Browse > Article
http://dx.doi.org/10.14348/molcells.2018.0092

Arabidopsis ACC Oxidase 1 Coordinated by Multiple Signals Mediates Ethylene Biosynthesis and Is Involved in Root Development  

Park, Chan Ho (Department of Life Science, Chung-Ang University)
Roh, Jeehee (Department of Life Science, Chung-Ang University)
Youn, Ji-Hyun (Department of Life Science, Chung-Ang University)
Son, Seung-Hyun (Department of Life Science, Chung-Ang University)
Park, Ji Hye (Department of Biological Science, Andong National University)
Kim, Soon Young (Department of Biological Science, Andong National University)
Kim, Tae-Wuk (Department of Life Science, College of Natural Sciences, Hanyang University)
Kim, Seong-Ki (Department of Life Science, Chung-Ang University)
Publication Information
Molecules and Cells / v.41, no.10, 2018 , pp. 923-932 More about this Journal
Abstract
Ethylene regulates numerous aspects of plant growth and development. Multiple external and internal factors coordinate ethylene production in plant tissues. Transcriptional and post-translational regulations of ACC synthases (ACSs), which are key enzymes mediating a rate-limiting step in ethylene biosynthesis have been well characterized. However, the regulation and physiological roles of ACC oxidases (ACOs) that catalyze the final step of ethylene biosynthesis are largely unknown in Arabidopsis. Here, we show that Arabidopsis ACO1 exhibits a tissue-specific expression pattern that is regulated by multiple signals, and plays roles in the lateral root development in Arabidopsis. Histochemical analysis of the ACO1 promoter indicated that ACO1 expression was largely modulated by light and plant hormones in a tissue-specific manner. We demonstrated that point mutations in two E-box motifs on the ACO1 promoter reduce the light-regulated expression patterns of ACO1. The aco1-1 mutant showed reduced ethylene production in root tips compared to wild-type. In addition, aco1-1 displayed altered lateral root formation. Our results suggest that Arabidopsis ACO1 integrates various signals into the ethylene biosynthesis that is required for ACO1's intrinsic roles in root physiology.
Keywords
ACC oxidase 1; Arabidopsis thaliana; ethylene biosynthesis; lateral root; transcriptional regulation;
Citations & Related Records
연도 인용수 순위
  • Reference
1 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.   DOI
2 Gomez-Lim, M.A., Valdes-Lopez, V., Cruz-Hernandez, A., and Saucedo-Arias, L.J. (1993). Isolation and characterization of a gene involved in ethylene biosynthesis from Arabidopsis thaliana. Gene 134, 217-221.   DOI
3 Iwamoto, M., Baba-Kasai, A., Kiyota, S., Hara, N., and Takano, M. (2010). ACO1, a gene for aminocyclopropane-1-carboxylate oxidase: effects on internode elongation at the heading stage in rice. Plant Cell Environ. 33, 805-815.
4 Kende, H. and Zeevaart, J.A.D. (1997). The five "classical" plant hormones. Plant Cell 9, 1197-1210.   DOI
5 Lasserre, E., Bouquin, T., Hernandez, J., Pech, J., Balague, C., and Bull, J. (1996). Structure and expression of three genes encoding ACC oxidase homologs from melon (Cucumis melo L.). Mol. Gen. Genet. 251, 81-90.
6 Lewis, D.R., Miller, N.D., Splitt, B.L., Wu, G., and Spalding, E.P. (2007). Separating the roles of acropetal and basipetal auxin transport on gravitropism with mutations in two Arabidopsis multidrug resistance-like ABC transporter genes. Plant Cell 19, 1838-1850.   DOI
7 Lewis, D.R., Negi, S., Sukumar, P., and Muday, G.K. (2011). Ethylene inhibits lateral root development, increases IAA transport and expression of PIN3 and PIN7 auxin efflux carriers. Development 138, 3485-3495.   DOI
8 Thain, S.C., Vandenbussche, F., Laarhoven, L.J.J., Dowson-Day, M.J., Wang, Z.-Y., Tobin, E.M., Harren, F.J.M., Millar, A.J., and Van Der Straeten, D. (2004). Circadian rhythms of ethylene emission in Arabidopsis. Plant Physiol. 136, 3751-3761.   DOI
9 Tsuchisaka, A., Yu, G., Jin, H., Alonso, J.M., Ecker, J.R., Zhang, X., Gao, S., and Theologis, A. (2009). A combinatorial interplay among the 1-aminocyclopropane-1-carboxylate isoforms regulates ethylene biosynthesis in Arabidopsis thaliana. Genetics 183, 979-1003.   DOI
