Skip to main content

Advertisement

Log in

ZmTIFY16, a novel maize TIFY transcription factor gene, promotes root growth and development and enhances drought and salt tolerance in Arabidopsis and Zea mays

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

The TIFY (a conserved core motif TIF[F/Y]XG) protein is a plant-specific transcription factor that regulates various plant growth/development and stress-related processes. Although many TIFY proteins have been reported in Arabidopsis thaliana, rice (Oryza sativa L.), and other plants, few studies have investigated the role of TIFY proteins in maize (Zea mays L.). In this study, we cloned and performed a preliminary structural and functional analysis of ZmTIFY16, a transcription factor gene that we previously identified in the genome of maize. This gene showed high expression in young and mature leaves and was strongly induced by low temperature (4ºC), dehydration, drought, salt, and abscisic acid. Its heterologous expression in Arabidopsis markedly improved drought and salt tolerance, increased chlorophyll and proline contents, enhanced superoxide dismutase activity, and decreased malondialdehyde content. Moreover, ZmTIFY16 interacted with ZmMYC2, an essential regulator of the jasmonic acid signaling pathway, promoted root growth, and improved salt tolerance in overexpressing maize lines. The results suggest that ZmTIFY16 may be critical for regulating maize growth and abiotic stress responses. ZmTIFY16 may be a novel candidate gene for promoting root growth and development and regulating drought and salt tolerance in maize.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Bai YH, Meng YJ, Huang DL, Qi YH, Chen M (2011) Origin and evolutionary analysis of the plant-specific TIFY transcription factor family. Genomics 98:128–136

    Article  CAS  PubMed  Google Scholar 

  • Chen Q, Sun JQ, Zhai QZ, Zhou WK, Qi LL, Xu L, Wang B, Chen R, Jiang HL, Qi J, Li XG, Palme K, Li CY (2011) The basic helix-loop-helix transcription factor MYC2 directly represses PLETHORA expression during jasmonate-mediated modulation of the root stem cell niche in Arabidopsis. Plant Cell 23:3335–3352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chico JM, Chini A, Fonseca S, Solano R (2008) JAZ repressors set the rhythm in jasmonate signaling. Curr Opin Plant Biol 11:486–494

    Article  CAS  PubMed  Google Scholar 

  • Chini A, Fonseca S, Fernandez G, Adie B, Chico JM, Lorenzo O, Garcia-Casado G, Lopez-Vidriero I, Lozano FM, Ponce MR (2007) The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448:666–671

    Article  CAS  PubMed  Google Scholar 

  • Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on crosstalk and specificity in abiotic stress signalling in plants. J Exp Bot 55:225–236

    Article  CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium mediated transformation of Arabidopsis thaliana. Plant J 16(6):735–743

    Article  CAS  PubMed  Google Scholar 

  • Ebel C, BenFeki A, Hanin M, Solano R, Chini A (2018) Characterization of wheat (Triticum aestivum) TIFY family and role of Triticum Durum TdTIFY11a in salt stress tolerance. PLoS ONE 13(7):e0200566

    Article  PubMed  PubMed Central  Google Scholar 

  • Fernandez-Calvo P, Chini A, Fernandez-Barbero G, Chico JM, Gimenez-Ibanez S, Geerinck J, Eeckhout D, Schweizer F, Godoy M, Franco-Zorrilla JM (2011) The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell 23:701–715

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu J, Wu H, Ma SQ, Xiang DH, Liu RY, Xiong LZ (2017) OsJAZ1 attenuates Drought Resistance by regulating JA and ABA signaling in Rice.Frontiers in Plant Science8: Article 2108

  • Fu JY, Liu LJ, Liu Q, Shen QQ, Wang C, Yang PP, Zhu CY, Wang Q (2020) ZmMYC2 exhibits diverse functions and enhances JA signaling in transgenic Arabidopsis. Plant Cell Rep 39:273–288

    Article  CAS  PubMed  Google Scholar 

  • Garcia-Abellan JO, Fernandez- Garcia N, Lopez-Berenguer C, Egea I, Flores FB, Angoso T, Capel J, Lozano R, Pineda B, Moreno V, Olmos E, Bolarin M (2015) The tomato res mutant which accumulates JA in roots in non-stressed conditions restores cell structure alterations under salinity. Physiol Plant 155(3):296–314

    Article  CAS  PubMed  Google Scholar 

  • Goharrizi KJ, Baghizadeh A, Kalantar M, Fatehi F (2020) Assessment of Changes in some biochemical Traits and Proteomic Profile of UCB-1 Pistachio Rootstock Leaf under salinity stress. J Plant Growth Regul 39:608–630 (a)

