Regulatory mechanisms tuning ethylen signaling in plants
https://doi.org/10.18699/VJ15.105
Abstract
About the Authors
E. V. ZemlyanskayaRussian Federation
N. A. Omelyanchuk
Russian Federation
A. A. Ermakov
Russian Federation
V. V. Mironova
Russian Federation
References
1. Abel S., Nguyen M.D., Chow W., Theologis A. ACS4, a primary indoleacetic acid- responsive gene encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis thaliana: structural characterization, expression in Escherichia coli, and expression characteristics in response to auxin [corrected]. J. Biol. Chem. 1995;270(32): 19093-19099.
2. Abeles F.B., Morgan P.W., Saltveit M.E. Ethylene in plant biology. San Diego: Acad. Press, 1992.
3. Alexander L., Grierson D. Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J. Exp. Bot. 2002;53(377): 2039-2055.
4. Alonso J.M., Stepanova A.N., Solano R., Wisman E., Ferrari S., Ausubel F.M., Ecker J.R. Five components of the ethylene-response pathway identified in a screen for weak ethylene-insensitive mutants in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2003;100(5):2992-2997.
5. An F., Zhang X., Zhu Z., Ji Y., He W., Jiang Z., Li M., Guo H. Coordinated regulation of apical hook development by gibberellins and ethylene in etiolated Arabidopsis seedlings. Cell Res. 2012;22(5): 915-927. DOI 10.1038/cr.2012.29
6. An F., Zhao Q., Ji Y., Li W., Jiang Z., Yu X., Zhang C., Han Y., He W., Liu Y., Zhang S., Ecker J.R., Guo H. Ethylene-induced stabilization of ETHYLENE-INSENSITIVE3 and EIN3-LIKE1 is mediated by proteasomal degradation of EIN3 binding F-box 1 and 2 that requires EIN2 in Arabidopsis. Plant Cell. 2010;22(7):2384-2401. DOI 10.1105/tpc.110.076588
7. Cary A.J., Liu W., Howell S.H. Cytokinin action is coupled to ethylene in its effects on the inhibition of root and hypocotyl elongation in Arabidopsis thaliana seedlings. Plant Physiol. 1995;107(4):1075- 1082. DOI 10.1104/pp.107.4.1075
8. Chae H.S., Faure F., Kieber J.J. The eto1, eto2 and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of the ACS protein. Plant Cell. 2003;15(2):545-559. DOI 10.1105/tpc.006882
9. Chang K.N., Zhong S., Weirauch M.T., Hon G., Pelizzola M., Li H., Huang S.S.C., Schmitz R.J., Urich M.A., Kuo D., Nery J.R., Qiao H., Yang A., Jamali A., Chen H., Ideker T., Ren B., Bar-Joseph Z., Hughes T.R., Ecker J.R. Temporal transcriptional response to ethylene gas drives growth hormone cross-regulation in Arabidopsis. eLife. 2013;2:e00675. DOI 10.7554/eLife.00675
10. Chen Y.F., Shakeel S.N., Bowers J., Zhao X.C., Etheridge N., Schaller G.E. Ligand- induced degradation of the ethylene receptor ETR2. J. Biol. Chem. 2007;282(34):24752-24758.
11. Chernykh O.A., Levitsky V.G., Omelyanchuk N.A., Mironova V.V. Computational analysis and functional annotation of AP2/ERF translocation factor binding sites in Arabidopsis thaliana L. genome. Vavilovskii Zhurnal Genetiki i Selektsii = Vavilov Journal of Genetics and Breeding. 2014;18(4/2):887-897.
12. Chilley P.M., Casson S.A., Tarkowski P., Hawkins N., Wang K.L., Hussey P.J., Beale M., Ecker J.R., Sandberg G.K., Lindsey K. The POLARIS peptide of Arabidopsis regulates auxin transport and root growth via effects on ethylene signaling. Plant Cell. 2006;18(11): 3058-3072.
