Advertisement

Plant Growth Regulation

, Volume 89, Issue 3, pp 251–258 | Cite as

Transcription factor TERF1 regulates nuclear genes expression through miRNAs in tobacco under drought stress condition

  • Wei Wu
  • Lili Liu
  • Yanchun YanEmail author
Original paper
  • 54 Downloads

Abstract

Ethylene is an important phytohormone that regulates plant response to drought stress. ETHYLENE RESPONSE FACTOR 1 (ERF1), a transcription factor of ERF/AP2 family, plays an important role in activating ethylene signaling pathway through binding the GCC box in the promoters of ethylene responsive genes. Although we know some protein-coding genes regulated by ERF1, we know nothing about how ERF1 regulates the expression of miRNAs. We utilized the tobacco overexpressing TOMATO ETHYLENE RESPONSE FACTOR1 (TERF1), an ERF1 transcription factor isolated from tomato, to investigate the miRNAs expression profile under natural dehydration condition by method of qRT-PCR. Results show that 25 miRNAs are significantly induced and only 10 miRNAs are significantly repressed by TERF1. Binding sites for ERF transcription factors are observed in six upregulated miRNAs and the core genes involved in the processing of pre-miRNA are also significantly induced by TERF1. We predicted the target genes regulated by the differentially expressed miRNAs by the on-line programme of psRNATarget. Gene ontology (GO) analysis shows that the significantly enriched biological processes for the target genes regulated by the downregulated miRNAs are located in chloroplast. We also predicted the important regulatory genes regulated by the differentially expressed miRNAs, including transcription factors, kinases and phosphatases. Our research provides novel mechanism for regulation of nuclear genes expression by TERF1 at posttranscriptional level under drought stress condition.

Keywords

Drought TERF1 miRNA Gene expression Chloroplast 

Abbreviations

AGO1

ARGONAUTE 1

DCL1

DICER-LIKE 1

ERF1

ETHYLENE RESPONSIVE FACTOR1

GO

Gene ontology

HYL1

HYPONASTIC LEAVES 1

RWC

Relative water content

SE

SERRATE

Notes

Acknowledgements

We thank Prof. Rongfeng Huang for providing the gene of TERF1 for our research. This research received the support by grants from Chinese Academy of Agricultural Sciences Basal Research Fund (No. 1610042018006).

Author contributions

Wei Wu and Yanchun Yan participated in the design of the experiment. Wei Wu performed the experiment. Wei Wu and Lili Liu analyzed the data. Wei Wu write the manuscript and Yanchun Yan provide the final revision.

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interest.

Supplementary material

10725_2019_532_MOESM1_ESM.eps (51 kb)
Fig.S1. Quantitative real-time polymerase chain reaction (qRT-PCR) of genes involved in miRNA processing in WT and TERF1 tobacco under drought stress condition. Means ± SDs, n = 3; bars with * and ** are significantly different at 5 % and 1%, respectively. Supplementary material 1 (EPS 51 kb)
10725_2019_532_MOESM2_ESM.eps (38 kb)
Fig.S2. Quantitative real-time polymerase chain reaction (qRT-PCR) for FtsH2 and FtsH5 in WT and TERF1 tobacco under drought stress condition. Means ± SDs, n = 3; bars with * and ** are significantly different at 5 % and 1%, respectively. Supplementary material 2 (EPS 38 kb)
10725_2019_532_MOESM3_ESM.eps (54 kb)
Fig.S3. Quantitative real-time polymerase chain reaction (qRT-PCR) analysis of miRNAs-regulated transcription factors and target genes in WT and TERF1 tobacco under drought stress condition. Means ± SDs, n = 3; bars with * and ** are significantly different at 5 % and 1%, respectively. Supplementary material 3 (EPS 53 kb)
10725_2019_532_MOESM4_ESM.xlsx (12 kb)
Supplementary material 4 (XLSX 11 kb)
10725_2019_532_MOESM5_ESM.xls (168 kb)
Supplementary material 5 (XLS 168 kb)
10725_2019_532_MOESM6_ESM.xlsx (47 kb)
Supplementary material 6 (XLSX 47 kb)
10725_2019_532_MOESM7_ESM.xls (1.8 mb)
Supplementary material 7 (XLS 1798 kb)
10725_2019_532_MOESM8_ESM.xlsx (163 kb)
Supplementary material 8 (XLSX 163 kb)
10725_2019_532_MOESM9_ESM.xls (217 kb)
Supplementary material 9 (XLS 217 kb)
10725_2019_532_MOESM10_ESM.xlsx (18 kb)
Supplementary material 10 (XLSX 17 kb)
10725_2019_532_MOESM11_ESM.xlsx (16 kb)
Supplementary material 11 (XLSX 15 kb)
10725_2019_532_MOESM12_ESM.xlsx (31 kb)
Supplementary material 12 (XLSX 30 kb)
10725_2019_532_MOESM13_ESM.xlsx (25 kb)
Supplementary material 13 (XLSX 24 kb)
10725_2019_532_MOESM14_ESM.docx (19 kb)
Supplementary material 14 (DOCX 19 kb)

