Transcription Factor FUS3 Counteracts ETR1 Overexpression-induced Salt Tolerance in Plant Cells

Authors

  • Wei Tang College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei 434025, China and Program of Cell and Molecular Biology, Duke University, 101 Science Drive, Durham, NC 27708, USA
  • Yongjun Fei College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei 434025, China
  • Bo Xiao College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei 434025, China
  • Mingqin Zhou College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei 434025, China
  • Xiaodong Cai College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei 434025, China
  • Yujie Yang College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei 434025, China
  • Zhen Yao College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei 434025, China
  • Die Hu College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei 434025, China
  • Hongna Mu College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei 434025, China
  • Jinwang Qu College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei 434025, China

DOI:

https://doi.org/10.12974/2311-858X.2018.06.01.6

Keywords:

Agrobacterium-mediated genetic transformation, Defense response genes, The ethylene receptor 1, Lipid peroxidation, NaCl stress, Pinus.

Abstract

The ethylene receptor 1 (ETR1) of Arabidopsis (Arabidopsis thaliana L.) plays critical roles in modulating expression of defense response genes during the developmental processes of plants. To examine the function of the ETR1 gene in NaCl stress tolerance, cell lines of A. thaliana, white pine (Pinus strobes L.), and rice (Oryza sativa L.) overexpressing ETR1 were generated using Agrobacterium-mediated genetic transformation. Physiological analysis of transgenic cell lines showed that overexpression of ETR1 increased cell viability and growth rate and decreased the level of thiobarbituric acid reactive substance (TBARS). Biochemical analysis of transgenic cell lines demonstrated that overexpression of ETR1 enhanced tolerance to NaCl stress by regulating expression of a set of defense response genes including of CTR1, EIN2, MPK11, EIN3, ERF1, BREB2A, NAC6, PDF1.2, WRKY13, bZIP23, ABI5, and LEA3. In rice cells, overexpression of FUS3 counteracts ETR1 enhanced expression of defense response genes under NaCl stress, and overexpression of SCFTIR1 reduces ETR1 enhanced expression of defense response genes under NaCl stress. Altogether, our results suggest that overexpression of ETR1 enhanced NaCl stress tolerance of transgenic plant cells by decreasing lipid peroxidation and by regulating expression of defense response genes. 

References

Bleecker AB, Kende H. Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 2000; 16: 1-18. https://doi.org/10.1146/annurev.cellbio.16.1.1

Guo H, Ecker JR. Plant responses to ethylene gas are mediated by SCF(EBF1/EBF2)-dependent proteolysis of EIN3 transcription factor. Cell 2003; 115: 667-677. https://doi.org/10.1016/S0092-8674(03)00969-3

Chao Q, Rothenberg M, Solano R, Roman G, Terzaghi W, et al. Activation of the ethylene gas response pathway in Arabidopsis by the nuclear protein ETHYLENEINSENSITIVE3 and related proteins. Cell 1997; 89: 1133- 1144. https://doi.org/10.1016/S0092-8674(00)80300-1

Hua J, Meyerowitz EM. Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell 1998; 94: 261-271. https://doi.org/10.1016/S0092-8674(00)81425-7

Stepanova AN, Ecker JR. Ethylene signaling: from mutants to molecules. Curr Opin Plant Biol 2000; 3: 353-360. https://doi.org/10.1016/S1369-5266(00)00096-0

Lewis DR, Negi S, Sukumar P, Muday GK. Ethylene inhibits lateral root development, increases IAA transport and expression of PIN3 and PIN7 auxin efflux carriers. Development 2011; 138: 3485-3495. https://doi.org/10.1242/dev.065102

Roman G, Lubarsky B, Kieber JJ, Rothenberg M, Ecker JR. Genetic analysis of ethylene signal transduction in Arabidopsis thaliana: five novel mutant loci integrated into a stress response pathway. Genetics 1995; 139: 1393-1409.

