SpringerLink
Log in

Comparative transcriptome analysis reveals function of TERF1 in promoting seed germination

  • Research Article
  • Published:
Physiology and Molecular Biology of Plants Aims and scope Submit manuscript

Abstract

Seed germination marks a new life cycle of a plant. Although ethylene promotes seed germination, the underlying molecular mechanism is poorly understood. Ethylene Responsive Factors (ERFs) play an essential role in ethylene signaling. Here we show that overexpression of Tomato Ethylene Responsive Factor 1 (TERF1), an ERF transcription factor isolated from tomato, can promote tobacco seed germination at 23 °C in darkness. Hormones analysis showed that salicylic acid (SA), 3-indoleacetic acid (IAA), abscisic acid (ABA) and gibberellic acids (GAs) were significantly increased by TERF1, while jasmonic acid (JA) was significantly reduced in TERF1 seeds. Transcriptome analysis identified 7,961 differentially expressed genes (DEGs), including 6,213 mRNAs, 25 miRNAs, 1,581 lncRNAs and 141 circRNAs. Gene Ontology (GO) enrichment analysis showed that cell cycles, sugar metabolism, microtubule-based processes were activated by TERF1, while DNA repair, lipid metabolism were repressed by TERF1. We also identified differentially expressed regulatory genes for ABA and GA biosynthesis or signaling in TERF1 seed, including transcription factors, kinases, phosphatases and ubiquitin protein ligases, non-coding RNAs (ncRNAs). At posttranscriptional level TERF1 also regulates gene expression through alternative splicing (AS). Protein–protein interaction (PPI) network analysis revealed three key biological processes regulated by TERF1, including nitrogen metabolism, light related processes and mitosis. Pheynotype and gene expression analysis showed that TERF1 significantly reduced seed sensitivity to ABA and auxin during germination through repressing key components of ABA signaling pathway. Our results unraveled the function of TERF1 in promoting seed germination.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (France)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ahammed GJ, Gantait S, Mitra M, Yang Y, Li X (2020) Role of ethylene crosstalk in seed germination and early seedling development: a review. Plant Physiol Biochem 151:124–131

    Article  CAS  PubMed  Google Scholar 

  • Arana MV, Sanchez-Lamas M, Strasser B, Ibarra SE, Cerdan PD, Botto JF, Sanchez RA (2014) Functional diversity of phytochrome family in the control of light and gibberellin-mediated germination in Arabidopsis. Plant Cell Environ 37:2014–2023

    Article  CAS  PubMed  Google Scholar 

  • Arc E, Sechet J, Corbineau F, Rajjou L, Marion-Poll A (2013) ABA crosstalk with ethylene and nitric oxide in seed dormancy and germination. Front Plant Sci 4:63

    PubMed  PubMed Central  Google Scholar 

  • Bai M, Sun J, Liu J, Ren H, Wang K, Wang Y, Wang C, Dehesh K (2019) The B-box protein BBX19 suppresses seed germination via induction of ABI5. Plant J 99:1192–1202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bi C, Ma Y, Wu Z, Yu YT, Liang S, Lu K, Wang XF (2017) Arabidopsis ABI5 plays a role in regulating ROS homeostasis by activating CATALASE 1 transcription in seed germination. Plant Mol Biol 94:197–213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carrera-Castano G, Calleja-Cabrera J, Pernas M, Gomez L, Onate-Sanchez L (2020) An updated overview on the regulation of seed germination. Plants (Basel) 9:703

    Article  CAS  PubMed Central  Google Scholar 

  • Chen LT, Luo M, Wang YY, Wu K (2010) Involvement of Arabidopsis histone deacetylase HDA6 in ABA and salt stress response. J Exp Bot 61:3345–3353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen Z, Huang Y, Yang W, Chang G, Li P, Wei J, Yuan X, Huang J, Hu X (2019) The hydrogen sulfide signal enhances seed germination tolerance to high temperatures by retaining nuclear COP1 for HY5 degradation. Plant Sci 285:34–43

    Article  CAS  PubMed  Google Scholar 

  • Cho SK, Ryu MY, Seo DH, Kang BG, Kim WT (2011) The Arabidopsis RING E3 ubiquitin ligase AtAIRP2 plays combinatory roles with AtAIRP1 in abscisic acid-mediated drought stress responses. Plant Physiol 157:2240–2257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Corbineau F, **a Q, Bailly C, El-Maarouf-Bouteau H (2014) Ethylene, a key factor in the regulation of seed dormancy. Front Plant Sci 5:539

    Article  PubMed  PubMed Central  Google Scholar 

  • D'Angelo C, Weinl S, Batistic O, Pandey GK, Cheong YH, Schultke S, Albrecht V, Ehlert B, Schulz B, Harter K, Luan S, Bock R, Kudla J (2006) Alternative complex formation of the Ca-regulated protein kinase CIPK1 controls abscisic acid-dependent and independent stress responses in Arabidopsis. Plant J 48:857–872