References

  1. Aharoni A, Dixit S, Jetter R et al (2004) The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. Plant Cell 16(9):2463–2480PubMedPubMedCentralGoogle Scholar
  2. Anjali N, Nadiya F, Thomas J et al (2019) Identification and characterization of drought responsive microRNAs and their target genes in cardamom (Elettaria cardamomum Maton). Plant Growth Regul 87(2):201–216Google Scholar
  3. Chan KX, Phua SY, Crisp P et al (2016) Learning the languages of the chloroplast: retrograde signaling and beyond. Annu Rev Plant Biol 67:25–53PubMedGoogle Scholar
  4. Chen Q, Li M, Zhang Z et al (2017) Integrated mRNA and microRNA analysis identifies genes and small miRNA molecules associated with transcriptional and post-transcriptional-level responses to both drought stress and re-watering treatment in tobacco. BMC Genom 18(1):62Google Scholar
  5. Cho HJ, Kim JJ, Lee JH et al (2012) SHORT VEGETATIVE PHASE (SVP) protein negatively regulates miR172 transcription via direct binding to the pri-miR172a promoter in Arabidopsis. FEBS Lett 586(16):2332–2337PubMedGoogle Scholar
  6. Choi K, Kim J, Muller SY et al (2016) Regulation of microRNA-mediated developmental changes by the SWR1 chromatin remodeling complex. Plant Physiol 171(2):1128–1143PubMedPubMedCentralGoogle Scholar
  7. Cuperus JT, Fahlgren N, Carrington JC (2011) Evolution and functional diversification of MIRNA genes. Plant Cell 23(2):431–442PubMedPubMedCentralGoogle Scholar
  8. Dai X, Zhuang Z, Zhao PX (2018) psRNATarget: a plant small RNA target analysis server (2017 release). Nucleic Acids Res 46(W1):W49–W54PubMedPubMedCentralGoogle Scholar
  9. Dossa K, Wei X, Li D et al (2016) Insight into the AP2/ERF transcription factor superfamily in sesame and expression profiling of DREB subfamily under drought stress. BMC Plant Biol 16(1):171PubMedPubMedCentralGoogle Scholar
  10. Fahlgren N, Howell MD, Kasschau KD et al (2007) High-throughput sequencing of Arabidopsis microRNAs: evidence for frequent birth and death of MIRNA genes. PLoS ONE 2(2):e219PubMedPubMedCentralGoogle Scholar
  11. Frazier TP, Sun G, Burklew CE et al (2011) Salt and drought stresses induce the aberrant expression of microRNA genes in tobacco. Mol Biotechnol 49(2):159–165PubMedGoogle Scholar
  12. Huang Z, Zhang Z, Zhang X et al (2004) Tomato TERF1 modulates ethylene response and enhances osmotic stress tolerance by activating expression of downstream genes. FEBS Lett 573(1–3):110–116PubMedGoogle Scholar
  13. Jin J, Tian F, Yang DC et al (2017) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res 45(D1):D1040–D1045PubMedGoogle Scholar
  14. Ju C, Chang C (2015) Mechanistic insights in ethylene perception and signal transduction. Plant Physiol 169(1):85–95PubMedPubMedCentralGoogle Scholar
  15. Kato Y, Sakamoto W (2018) FtsH protease in the thylakoid membrane: physiological functions and the regulation of protease activity. Front Plant Sci 9:855PubMedPubMedCentralGoogle Scholar
  16. Kawashima CG, Matthewman CA, Huang S et al (2011) Interplay of SLIM1 and miR395 in the regulation of sulfate assimilation in Arabidopsis. Plant J 66(5):863–876PubMedGoogle Scholar
  17. Kim W, Benhamed M, Servet C et al (2009) Histone acetyltransferase GCN5 interferes with the miRNA pathway in Arabidopsis. Cell Res 19(7):899–909PubMedGoogle Scholar
