Genomic organization of a diverse ACC synthase gene family in banana and expression characteristics of the gene member involved in ripening of banana fruits

Journal of Agricultural and Food Chemistry

Volumn 54, Issue 11, 2006, Pages 3859-3868

  Huang, Fong Chin ^a   Do, Yi Yin ^a   Huang, Pung Ling ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

Author keywords

1 Aminocyclopropane 1 carboxylate (ACC) synthase; Ethylene; Gene expression; Multigene family

Indexed keywords

ARABIDOPSIS; LYCOPERSICON ESCULENTUM;

1 AMINOCYCLOPROPANECARBOXYLATE SYNTHASE; 1-AMINOCYCLOPROPANECARBOXYLATE SYNTHASE; LYASE;

AMINO ACID SEQUENCE; ARTICLE; BANANA; CHEMISTRY; ENZYMOLOGY; FRUIT; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; INTRON; MOLECULAR GENETICS; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; RESTRICTION MAPPING; SOUTHERN BLOTTING; TRANSCRIPTION INITIATION SITE;

AMINO ACID SEQUENCE; BASE SEQUENCE; BLOTTING, NORTHERN; BLOTTING, SOUTHERN; FRUIT; GENE EXPRESSION; INTRONS; LYASES; MOLECULAR SEQUENCE DATA; MUSA; POLYMERASE CHAIN REACTION; RESTRICTION MAPPING; TRANSCRIPTION INITIATION SITE;

EID: 33745484906     PISSN: 00218561     EISSN: None     Source Type: Journal    
DOI: 10.1021/jf060001w     Document Type: Article

References (61)

