A unique short-chain dehydrogenase/reductase in arabidopsis glucose signaling and abscisic acid biosynthesis and functions

Plant Cell

Volumn 14, Issue 11, 2002, Pages 2723-2743

  Cheng, Wan Hsing ^a   Endo, Akira ^a   Zhou, Li ^a   Penney, Jessica ^a   Chen, Huei Chi ^a   Arroyo, Analilia ^a   Leon, Patricia ^a   Nambara, Eiji ^a   Asami, Tadao ^a   Seo, Mitsunori ^a   Koshiba, Tomokazu ^a   Sheen, Jen ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; CELLS; CLONING; ENZYMES; GENES; GLUCOSE; HORMONES; NUTRITION; ORGANIC ACIDS;

SEX DETERMINATION;

PLANTS (BOTANY);

ARABIDOPSIS; MAMMALIA; ZEA MAYS;

EID: 0036847621     PISSN: 10404651     EISSN: None     Source Type: Journal    
DOI: 10.1105/tpc.006494     Document Type: Article

References (80)

1. Alonso, J.M., Hirayama, T., Roman, G., Nourizadeh, S., and Ecker, J.R. (1999). EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284, 2148-2152.
2. Arenas-Huertero, F., Arroyo, A., Zhou, L., Sheen, J., and Leon, P. (2000). Analysis of Arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar. Genes Dev. 14, 2085-2096.
3. 2]abscisic acid for use as a stable and pure internal standard. J. Chem. Res. (Synop.) 11, 658-659.
4. Audran, C., Borel, C., Frey, A., Sotta, B., Meyer, C., Simonneau, T., and Marion-Poll, A. (1998). Expression studies of the zeaxanthin epoxidase gene in Nicotiana plumbaginifolia. Plant Physiol. 118, 1021-1028.
5. Beaudoin, N., Serizet, C., Gosti, F., and Giraudat, J. (2000). Interactions between abscisic acid and ethylene signaling cascades. Plant Cell 12, 1103-1115.
6. Bell, C.J., and Ecker, J.R. (1994). Assignment of 30 microsatellite loci to the linkage map of Arabidopsis. Genomics 19, 137-144.
7. Bewley, J.D. (1997). Seed germination and dormancy. Plant Cell 9, 1055-1066.
8. Bishop, G.J., and Yokota, T. (2001). Plants steroid hormones, brassinosteroids: Current highlights of molecular aspects on their synthesis/metabolism, transport, perception and response. Plant Cell Physiol. 42, 114-120.
9. Coruzzi, G.M., and Zhou, L. (2001). Carbon and nitrogen sensing and signaling in plants: Emerging 'matrix effects.' Curr. Opin. Plant Biol. 4, 247-253.
10. Cowan, A.K. (2000). Is abscisic aldehyde really the immediate precursor to stress-induced ABA? Trends Plant Sci. 5, 191-192.
11. Cutler, A.J., and Krochko, J.E. (1999). Formation and breakdown of ABA. Trends Plant Sci. 4, 472-478.
12. DeLong, A., Calderon-Urrea, A., and Dellaporta, S.L. (1993). Sex determination gene TASSELSEED2 of maize encodes a short-chain alcohol dehydrogenase required for stage-specific floral organ abortion. Cell 74, 757-768.
13. Finkelstein, R.R., Gampala, S.S.L., and Rock, C.D. (2002). Abscisic acid signaling in seeds and seedlings. Plant Cell 14 (suppl.), S15-S45.
14. Finkelstein, R.R., and Gibson, S.I. (2001). ABA and sugar interactions regulating development: Cross-talk or voices in a crowd. Curr. Opin. Plant Biol. 5, 26-32.
15. Finkelstein, R.R., and Zeevaart, J.A. (1994). Gibberellin and abscisic acid biosynthesis and response. In The Arabidopsis Book, C.R. Somerville and E.M. Meyerowitz, eds (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
16. Gazzarrini, S., and McCourt, P. (2001). Genetic interactions between ABA, ethylene and sugar signaling pathways. Curr. Opin. Plant Biol. 4, 387-391.
17. Ghassemian, M., Nambara, E., Cutler, S., Kawaide, H., Kamiya, Y., and McCourt, P. (2000). Regulation of abscisic acid signaling by the ethylene response pathway in Arabidopsis. Plant Cell 12, 1117-1126.
18. Gibson, S.I., Laby, R.J., and Kim, D. (2001). The sugar-insensitive1 (sis1) mutant of Arabidopsis is allelic to ctr1. Biochem. Biophys. Res. Commun. 280, 196-203.
