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The AP2/ERF transcription factor SlERF.F5 functions in leaf senescence in tomato

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Our results confirmed that SlERF.F5 can directly regulate the promoter activity of ACS6 and interact with SlMYC2 to regulate tomato leaf senescence.

The process of plant senescence is complex and highly coordinated, and is regulated by many endogenous and environmental signals. Ethylene and jasmonic acid are well-known senescence inducers, but their molecular mechanisms for inducing leaf senescence have not been fully elucidated. Here, we isolated an ETHYLENE RESPONSE FACTOR F5 (SlERF.F5) from tomato. Silencing of SlERF.F5 causes accelerated senescence induced by age, darkness, ethylene, and jasmonic acid. However, overexpression of SlERF.F5 would not promote senescence. Moreover, SlERF.F5 can regulate the promoter activity of ACS6 in vitro and in vivo. Suppression of SlERF.F5 resulted in increased sensitivity to ethylene and jasmonic acid, decreased accumulation of chlorophyll content, and inhibited the expression of chlorophyll- and light response-related genes. Compared with the wild type, the qRT-PCR analysis showed the expression levels of genes related to the ethylene biosynthesis pathway and the jasmonic acid signaling pathway in SlERF.F5-RNAi lines increased. Yeast two-hybrid experiments showed that SlERF.F5 and SlMYC2 (a transcription factor downstream of the JA receptor) can interact physically, thereby mediating the role of SlERF.F5 in jasmonic acid-induced leaf senescence. Collectively, our research provides new insights into how ethylene and jasmonic acid promote leaf senescence in tomato.

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References

  • Abeles FB, Dunn LJ, Morgens P, Callahan A, Dinterman RE, Schmidt J (1988) Induction of 33-Kd and 60-Kd peroxidases during ethylene-induced senescence of cucumber cotyledons. Plant Physiol 87(3):609–615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bresson J, Bieker S, Riester L, Doll J, Zentgraf U (2018) A guideline for leaf senescence analyses: from quantification to physiological and molecular investigations. J Exp Bot 69(4):769–786

    Article  CAS  PubMed  Google Scholar 

  • Chen G, Hu Z, Grierson D (2008) Differential regulation of tomato ethylene responsive factor LeERF3b, a putative repressor, and the activator Pti4 in ripening mutants and in response to environmental stresses. J Plant Physiol 165(6):662–670

    Article  CAS  PubMed  Google Scholar 

  • Gan SS, Amasino RM (1997) Making sense of senescence - molecular genetic regulation and manipulation of leaf senescence. Plant Physiol 113(2):313–319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He YH, Fukushige H, Hildebrand DF, Gan SS (2002) Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiol 128(3):876–884

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang YJ, Liang G, Yang SZ, Yu DQ (2014) Arabidopsis WRKY57 functions as a node of convergence for jasmonic acid- and auxin-mediated signaling in jasmonic acid-induced leaf senescence. Plant Cell 26(1):230–245

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jibran R, Hunter DA, Dijkwel PP (2013) Hormonal regulation of leaf senescence through integration of developmental and stress signals. Plant Mol Biol 82(6):547–561

    Article  CAS  PubMed  Google Scholar 

  • Johnson PR, Ecker JR (1998) The ethylene gas signal transduction pathway: a molecular perspective. Annu Rev Genet 32:227–254

    Article  CAS  PubMed  Google Scholar 

  • Jung C, Lyou SH, Yeu S, Kim MA, Rhee S, Kim M, Lee JS, Do Choi Y, Cheong JJ (2007) Microarray-based screening of jasmonate-responsive genes in Arabidopsis thaliana. Plant Cell Rep 26(7):1053–1063

    Article  CAS  PubMed  Google Scholar 

  • Kim J, Park SJ, Lee IH, Chu H, Penfold CA, Kim JH, Buchanan-Wollaston V, Nam HG, Woo HR, Lim PO (2018) Comparative transcriptome analysis in Arabidopsis ein2/ore3 and ahk3/ore12 mutants during dark-induced leaf senescence. J Exp Bot 69(12):3023–3036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee JM, Joung JG, McQuinn R, Chung MY, Fei Z, Tieman D, Klee H, Giovannoni J (2012) Combined transcriptome, genetic diversity and metabolite profiling in tomato fruit reveals that the ethylene response factor SlERF6 plays an important role in ripening and carotenoid accumulation. Plant J 70(2):191–204

