The sucrose synthase-1 promoter from Citrus sinensis directs expression of the β-glucuronidase reporter gene in phloem tissue and in response to wounding in transgenic plants

Planta

Volumn 234, Issue 3, 2011, Pages 623-637

  Singer, Stacy D ^a   Hily, Jean Michel ^a   Cox, Kerik D ^a  

^a New York State Agricultural Experiment Station   (United States)

Author keywords

Citrus sinensis; GUS reporter gene; Phloem; SUS1 promoter; Transgenic plants; Wound inducible expression

Indexed keywords

BETA GLUCURONIDASE; GLUCOSYLTRANSFERASE; PHYTOHORMONE; SUCROSE SYNTHASE; VEGETABLE PROTEIN;

ARABIDOPSIS; ARTICLE; BIOSYNTHESIS; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHLOEM; PLASMID; PROMOTER REGION; REPORTER GENE; SWEET ORANGE; TOBACCO; TRANSGENIC PLANT;

ARABIDOPSIS; BASE SEQUENCE; CITRUS SINENSIS; CLONING, MOLECULAR; GENE EXPRESSION REGULATION, PLANT; GENES, REPORTER; GLUCOSYLTRANSFERASES; GLUCURONIDASE; MOLECULAR SEQUENCE DATA; PHLOEM; PLANT GROWTH REGULATORS; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; PLASMIDS; PROMOTER REGIONS, GENETIC; TOBACCO;

ARABIDOPSIS; ARABIDOPSIS THALIANA; CITRUS; CITRUS SINENSIS; NICOTIANA TABACUM;

EID: 80052043997     PISSN: 00320935     EISSN: 14322048     Source Type: Journal    
DOI: 10.1007/s00425-011-1432-x     Document Type: Article

References (70)