1. Abeles, F. B.; Morgan, P. W.; Saltveit, M. E., Jr. Ethylene in Plant Biology, 2nd ed.; Academic Press: New York, 1992.
2. Theologis, A. One rotten apple spoils the whole bushel: the role of ethylene in fruit ripening. Cell 1992, 70, 181-184.
3. Bleecker, A. B.; Kende, H. Ethylene: a gaseous signal molecule in plants. Annu. Rev. Cell Dev. Biol. 2000, 16, 1-18.
4. Yang, S. F.; Hoffman, N. E. Ethylene biosynthesis and its regulation in higher plants. Annu. Rev. Plant Physiol. 1984, 35, 155-189.
5. Adams, D. O.; Yang, S. F. Ethylene biosynthesis: identification of 1-aminocyclopropane-1-carboxylic acid as an intermediate in the conversion of methionine to ethylene. Proc. Natl. Acad. Sci. U.S.A. 1979, 76, 170-174.
6. Rottmann, W. H.; Peter, G. F.; Oeller, P. W.; Keller, J. A.; Shen, N. F.; Taylor, B. P.; Campbelln, A. D.; Theologis, A. 1-Aminocyclopropane-1- carboxylate synthase in tomato is encoded by a multigene family whose transcription is induced during fruit and floral senescence. J. Mol. Biol. 1991, 222, 937-961.
7. Lincoln, J. E.; Campbell, A. D.; Oetiker, J.; Rottmann, W. H.; Oeller, P. W.; Shen, N. F.; Theologis, A. LE-ACS4, a fruit ripening and wound-induced 1-aminocyclopropane-1-carboxylate synthase gene of tomato (Lycopersicon esculentum). J. Biol. Chem. 1993, 268, 19422-19430.
8. Oetiker, J. H.; Olsen, D. C.; Shiu, O. Y.; Yang, S. F. Differential induction of seven 1-aminocyclopropane-1-carboxylic acid synthase genes by elicitor in suspension cultures of tomato (Lycopersicon esculentum). Plant Mol. Biol. 1997, 34, 275-286.
9. Shiu, O. Y.; Oetiker, J. H.; Yip, W. K.; Yang, S. F. The promoter of LE-ACS7, an early flooding-induced 1-aminocyclopropane-1-carboxylate synthase gene of the tomato, is tagged by a Sol3 transposon. Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 10334-10339.
10. Huang, P. L.; Parks, J. E.; Rottmann, W. H.; Theologis, A. Two genes encoding 1-aminocyclopropane-1-carboxylate synthase in zucchini (Cucurbita pepo) are clustered and similar but differentially regulated. Proc. Natl. Acad. Sci. U.S.A. 1991, 88, 7021-7025.
11. Botella, J. R.; Arteca, J. M.; Schlagnhaufer, C. D.; Arteca, R. N.; Phillips, A. T. Identification and characterization of a full length cDNA encoding for an auxin-induced 1-aminocyclopropane-1-carboxylate synthase from etiolated mung bean hypocotyl segments and expression of its mRNA in response to indole-3-acetic acid. Plant Mol. Biol. 1992, 20, 425-436.
12. Zarembinski, T. I.; Theologis, A. Anaerobiosis and plant growth hormones induce two genes encoding 1-aminocyclopropane-1-carboxylate synthase in rice (Oryza sativa L.). Mol. Biol. Cell 1993, 4, 363-373.
13. Beltran-Destefano, L. G. C.; Caeneghem, W. V.; Gielen, J.; Richard, L.; van Montagu, M.; van der Straeten, D. Characterization of three members of the ACC synthase gene family in Solanum tuberosum L. Mol. Gen. Genet. 1995, 246, 496-508.
14. ten Have, A.; Woltering, E. J. Ethylene biosynthetic genes are differentially expressed during carnation (Dianthus caryophyllus L.) flower senescence. Plant Mol. Biol. 1997, 34, 89-97.
15. Avni, A.; Bailey, B. A.; Mattoo, A. K.; Anderson, J. D. Induction of ethylene biosynthesis in Nicotiana tabacum by a Trichoderma viride xylanase is correlated to the accumulation of 1-aminocyclopropane-1-carboxylic acid (ACC) synthase and ACC oxidase transcripts. Plant Physiol. 1994 106, 1049-1055.
16. Ge, L.; Liu, J. Z.; Wong, W. S.; Hsiao, W. L. W.; Chong, K.; Xu, Z. K.; Yang, S. F.; Kung, S. D.; Li, N. Identification of novel multiple environmental factor-responsive 1-aminocyclopropane-1-carboxylate synthase gene, NT-ACS2, from tobacco. Plant Cell Environ. 2000, 23, 1169-1182.
17. Takahashi, H.; Iwasa, T.; Shinkawa, T.; Kawahara, A.; Kurusu, T.; Inoue, Y. Isolation and characterization of the ACC synthase genes from lettuce (Lactuca sativa L.), and the involvement in low pH-induced root hair initiation. Plant Cell Physiol. 2003, 44, 62-69.
18. Yamagami, T.; Tsuchisaka, A.; Yamada, K.; Haddon, W. F.; Harden, L. A.; Theologis, A. Biochemical diversity among the 1-aminocyclopropane-1-carboxylate synthase isozymes encoded by the Arabidopsis gene family. J. Biol. Chem. 2003, 278, 49102-49112.