    Article  CAS  PubMed  Google Scholar 

  • Li HJ, Guo HW (2007) Molecular basis of the ethylene signaling and response pathway in Arabidopsis. J Plant Growth Regul 26(2):106–117

    Article  CAS  Google Scholar 

  • Li L, Zhu B, Yang P, Fu D, Zhu Y, Luo Y (2011a) The regulation mode of RIN transcription factor involved in ethylene biosynthesis in tomato fruit. J Sci Food Agric 91(10):1822–1828

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Zhang L, Yu Y, Quan R, Zhang Z, Zhang H, Huang R (2011b) The ethylene response factor AtERF11 that is transcriptionally modulated by the bZIP transcription factor HY5 is a crucial repressor for ethylene biosynthesis in Arabidopsis. Plant J 68(1):88–99

    Article  CAS  PubMed  Google Scholar 

  • Li ZH, Peng JY, Wen X, Guo HW (2013) ETHYLENE-INSENSITIVE3 Is a senescence-associated gene that accelerates age-dependent leaf senescence by directly repressing miR164 transcription in Arabidopsis. Plant Cell 25(9):3311–3328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li ZJ, Tian YS, Xu J, Fu XY, Gao JJ, Wang B, Han HJ, Wang LJ, Peng RH, Yao QH (2018) A tomato ERF transcription factor, SlERF84, confers enhanced tolerance to drought and salt stress but negatively regulates immunity against pseudomonas syringae pv. tomato DC3000. Plant Physiol Bioch 132:683–695

    Article  CAS  Google Scholar 

  • Lim PO, Nam HG (2005) The molecular and genetic control of leaf senescence and longevity in Arabidopsis. Curr Top Dev Biol 67:49–83

    Article  CAS  PubMed  Google Scholar 

  • Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136

    Article  CAS  PubMed  Google Scholar 

  • Liu M, Diretto G, Pirrello J, Roustan JP, Li Z, Giuliano G, Regad F, Bouzayen M (2014) The chimeric repressor version of an ethylene response factor (ERF) family member, Sl-ERF.B3, shows contrasting effects on tomato fruit ripening. New Phytol 203(1):206–218

    Article  CAS  PubMed  Google Scholar 

  • Liu MC, Gomes BL, Mila I, Purgatto E, Peres LEP, Frasse P, Maza E, Zouine M, Roustan JP, Bouzayen M, Pirrello J (2016) Comprehensive profiling of ethylene response factor expression identifies ripening-associated ERF genes and their link to key regulators of fruit ripening in tomato. Plant Physiol 170(3):1732–1744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu W, Li QW, Wang Y, Wu T, Yang YF, Zhang XZ, Han ZH, Xu XF (2017) Ethylene response factor AtERF72 negatively regulates Arabidopsis thaliana response to iron deficiency. Biochem Bioph Res Co 491(3):862–868

    Article  CAS  Google Scholar 

  • Ma X, Zhang Y, Tureckova V, Xue GP, Fernie AR, Mueller-Roeber B, Balazadeh S (2018) The NAC transcription factor SlNAP2 regulates leaf senescence and fruit yield in tomato. Plant Physiol 177(3):1286–1302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140(2):411–432

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakano T, Fujisawa M, Shima Y, Ito Y (2014) The AP2/ERF transcription factor SlERF52 functions in flower pedicel abscission in tomato. J Exp Bot 65(12):3111–3119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nicot N, Hausman JF, Hoffmann L, Evers D (2005) Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. J Exp Bot 56(421):2907–2914

    Article  CAS  PubMed  Google Scholar 

  • Niu YH, Guo FQ (2012) Nitric oxide regulates dark-induced leaf senescence through EIN2 in arabidopsis. J Integr Plant Biol 54(8):516–525