13. Cho Y.H., Yoo S.D. Novel connections and gaps in ethylene signaling from the ER membrane to the nucleus. Front. Plant Sci. 2015;5:733. DOI 10.3389/fpls.2014.00733
14. De Paepe A., Vuylsteke M., Van Hummelen P., Zabeau M., Van Der Straeten D. Transcriptional profiling by cDNA-AFLP and microarray analysis reveals novel insights into the early response to ethylene in Arabidopsis. Plant J. 2004;39(4):537-559. DOI 10.1111/j.1365-313X.2004.02156.x
15. Díaz J., Álvarez-Buylla E.R. A model of the ethylene signaling pathway and its gene response in Arabidopsis thaliana: Pathway crosstalk and noise-filtering properties. Chaos. 2006;16(2):023112. DOI 10.1063/1.2189974
16. Dong C.H., Rivarola M., Resnick J.S., Maggin B.D., Chang C. Subcellular co- localization of Arabidopsis RTE1 and ETR1 supports a regulatory role for RTE1 in ETR1 ethylene signaling. Plant J. 2008; 53(2):275-286.
17. Dugardeyn J., Vandenbussche F., Van Der Straeten D. To grow or not to grow: what can we learn on ethylene–gibberellin cross-talk by in silico gene expression analysis? J. Exp. Bot. 2008;59(1):1-16. DOI 10.1093/jxb/erm349
18. Ecker J.R. The ethylene signal transduction pathway in plants. Science. 1995;268:667-675.
19. Fujimoto S.Y., Ohta M., Usui A., Shinshi H., Ohme-Takagi M. Arabidopsis ethylene- responsive element binding factors act as transcriptional activators or repressors of GCC box-mediated gene expression. Plant Cell. 2000;12(3):393-404.
20. Gallie D.R., Geisler-Lee J., Chen J., Jolley B. Tissue-specific expression of the ethylene biosynthetic machinery regulates root growth in maize. Plant. Mol. Biol. 2009;69(1-2):195-211. DOI 10.1007/s11103-008-9418-1
21. Gazzarrini S., McCourt P. Cross-talk in plant hormone signalling: What Arabidopsis mutants are telling us. Ann. Bot. 2003;91(6):605-612.DOI 10.1093/aob/mcg064
22. Giovannoni J.J. Fruit ripening mutants yield insights into ripening control. Curr. Opin. Plant Biol. 2007;10(3):283-289. DOI 10.1016/j.pbi.2007.04.008
23. Han L., Li G.J., Yang KY., Mao G., Wang R., Liu Y., Zhang S. Mitogenactivated protein kinase 3 and 6 regulate Botrytis cinerea-induced ethylene production in Arabidopsis. Plant J. 2010;64(1):114-127. DOI 10.1111/j.1365-313X.2010.04318.x
24. Hansen M., Chae H.S., Kieber J.J. Regulation of ACS protein stability by cytokinin and brassinosteroid. Plant J. 2009;57(4):606-614. DOI 10.1111/j.1365- 313X.2008.03711.x
25. Ikeda Y., Men S., Fischer U., Stepanova A.N., Alonso J.M., Ljung K., Grebe M. Local auxin biosynthesis modulates gradient-directed planar polarity in Arabidopsis. Nat. Cell Biol. 2009;11(6):731-738. DOI 10.1038/ncb1879
26. Itkin M., Seybold H., Breitel D., Rogachev I., Meir S., Aharoni A. TOMATO AGAMOUS- LIKE 1 is a component of the fruit ripening regulatory network. Plant J. 2009;60(6):1081-1095. DOI 10.1111/j.1365-313X.2009.04064.x
27. Ito Y., Kitagawa M., Ihashi N., Yabe K., Kimbara J., Yasuda J., Ito H., Inakuma T., Hiroi S., Kasumi T. DNA-binding specificity, transcriptional activation potential, and the rin mutation effect for the tomato fruit-ripening regulator RIN. Plant J. 2008;55(2):212-223. DOI 10.1111/j.1365-313X.2008.03491.x
28. Joo S., Seo Y.S., Kim S.M., Hong D.K., Park K.Y., Kim W.T. Brassinosteroid induction of AtACS4 encoding an auxin-responsive 1-aminocyclopropane-1-carboxylate synthase 4 in Arabidopsis seedlings. Physiol. Plant. 2006;126(4):592-604. DOI 10.1111/j.1399-3054.2005.00602.x
29. Ju C., Chang C. Advances in ethylene signalling: protein complexes at the endoplasmic reticulum membrane. AoB Plants. 2012:pls031. DOI 10.1093/aobpla/pls031