19. González-Guzmán, M., Apostolova, N., Belles, J.M., Barrero, J.M., Piqueras, P., Ponce, M.R., Micol, J.L., Serrano, R., and Rodríguez, P.L. (2002). The short-chain alcohol dehydrogenase ABA2 catalyzes the conversion of xanthoxin into abscisic aldehyde. Plant Cell 14, 1833-1846.
20. Huijser, C., Kortstee, A., Pego, J., Weisbeek, P., Wisman, E., and Smeekens, S. (2000). The Arabidopsis SUCROSE UNCOUPLED-6 gene is identical to ABSCISIC ACID INSENSITIVE-4: Involvement of abscisic acid in sugar responses. Plant J. 23, 577-585.
21. Hwang, I., and Sheen, J. (2001). Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413, 383-389.
22. Iuchi, S., Kobayashi, M., Taji, T., Naramoto, M., Seki, M., Kato, T., Tabata, S., Kakubari, Y., Yamaguchi-Shinozaki, K., and Shinozaki, K. (2001). Regulation of drought tolerance by gene manipulation of 9-cis-epoxycarotenoid dioxygenase, a key enzyme in abscisic acid biosynthesis in Arabidopsis. Plant J. 27, 325-333.
23. Iuchi, S., Kobayashi, M., Yamaguchi-Shinozaki, K., and Shinozaki, K. (2000). A stress-inducible gene for 9-cis-epoxycarotenoid dioxygenase involved in abscisic acid biosynthesis under water stress in drought-tolerant cowpea. Plant Physiol. 123, 553-562.
24. Jang, J.C., Fujioka, S., Tasaka, M., Seto, H., Takatsuto, S., Ishii, A., Aida, M., Yoshida, S., and Sheen, J. (2000). A critical role of sterols in embryonic patterning and meristem programming revealed by the fakcel mutants of Arabidopsis thaliana. Genes Dev. 14, 1485-1497.
25. Jang, J.C., Leon, P., Zhou, L., and Sheen, J. (1997). Hexokinase as a sugar sensor in higher plants. Plant Cell 9, 5-19.
26. Jörnvall, H. (1999). Multiplicity and complexity of SDR and MDR enzymes. Adv. Exp. Med. Biol. 463, 359-364.
27. Jörnvall, H., Höög, J.O., and Persson, B. (1999). SDR and MDR: Completed genome sequences show these protein families to be large, of old origin, and of complex nature. FEBS Lett. 445, 261-264.
28. Koch, K.E. (1996). Carbohydrate modulated gene expression in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47, 509-540.
29. Koiwai, H., Akaba, S., Seo, M., Komano, T., and Koshiba, T. (2000). Functional expression of two Arabidopsis aldehyde oxidases in the yeast Pichia pastoris. J. Biochem. 127, 659-664.
30. Koornneef, M. (1986). Genetic aspects of abscisic acid. In A Genetic Approach to Plant Biochemistry, A.D. Blonstein and P.J. King, eds (Vienna: Springer Verlag), pp. 35-54.
31. Koornneef, M., Bentsink, L., and Hilhorst, H. (2001). Seed dormancy and germination. Curr. Opin. Plant Biol. 5, 33-36.
32. Koshiba, T., Saito, E., Ono, N., Yamamoto, N., and Sato, M. (1996). Purification and properties of flavin- and molybdenumcontaining aldehyde oxidase from coleoptiles of maize. Plant Physiol. 110, 781-789.
33. Laby, R.J., Kincaid, M.S., Kim, D., and Gibson, S.I. (2000). The Arabidopsis sugar-insensitive mutants sis4 and sis5 are defective in abscisic acid synthesis and response. Plant J. 23, 587-596.
34. Leon-Kloosterziel, K.M., Gil, M.A., Ruijs, G.J., Jacobsen, S.E., Olszewski, N.E., Schwartz, S.H., Zeevaart, J.A., and Koornneef, M. (1996). Isolation and characterization of abscisic acid-deficient Arabidopsis mutants at two new loci. Plant J. 10, 655-661.
35. Leung, J., and Giraudat, J. (1998). Abscisic acid signal transduction. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49, 199-222.
36. Leung, J., Merlot, S., and Giraudat, J. (1997). The Arabidopsis ABSCISIC ACID-INSENSITIVE2 (ABI2) and ABI1 genes encode homologous protein phosphatases 2C involved in abscisic acid signal transduction. Plant Cell 9, 759-771.
37. Lopez-Molina, L., Mongrand, S., and Chua, N.H. (2001). A post-germination developmental arrest checkpoint is mediated by abscisic acid and requires the ABI5 transcription factor in Arabidopsis. Proc. Natl. Acad. Sci. USA 98, 4782-4787.