Clark KL, Larsen PB, Wang X, Chang C. Association of the Arabidopsis CTR1 Raf-like kinase with the ETR1 and ERS ethylene receptors. Proc Natl Acad Sci U S A 1998; 95: 5401-5406. https://doi.org/10.1073/pnas.95.9.5401

Gamble RL, Coonfield ML, Schaller GE. Histidine kinase activity of the ETR1 ethylene receptor from Arabidopsis. Proc Natl Acad Sci U S A 1998; 95: 7825-7829. https://doi.org/10.1073/pnas.95.13.7825

Zhou L, Jang JC, Jones TL, Sheen J. Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucose-insensitive mutant. Proc Natl Acad Sci U S A 1998; 95: 10294-10299. https://doi.org/10.1073/pnas.95.17.10294

Schmidt JS, Harper JE, Hoffman TK, Bent AF. Regulation of soybean nodulation independent of ethylene signaling. Plant Physiol 1999; 119: 951-960. https://doi.org/10.1104/pp.119.3.951

Beaudoin N, Serizet C, Gosti F, Giraudat J. Interactions between abscisic acid and ethylene signaling cascades. Plant Cell 2000; 12: 1103-1115. https://doi.org/10.1105/tpc.12.7.1103

Urao T, Yamaguchi-Shinozaki K, Shinozaki K. Twocomponent systems in plant signal transduction. Trends Plant Sci 2000; 5: 67-74. https://doi.org/10.1016/S1360-1385(99)01542-3

Gamble RL, Qu X, Schaller GE. Mutational analysis of the ethylene receptor ETR1. Role of the histidine kinase domain in dominant ethylene insensitivity. Plant Physiol 2002; 128: 1428-1438. https://doi.org/10.1104/pp.010777

Hung YL, Jiang I, Lee YZ, Wen CK, Sue SC. NMR Study Reveals the Receiver Domain of Arabidopsis ETHYLENE RESPONSE1 Ethylene Receptor as an Atypical Type Response Regulator. PLoS One 2016; 11: e0160598. https://doi.org/10.1371/journal.pone.0160598

Zhang W, Lu LY, Hu LY, Cao W, Sun K, et al. Evidences for the Involvement of Auxin, Ethylene and ROS Signaling during Allelochemical Benzoic Acid-Mediated Primary Root Inhibition of Arabidopsis. Plant Cell Physiol 2018.

Pekarova B, Klumpler T, Triskova O, Horak J, Jansen S, et al. Structure and binding specificity of the receiver domain of sensor histidine kinase CKI1 from Arabidopsis thaliana. Plant J 2011; 67: 827-839. https://doi.org/10.1111/j.1365-313X.2011.04637.x

Hall BP, Shakeel SN, Amir M, Ul Haq N, Qu X, et al. Histidine kinase activity of the ethylene receptor ETR1 facilitates the ethylene response in Arabidopsis. Plant Physiol 2012; 159: 682-695. https://doi.org/10.1104/pp.112.196790

Deslauriers SD, Alvarez AA, Lacey RF, Binder BM, Larsen PB. Dominant gain-of-function mutations in transmembrane domain III of ERS1 and ETR1 suggest a novel role for this domain in regulating the magnitude of ethylene response in Arabidopsis. New Phytol 2015; 208: 442-455. https://doi.org/10.1111/nph.13466

Mayerhofer H, Panneerselvam S, Kaljunen H, Tuukkanen A, Mertens HD, et al. Structural model of the cytosolic domain of the plant ethylene receptor 1 (ETR1). J Biol Chem 2015; 290: 2644-2658. https://doi.org/10.1074/jbc.M114.587667

Wu JX, Wu JL, Yin J, Zheng P, Yao N. Ethylene Modulates Sphingolipid Synthesis in Arabidopsis. Front Plant Sci 2015; 6: 1122.

Piya S, Binder BM, Hewezi T. Canonical and noncanonical ethylene signaling pathways that regulate Arabidopsis susceptibility to the cyst nematode Heterodera schachtii. New Phytol 2018.

Iqbal N, Trivellini A, Masood A, Ferrante A, Khan NA. Current understanding on ethylene signaling in plants: the influence of nutrient availability. Plant Physiol Biochem 2013; 73: 128- 138. https://doi.org/10.1016/j.plaphy.2013.09.011

Wang F, Cui X, Sun Y, Dong CH. Ethylene signaling and regulation in plant growth and stress responses. Plant Cell Rep 2013; 32: 1099-1109. https://doi.org/10.1007/s00299-013-1421-6