1. Alonso JM, Stepanova AN, Leisse TJ, Kim CJ et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301: 653-657.
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
3. Baud S, Vaultier MN, Rochat C (2004) Structure and expression profile of the sucrose synthase multigene family in Arabidopsis. J Exp Bot 55: 397-409.
4. Bieniawska Z, Barratt DHP, Garlick AP, Thole V, Kruger NJ, Martin C, Zrenner R, Smith AM (2007) Analysis of the sucrose synthase gene family in Arabidopsis. Plant J 49: 810-828.
5. Block M, Debrouwer D, Moens T (1997) The development of a nuclear male sterility system in wheat: expression of the barnase gene under the control of tapetum specific promoters. Theor Appl Genet 95: 125-131.
6. Chiu W-B, Lin C-H, Chang C-J, Hsieh M-H, Wang A-Y (2006) Molecular characterization and expression of four cDNAs encoding sucrose synthase from green bamboo Bambusa oldhamii. New Phytol 170: 53-63.
7. Chopra S, Del-Favero J, Dolferus R, Jacobs M (1992) Sucrose synthase of Arabidopsis: genomic cloning and sequence characterization. Plant Mol Biol 18: 131-134.
8. Chopra S, Brendel V, Zhang JB, Axtell JD, Peterson T (1999) Molecular characterization of a mutable pigmentation phenotype and isolation of the first active transposable element from Sorghum bicolor. Proc Natl Acad Sci USA 96: 15330-15335.
9. Clancy M, Hannah LC (2002) Splicing of the maize Sh1 first intron is essential for enhancement of gene expression, and a T-rich motif increases expression without affecting splicing. Plant Physiol 130: 918-929.
10. Clancy M, Vasil V, Hannah LC, Vasil IK (1994) Maize Shrunken-1 intron and exon regions increase gene expression in maize protoplasts. Plant Sci 98: 151-161.
11. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743.
12. Daie J (1989) Phloem loading of sucrose: update and opportunities in molecular biology. Plant Mol Biol Rep 7: 106-115.
13. Fu H, Park WD (1995) Sink- and vascular-associated sucrose synthase functions are encoded by different gene classes in potato. Plant Cell 7: 1369-1385.
14. Fu H, Kim SY, Park WD (1995a) High-level tuber expression and sucrose inducibility of a potato Sus4 sucrose synthase gene require 5′ and 3′ flanking sequences and the leader intron. Plant Cell 7: 1387-1394.
15. Fu H, Kim SY, Park WD (1995b) A potato Sus3 sucrose synthase gene contains a context-dependent 3′ element and a leader intron with both positive and negative tissue-specific effects. Plant Cell 7: 1395-1403.
16. Gibson S (2000) Plant sugar-response pathways: part of a complex regulatory web. Plant Physiol 124: 1532-1539.
17. Goto K, Okada TS, Kondoh H (1990) Functional cooperation of lens-specific and nonspecific elements in the d1-crystallin enhancer. Mol Cell Biol 10: 958-964.
18. Graham MW, Craig S, Waterhouse PM (1997) Expression patterns of vascular-specific promoters RolC and Sh in transgenic potatoes and their use in engineering PLRV-resistant plants. Plant Mol Biol 33: 729-735.
19. Guo H, Chen X, Zhang H, Fang R, Yuan Z, Zhang Z, Tian Y (2004) Characterization and activity enhancement of the phloem-specific pumpkin PP2 gene promoter. Transgenic Res 13: 559-566.
20. Hajdukiewicz P, Svab Z, Maliga P (1994) The small, versatile pPZP family of Agrobacterium binary vectors for plant transformation. Plant Mol Biol 25: 989-994.
21. Hehn A, Rohde W (1998) Characterization of cis-acting elements affecting strength and phloem specificity of the coconut decay virus promoter. J Gen Virol 79: 1495-1499.
22. Higo K, Ugawa Y, Iwamoto M, Korenaga K (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27: 297-300.
23. Hily JM, Liu Z (2009) A simple and sensitive high-throughput GFP screening in woody and herbaceous plants. Plant Cell Rep 28: 493-501.
24. Hily JM, Singer SD, Yang Y, Liu Z (2009) A transformation booster sequence (TBS) from Petunia hybrida functions as an enhancer-blocking insulator in Arabidopsis thaliana. Plant Cell Rep 28: 1095-1104.
25. Hohnjec N, Becker JD, Pühler A, Perlick AM, Küster H (1999) Genomic organization and expression properties of the MtSUcS1 gene, which encodes a nodule-enhanced sucrose synthase in the model legume Medicago truncatula. Mol Gen Genet 261: 514-522.
26. Horsch RB, Fry JE, Hoffmann NL, Wallroth M, Eichholtz D, Rogers SG, Fraley RT (1985) A simple and general method for transferring genes into plants. Science 227: 1229-1231.
27. Ibraheem O, Hove RM, Bradley G (2008) Sucrose assimilation and the role of sucrose transporters in plant wound response. Afr J Biotechnol 7: 4850-4855.
28. Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6: 3901-3907.
29. Kay R, Chan A, Daly M, McPherson J (1987) Duplication of CaMV 35S promoter sequences creates a strong enhancer for plant genes. Science 236: 1299-1302.
30. Koch KE, Nolte KD, Duke ER, McCarthy DR, Avigne WT (1992) Sugar levels modulate differential expression of maize sucrose synthase genes. Plant Cell 4: 59-69.
31. Komatsu A, Moriguchi T, Koyama K, Omura M, Akihama T (2002) Analysis of sucrose synthase genes in citrus suggests different roles and phylogenetic relationships. J Exp Bot 53: 61-71.
32. Lescot M, Dehais P, Moreau Y, De Moor B, Rouze P, Rombauts S (2002) PlantCARE: 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.
33. Lingle SE, Dyer JM (2004) Polymorphisms in the promoter region of the sucrose synthase-2 gene of Saccharum genotypes. J Am Soc Sugar Cane Technol 24: 241-249.
34. Liu X, Baird WV (2001) Rapid amplification of genomic DNA ends by NlaIII partial digestion and polynucleotide tailing. Plant Mol Biol Rep 19: 261-267.
35. Liu Z, Liu Z (2008) The second intron of AGAMOUS drives carpel- and stamen-specific expression sufficient to induce complete sterility in Arabidopsis. Plant Cell Rep 27: 855-863.
36. Luo H, Lee J-Y, Hu Q, Nelson-Vasilchik K, Eitas TK, Lickwar C, Kausch AP, Chandlee JM, Hodges TK (2006) RTS, a rice anther-specific gene is required for male fertility and its promoter sequence directs tissue-specific gene expression in different plant species. Plant Mol Biol 62: 397-408.