38. Milborrow, B.V. (2001). The pathway of biosynthesis of abscisic acid in vascular plants: A review of the present state of knowledge of ABA biosynthesis. J. Exp. Bot. 52, 1145-1164.
39. Murashige, T., and Skoog, F. (1962). A revised medium for rapid growth and bioassays with tobacco tissue culture. Physiol. Plant. 15, 473-497.
40. Nambara, E., Kawaide, N., Kamiya, Y., and Naito, S. (1998). Characterization of an Arabidopsis thaliana mutant that has a defect in ABA accumulation: ABA-dependent and ABA-independent accumulation of free amino acids during dehydration. Plant Cell Physiol. 39, 853-858.
41. Oppermann, U., Salim, S., Hult, M., Eissner, G., and Jörnvall, H. (1999). Regulatory factors and motifs in SDR enzymes. Adv. Exp. Med. Biol. 463, 365-371.
42. Oppermann, U.C., Filling, C., and Jörnvall, H. (2001). Forms and functions of human SDR enzymes. Chem. Biol. Interact. 130-132, 699-705.
43. Qin, X., and Zeevaart, J.A. (1999). The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proc. Natl. Acad. Sci. USA 96, 15354-15361.
44. Qin, X., and Zeevaart, J.A. (2002). Overexpression of a 9-cis-epoxycarotenoid dioxygenase gene in Nicotiana plumbaginifolia increases abscisic acid and phaseic acid levels and enhances drought tolerance. Plant Physiol. 128, 544-551.
45. Quesada, V., Ponce, M.R., and Micol, J.L. (2000). Genetic analysis of salt-tolerant mutants in Arabidopsis thaliana. Genetics 154, 421-436.
46. Raschke, K., Fim, R.D., and Pierce, M. (1975). Stomatal closure in response to xanthoxin and abscisic acid. Planta 125, 149-160.
47. Raz, V., Bergervoet, J.H., and Koornneef, M. (2001). Sequential steps for developmental arrest in Arabidopsis seeds. Development 128, 243-252.
48. Rock, C.D., and Quatrano, R. (1995). The role of hormones during seed development. In Plant Hormones: Physiology, Biochemistry and Molecular Biology, P.J. Davies, ed (Dordrecht, The Netherlands: Kluwer Academic Publishers), pp. 671-697.
49. Rock, C.D., and Zeevaart, J.A. (1991). The aba mutant of Arabidopsis thaliana is impaired in epoxy-carotenoid biosynthesis. Proc. Natl. Acad. Sci. USA 88, 7496-7499.
50. Rolland, F., Moore, B., and Sheen, J. (2002). Plant sugar sensing and signaling. Plant Cell 14 (suppl.), S185-S205.
51. Rook, F., Corke, F., Card, R., Munz, G., Smith, C., and Bevan, M.W. (2001). Impaired sucrose-induction mutants reveal the modulation of sugar-induced starch biosynthetic gene expression by abscisic acid signalling. Plant J. 26, 421-433.
52. Sagi, M., Fluhr, R., and Lips, S.H. (1999). Aldehyde oxidase and xanthine dehydrogenase in a flacca tomato mutant with deficient abscisic acid and wilty phenotype. Plant Physiol. 120, 571-578.
53. Schroeder, J.I., Kwak, J.M., and Allen, G.J. (2001). Guard cell abscisic acid signalling and engineering drought hardiness in plants. Nature 410, 327-330.
54. Schwartz, S.H., Leon-Kloosterziel, K.M., Koornneef, M., and Zeevaart, J.A. (1997a). Biochemical characterization of the aba2 and aba3 mutants in Arabidopsis thaliana. Plant Physiol. 114, 161-166.
55. Schwartz, S.H., Tan, B.C., Gage, D.A., Zeevaart, J.A., and McCarty, D.R. (1997b). Specific oxidative cleavage of carotenoids by VP14 of maize. Science 276, 1872-1874.
56. Seo, M., Koiwai, H., Akaba, S., Komano, T., Oritani, T., Kamiya, Y., and Koshiba, T. (2000a). Abscisic aldehyde oxidase in leaves of Arabidopsis thaliana. Plant J. 23, 481-488.
57. Seo, M., and Koshiba, T. (2002). The complex regulation of ABA biosynthesis in plants. Trends Plant Sci. 7, 41-48.
58. Seo, M., Peeters, A.J., Koiwai, H., Oritani, T., Marion-Poll, A., Zeevaart, J.A., Koornneef, M., Kamiya, Y., and Koshiba, T. (2000b). The Arabidopsis aldehyde oxidase 3 (AAO3) gene product catalyzes the final step in abscisic acid biosynthesis in leaves. Proc. Natl. Acad. Sci. USA 97, 12908-12913.