    Article  CAS  PubMed  Google Scholar 

  • Ohmetakagi M, Shinshi H (1990) Structure and expression of a tobacco beta-1,3-glucanase gene. Plant Mol Biol 15(6):941–946

    Article  CAS  Google Scholar 

  • Ohmetakagi M, Shinshi H (1995) Ethylene-inducible DNA-binding proteins that interact with an ethylene-responsive element. Plant Cell 7(2):173–182

    CAS  Google Scholar 

  • Ouyang Z, Liu S, Huang L, Hong Y, Li X, Huang L, Zhang Y, Zhang H, Li D, Song F (2016) Tomato SlERF.A1, SlERF.B4, SlERF.C3 and SlERF.A3, members of B3 group of ERF Family, are required for resistance to botrytis cinerea. Front Plant Sci 7:1964

    PubMed  PubMed Central  Google Scholar 

  • Pan Y, Seymour GB, Lu C, Hu Z, Chen X, Chen G (2012) An ethylene response factor (ERF5) promoting adaptation to drought and salt tolerance in tomato. Plant Cell Rep 31(2):349–360

    Article  CAS  PubMed  Google Scholar 

  • Qiu K, Li Z, Yang Z, Chen J, Wu S, Zhu X, Gao S, Gao J, Ren G, Kuai B, Zhou X (2015) EIN3 and ORE1 accelerate degreening during ethylene-mediated leaf senescence by directly activating chlorophyll catabolic genes in Arabidopsis. PLoS Genet 11(7):e1005399

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sakuma Y, Liu Q, Dubouzet JG, Abe H, Shinozaki K, Yamaguchi-Shinozaki K (2002) DNA-binding specificity of the ERF/AP2 domain of Arabidopsis DREBs, transcription factors involved in dehydration- and cold-inducible gene expression. Biochem Bioph Res Co 290(3):998–1009

    Article  CAS  Google Scholar 

  • Sanjaya HPY, Su RC, Ko SS, Tong CG, Yang RY, Chan MT (2008) Overexpression of Arabidopsis thaliana tryptophan synthase beta 1 (AtTSB1) in Arabidopsis and tomato confers tolerance to cadmium stress. Plant Cell Environ 31(8):1074–1085

    Article  CAS  PubMed  Google Scholar 

  • Shan X, Wang J, Chua L, Jiang D, Peng W, Xie D (2011) The role of Arabidopsis Rubisco activase in jasmonate-induced leaf senescence. Plant Physiol 155(2):751–764

    Article  CAS  PubMed  Google Scholar 

  • Song SS, Huang H, Wang JJ, Liu B, Qi TC, Xie DX (2017) MYC5 is Involved in jasmonate-regulated plant growth, leaf senescence and defense responses. Plant and Cell Physiol 58(10):1752–1763

    Article  CAS  Google Scholar 

  • Trujillo LE, Sotolongo M, Menendez C, Ochogavia ME, Coll Y, Hernandez I, Borras-Hidalgo O, Thomma BPHJ, Vera P, Hernandez L (2008) SodERF3, a novel sugarcane ethylene responsive factor (ERF), enhances salt and drought tolerance when overexpressed in tobacco plants. Plant Cell Physiol 49(4):512–525

    Article  CAS  PubMed  Google Scholar 

  • Upadhyay RK, Soni DK, Singh R, Dwivedi UN, Pathre UV, Nath P, Sane AP (2013) SlERF36, an EAR-motif-containing ERF gene from tomato, alters stomatal density and modulates photosynthesis and growth. J Exp Bot 64(11):3237–3247

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wellburn AR (1994) The spectral determination of chlorophyll-a and chlorophhyll-B, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144(3):307–313

    Article  CAS  Google Scholar 

  • Woo HR, Kim HJ, Nam HG, Lim PO (2013) Plant leaf senescence and death - regulation by multiple layers of control and implications for aging in general. J Cell Sci 126(21):4823–4833

    CAS  PubMed  Google Scholar 

  • Xie Q, Hu Z, Zhu Z, Dong T, Zhao Z, Cui B, Chen G (2014) Overexpression of a novel MADS-box gene SlFYFL delays senescence, fruit ripening and abscission in tomato. Sci Rep 4:4367