    Article  Google Scholar 

  • Goharrizi KJ, Riahi-Madvar A, Rezaee F, Pakzad R, Bonyad FJ, Ahsaei MG (2020) Effect of salinity stress on enzymes’ activity, Ions Concentration, oxidative stress parameters, biochemical traits, content of sulforaphane, and CYP79F1 gene expression level in Lepidium draba Plant. J Plant Growth Regul 39:1075–1094 (b)

    Article  Google Scholar 

  • Goharrizi KJ, Geoffrey M, Kermani SG, Heidarinezhad A, Salehi F (2021) Short-term cold stress affects physiological and biochemical traits of pistachio rootstocks. South Afr J Bot 141:90–98

    Article  Google Scholar 

  • Jiang XQ, Zhang CQ, Lü PT, Jiang GM, Liu XW, Dai FW, Gao JP (2014) RhNAC3, a stress-associated NAC transcription factor, has a role in dehydration tolerance through regulating osmotic stress related genes in rose petals. Plant Biotechnol J 12:38–48

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2–∆∆CT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Kiarash JG, Dayton WH, Amirmahani F, Mehdi MM, Zaboli M, Nazari M, Moosavi SS, Jamalvandi M (2018) Selection and validation of reference genes for normalization of qRT-PCR gene expression in wheat (Triticum durum L.) under drought and salt stresses. J Genet 97(5):1433–1444

    Article  CAS  PubMed  Google Scholar 

  • Lorenzo O, Chico JM, Sánchez-Serrano JJ, Solano R (2004) JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16:1938–1950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meng L, Zhang T, Ge SS, Scott PB, Li HY, Chen SX (2019) Comparative proteomics and metabolomics of JAZ7-mediated drought tolerance in Arabidopsis. J Proteom 196:81–91

    Article  CAS  Google Scholar 

  • Nazari M, Moosavi SS, Maleki M, Goharrizi KJ (2020) Chloroplastic acyl carrier protein synthase I and chloroplastic 20 kDa chaperonin proteins are involved in wheat (Triticum aestivum) in response to moisture stress. J Plant Interact 15(1):180–187

    Article  CAS  Google Scholar 

  • Nazari M, Goharrizi KJ, Moosavi SS, Maleki M (2019) Expression changes in the TaNAC2 and TaNAC69-1 transcription factors in drought stress tolerant and susceptible accessions of Triticum boeoticum. Plant Genetic Resources 17(6):1–9

    Article  Google Scholar 

  • Nishii A, Takemura M, Fujita H, Shikata M, Yokota A, Kohchi T (2000) Characterization of a novel gene encoding a putative single Zinc-finger protein, ZIM, expressed during the reproductive phase in Arabidopsis thaliana. Bioscience, Biotechnology, and Biochemistry 64(7): 1402–1409

  • Oblessuc PR, Obulareddy N, DeMott L, Matiolli CC, Thompson BK, Melotto M (2020) JAZ4 is involved in plant defense, growth, and development in Arabidopsis.The Plant Journal101(2)

  • Orsini F, Cascone P, Pascale SD, Barbieri G, Corrado G, Rao R, Maggio A (2010) Systemin-dependent salinity tolerance in tomato: evidence of specific convergence of abiotic and biotic stress responses. Physiol Plant 138(1):10–21

    Article  CAS  PubMed  Google Scholar 

  • Qi TC, Song SS, Ren QC, Wu DW, Huang H, Chen Y, Fan M, Peng W, Ren CM, Xie DX (2011) The Jasmonate-ZIM-domain proteins interact with the WD-Repeat/bHLH/MYB complexes to regulate Jasmonate-mediated anthocyanin accumulation and trichome initiation in Arabidopsis thaliana. Plant Cell 23:1795–1814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qiu ZB, Guo JL, Zhu AJ, Zhang L, Zhang MM (2014) Exogenous jasmonic acid can enhance tolerance of wheat seedling to salt stress. Ecotoxicol Environ Saf 104:202–208

    Article  CAS  PubMed  Google Scholar 

  • Seo JS, Joo J, Kim MJ, Kim YK, Nahm BH, Song SI, Cheong JJ, Lee JS, Kim JK, Choi YD (2011) OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. Plant J 65(6):907–921

    Article  CAS  PubMed  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24(8):1596–1599

    Article  CAS  PubMed  Google Scholar 

  • Vanholme B, Grunewald W, Bateman A, Kohchi T, Gheysen G (2007) The tify family previously known as ZIM. Trends Plant Sci 12:239–244

