annu. Rev. Plant Physiol. Plant Mol. Biol. 48:461–491; 1997.
Taylor, S. L.; Hefle, S. L. Genetically engineered foods: implications for food allergies. Curr. Opin. Allergy Clin. Immunol. 2:249–252; 2002.
Thorsness, M. K.; Kandasamy, M. K.; Nasrallah, M. E.; Nasrallah, J. B. A Brassica S-locus gene promoter targets toxie gene expression and cell death to the pistil and pollen of transgenic Nicotiana. Dev. Biol. 143:173–184; 1991.
Toriyama, K.; Thorsness, M. K.; Nasrallah, J. B.; Nasrallah, M. E. A Brassica S locus gene promoter directs sporophytic expression in the anther tapetum of transgenio Arabidopsis. Dev. Biol. 143:427–431; 1991.
Truernit, E.; Sauer, N. The promoter of the Arabidopsis thaliana SUC2 sucrose-H+ symporter gene directs expression of ß-glucuronidase to the phloem: evidence for phloem loading and unloading by SUC2. Planta 196:564–570; 1995.
Twell, D.; Wing, R.; Yamaguchi, J.; McCormick, S. Isolation and expression of an anther-specific gene from tomato. Mol. Gen. Genet. 217:240–245; 1989.
Twell, D.; Yamaguchi, J.; McCormick, S. Pollen-specific gene expression in transgenic plants: coordinate regulation of two different tomato gene promoters during microsporogenesis. Development 109:705–713; 1990.
Ulmasov, T.; Murfett, J.; Hagen, G.; Guilfoyle, T. J. Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971; 1997.
Uno, Y.; Furihata, T.; Abe, H.; Yoshida, R.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Novel Arabidopsis bZIP transcription factors involved in an abscisic-acid-dependent signal transduction pathway under drought and high salinity conditions. Proc. Natl Acad. Sci. USA 97:11632–11637; 2000.
Ursin, V. M.; Yamaguchi, J.; McCormick, S. Gametophytic and sporophytic expression of anther-specific genes in developing tomato anthers. Plant Cell 1:727–736; 1989.
Urwin, P. F.; Moller, S. G.; Lilley, C. J.; McPherson, M. J.; Atkinson, H. J. Continual green-fluorescent protein monitoring of cauliflower mosaic virus 35S promoter activity in nematode-induced feeding cells in Arabidopsis thaliana. Mol. Plant Microbe Interact. 10:394–400; 1997.
Vaden, V. R.; Melcher, U. Recombination sites in cauliflower mosaic virus DNAs: implications for mechanisms of recombination. Virology 177: 717–726.
van der Geest, A. H. M.; Hall, T. C. A 68bp element of the ß-phaseolin promoter functions as a seed-specific enhancer. Plant Mol. Biol. 32:579–588; 1996.
van der Geest, A. H. M.; Hall, T. C. The ß-phascolin 5' matrix attachment region acts as an enhancer facilitator. Plant Mol. Biol. 33:553–557; 1997.
van der Geest, A. H. M.; Hall, G. E. J.; Spiker, S.; Hall, T. C. The ß-phaseolin gene is flanked by matrix attachment regions. Plant J. 6:413–423; 1994.
Verdaguer, B.; de Kochko, A.; Beachy, R. N.; Fauquet, C. Isolation and expression in transgenic tobacco and rice plants, of the cassava yein mosaic virus (CsVMV) promoder. Plant Mol. Biol. 31:1129–1139; 1996.
Verdaguer, B.; de Kochko, A.; Fux, C. L.; Beachy, R. N.; Fauquet, C. Functional organization of the cassava vein mosaic virus (CsVMV) promoter. Plant Mol. Biol. 37:1055–1067; 1998.
Vernhettes, S.; Grandbastien, M. A.; Casacuberta, J. M. In vivo characterization of transcriptional regulatory sequences involved in the defense-associated expression of the tobacco retrotransposon Tntl. Plant Mol. Biol. 35:673–679; 1997.
Vijn, L.; Christiansen, H.; Lauridsen, P.; Kardailsky, I.; Quandt, H.-J.; Broet, I.; Drenth, J.; Jensen, E. O.; van Kammen, A.; Bisseling, T. A 200 bp region of the pea ENOD12 promoter is sufficient for nodule-specific and Nod factor induced expression. Plant Mol. Biol. 28:1103–1110; 1995.
Vissor, R. G. F.; Stolte, A.; Jacobsen, E. Expression of a chimacric granulebound starch synthase-GUS gene in transgenic potato plants. Plant Mol. Biol. 17:691–699; 1991.