Wilson RL, Kim H, Bakshi A, Binder BM. The Ethylene Receptors ETHYLENE RESPONSE1 and ETHYLENE RESPONSE2 Have Contrasting Roles in Seed Germination of Arabidopsis during Salt Stress. Plant Physiol 2014; 165: 1353-1366. https://doi.org/10.1104/pp.114.241695

Ma Q, Du W, Brandizzi F, Giovannoni JJ, Barry CS. Differential control of ethylene responses by GREEN-RIPE and GREEN-RIPE LIKE1 provides evidence for distinct ethylene signaling modules in tomato. Plant Physiol 2012; 160: 1968-1984. https://doi.org/10.1104/pp.112.205476

Jeong SW, Das PK, Jeoung SC, Song JY, Lee HK, et al. Ethylene suppression of sugar-induced anthocyanin pigmentation in Arabidopsis. Plant Physiol 2010; 154: 1514- 1531. https://doi.org/10.1104/pp.110.161869

Mersmann S, Bourdais G, Rietz S, Robatzek S. Ethylene signaling regulates accumulation of the FLS2 receptor and is required for the oxidative burst contributing to plant immunity. Plant Physiol 2010; 154: 391-400. https://doi.org/10.1104/pp.110.154567

Zhang ZG, Zhou HL, Chen T, Gong Y, Cao WH, et al. Evidence for serine/threonine and histidine kinase activity in the tobacco ethylene receptor protein NTHK2. Plant Physiol 2004; 136: 2971-2981. https://doi.org/10.1104/pp.103.034686

Zhao XC, Schaller GE. Effect of salt and osmotic stress upon expression of the ethylene receptor ETR1 in Arabidopsis thaliana. FEBS Lett 2004; 562: 189-192. https://doi.org/10.1016/S0014-5793(04)00238-8

Chotikacharoensuk T, Arteca RN, Arteca JM. Use of differential display for the identification of touch-induced genes from an ethylene-insensitive Arabidopsis mutant and partial characterization of these genes. J Plant Physiol 2006; 163: 1305-1320. https://doi.org/10.1016/j.jplph.2005.12.005

Bueso E, Alejandro S, Carbonell P, Perez-Amador MA, Fayos J, et al. The lithium tolerance of the Arabidopsis cat2 mutant reveals a cross-talk between oxidative stress and ethylene. Plant J 2007; 52: 1052-1065. https://doi.org/10.1111/j.1365-313X.2007.03305.x

Wang H, Liang X, Wan Q, Wang X, Bi Y. Ethylene and nitric oxide are involved in maintaining ion homeostasis in Arabidopsis callus under salt stress. Planta 2009; 230: 293- 307. https://doi.org/10.1007/s00425-009-0946-y

Wang H, Liang X, Huang J, Zhang D, Lu H, et al. Involvement of ethylene and hydrogen peroxide in induction of alternative respiratory pathway in salt-treated Arabidopsis calluses. Plant Cell Physiol 2010; 51: 1754-1765. https://doi.org/10.1093/pcp/pcq134

Li J, Jia H, Wang J. cGMP and ethylene are involved in maintaining ion homeostasis under salt stress in Arabidopsis roots. Plant Cell Rep 2014; 33: 447-459. https://doi.org/10.1007/s00299-013-1545-8

Liu S, Hao H, Lu X, Zhao X, Wang Y, et al. Transcriptome profiling of genes involved in induced systemic salt tolerance conferred by Bacillus amyloliquefaciens FZB42 in Arabidopsis thaliana. Sci Rep 2017; 7: 10795. https://doi.org/10.1038/s41598-017-11308-8

Bakshi A, Piya S, Fernandez JC, Chervin C, Hewezi T, et al. Ethylene Receptors Signal via a Noncanonical Pathway to Regulate Abscisic Acid Responses. Plant Physiol 2018; 176: 910-929. https://doi.org/10.1104/pp.17.01321

Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, et al. Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol 2005; 138: 2337-2343. https://doi.org/10.1104/pp.105.063503

Testerink C, Larsen PB, van der Does D, van Himbergen JA, Munnik T. Phosphatidic acid binds to and inhibits the activity of Arabidopsis CTR1. J Exp Bot 2007; 58: 3905-3914. https://doi.org/10.1093/jxb/erm243

Sos-Hegedus A, Juhasz Z, Poor P, Kondrak M, Antal F, et al. Soil drench treatment with ss-aminobutyric acid increases drought tolerance of potato. PLoS One 2014; 9: e114297.