59. Sharp, R.E., LeNoble, M.E., Else, M.A., Thorne, E.T., and Gherardi, F. (2000). Endogenous ABA maintains shoot growth in tomato independently of effects on plant water balance: Evidence for an interaction with ethylene. J. Exp. Bot. 51, 1575-1584.
60. Sheen, J. (1994). Feedback control of gene expression. Photosynth. Res. 39, 427-438.
61. Sheen, J., Zhou, L., and Jang, J.C. (1999). Sugars as signaling molecules. Curr. Opin. Plant Biol. 2, 410-418.
62. Silverstone, A.L., Chang, C., Krol, E., and Sun, T.P. (1997). Developmental regulation of the gibberellin biosynthetic gene GA1 in Arabidopsis thaliana. Plant J. 12, 9-19.
63. Sindhu, R.K., and Walton, D.C. (1987). Conversion of xanthoxin to ABA by cell-free preparations from bean leaves. Plant Physiol. 85, 916-921.
64. Smalle, J., Haegman, M., Kurepa, J., Van Montagu, M., and Straeten, D.V. (1997). Ethylene can stimulate Arabidopsis hypocotyl elongation in the light. Proc. Natl. Acad. Sci. USA 94, 2756-2761.
65. Smeekens, S. (2000). Sugar-induced signal transduction in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51, 49-81.
66. Söderman, E.M., Brocard, I.M., Lynch, T.J., and Finkelstein, R.R. (2000). Regulation and function of the Arabidopsis ABA-insensitive4 gene in seed and abscisic acid response signaling networks. Plant Physiol. 124, 1752-1765.
67. Stepanova, A.N., and Ecker, J.R. (2000). Ethylene signaling: From mutants to molecules. Curr. Opin. Plant Biol. 3, 353-360.
68. Stitt, M., and Krapp, A. (1999). The interaction between elevated carbon dioxide and nitrogen nutrition: The physiological and molecular background. Plant Cell Environ. 22, 583-621.
69. Tan, B.C., Cline, K., and McCarty, D.R. (2001). Localization and targeting of the VP14 epoxy-carotenoid dioxygenase to chloroplast membranes. Plant J. 27, 373-382.
70. Tan, B.C., Schwartz, S.H., Zeevaart, J.A., and McCarty, D.R. (1997). Genetic control of abscisic acid biosynthesis in maize. Proc. Natl. Acad. Sci. USA 94, 12235-12240.
71. Thompson, A.J., Jackson, A.C., Parker, R.A., Morpeth, D.R., Burbidge, A., and Taylor, I.B. (2000). Abscisic acid biosynthesis in tomato: Regulation of zeaxanthin epoxidase and 9-cis-epoxy-carotenoid dioxygenase mRNAs by light/dark cycles, water stress and abscisic acid. Plant Mol. Biol. 42, 833-845.
72. Wobus, U., and Weber, H. (1999). Sugars as signal molecules in plant seed development. Biol. Chem. 380, 937-944.
73. Xiang, C., Han, P., Lutziger, I., Wang, K., and Oliver, D.J. (1999). A mini binary vector series for plant transformation. Plant Mol. Biol. 40, 711-717.
74. Xiao, W., Sheen, J., and Jang, J.C. (2000). The role of hexokinase in plant sugar signal transduction and growth and development. Plant Mol. Biol. 44, 451-461.
75. Xiong, L., Ishitani, M., Lee, H., and Zhu, J.K. (2001). The Arabidopsis LOS5/ABA3 locus encodes a molybdenum cofactor suifurase and modulates cold stress- and osmotic stress-responsive gene expression. Plant Cell 13, 2063-2083.
76. Xiong, L., Lee, H., Ishitani, M., and Zhu, J.K. (2002). Regulation of osmotic stress-responsive gene expression by the Los6/ABA1 locus in Arabidopsis. J. Biol. Chem. 277, 8588-8596.
77. Yamamoto, H., and Oritani, T. (1996). Stereoselectivity in the biosynthetic conversion of xanthoxin into abscisic acid. Planta 200, 319-325.
78. Zeevaart, J.A., and Creelman, R.A. (1988). Metabolism and physiology of abscisic acid. Annu. Rev. Plant Physiol. Plant Mol. Biol. 39, 439-473.
79. Zhou, L., Jang, J.C., Jones, T.L., and Sheen, J. (1998). Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucose-insensitive mutant. Proc. Natl. Acad. Sci. USA 95, 10294-10299.
80. Zimmerman, J.L. (1993). Somatic embryogenesis: A model for early development in higher plants. Plant Cell 5, 1411-1423.