    Article  CAS  PubMed  Google Scholar 

  • Wang ZP, Zhang ZB, Zheng DY, Zhang TT, Li XL, Zhang C, Yu R, Wei JH, Wu ZY (2022) Efficient and genotype independent maize transformation using pollen transfected by DNA-coated magnetic nanoparticles. J Integr Plant Biol 64:1145–1156

    Article  CAS  PubMed  Google Scholar 

  • Xia XJ, Zhou YH, Shi K, Zhou J, Foyer CH, Yu JQ (2015) Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. J Exp Bot 66:2839–2856

    Article  CAS  PubMed  Google Scholar 

  • Ye HY, Du H, Tang N, Li XH, Xiong LZ (2009) Identification and expression profiling analysis of TIFY family genes involved in stress and phytohormone responses in rice. Plant Mol Biol 71(3):291–305

    Article  CAS  PubMed  Google Scholar 

  • Zhang ZB, Li XL, Yu R, Han M, Wu ZY (2015) Isolation, structural analysis, and expression characteristics of the maize TIFY gene family. Mol Genet Genomics 290:1849–1858

    Article  CAS  PubMed  Google Scholar 

  • Zhao CY, Pan XW, Yu Y, Zhu YM, Kong FJ, Sun X, Wang FF (2020) Overexpression of a TIFY family gene, GsJAZ2, exhibits enhanced tolerance to alkaline stress in soybean. Mol Breeding 40(3):255–265

    Article  Google Scholar 

  • Zhao Q, Zhang H, Wang T, Chen SX, Dai SJ (2013) Proteomics-based investigation of salt-responsive mechanisms in plant roots. J Proteoeme 82:230–253

    Article  CAS  Google Scholar 

  • Zhao SX, Li L, Zhi YN, Pei L, Ming C, Lian CL, Yao FC, You ZM (2009) W55a encodes a novel protein kinase that is involved in multiple stress responses. J Integr Plant Biol 51(1):58–66

    Article  Google Scholar 

  • Zhao X, Meng ZG, Wang Y, Chen WJ, Sun CJ, Cui B, Cui JH, Yu ML, Zeng ZH, Guo SD, Luo D, Cheng JQ, Zhang R, Cui HX (2017) Pollen magnetofection for genetic modification with magnetic nanoparticles as gene carriers. Nat Plants 3:956–964

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Dong W, Zhang NB, Ai XH, Wang MC, Huang ZG, Xiao LT, Xia GM (2014) A wheat allene oxide cyclase gene enhances salinity tolerance via jasmonate signaling. Plant Physiol 164(2):1068–1076

    Article  CAS  PubMed  Google Scholar 

  • Zhou XJ, Yan SG, Sun C, Li SZ, Li J, Xu MY, Liu XQ, Zhang SJ, Zhao QQ, Li Y, Fan YL, Chen RM, Wang L (2015) A Maize Jasmonate Zim-Domain protein, ZmJAZ14, associates with the JA, ABA, and GA signaling pathways in transgenic Arabidopsis. PLoS ONE 10(3):e0121824

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu D, Bai X, Chen C, Chen Q, Cai H, Li Y, Ji W, Zhai H, Lv D, Luo X, Zhu YM (2011) GsTIFY10, a novel positive regulator of plant tolerance to bicarbonate stress and a repressor of jasmonate signaling. Plant Mol Biol 77(3):285–297

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (NSFC) 32001430, the Beijing Natural Science Foundation (No.6222009), the Foundation of Beijing Academy of Agriculture and Forestry Sciences KJCX20200205, KJCX20200407, and KJCX20220402.

Author information

Authors and Affiliations

Authors

Contributions

Chun Zhang: Conceptualization, Methodology, Formal Analysis, Funding Acquisition, Validation, Writing-Review & Editing; Ruijia Yang: Data Curation, Formal Analysis, Visualization, Writing-Original Draft; Tongtong Zhang, Dengyu Zheng and Xianglong Li: Data Curation; Zhongbao Zhang: Conceptualization, Funding Acquisition, Writing-Review & Editing; Legong Li: Writing-Review & Editing; Zhongyi Wu: Conceptualization, Project Administration, Writing-Review & Editing. These authors contributed equally: Chun Zhang, Ruijia Yang

Corresponding authors

Correspondence to Zhongbao B. Zhang, Legong G. Li or Zhongyi Y. Wu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Luca Sebastiani.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, C., Yang, R., Zhang, T. et al. ZmTIFY16, a novel maize TIFY transcription factor gene, promotes root growth and development and enhances drought and salt tolerance in Arabidopsis and Zea mays. Plant Growth Regul 100, 149–160 (2023). https://doi.org/10.1007/s10725-022-00946-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-022-00946-2

Keywords

Navigation