30. Ju C., Yoon G.M., Shemansky J.M., Lin D.Y., Ying Z.I., Chang J., Garrett W.M., Kessenbrock M., Groth G., Tucker M.L., Cooper B., Kieber J.J., Chang C. CTR1 phosphorylates the central regulator EIN2 to control ethylene hormone signaling from the ER membrane to the nucleus in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2012; 109(47):19486-19491. DOI 10.1073/pnas.1214848109
31. Karlova R., Chapman N., David K., Angenent G.C., Seymour G.B., de Maagd R.A. Transcriptional control of fleshy fruit development and ripening. J. Exp. Bot. 2014;65(16):4527-4541. DOI 10.1093/jxb/eru316
32. Kendrick M.D., Chang C. Ethylene signaling: new levels of complexity and regulation. Curr. Opin. Plant Biol. 2008;11(5):479-485. DOI 10.1016/j.pbi.2008.06.011
33. Kevany B.M., Tieman D.M., Taylor M.G., Cin V.D., Klee H.J. Ethylene receptor degradation controls the timing of ripening in tomato fruit. Plant J. 2007;51(3):458-467. DOI 10.1111/j.1365-313X.2007.03170.x
34. Konishi M., Yanagisawa S. Ethylene signaling in Arabidopsis involves feedback regulation via the elaborate control of EBF2 expression by EIN3. Plant J. 2008;55(5):821-831. DOI 10.1111/j.1365-313X.2008.03551.x
35. Kosugi S., Ohashi Y. Cloning and DNA-binding properties of a tobacco Ethylene- Insensitive3 (EIN3) homolog. Nucleic Acids Res. 2000; 28(4):960-967.
36. Kudryakova N.V., Burkhanova E.A., Yakovleva L.A., Rakitin V.Yu., Smith A.R., Hall M.A., Kulaeva O.N. Ethylene and cytokinin in the control of senescence in detached leaves of Arabidopsis thaliana eti- 5 mutant and wild-type plants. Fiziologiya rasteniy = Plant Physiology (Moscow). 2001;48(5):723-727.
37. Lacey R.F., Binder B.M. How plants sense ethylene gas – The ethylene receptors. J. Inorg. Biochem. 2014;133:58-62. DOI 10.1016/j.jinorgbio
38. Lewis D.R., Negi S., Sukumar P., Muday G.K. Ethylene inhibits lateral root development, increases IAA transport and expression of PIN3 and PIN7 auxin efflux carriers. Development. 2011;138(16):3485-3495. DOI 10.1242/dev.065102
39. Li G., Meng X., Wang R., Mao G., Han L., Liu Y., Zhang S. Duallevel regulation of ACC synthase activity by MPK3/MPK6 cascade and its downstream WRKY transcription factor during ethylene induction in Arabidopsis. PLoS Genetics. 2012;8(6):e1002767. DOI 10.1371/journal.pgen.1002767
40. Li W., Ma M., Feng Y., Li H., Wang Y., Ma Y., Li M., An F., Guo H. EIN2-directed translational regulation of ethylene signaling in Arabidopsis. Cell. 2015;163(3):670-683. DOI 10.1016/j.cell.2015.09.037
41. Liu Q., Wen C.K. Cooperative ethylene receptor signaling. Plant Signal. Behav. 2012a;7(8):1009-1013. DOI 10.4161/psb.20937
42. Liu Q., Wen C.K. Arabidopsis ETR1 and ERS1 differentially repress the ethylene response in combination with other ethylene receptor genes. Plant Physiol. 2012b;158(3):1193-1207. DOI 10.1104/pp.111.187757
43. Lorenzo O., Piqueras R., Sanchez-Serrano J.J., Solano R. ETHYLENE RESPONSE FACTOR1 integrates signals from ethylene and jasmonate pathways in plant defense. Plant Cell. 2003;15(1):165-178. DOI 10.1105/tpc.007468
44. Ludwikówa A., Cieśla A., Kasprowicz-Maluśki A., Mituła F., Tajdel M., Gałgański Ł., Ziółkowski P.A., Kubiak P., Małecka A., Piechalak A., Szabat M., Górska A., Dąbrowski M., Ibragimow I., Sadowski J. Arabidopsis protein phosphatase 2C ABI1 interacts with type I ACC synthases and is involved in the regulation of ozone- induced ethylene biosynthesis. Mol. Plant. 2014;7(6):960-976. DOI 10.1093/mp/ssu025
45. Lyzenga W.J., Stone S.L. Regulation of ethylene biosynthesis through protein degradation. Plant Signal. Behav. 2012;7(11):1438-1442. DOI 10.4161/psb.21930
46. McKeon T., Yang S.F. Biosynthesis and metabolism of ethylene. Plant Hormones and Their Role in Plant Growth and Development. Ed. P.J. Davides. Dordrecht: Martinus Nijhoff Publ., 1987.