    Article  CAS  PubMed  Google Scholar 

  • Feng C-Z, Chen Y, Wang C, Kong Y-H, Wu W-H, Chen Y-F (2014) Arabidopsis RAV1 transcription factor, phosphorylated by SnRK2 kinases, regulates the expression of ABI3, ABI4, and ABI5 during seed germination and early seedling development. Plant J 80:654–668. https://doi.org/10.1111/tpj.12670

    Article  CAS  PubMed  Google Scholar 

  • Gabriele S, Rizza A, Martone J, Circelli P, Costantino P, Vittorioso P (2010) The Dof protein DAG1 mediates PIL5 activity on seed germination by negatively regulating GA biosynthetic gene AtGA3ox1. Plant J 61:312–323

    Article  CAS  PubMed  Google Scholar 

  • Gibbs DJ, Md IN, Movahedi M, Lozano-Juste J, Mendiondo GM, Berckhan S, Marin-de LRN, Vicente CJ, Sousa CC, Pearce SP, Bassel GW, Hamali B, Talloji P, Tome DF, Coego A, Beynon J, Alabadi D, Bachmair A, Leon J, Gray JE, Theodoulou FL, Holdsworth MJ (2014) Nitric oxide sensing in plants is mediated by proteolytic control of group VII ERF transcription factors. Mol Cell 53:369–379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang Z, Zhang Z, Zhang X, Zhang H, Huang D, Huang R (2004) Tomato TERF1 modulates ethylene response and enhances osmotic stress tolerance by activating expression of downstream genes. Febs Lett 573:110–116

    Article  CAS  PubMed  Google Scholar 

  • Huang Y, Sun MM, Ye Q, Wu XQ, Wu WH, Chen YF (2017) Abscisic acid modulates seed germination via ABA INSENSITIVE5-Mediated PHOSPHATE1. Plant Physiol 175:1661–1668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Je J, Chen H, Song C, Lim CO (2014) Arabidopsis DREB2C modulates ABA biosynthesis during germination. Biochem Biophys Res Commun 452:91–98

    Article  CAS  PubMed  Google Scholar 

  • Jiang A, Guo Z, Pan J, Yang Y, Zhuang Y, Zuo D, Hao C, Gao Z, **n P, Chu J, Zhong S, Li L (2021) The PIF1-miR408-PLANTACYANIN repression cascade regulates light-dependent seed germination. Plant Cell 33:1506–1529

    Article  PubMed  PubMed Central  Google Scholar 

  •  Ju L, **g Y, Shi P, Liu J, Chen J, Yan J, Chu J, Chen KM, Sun J (2019) JAZ proteins modulate seed germination through interaction with ABI5 in bread wheat and Arabidopsis. New Phytol 223:246–260

    Article  CAS  PubMed  Google Scholar 

  • Kawakatsu T, Nery JR, Castanon R, Ecker JR (2017) Dynamic DNA methylation reconfiguration during seed development and germination. Genome Biol 18:171

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lin JH, Yu LH, **ang CB (2020) ARABIDOPSIS NITRATE REGULATED 1 acts as a negative modulator of seed germination by activating ABI3 expression. New Phytol 225:835–847

    Article  CAS  PubMed  Google Scholar 

  • Liu PP, Koizuka N, Martin RC, Nonogaki H (2005) The BME3 (Blue Micropylar End 3) GATA zinc finger transcription factor is a positive regulator of Arabidopsis seed germination. Plant J 44:960–971

    Article  CAS  PubMed  Google Scholar 

  • Liu X, Zhang H, Zhao Y, Feng Z, Li Q, Yang HQ, Luan S, Li J, He ZH (2013) Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis. Proc Natl Acad Sci USA 110:15485–15490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu X, Hu P, Huang M, Tang Y, Li Y, Li L, Hou X (2016) The NF-YC-RGL2 module integrates GA and ABA signalling to regulate seed germination in Arabidopsis. Nat Commun 7:12768 

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu L, **a W, Li H, Zeng H, Wei B, Han S, Yin C (2018) Salinity inhibits rice seed germination by reducing alpha-Amylase activity via decreased bioactive Gibberellin content. Front Plant Sci 9:275

    Article  PubMed  PubMed Central  Google Scholar 

  • Luo J, Shen G, Yan J, He C, Zhang H (2006) AtCHIP functions as an E3 ubiquitin ligase of protein phosphatase 2A subunits and alters plant response to abscisic acid treatment. Plant J 46:649–657

    Article  CAS  PubMed  Google Scholar 

  • Nakashima K, Fujita Y, Kanamori N, Katagiri T, Umezawa T, Kidokoro S, