Transcriptional Regulation of the Ethylene Response Factor LeERF2 in the Expression of Ethylene Biosynthesis Genes Controls Ethylene Production in Tomato and Tobacco

Overview

Journal Plant Physiol

Specialty Physiology

Date 2009 Mar 6

PMID 19261734

Citations 78

Authors

Zhijin Zhang

Haiwen Zhang

Ruidan Quan

Xue-Chen Wang

Rongfeng Huang

Affiliations

Soon will be listed here.

Abstract

Fine-tuning of ethylene production plays an important role in developmental processes and in plant responses to stress, but very little is known about the regulation of ethylene response factor (ERF) proteins in ethylene biosynthesis genes and ethylene production. Identifying cis-acting elements and transcription factors that play a role in this process, therefore, is important. Previously, a tomato (Solanum lycopersicum [f. sp. Lycopersicon esculentum]) ERF protein, LeERF2, an allele of TERF2, was reported to confer ethylene triple response on plants. This paper reports the transcriptional modulation of LeERF2/TERF2 in ethylene biosynthesis in tomato and tobacco (Nicotiana tabacum). Using overexpressing and antisense LeERF2/TERF2 transgenic tomato, we found that LeERF2/TERF2 is an important regulator in the expression of ethylene biosynthesis genes and the production of ethylene. Expression analysis revealed that LeERF2/TERF2 is ethylene inducible, and ethylene production stimulated by ethylene was suppressed in antisense LeERF2/TERF2 transgenic tomato, indicating LeERF2/TERF2 to be a positive regulator in the feedback loop of ethylene induction. Further research showed that LeERF2/TERF2 conservatively modulates ethylene biosynthesis in tobacco and that such regulation in tobacco is associated with the elongation of the hypocotyl and insensitivity to abscisic acid and glucose during germination and seedling development. The effects on ethylene synthesis were similar to those of another ERF protein, TERF1, because TERF1 and LeERF2/TERF2 have overlapping roles in the transcriptional regulation of ethylene biosynthesis in tobacco. Biochemical analysis showed that LeERF2/TERF2 interacted with GCC box in the promoter of NtACS3 and with dehydration-responsive element in the promoter of LeACO3, resulting in transcriptional activation of the genes for ethylene biosynthesis in tomato and tobacco, which is a novel regulatory function of ERF proteins in plant ethylene biosynthesis.

Citing Articles

The transcription factors ERF105 and NAC72 regulate expression of a sugar transporter gene and hexose accumulation in grape.

Lu L, Delrot S, Fan P, Zhang Z, Wu D, Dong F Plant Cell. 2024; 37(1).

PMID: 39691057 PMC: 11852290. DOI: 10.1093/plcell/koae326.

Transcription factor PbrERF114 is involved in the regulation of ethylene synthesis during pear fruit ripening.

Wang G, Guo Z, Wang T, Wang X, Qi K, Xuan J Mol Hortic. 2024; 4(1):38.

PMID: 39543765 PMC: 11566906. DOI: 10.1186/s43897-024-00114-2.

Ectopic expression of poplar gene in tobacco confers salt stress tolerance and growth advantages.

Liu L, Cheng Z, Yao W, Wang X, Jia F, Zhou B For Res (Fayettev). 2024; 1:13.

PMID: 39524516 PMC: 11524295. DOI: 10.48130/FR-2021-0013.

Auxin responsive factor MdARF17 promotes ethylene synthesis in apple fruits by activating MdERF003 expression.

Wang T, Zhang J, Zhang S, Gong Y, Wang N, Zhang Z Plant Cell Rep. 2024; 43(9):212.

PMID: 39127969 DOI: 10.1007/s00299-024-03293-w.

Cytokinins regulate spatially specific ethylene production to control root growth in Arabidopsis.

Yamoune A, Zdarska M, Depaepe T, Rudolfova A, Skalak J, Berendzen K Plant Commun. 2024; 5(11):101013.

PMID: 38961625 PMC: 11589326. DOI: 10.1016/j.xplc.2024.101013.