47. McManus M.T. The plant hormone ethylene. Annual Plant Reviews. Oxford: Wiley-Blackwell, 2012;44.
48. Merchante C., Alonso J.M., Stepanova A.N. Ethylene signaling: simple ligand, complex regulation. Curr. Opin. Plant Biol. 2013;16(5):554- 560. DOI 10.1016/j.pbi.2013.08.001
49. Muday G.K., Rahman A., Binder B.M. Auxin and ethylene: collaborators or competitors? Trends Plant Sci. 2012;17(4):181-195. DOI 10.1016/j.tplants.2012.02.001
50. Murr D.P., Yang S.F. Conversion of 5’-methylthioadenosine to methionine by apple tissue. Phytochemistry. 1975;14:1291-1292. DOI 10.1016/S0031-9422(00)98613-8
51. Ohme-Takagi M., Shinshi H. Ethylene-lnducible DNA binding proteins that interact with an ethylene-responsive element. Plant Cell. 1995;7(2):173-182.
52. Pirrello J., Prasad B.C., Zhang W., Chen K., Mila I., Zouine M., Latché A., Pech J.C., Ohme-Takagi M., Regad F., Bouzayen M. Functional analysis and binding affinity of tomato ethylene response factors provide insight on the molecular bases of plant differential responses to ethylene. BMC Plant Biol. 2012;12:190. DOI 10.1186/1471- 2229-12-190
53. Pre M., Atallah M., Champion A., De Vos M., Pieterse C.M., Memelink J. The AP2/ERF domain transcription factor ORA59 integrates jasmonic acid and ethylene signals in plant defense. Plant Physiol. 2008;147(3):1347-1357. DOI 10.1104/pp.108.117523
54. Qiao H., Shen Z., Huang S.C., Schmitz R.J., Urich M.A., Briggs S.P., Ecker J.R. Processing and subcellular trafficking of ER-tethered EIN2 control response to ethylene gas. Science. 2012;338(6105):390-393. DOI 10.1126/science.1225974
55. Riechmann J.L., Heard J., Martin G., Reuber L., Jiang C.-Z., Keddie J., Adam L., Pineda O., Ratcliffe O.J., Samaha R.R., Creelman R., Pilgrim M., Broun P., Zhang J.Z., Ghandehari D., Sherman B.K., Yu G.- L. Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science. 2000;290(5499):2105- 2110.