37. Maas C, Laufs J, Grant S, Korfhage C, Werr W (1991) The combination of a novel stimulatory element in the first exon of the maize Shrunken-1 gene with the following intron enhances reporter gene expression up to 1000-fold. Plant Mol Biol 16: 199-207.
38. Maraña C, García-Olmedo F, Carbonero P (1990) Differential expression of two types of sucrose-synthase-coding genes in wheat in response to anaerobiosis, cold shock and light. Gene 88: 167-172.
39. Martin T, Frommer WB, Salanoubat M, Willmitzer L (1993) Expression of an Arabidopsis sucrose synthase gene indicates a role in metabolization of sucrose both during phloem loading and in sink organs. Plant J 4: 367-377.
40. McElroy D, Zhang W, Cao J, Wu R (1990) Isolation of an efficient actin promoter for use in rice transformation. Plant Cell 2: 163-171.
41. Moffat AS (2001) Finding new ways to fight plant disease. Science 292: 2270-2273.
42. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15: 473-497.
43. Nagadhara D, Ramesh S, Pasalu IC, Rao K, Krishnaiah NV, Sarma NP, Bown DP, Gatehouse JA, Reddy VD, Rao KV (2003) Transgenic indica rice resistant to sap-sucking insects. Plant Biotechnol J 1: 231-240.
44. Nishiuchi T, Shinshi H, Suzuki K (2004) Rapid and transient activation of transcription of the ERF3 gene by wounding in tobacco leaves: possible involvement of NtWRKYs and autorepression. J Biol Chem 279: 55355-55361.
45. Nolte KD, Koch KE (1993) Companion-cell specific localization of sucrose synthase in zones of phloem loading and unloading. Plant Physiol 101: 899-905.
46. Ohta S, Mita S, Hattori T, Nakamura K (1990) Construction and expression in tobacco of a β-glucuronidase (GUS) reporter gene containing an intron within the coding sequence. Plant Cell Physiol 31: 805-813.
47. Oshima RG, Abrams L, Kulesh D (1990) Activation of an intron enhancer within the keratin 18 gene by expression of c-fos and c-jun in undifferentiated F9 embryonal carcinoma cells. Genes Dev 4: 835-848.
48. Potenza C, Aleman L, Sengupta-Gopalan C (2004) Targeting transgene expression in research, agricultural, and environmental applications: promoters used in plant transformation. In Vitro Cell Dev Pl 40: 1-22.
49. Ricard B, Rivoai J, Spiteri A, Pradet A (1991) Anaerobic stress induced the transcription and translation of sucrose synthase in rice. Plant Physiol 95: 669-674.
50. Ricard B, VanToai T, Chourey P, Saglio P (1998) Evidence for the critical role of sucrose synthase for anoxic tolerance of maize roots using a double mutant. Plant Physiol 116: 1323-1331.
51. Roque E, Gomez MD, Ellul P, Wallbraun M, Madueno F, Beltran JP, Canas LA (2007) The PsEND1 promoter: a novel tool to produce genetically engineered male-sterile plants by early anther ablation. Plant Cell Rep 26: 313-325.
52. Rose AB, Beliakoff JA (2000) Intron-mediated enhancement of gene expression independent of unique intron sequence and splicing. Plant Physiol 122: 535-542.
53. Rosso MG, Li Y, Strizhov N, Reiss B, Dekker K, Weisshaar B (2003) An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol Biol 53: 247-259.
54. Rushton PJ, Torres JT, Parniske M, Wernert P, Hahlbrock K, Somssich IE (1996) Interaction of elicitor-induced DNA binding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO J 15: 5690-5700.
55. Rushton PJ, Reinstädler A, Lipka V, Lippok B, Somssich IE (2002) Synthetic plant promoters containing defined regulatory elements provide novel insights into pathogen- and wound-induced signaling. Plant Cell 14: 749-762.
56. Sadeghi A, Broeders S, De Greve H, Hernalsteens J-P, Peumans WJ, van Damme EJM, Smagghe G (2007) Expression of garlic leaf lectin under the control of the phloem-specific promoter Asus1 from Arabidopsis thaliana protects tobacco plants against the tobacco aphid (Myzus nicotianae). Pest Manage Sci 63: 1215-1223.
57. Saha P, Dasgupta I, Das S (2006) A novel approach for developing resistance in rice against phloem limited viruses by antagonizing the phloem feeding hemipteran vectors. Plant Mol Biol 62: 735-752.
58. Shelton AM, Zhao JZ, Roush RT (2002) Economic, ecological, food safety and social consequences of the development of Bt transgenic plants. Annu Rev Entomol 47: 845-881.
59. Shi Y, Wang MB, Powell KS, van Damme E, Hilder VA, Gatehouse AMR, Boulter D, Gatehouse JA (1994) Use of the rice sucrose synthase-1 promoter to direct phloem-specific expression of β-glucuronidase and snowdrop lectin genes in transgenic tobacco plants. J Exp Bot 45: 623-631.
60. Sturm A, Tang G-Q (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends Plant Sci 4: 401-407.
61. Sturm A, Lienhard S, Schatt S, Hardegger M (1999) Tissue-specific expression of two genes for sucrose synthase in carrot (Daucus carota L.). Plant Mol Biol 39: 349-360.
62. Sun J, Lobods T, Sung SS, Black CC (1992) Sucrose synthase in wild tomato, Lycopersicon chmielewskii, and tomato fruit sink strength. Plant Physiol 98: 1163-1169.
63. Thompson JD, Higgins DJ, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
64. van Engelen FA, Molthoff JW, Conner AJ, Nap J-P, Pereira A, Stiekema WJ (1995) pBINPLUS: an improved plant transformation vector based on pBIN19. Transgenic Res 4: 288-290.
65. Vasil V, Clancy M, Ferl RJ, Vasil IK, Hannah C (1990) Increased gene expression by the first intron of maize Shrunken-1 locus in grass species. Plant Physiol 91: 1575-1579.
66. Wang M, Boulter D, Gatehouse JA (1992) A complete sequence of the rice sucrose synthase-1 (RSs1) gene. Plant Mol Biol 19: 881-885.
67. Wang F, Smith A, Brenner ML (1994) Temporal and spatial expression pattern of sucrose synthase during tomato fruit development. Plant Physiol 104: 535-540.
68. Winter H, Huber SC (2000) Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. Crit Rev Plant Sci 19: 31-67.
69. Yang N-S, Russell D (1990) Maize sucrose synthase-1 promoter directs phloem cell-specific expression of Gus gene in transgenic tobacco plants. Proc Natl Acad Sci USA 87: 4144-4148.
70. Zeng Y, Wu Y, Avigne WT, Koch KE (1998) Differential regulation of sugar-sensitive sucrose synthases by hypoxia and anoxia indicate complementary transcriptional and posttranscriptional responses. Plant Physiol 116: 1573-1583.