References

Tanaka Y, Sano T, Tamaoki M, Nakajima N, Kondo N, Hasezawa S . Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol. 2005; 138(4):2337-43. PMC: 1183419. DOI: 10.1104/pp.105.063503. View

Huang Z, Zhang Z, Zhang X, Zhang H, Huang D, Huang R . Tomato TERF1 modulates ethylene response and enhances osmotic stress tolerance by activating expression of downstream genes. FEBS Lett. 2004; 573(1-3):110-6. DOI: 10.1016/j.febslet.2004.07.064. View

Wu L, Zhang Z, Zhang H, Wang X, Huang R . Transcriptional modulation of ethylene response factor protein JERF3 in the oxidative stress response enhances tolerance of tobacco seedlings to salt, drought, and freezing. Plant Physiol. 2008; 148(4):1953-63. PMC: 2593663. DOI: 10.1104/pp.108.126813. View

McMurchie E, McGlasson W, Eaks I . Treatment of fruit with propylene gives information about the biogenesis of ethylene. Nature. 1972; 237(5352):235-6. DOI: 10.1038/237235a0. View

Hua J, Meyerowitz E . Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell. 1998; 94(2):261-71. DOI: 10.1016/s0092-8674(00)81425-7. View

Blume B, Grierson D . Expression of ACC oxidase promoter-GUS fusions in tomato and Nicotiana plumbaginifolia regulated by developmental and environmental stimuli. Plant J. 1998; 12(4):731-46. DOI: 10.1046/j.1365-313x.1997.12040731.x. View

Oeller P, Lu M, Taylor L, Pike D, Theologis A . Reversible inhibition of tomato fruit senescence by antisense RNA. Science. 1991; 254(5030):437-9. DOI: 10.1126/science.1925603. View

Allen M, Yamasaki K, Ohme-Takagi M, Tateno M, Suzuki M . A novel mode of DNA recognition by a beta-sheet revealed by the solution structure of the GCC-box binding domain in complex with DNA. EMBO J. 1998; 17(18):5484-96. PMC: 1170874. DOI: 10.1093/emboj/17.18.5484. View

Alexander L, Grierson D . Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. J Exp Bot. 2002; 53(377):2039-55. DOI: 10.1093/jxb/erf072. View

10.

Wu K, Tian L, Hollingworth J, Brown D, Miki B . Functional analysis of tomato Pti4 in Arabidopsis. Plant Physiol. 2002; 128(1):30-7. PMC: 148941. View

11.

Ghassemian M, Nambara E, Cutler S, Kawaide H, Kamiya Y, McCourt P . Regulation of abscisic acid signaling by the ethylene response pathway in Arabidopsis. Plant Cell. 2000; 12(7):1117-26. PMC: 149053. DOI: 10.1105/tpc.12.7.1117. View

12.

Zhou J, Tang X, Martin G . The Pto kinase conferring resistance to tomato bacterial speck disease interacts with proteins that bind a cis-element of pathogenesis-related genes. EMBO J. 1997; 16(11):3207-18. PMC: 1169938. DOI: 10.1093/emboj/16.11.3207. View

13.

Christians M, Gingerich D, Hansen M, Binder B, Kieber J, Vierstra R . The BTB ubiquitin ligases ETO1, EOL1 and EOL2 act collectively to regulate ethylene biosynthesis in Arabidopsis by controlling type-2 ACC synthase levels. Plant J. 2008; 57(2):332-45. PMC: 2807402. DOI: 10.1111/j.1365-313X.2008.03693.x. View

14.

Giovannoni J . MOLECULAR BIOLOGY OF FRUIT MATURATION AND RIPENING. Annu Rev Plant Physiol Plant Mol Biol. 2001; 52:725-749. DOI: 10.1146/annurev.arplant.52.1.725. View

15.

Wang K, Li H, Ecker J . Ethylene biosynthesis and signaling networks. Plant Cell. 2002; 14 Suppl:S131-51. PMC: 151252. DOI: 10.1105/tpc.001768. View

16.

Hahn A, Harter K . Mitogen-activated protein kinase cascades and ethylene: signaling, biosynthesis, or both?. Plant Physiol. 2008; 149(3):1207-10. PMC: 2649397. DOI: 10.1104/pp.108.132241. View

17.

Yu X, Griffith M, Wiseman S . Ethylene induces antifreeze activity in winter rye leaves. Plant Physiol. 2001; 126(3):1232-40. PMC: 116479. DOI: 10.1104/pp.126.3.1232. View

18.

Zhang X, Zhang Z, Chen J, Chen Q, Wang X, Huang R . Expressing TERF1 in tobacco enhances drought tolerance and abscisic acid sensitivity during seedling development. Planta. 2005; 222(3):494-501. DOI: 10.1007/s00425-005-1564-y. View

19.

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. PMC: 523360. DOI: 10.1104/pp.104.049999. View

20.

Joo S, Liu Y, Lueth A, Zhang S . MAPK phosphorylation-induced stabilization of ACS6 protein is mediated by the non-catalytic C-terminal domain, which also contains the cis-determinant for rapid degradation by the 26S proteasome pathway. Plant J. 2008; 54(1):129-40. DOI: 10.1111/j.1365-313X.2008.03404.x. View