10 Ulmasov, T., Hagen, G., and Guilfoyle, T.J. (1999). Dimerization and DNA binding of auxin response factors. Plant J. 19, 309-319.   DOI
11 Vriezen, W.H., Hulzink, R., Mariani, C., and Voesenek, L.A. (1999). 1-aminocyclopropane-1-carboxylate oxidase activity limits ethylene biosynthesis in Rumex palustris during submergence. Plant Physiol. 121, 189-196.   DOI
12 Weigel, D., and Glazebrook, J. (2002). Arabidopsis: A Laboratory Manual (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
13 Martinez-Garcia, J.F., Huq, E., and Quail, P.H. (2000). Direct targeting of light signals to a promoter element-bound transcription factor. Science 288, 859-863.   DOI
14 Li, Z., Peng, J., Wen, X., and Guo, H. (2013). ETHYLENE-INSENSITIVE3 is a senescence-associated gene that accelerates age-dependent leaf senescence by directly repressing miR164 transcription in Arabidopsis. Plant Cell 25, 3311-3328.   DOI
15 Yamagami, T., Tsuchisaka, A., Yamada, K., Haddon, W.F., Harden, L.A., and Theologis, A. (2003). Biochemical diversity among the 1-amino-cyclopropane-1-carboxylate synthase isozymes encoded by the Arabidopsis gene family. J. Biol. Chem. 278, 49102-49112.   DOI
16 Yang, S.F., and Hoffman, N.E. (1984). Ethylene biosynthesis and its regulation in higher plants. Annu. Rev. Plant Physiol. 35, 155-189.   DOI
17 Ye, L., Li, L., Wang, L., Wang, S., Li, S., Du, J., Zhang, S., and Shou, H. (2015). MPK3/MPK6 are involved in iron deficiency-induced ethylene production in Arabidopsis. Front. Plant Sci.6, 953.
18 Yi, H.C., Joo, S., Nam, K.H., Lee, J.S., Kang, B.G., and Kim, W.T. (1999). Auxin and brassinosteroid differentially regulate the expression of three members of the 1-aminocyclopropane-1-carboxylate synthase gene family in mung bean (Vigna radiata L.). Plant Mol. Biol. 41, 443-454.   DOI
19 Linkies, A., Muller, K., Morris, K., Tureckova, V., Wenk, M., Cadman, C.S.C., Corbineau, F., Strnad, M., Lynn, J.R., Finch-Savage, W.E., and Leubner-Metzger, G. (2009). Ethylene interacts with abscisic acid to regulate endosperm rupture during germination: a comparative approach using lepidium sativum and Arabidopsis thaliana. Plant Cell 21, 3803-3822.   DOI
20 Liu, Y., and Zhang, S. (2004). Phosphorylation of 1-aminocyclopropane-1-carboxylic acid synthase by MPK6, a stressresponsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16, 3386-3399.   DOI
21 Maunders, M.J., Holdsworth, M.J., Slater, A., Knapp, J.E., Bird, C.R., Schuch, W., and Grierson, D. (1987). Ethylene stimulates the accumulation of ripening-related mRNAs in tomatoes. Plant Cell Environ. 10, 177-184.
22 Mazzella, M.A., Arana, M.V., Staneloni, R.J., Perelman, S., Rodriguez Batiller, M.J., Muschietti, J., Cerdan, P.D., Chen, K., Sanchez, R.A., Zhu, T., Chory, J., and Casal, J.J. (2005). Phytochrome control of the Arabidopsis transcriptome anticipates seedling exposure to light. Plant Cell 17, 2507-2516.   DOI
23 Oh, E., Zhu, J.-Y., and Wang, Z.-Y. (2012). Interaction between BZR1 and PIF4 integrates brassinosteroid and environmental responses. Nat. Cell Biol. 14, 802-809.   DOI
24 Oh, E., Zhu, J.-Y., Bai, M.-Y., Arenhart, R.A., Sun, Y., and Wang, Z.-Y. (2014). Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl. eLife 3: e03031.   DOI
25 Barry, C.S., Llop-Tous, M.I., and Grierson, D. (2000). The regulation of 1-aminocyclopropane-1-carboxylic acid synthase gene expression during the transition from system-1 to system-2 ethylene synthesis in tomato. Plant Physiol. 123, 979-986.   DOI
26 Aloni, R., Schwalm, K., Langhans, M., and Ullrich, C. (2003). Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis in Arabidopsis. Planta 216, 841-853.
27 Alonso, J.M. and Ecker, J.R. (2001). The ethylene pathway: A paradigm for plant hormone signaling and interaction. Sci STKE 2001: RE1.
28 Barry, C.S., Blume, B., Bouzayen, M., Cooper, W., Hamilton, A.J., and Grierson, D. (1996). Differential expression of the 1-aminocyclopropane-1-carboxylate oxidase gene family of tomato. Plant J. 9, 525-535.   DOI
29 Van de Poel, B., and Van Der Straeten, D. (2014). 1-aminocyclopropane-1-carboxylic acid (ACC) in plants: more than just the precursor of ethylene! Front. Plant Sci.5: 640.