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yang Z, Tian LN, Latoszek-Green M, Brown D, Wu KQ (2005) Arabidopsis ERF4 is a transcriptional repressor capable of modulating ethylene and abscisic acid responses. Plant Mol Biol 58(4):585–596

    Article  CAS  PubMed  Google Scholar 

  • Yu J, Zhang Y, Di C, Zhang Q, Zhang K, Wang C, You Q, Yan H, Dai SY, Yuan JS, Xu W, Su Z (2016) JAZ7 negatively regulates dark-induced leaf senescence in Arabidopsis. J Exp Bot 67(3):751–762

    Article  CAS  PubMed  Google Scholar 

  • Zhang ZJ, Huang RF (2010) Enhanced tolerance to freezing in tobacco and tomato overexpressing transcription factor TERF2/LeERF2 is modulated by ethylene biosynthesis. Plant Mol Biol 73(3):241–249

    Article  CAS  PubMed  Google Scholar 

  • Zhang L, Tian LH, Zhao JF, Song Y, Zhang CJ, Guo Y (2009) Identification of an Apoplastic protein involved in the initial phase of salt stress response in rice root by two-dimensional electrophoresis. Plant Physiol 149(2):916–928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao L, Xia Y, Wu XY, Schippers JHM, Jing HC (2018) Phenotypic analysis and molecular markers of leaf senescence. Methods Mol Biol 1744:35–48

    Article  CAS  PubMed  Google Scholar 

  • Zhou S, Cheng X, Li F, Feng P, Hu G, Chen G, Xie Q, Hu Z (2019) Overexpression of SlOFP20 in tomato affects plant growth, chlorophyll accumulation, and leaf senescence. Front Plant Sci 10:1510

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu ZQ, An FY, Feng Y, Li PP, Xue L, Mu A, Jiang ZQ, Kim JM, To TK, Li W, Zhang XY, Yu Q, Dong Z, Chen WQ, Seki M, Zhou JM, Guo HW (2011) Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc Natl Acad Sci U S A 108(30):12539–12544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu X, Chen J, Xie Z, Gao J, Ren G, Gao S, Zhou X, Kuai B (2015) Jasmonic acid promotes degreening via MYC2/3/4- and ANAC019/055/072-mediated regulation of major chlorophyll catabolic genes. Plant J 84(3):597–610

    Article  CAS  PubMed  Google Scholar 

  • Zhuo M, Sakuraba Y, Yanagisawa S (2020) A jasmonate-activated MYC2-Dof2.1-MYC2 transcriptional loop promotes leaf senescence in Arabidopsis. Plant Cell 32(1):242–262

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by the Natural Science Foundation of Chongqing of China (csts2019jcyj-msxmX0094), and the National Natural Science Foundation of China (31872121), and the Innovation project of people returned from studying abroad of Chongqing (cx2019158).

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Authors and Affiliations

  1. Laboratory of Molecular Biology of Tomato, Bioengineering College, Chongqing University, Campus B, 174 Shapingba Main Street, Chongqing, 400030, People’s Republic of China

    Yanan Chen, Panpan Feng, Boyan Tang, Zongli Hu, Qiaoli Xie & Guoping Chen

  2. College of Agriculture/Mudan, Henan University of Science and Technology, No. 263 of Kaiyuan Avenue, Luolong District, Luoyang, 471000, Henan, People’s Republic of China

    Shuang Zhou

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  1. Yanan Chen
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Contributions

GC, SZ, and ZH: designed and managed the research work and improved the manuscript. YC, PF, BT, QX: performed the experiments. YC: wrote the manuscript. All authors read and approved the manuscript.

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Correspondence to Shuang Zhou or Guoping Chen.

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Chen, Y., Feng, P., Tang, B. et al. The AP2/ERF transcription factor SlERF.F5 functions in leaf senescence in tomato. Plant Cell Rep 41, 1181–1195 (2022). https://doi.org/10.1007/s00299-022-02846-1

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