Li C, Li C, Wang B, Zhang R, Fu K, et al. Programmed cell death in wheat (Triticum aestivum L.) endosperm cells is affected by drought stress. Protoplasma 2018; 255: 1039- 1052. https://doi.org/10.1007/s00709-018-1203-7

El-Sharkawy I, Jones B, Li ZG, Lelievre JM, Pech JC, et al. Isolation and characterization of four ethylene perception elements and their expression during ripening in pears (Pyrus communis L) with/without cold requirement. J Exp Bot 2003; 54: 1615-1625. https://doi.org/10.1093/jxb/erg158

Shi Y, Tian S, Hou L, Huang X, Zhang X, et al. Ethylene signaling negatively regulates freezing tolerance by repressing expression of CBF and type-A ARR genes in Arabidopsis. Plant Cell 2012; 24: 2578-2595. https://doi.org/10.1105/tpc.112.098640

Wang H, Huang J, Liang X, Bi Y. Involvement of hydrogen peroxide, calcium, and ethylene in the induction of the alternative pathway in chilling-stressed Arabidopsis callus. Planta 2012; 235: 53-67. https://doi.org/10.1007/s00425-011-1488-7

Zou Y, Zhang L, Rao S, Zhu X, Ye L, et al. The relationship between the expression of ethylene-related genes and papaya fruit ripening disorder caused by chilling injury. PLoS One 2014; 9: e116002.

Hao X, Yang Y, Yue C, Wang L, Horvath DP, et al. Comprehensive Transcriptome Analyses Reveal Differential Gene Expression Profiles of Camellia sinensis Axillary Buds at Para-, Endo-, Ecodormancy, and Bud Flush Stages. Front Plant Sci 2017; 8: 553.

Tang W, Page M. Transcription factor AtbZIP60 regulates expression of Ca2+ -dependent protein kinase genes in transgenic cells. Mol Biol Rep 2013; 40: 2723-2732. https://doi.org/10.1007/s11033-012-2362-9

Tang W, Newton RJ, Weidner DA. Genetic transformation and gene silencing mediated by multiple copies of a transgene in eastern white pine. J Exp Bot 2007; 58: 545- 554. https://doi.org/10.1093/jxb/erl228

Tang W, Newton RJ, Li C, Charles TM. Enhanced stress tolerance in transgenic pine expressing the pepper CaPF1 gene is associated with the polyamine biosynthesis. Plant Cell Rep 2007; 26: 115-124. https://doi.org/10.1007/s00299-006-0228-0

Tang W, Newton RJ, Lin J, Charles TM. Expression of a transcription factor from Capsicum annuum in pine calli counteracts the inhibitory effects of salt stress on adventitious shoot formation. Mol Genet Genomics 2006; 276: 242-253. https://doi.org/10.1007/s00438-006-0137-5

Fei Y, Xiao B, Yang M, Ding Q, Tang W. MicroRNAs, polyamines, and the activities antioxidant enzymes are associated with in vitro rooting in white pine (Pinus strobus L.). Springerplus 2016; 5: 416. https://doi.org/10.1186/s40064-016-2080-1

Chang C, Meyerowitz EM. The ethylene hormone response in Arabidopsis: a eukaryotic two-component signaling system. Proc Natl Acad Sci U S A 1995; 92: 4129-4133. https://doi.org/10.1073/pnas.92.10.4129

Imamura A, Hanaki N, Umeda H, Nakamura A, Suzuki T, et al. Response regulators implicated in His-to-Asp phosphotransfer signaling in Arabidopsis. Proc Natl Acad Sci U S A 1998; 95: 2691-2696. https://doi.org/10.1073/pnas.95.5.2691

Sakai H, Hua J, Chen QG, Chang C, Medrano LJ, et al. ETR2 is an ETR1-like gene involved in ethylene signaling in Arabidopsis. Proc Natl Acad Sci U S A 1998; 95: 5812-5817. https://doi.org/10.1073/pnas.95.10.5812

Suzuki T, Imamura A, Ueguchi C, Mizuno T. Histidinecontaining phosphotransfer (HPt) signal transducers implicated in His-to-Asp phosphorelay in Arabidopsis. Plant Cell Physiol 1998; 39: 1258-1268. https://doi.org/10.1093/oxfordjournals.pcp.a029329