30 Yun, H.R., Joo, S.-H., Park, C.H., Kim, S.-K., Chang, S.C., and Kim, S.Y. (2009). Effects of brassinolide and IAA on ethylene production and elongation in maize primary roots. J. Plant Biol. 52, 268-274.   DOI
31 Clough, S.J., and Bent, A.F. (1998). Floral dip: a simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735-743.   DOI
32 Beaudoin, N., Serizet, C., Gosti, F., and Giraudat, J. (2000). Interactions between abscisic acid and ethylene signaling cascades. Plant Cell 12, 1103-1115.   DOI
33 Booker, M.A., and DeLong, A. (2015). Producing the ethylene signal: regulation and diversification of ethylene biosynthetic enzymes. Plant Physiol. 169, 42-50.   DOI
34 Bradford, K.J., and Yang, S.F. (1980). Xylem transport of 1-aminocyclopropane-1-carboxylic acid, an ethylene precursor, in waterlogged tomato plants. Plant Physiol. 65, 322-326.   DOI
35 Yoon, G.M., and Kieber, J.J. (2013). 14-3-3 Regulates 1-Aminocyclopropane-1-Carboxylate synthase protein turnover in Arabidopsis. Plant Cell 25, 1016-1028.   DOI
36 Buer, C.S., Sukumar, P., and Muday, G.K. (2006). Ethylene modulates flavonoid accumulation and gravitropic responses in roots of Arabidopsis. Plant Physiol. 140, 1384-1396.   DOI
37 Chae, H.S., Faure, F., and Kieber, J.J. (2003). The eto1, eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS protein. Plant Cell 15, 545-559.   DOI
38 Chang, S.C., Kim, Y.-S., Lee, J.Y., Kaufman, P.B., Kirakosyan, A., Yun, H.S., Kim, T.-W., Kim, S.Y., Cho, M.H., Lee, J.S., and Kim, S.-K. (2004). Brassinolide interacts with auxin and ethylene in the root gravitropic response of maize (Zea mays). Physiol. Plantarum 121, 666-673.   DOI
39 Dugardeyn, J., Vandenbussche, F., and Van Der Straeten, D. (2008). To grow or not to grow: what can we learn on ethylene-gibberellin cross-talk by in silico gene expression analysis?. J. Exp. Bot. 59, 1-16.
40 Edelmann, H.G., Sabovljevic, A., Njio, G., and Roth, U. (2005). The role of auxin and ethylene for gravitropic differential growth of coleoptiles and roots of rye- and maize seedlings. Adv. Space Res. 36, 1167-1174.   DOI
41 Qin, Y.-M., Hu, C.-Y., Pang, Y., Kastaniotis, A.J., Hiltunen, J.K., and Zhu, Y.-X. (2007). Saturated very-long-chain fatty acids promote cotton fiber and Arabidopsis cell elongation by activating ethylene biosynthesis. Plant Cell 19, 3692-3704.   DOI
42 Okushima, Y., Fukaki, H., Onoda, M., Theologis, A., and Tasaka, M. (2007). ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19, 118-130.   DOI
43 Park, C.H., Kim, T.-W., Son, S.-H., Hwang, J.-Y., Lee, S.C., Chang, S. C., Kim, S.-H., Kim, S.W., and Kim, S.-K. (2010). Brassinosteroids control AtEXPA5 gene expression in Arabidopsis thaliana. Phytochemistry 71, 380-387.   DOI
44 Picton, S., Barton, S.L., Bouzayen, M., Hamilton, A.J., and Grierson, D. (1993). Altered fruit ripening and leaf senescence in tomatoes expressing an antisense ethylene-forming enzyme transgene. Plant J. 3, 469-481.   DOI
45 Rudus, I., Sasiak, M., and Kepczynski, J. (2013). Regulation of ethylene biosynthesis at the level of 1-aminocyclopropane-1-carboxylate oxidase (ACO) gene. Acta Physiol. Plant 35, 295-307.   DOI
46 Skottke, K.R., Yoon, G.M., Kieber, J.J., and DeLong, A. (2011). Protein phosphatase 2A controls ethylene biosynthesis by differentially regulating the turnover of ACC synthase isoforms. PLoS Genet. 7: e1001370.   DOI
47 Sun, Y., Fan, X.-Y., Cao, D.-M., Tang, W., He, K., Zhu, J.-Y., He, J.-X., Bai, M.-Y., Zhu, S., Oh, E., et al. (2010). Integration of brassinosteroid signal transduction with the transcription network for plant growth regulation in Arabidopsis. Developmental Cell 19, 765-777.   DOI
48 Garcia, M.J., Lucena, C., Romera, F.J., Alcantara, E., and Perez-Vicente, R. (2010). Ethylene and nitric oxide involvement in the up-regulation of key genes related to iron acquisition and homeostasis in Arabidopsis. J. Exp. Bot. 61, 3885-3899.   DOI
49 Sukumar, P., Edwards, K.S., Rahman, A., DeLong, A., and Muday, G.K. (2009). PINOID kinase regulates root gravitropism through modulation of PIN2-dependent basipetal auxin transport in Arabidopsis. Plant Physiol. 150, 722-735.   DOI