56. Rudus I., Sasiak M., Kepczynski J. Regulation of ethylene biosynthesis at the level of 1-aminocyclopropane-1-carboxylate oxidase (ACO) gene. Acta Physiol. Plant. 2013;35(2):295-307. DOI 10.1007/s11738-012-1096-6
57. Ruzicka K., Ljung K., Vanneste S., Podhorska R., Beeckman T., Friml J., Benkova E. Ethylene regulates root growth through effects on auxin biosynthesis and transport- dependent auxin distribution. Plant Cell. 2007;19(7):2197-2212. DOI 10.1105/tpc.107.052126
58. Rzewuski G., Suter M. Ethylene biosynthesis and signaling in rice. Plant Sci. 2008;175:32-42. DOI 10.1016/j.plantsci.2008.01.012
59. Shakeel S., Gao Z., Amir M., Chen Y.F., Rai M.I., Haq N.U., Schaller G.E. Ethylene regulates levels of ethylene-receptor/CTR1 signaling complexes in Arabidopsis thaliana. J. Biol. Chem. 2015; 290(19):12415-12424. DOI 10.1074/jbc.M115.652503
60. Shin K., Lee S., Song W.Y., Lee R.A., Lee I., Ha K., Koo J.C., Park S.K., Nam H.G., Lee Y., Soh M.S. Genetic Identification of ACC-RESISTANT2 reveals involvement of LYSINE HISTIDINE TRANSPORTER1 in the uptake of 1-aminocyclopropane-1-carboxylic acid in Arabidopsis thaliana. Plant Cell Physiol. 2015;56(3):572-582.DOI 10.1093/pcp/pcu201
61. Skottke K.R., Yoon G.M., Kieber J.J., DeLong A. Protein phosphatase 2A controls ethylene biosynthesis by differentially regulating the turnover of ACC synthase isoforms. PLoS Genet. 2011;7(4):e1001370. DOI 10.1371/journal.pgen.1001370
62. Solano R., Stepanova A., Chao Q., Ecker J.R. Nuclear events in ethylene signaling: a transcriptional cascade mediated by ETHYLENEINSENSITIVE3 and ETHYLENE-RESPONSE- FACTOR1. Genes Dev. 1998;12(23):3703-3714.
63. Stepanova A.N., Alonso J.M. Ethylene signaling and response: where different regulatory modules meet. Curr. Opin. Plant Biol. 2009; 12(5):548-555. DOI 10.1016/j.pbi.2009.07.009
64. Stepanova A.N., Hoyt J.M., Hamilton A.A., Alonso J.M. A link between ethylene and auxin uncovered by the characterization of two root-specific ethylene-insensitive mutants in Arabidopsis. Plant Cell. 2005;17(8):2230-2242. DOI 10.1105/tpc.105.033365
65. Stepanova A.N., Yun J., Likhacheva A.V., Alonso J.M. Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell. 2007;19(7):2169-2185. DOI 10.1105/tpc.107.052068
66. Swarup R., Perry P., Hagenbeek D., Van Der Straeten D., Beemster G.T.S., Sandberg G., Bhalerao R., Ljung K., Bennett M.J. Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell. 2007;19(7): 2186-2196. DOI 10.1105/tpc.107.052100
67. Takatsuka H., Umeda M. Hormonal control of cell division and elongation along differentiation trajectories in roots. J. Exp. Bot. 2014;65(10):2633-2643. DOI 10.1093/jxb/ert485
68. Tsuchisaka A., Theologis A. Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members. Plant Physiol. 2004;136(2):2982-3000. DOI 10.1104/pp.104.049999
69. Tsuchisaka A., Yu G., Jin H., Alonso J.M., Ecker J.R., Zhang X., Gao S., Theologis A. A combinatorial interplay among the 1-aminocyclopropane- 1-carboxylate isoforms regulates ethylene biosynthesis in Arabidopsis thaliana. Genetics. 2009;183(3):979- 1003. DOI 10.1534/genetics.109.107102
70. Van de Poel B., Bulens I., Hertog M.L., Nicolai B.M., Geeraerd A.H. A transcriptomics-based kinetic model for ethylene biosynthesis in tomato (Solanum lycopersicum) fruit: development, validation and exploration of novel regulatory mechanisms. New Phytol. 2014; 202(3):952-963. DOI 10.1111/nph.12685
71. Van de Poel B., Bulens I., Markoula A., Hertog M.L.A.T.M., Dreesen R., Wirtz M., Vandoninck S., Oppermann Y., Keulemans J., Hell R., Waelkens E., De Proft M.P., Sauter M., Nicolai B.M., Geeraerd A.H. Targeted systems biology profiling of tomato fruit reveals coordination of the Yang Cycle and a distinct regulation of ethylene biosynthesis during postclimacteric ripening. Plant Physiol. 2012; 160(3):1498-1514. DOI 10.1104/pp.112.206086
72. Van de Poel B., Van Der Straeten D. 1-aminocyclopropane-1-carboxylic acid (ACC) in plants: more than just the precursor of ethylene! Front. Plant Sci. 2014;5:640. DOI 10.3389/fpls.2014.00640
73. Voß U., Bishopp A., Farcot E., Bennett M.J. Modelling hormonal response and development. Trends Plant Sci. 2014;19(5):311-319. DOI 10.1016/j.tplants.2014.02.004
74. Vogel J.P., Woeste K.E., Theologis A., Kieber J.J. Recessive and dominant mutations in the ethylene biosynthetic gene ACS5 of Arabidopsis confer cytokinin insensitivity and ethylene overproduction, respectively. Proc. Natl. Acad. Sci. USA. 1998;95(8):4766-4771.