  18. Kim BH, Kwon Y, Lee BH et al (2014) Overexpression of miR172 suppresses the brassinosteroid signaling defects of bak1 in Arabidopsis. Biochem Biophys Res Commun 447(3):479–484PubMedGoogle Scholar
  19. Kumar A, Gautam V, Kumar P et al (2019) Identification and co-evolution pattern of stem cell regulator miR394s and their targets among diverse plant species. BMC Evol Biol 19(1):55PubMedPubMedCentralGoogle Scholar
  20. Leyva-Gonzalez MA, Ibarra-Laclette E, Cruz-Ramirez A et al (2012) Functional and transcriptome analysis reveals an acclimatization strategy for abiotic stress tolerance mediated by Arabidopsis NF-YA family members. PLoS ONE 7(10):e48138PubMedPubMedCentralGoogle Scholar
  21. Li WX, Oono Y, Zhu J et al (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and posttranscriptionally to promote drought resistance. Plant Cell 20(8):2238–2251PubMedPubMedCentralGoogle Scholar
  22. Li A, Zhang Z, Wang XC et al (2009) Ethylene response factor TERF1 enhances glucose sensitivity in tobacco through activating the expression of sugar-related genes. J Integr Plant Biol 51(2):184–193PubMedGoogle Scholar
  23. Liu Y, Ji X, Nie X et al (2015) Arabidopsis AtbHLH112 regulates the expression of genes involved in abiotic stress tolerance by binding to their E-box and GCG-box motifs. New Phytol 207(3):692–709PubMedGoogle Scholar
  24. Ma Z, Hu X, Cai W et al (2014) Arabidopsis miR171-targeted scarecrow-like proteins bind to GT cis-elements and mediate gibberellin-regulated chlorophyll biosynthesis under light conditions. PLoS Genet 10(8):e1004519PubMedPubMedCentralGoogle Scholar
  25. Mallory AC, Vaucheret H (2006) Functions of microRNAs and related small RNAs in plants. Nat Genet 38(Suppl):S31–S36PubMedGoogle Scholar
  26. Mi H, Muruganujan A, Huang X et al (2019) Protocol update for large-scale genome and gene function analysis with the PANTHER classification system (v.14.0). Nat Protoc 14(3):703–721PubMedPubMedCentralGoogle Scholar
  27. Oliver C, Pradillo M, Jover-Gil S et al (2017) Loss of function of Arabidopsis microRNA-machinery genes impairs fertility, and has effects on homologous recombination and meiotic chromatin dynamics. Sci Rep 7(1):9280PubMedPubMedCentralGoogle Scholar
  28. Qu B, He X, Wang J et al (2015) A wheat CCAAT box-binding transcription factor increases the grain yield of wheat with less fertilizer input. Plant Physiol 167(2):411–423PubMedGoogle Scholar
  29. Rajagopalan R, Vaucheret H, Trejo J et al (2006) A diverse and evolutionarily fluid set of microRNAs in Arabidopsis thaliana. Genes Dev 20(24):3407–3425PubMedPubMedCentralGoogle Scholar
  30. Ren G, Chen X, Yu B (2012) Uridylation of miRNAs by hen1 suppressor1 in Arabidopsis. Curr Biol 22(8):695–700PubMedPubMedCentralGoogle Scholar
  31. Samad A, Sajad M, Nazaruddin N et al (2017) MicroRNA and transcription factor: key players in plant regulatory network. Front Plant Sci 8:565PubMedPubMedCentralGoogle Scholar
  32. Song JB, Gao S, Sun D et al (2013) miR394 and LCR are involved in Arabidopsis salt and drought stress responses in an abscisic acid-dependent manner. BMC Plant Biol 13:210PubMedPubMedCentralGoogle Scholar