Cancel JD, Larsen PB. Loss-of-function mutations in the ethylene receptor ETR1 cause enhanced sensitivity and exaggerated response to ethylene in Arabidopsis. Plant Physiol 2002; 129: 1557-1567. https://doi.org/10.1104/pp.003780

Parcy F, Valon C, Kohara A, Misera S, Giraudat J. The ABSCISIC ACID-INSENSITIVE3, FUSCA3, and LEAFY COTYLEDON1 loci act in concert to control multiple aspects of Arabidopsis seed development. Plant Cell 1997; 9: 1265- 1277. https://doi.org/10.1105/tpc.9.8.1265

Nambara E, Hayama R, Tsuchiya Y, Nishimura M, Kawaide H, et al. The role of ABI3 and FUS3 loci in Arabidopsis thaliana on phase transition from late embryo development to germination. Dev Biol 2000; 220: 412-423. https://doi.org/10.1006/dbio.2000.9632

Baumbusch LO, Hughes DW, Galau GA, Jakobsen KS. LEC1, FUS3, ABI3 and Em expression reveals no correlation with dormancy in Arabidopsis. J Exp Bot 2004; 55: 77-87. https://doi.org/10.1093/jxb/erh014

Tsuchiya Y, Nambara E, Naito S, McCourt P. The FUS3 transcription factor functions through the epidermal regulator TTG1 during embryogenesis in Arabidopsis. Plant J 2004; 37: 73-81. https://doi.org/10.1046/j.1365-313X.2003.01939.x

D WKN, Hall TC. PvALF and FUS3 activate expression from the phaseolin promoter by different mechanisms. Plant Mol Biol 2008; 66: 233-244. https://doi.org/10.1007/s11103-007-9265-5

Lu QS, Paz JD, Pathmanathan A, Chiu RS, Tsai AY, et al. The C-terminal domain of FUSCA3 negatively regulates mRNA and protein levels, and mediates sensitivity to the hormones abscisic acid and gibberellic acid in Arabidopsis. Plant J 2010; 64: 100-113.

Tsai AY, Gazzarrini S. AKIN10 and FUSCA3 interact to control lateral organ development and phase transitions in Arabidopsis. Plant J 2012; 69: 809-821. https://doi.org/10.1111/j.1365-313X.2011.04832.x

Wang F, Perry SE. Identification of direct targets of FUSCA3, a key regulator of Arabidopsis seed development. Plant Physiol 2013; 161: 1251-1264. https://doi.org/10.1104/pp.112.212282

Zhang M, Cao X, Jia Q, Ohlrogge J. FUSCA3 activates triacylglycerol accumulation in Arabidopsis seedlings and tobacco BY2 cells. Plant J 2016; 88: 95-107. https://doi.org/10.1111/tpj.13233

Duong S, Vonapartis E, Li CY, Patel S, Gazzarrini S. The E3 ligase ABI3-INTERACTING PROTEIN2 negatively regulates FUSCA3 and plays a role in cotyledon development in Arabidopsis thaliana. J Exp Bot 2017; 68: 1555-1567. https://doi.org/10.1093/jxb/erx046

Van der Does D, Leon-Reyes A, Koornneef A, Van Verk MC, Rodenburg N, et al. Salicylic acid suppresses jasmonic acid signaling downstream of SCFCOI1-JAZ by targeting GCC promoter motifs via transcription factor ORA59. Plant Cell 2013; 25: 744-761. https://doi.org/10.1105/tpc.112.108548

Downloads

Published

03-05-2018

How to Cite

Tang, W., Fei, Y., Xiao, B., Zhou, M., Cai, X., Yang, Y., Yao, Z., Hu, D., Mu, H., & Qu, J. (2018). Transcription Factor FUS3 Counteracts ETR1 Overexpression-induced Salt Tolerance in Plant Cells. Global Journal Of Botanical Science, 6, 46–59. https://doi.org/10.12974/2311-858X.2018.06.01.6

Issue

Vol. 6 (2018)

Section

Articles

License

Copyright (c) 2018 Wei Tang, Yongjun Fei, Bo Xiao, Mingqin Zhou, Xiaodong Cai, Yujie Yang, Zhen Yao, Die Hu, Hongna Mu, Jinwang Qu

Creative Commons License

This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.