19. 2 concentrations, pulp fructose 2,6-bisphosphate concentration, and activity of some glycolytic enzymes. Plant Physiol. 1987, 85, 277-282.
20. Beaudry, R. M.; Severon, R. F.; Black, C. C.; Kays, S. J. Banana ripening: implications of changes in glycolytic intermediate concentrations, glycolytic and gluconeogenic carbon flux, and fructose 2,6-bisphosphate concentration. Plant Physiol. 1989, 91, 1436-1444.
21. 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. 1988, 7, 3315-3320.
22. Gu, Y. Q.; Yang, C.; Thara, V. K.; Zhou, J.; Martin, G. B. Pti4 is induced by ethylene and salicylic acid, and its product is phosphorylated by the Pto kinase. Plant Cell 2000, 12, 771-786.
23. Chakravarthy, S.; Tuori, R. P.; D'Ascenzo, M. D.; Fobert, P. R.; Despres, C.; Martin, G. B. The tomato transcription factor Pti4 regulates defense-related gene expression via GCC box and non-GCC box cis elements. Plant Cell 2003, 15, 3033-3050.
24. Wang, N. N.; Shin, M.-C.; Li, N. The GUS reporter-aided analysis of the promoter activities of Arabidopsis ACC synthase genes AtACS4, AtACS5, and AtACS7 induced by hormones and stresses. J. Exp. Bot. 2005, 56, 909-920.
25. Commonwealth Scientific and Industrial Research Organization (CSIRO). Banana ripening guide; CSIRO Division of Food Research: 1972; Circular, 8, pp 1-12.
26. Dellaporta, S. L.; Wood, L.; Hicks, J. B. A plant DNA minipreparation: Version II. Plant Mol. Biol. Rep. 1983, 1, 19-21.
27. Frischauf, A. M.; Lehrach, H.; Poustka, A.; Murray, N. Lambda replacement vector carrying poly linker sequences. J. Mol. Biol. 1983, 170, 827-842.
28. Benton, W. D.; Davis, R. W. Screening λgt recombinant clones by hybridization to single plaques in situ. Science 1977, 196, 180-182.
29. Lysák, M. A.; Doleželová, M.; Horry, J. P.; Swennen, R.; Doležel, J. Flow cytometric analysis of nuclear DNA content in Musa. Theor. Appl. Genet. 1999, 98, 1344-1350.
30. Clark, L.; Carbon, J. Biochemical construction and selection of hybrid plasmids containing specific segments of the Escherichia coli genome. Proc. Natl. Acad. Sci. U.S.A. 1975, 72, 4361-4365.
31. Sambrook, J.; Fritsch, E. F.; Maniatis, T. Molecular Cloning: A Laboratory Manual, 2nd ed.; Cold Spring Harbor Laboratory Press: Cold Spring Harbor, NY, 1989.
32. Sanger, F.; Nicklen, S.; Coulson, A. R. DNA sequencing with chain-termination inhibitors. Proc. Natl. Acad. Sci. U.S.A. 1977, 74, 5463-5467.
33. Bond, B. J.; Davidson, N. The Drosophila melanogaster actin 5C gene uses two transcription start sites and three polyadenylation sites to express multiple mRNA species. Mol. Cell Biol. 1986, 6, 2080-2088.
34. Buchman, A.; Fromm, M.; Berg, P. Complex regulation of simian virus 40 early-region transcription from different overlapping promoters. Mol. Cell Biol. 1984, 4, 1900-1914.
35. Feinberg, A. P.; Vogelstein, B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 1983, 132, 6-13.
36. Taylor, B.; Powell, A. Isolation of plant DNA and RNA. Focus 1982, 4, 4-6.
37. Dong, J. G.; Kim, W. T.; Yip, W. K.; Thompson, G. A.; Li, L.; Bennett, A. B.; Yang, S. F. Cloning of cDNA encoding 1-aminocyclopropane-1-carboxylate synthase and expression of its mRNA in ripening apple fruit. Planta 1991, 185, 38-45.
38. Liu, X.; Shiomi, S.; Nakatsuka, A.; Kubo, Y.; Nakamura, R.; Inaba, A. Characterization of ethylene biosynthesis associated with ripening in banana fruit. Plant Physiol. 1999, 121, 1257-1265.
39. Yip, W. K.; Moore, T.; Yang, S. F. Differential accumulation of transcripts for four tomato 1-aminocyclopropane-1-carboxylate synthase homologs under various conditions. Proc. Natl. Acad. Sci. U.S.A. 1992, 89, 2475-2479.
40. Abel, S.; Nguyen, M. D.; Chow, W.; Theologis, A. ACS4, a primary indoleacetic acid-responsive gene encoding 1-aminocyclopropane-1-carboxylate synthase gene in Arabidopsis thaliana. Structural characterization, expression in Escherichia coli, and expression characteristics in response to auxin. J. Biol. Chem. 1995, 270, 19093-19099.
41. Yoon, I. S.; Park, D. H.; Mori, H.; Imaseki, H.; Kang, B. G. Characterization of an auxin-inducible 1-aminocyclopropane-1-carboxylate synthase gene, VR-ACS6, of mungbean (Vigna radiata (L.) Wilczek) and hormonal interactions on the promoter activity in transgenic tobacco. Plant Cell Physiol. 1999, 40, 431-438.