  33. Vaucheret H, Vazquez F, Crete P et al (2004) The action of ARGONAUTE1 in the miRNA pathway and its regulation by the miRNA pathway are crucial for plant development. Genes Dev 18(10):1187–1197PubMedPubMedCentralGoogle Scholar
  34. Wang F, Perry SE (2013) Identification of direct targets of FUSCA3, a key regulator of Arabidopsis seed development. Plant Physiol 161(3):1251–1264PubMedPubMedCentralGoogle Scholar
  35. Wang L, Kim C, Xu X et al (2016) Singlet oxygen- and EXECUTER1-mediated signaling is initiated in grana margins and depends on the protease FtsH2. Proc Natl Acad Sci USA 113(26):E3792–E3800PubMedGoogle Scholar
  36. Wang X, Wang Y, Dou Y et al (2018) Degradation of unmethylated miRNA/miRNA*s by a DEDDy-type 3′ to 5′ exoribonuclease Atrimmer 2 in Arabidopsis. Proc Natl Acad Sci USA 115(28):E6659–E6667PubMedGoogle Scholar
  37. Winter D, Vinegar B, Nahal H et al (2007) An “Electronic Fluorescent Pictograph” browser for exploring and analyzing large-scale biological data sets. PLoS ONE 2(8):e718PubMedPubMedCentralGoogle Scholar
  38. Wu W, Yan Y (2018) Chloroplast proteome analysis of Nicotiana tabacum overexpressing TERF1 under drought stress condition. Bot Stud 59(1):26PubMedPubMedCentralGoogle Scholar
  39. Wu L, Zhou H, Zhang Q et al (2010) DNA methylation mediated by a microRNA pathway. Mol Cell 38(3):465–475PubMedGoogle Scholar
  40. Wu W, Liu LL, Yang T et al (2018) Gene expression analysis reveals function of TERF1 in plastid-nucleus retrograde signaling under drought stress conditions. Biol Plant 62(3):428–438Google Scholar
  41. Xie Z, Allen E, Fahlgren N et al (2005) Expression of Arabidopsis MIRNA genes. Plant Physiol 138(4):2145–2154PubMedPubMedCentralGoogle Scholar
  42. Yang Z, Ebright YW, Yu B et al (2006) HEN1 recognizes 21-24 nt small RNA duplexes and deposits a methyl group onto the 2′ OH of the 3′ terminal nucleotide. Nucleic Acids Res 34(2):667–675PubMedPubMedCentralGoogle Scholar
  43. Yant L, Mathieu J, Dinh TT et al (2010) Orchestration of the floral transition and floral development in Arabidopsis by the bifunctional transcription factor APETALA2. Plant Cell 22(7):2156–2170PubMedPubMedCentralGoogle Scholar
  44. Yuan N, Yuan S, Li Z et al (2016) Heterologous expression of a rice miR395 gene in Nicotiana tabacum impairs sulfate homeostasis. Sci Rep 6:28791PubMedPubMedCentralGoogle Scholar
  45. Zhang X, Zhang Z, Chen J et al (2005) Expressing TERF1 in tobacco enhances drought tolerance and abscisic acid sensitivity during seedling development. Planta 222(3):494–501PubMedGoogle Scholar
  46. Zhang H, Li A, Zhang Z et al (2016) Ethylene response factor TERF1, regulated by ETHYLENE-INSENSITIVE3-like factors, functions in reactive oxygen species (ROS) scavenging in tobacco (Nicotiana tabacum L.). Sci Rep 6:29948PubMedPubMedCentralGoogle Scholar
  47. Zhao M, Ding H, Zhu JK et al (2011) Involvement of miR169 in the nitrogen-starvation responses in Arabidopsis. New Phytol 190(4):906–915PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Graduate School of Chinese Academy of Agricultural SciencesBeijingPeople’s Republic of China
  2. 2.Beijing Key Laboratory of Fishery BiotechnologyBeijing Fisheries Research InstituteBeijingPeople’s Republic of China

Personalised recommendations