75. Vrebalov J., Ruezinsky D., Padmanabhan V., White R., Medrano D., Drake R., Schuch W., Giovannoni J. A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science. 2002;296:343-346. DOI 10.1126/science.1068181
76. Wang K.L.-C., Yoshida H., Lurin C., Ecker J.R. Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein. Nature. 2004; 428(6986):945-950.
77. Xiong L., Xiao D., Xu X., Guo Z., Wang N.N. The non-catalytic Nterminal domain of ACS7 is involved in the post-translational regulation of this gene in Arabidopsis. J. Exp. Bot. 2014;65(15):4397-4408. DOI 10.1093/jxb/eru211
78. Yamagami T., Tsuchisaka A., Yamada K., Haddon W.F., Harden L.A., Theologis A. Biochemical diversity among the 1-amino-cyclopropane- 1-carboxylate synthase isozymes encoded by the Arabidopsis gene family. J. Biol. Chem. 2003;278(49):49102- 49112.
79. Yang S.F., Hoffman N.E. Ethylene biosynthesis and its regulation in higher-plants. Annu. Rev. Plant Physiol. Mol. Biol. 1984;35:155- 189. DOI 10.1146/annurev.pp.35.060184.001103
80. Zarei A., Korbes A.P., Younessi P., Montiel G., Champion A., Memelink J. Two GCC boxes and AP2/ERF-domain transcription factor ORA59 in jasmonate/ethylene-mediated activation of the PDF1.2 promoter in Arabidopsis. Plant Mol. Biol. 2011;75(4-5):321- 331. DOI 10.1007/s11103-010-9728-y
81. Zhang J., Yu J., Wen C.K. An alternate route of ethylene receptor signaling. Front. Plant Sci. 2014a;5:648. DOI 10.3389/fpls.2014.00648
82. Zhang X., Zhu Z., An F., Hao D., Li P., Song J., Yi C., Guo H. Jasmonate-activated MYC2 represses ETHYLENE INSENSITIVE3 activity to antagonize ethylene-promoted apical hook formation in Arabidopsis. Plant Cell. 2014b;26(3):1105-1117. DOI 10.1105/tpc.113.122002
83. Zhao Q., Guo H.W. Paradigms and paradox in the ethylene signaling pathway and interaction network. Mol. Plant. 2011;4(4):626-634. DOI 10.1093/mp/ssr042
84. Zhao R., Xie H., Lv S., Zheng Y., Yu M., Shen L., Sheng J. LeMAPK4 participated in cold-induced ethylene production in tomato fruit. J. Sci. Food Agric. 2013;93(5):1003-1009. DOI 10.1002/jsfa.5790
85. Zhu Z., An F., Feng Y., Li P., Xue L., Mu A., Jiang Z., Kim J.M., To T.K., Li W., Zhang X., Yu Q., Dong Z., Chen W.Q., Seki M., Zhou J.M., Guo H. Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc. Natl. Acad. Sci. USA. 2011;108(30):12539-12544. DOI 10.1073/pnas.1103959108
86. Zhu Z., Lee B. Friends or Foes: New insights in jasmonate and ethylene co-actions. Plant Cell Physiol. 2015;56(3):414-420.