42. van der Straeten, D.; Wiemeersch, L. V.; Goodman, H. M.; van Montagu, M. Cloning and sequence of two different cDNAs encoding 1-aminocyclopropane-1- carboxylate synthase in tomato. Proc. Natl. Acad. Sci. U.S.A. 1990, 87, 4859-4853.
43. Nakajima, N.; Mori, H.; Yamazaki, K.; Imaseki, H. Molecular cloning and sequence of a complementary DNA encoding 1-aminocyclopropane-1-carboxylate synthase induced by tissue wounding. Plant Cell Physiol. 1990, 31, 1021-1029.
44. Olsen, D. C.; Oetiker, J. H.; Yang, S. F. Analysis of LE-ACS3, a 1-aminocyclopropane-1-carboxylate acid synthase gene expressed during flooding in the roots of tomato plants. J. Biol. Chem. 1995, 270, 14056-14061.
45. Liang, X.; Abel, S.; Keller, J. A.; Shen, N. F.; Theologis, A. The 1-aminocyclopropane-1-carboxylate synthase gene family of Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 1992, 89, 11046-11050.
46. van der Straeten, D.; Rodrigues-Pousada, R. A.; Villarroel, R.; Hanley, S.; Goodman, H. M.; van Montagu, M. Cloning, genetic mapping, and expression analysis of an Arabidopsis thaliana gene that encodes 1-aminocyclopropane-1- carboxylate synthase. Proc. Natl. Acad. Sci. U.S.A. 1992, 89, 9969-9973.
47. Peck, S. C.; Kende, H. A gene encoding 1-aminocyclopropane-1-carboxylate (ACC) synthase produces two transcripts: elucidation of a conserved response. Plant J. 1998, 14, 573-581.
48. Cordes, S.; Deikman, J.; Margossian, L. J.; Fischer, R. L. Interaction of a developmentally regulated DNA-binding factor with sites flanking two different fruit-ripening genes from tomato. Plant Cell 1989, 1, 1025-1034.
49. Holdsworth, M. J.; Laties, G. G. Site-specific binding of a nuclear factor to the carrot extension gene is influenced by both ethylene and wounding. Planta 1989, 179, 17-23.
50. Huang, P.-L.; Do, Y.-Y.; Huang, F.-C.; Thay, T.-S.; Chang, T.-W. Characterization and expression analysis of a banana gene encoding 1-aminocyclopropane-1-carboxylate oxidase. Biochem. Mol. Biol. Int. 1997, 41, 941-950.
51. Lescot, M.; Dehais, P.; Thijs, G.; Marchai, K.; Moreau, Y.; van der Peer, Y.; Rouze, P.; Rombauts, S. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silica analysis of promoter sequences. Nucleic Acids Res. 2002, 30, 325-327.
52. Arguello-Astorga, G. R.; Herrera-Estrella, L. R. Ancestral multipartite units in light-responsive plant promoters have structural features correlating with specific phototransduction pathways. Plant Physiol. 1996, 112, 1151-1166.
53. Itzhaki, H.; Maxson, J. M.; Woodson, W. R. An ethylene responsive enhancer element is involved in the senescence-related expression of the carnation glutathione-S-transferase (GST1) gene. Proc. Natl. Acad. Sci. U.S.A. 1994, 91, 8925-8929.
54. Rouster, J.; Leah, R.; Mundy, J.; Cameron-Mills, V. Identification of a methyl jasmonate-responsive region in the promoter of a lipoxygenase 1 gene expressed in barley grain. Plant J. 1997, 11, 513-523.
55. Feldbrugge, M.; Sprenger, M.; Hahlbrock, K.; Weisshaar, B. PcMYB1, a novel plant protein containing a DNA-binding domain with one MYB repeat, interacts in vivo with a light-regulatory promoter unit. Plant J. 1997, 11, 1079-1093.
56. Baker, S. S.; Wilhelm, K. S.; Thomashow, M. F. The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol. Biol 1994, 24, 701-713.
57. 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. 1996, 15, 5690-5700.
58. Buettner, M.; Singh, K. B. Arabidopsis thaliana ethylene-responsive element binding protein (AtEBP), an ethylene-inducible, GCC box DNA-binding protein interacts with an ocs element binding protein. Proc. Natl. Acad. Sci. U.S.A. 1997, 94, 5961-5966.
59. Gu, Y. Q.; Wildermuth, M. C.; Chakravarthy, S.; Loh, Y. T.; Yang, C.; He, X.; Han, Y.; Martin, G. B. Tomato transcription factors Pti4, Pti5, and Pti6 activate defense responses when expressed in Arabidopsis. Plant Cell 2002, 14, 817-831.
60. Zarembrinski, T.; Theologis, A. Ethylene biosynthesis and action: a case of conservation. Plant Mol. Biol. 1994, 26, 1579-1597.
61. Waterhouse, P. M.; Wang, M.-B.; Finnegan, E. J. Role of short RNAs in gene silencing. Trends Plant Sci. 2001, 6, 297-301.