Wakeley, P. R.; Rogers, H. J.; Rozyeka, M.; Greenland, A. J.; Hussey, P. J. A maize pectin methylesterase-like gene, ZmC5, specifically expressed in pollen. Plant Mol Biol. 37:187–192; 1998.
Wang, E.; Gan, S.; Wagner, G. J. Isolation and characterization of the GYP71D16 trichome-specific promoter from Nicotiana tabacum L. J. Exp. Bot. 53:1891–1897; 2002.
Wang, X.; Zafian, P.; Choudhary, M.; Lawton, M. The PR5K receptor protein kinase from Arabidopsis thaliana is structurally related to a family of plant defense proteins. Proc. Natl Acad. Sci. USA 93:2598–2602; 1996.
Weeks, J. T.; Anderson, O. D.; Blechl, A. E. Rapid production of multiple independent lines of fertile transgenic wheat (Triticum aestirum). Plant Physiol. 102:1077–1084; 1993.
Weinmann, P.; Gossen, M.; Hillen, W.; Bujard, H.; Gatz, C. A chimeric transactivator allows tetracycline responsive gene expression in whole plants. Plant J. 5:559–569; 1994.
Wingender, F.; Chen, X.; Hehl, R.; Karas, H.; Liebich, I.; Matys, V.; Meinhardt, T.; Prüß, M.; Reuter, I.; Schacherer, F. TRANSFAC: an integrated system for gene expression regulation. Nucleic Acids Res. 28:316–319; 2000.
Wright, K. M.; Roberts, A. G.; Martens, H. J.; Sauer, N.; Oparka, K. J. Structural and functional vein maturation in developing tobacco leaves in relation to AISUC2 promoter activity. Plant Physiol. 131:1555–1565; 2003.
Xu, D.; Duan, X.; Wang, B.; Hong, B.; Ho, T.-H.D.; Wu, R. Expression of a late embryogenesis abundant protein gene. HVAI, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol. 110:249–257; 1996.
Xu, D.; McElroy, D.; Thornburg, R. W.; Wu, R. Systemic induction of a potato pin2 promoter by wounding, methyl jasmonate, and abscisic acid in transgenic rice plants. Plant Mol. Biol. 22:573–588; 1993.
Yamada, T.; Ishige, T.; Shiota, N.; Inui, H.; Ohkawa, H.; Ohkawa, Y. Enhancement of metabolizing herbicides in young tubers of transgenic potato plants with the rat CYPIAI gene. Theor. Appl. Genet. 105:515–520; 2002.
Yamaguchi-Shinozaki, K.; Shinozaki, K. A novel cis-acting element in a Arabidopsis gene is involved in responsivenness to drought, low—temperature, or high-salinity stress. Plant Cell 6:251–264; 1994.
Yamamoto, Y. T.; Taylor, C. G.; Acedo, C. N.; Cheng, C.-L.; Conkling, M. A. Characterization of cis-acting sequences regulating root-specific gene expression in tobacco. Plant Cell 3:371–382; 1991.
Yanagisawa, S.; Schmidt, R. J. Diversity and similarity among recognition sequences of Dof transcription factors. Plant J. 17:209–214; 1999.
Ye, G. N.; Hajdukiewicz, P. T.; Broyles, D.; Rodriguez, D.; Xu, C. W.; Nehra, N.; Staub, J. M. Plastid-expressed 5-enolpyrurylshikimate-3-phosphate synthase genes provide high level glyphosate tolerance in tobacco. Plant J. 25:261–270; 2001.
Ye, X.; Al Babili, S.; Kloti, A.; Zhang, J.; Lucca, P.; Beyer, P.; Potrykus, I. Engineering the provitamin A (beta-carotene) biosynthetic pathway into (earotenoid-free) rice endosperm. Science 287:303–305; 2000.
Yun, D.-J.; Hashimoto, T.; Yamada, T. Metabolic engineering of medicinal plants: transgenic Altropa belladonna with an improved alkaloid composition. Proc. Natl Acad Sci. USA 89:11799–11803; 1992.
Zhang, W.; McElroy, D.; Wu, R. Analysis of rice Actl 5' region activity in transgenic rice plants. Plant Cell 3:1155–1165; 1991.
Zuo, J.; Niu, Q.-W.; Chua, N.-H. An estrogen receptor-based transactivator XVE mediates highly inducible gene expression in transgenic plants. Plant J. 24:266–273; 2000.
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Potenza, C., Aleman, L. & Sengupta-Gopalan, C. Targeting transgene expression in research, agricultural, and environmental applications: Promoters used in plant transformation. In Vitro Cell.Dev.Biol.-Plant 40, 1–22 (2004). https://doi.org/10.1079/IVP2003477
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DOI: https://doi.org/10.1079/IVP2003477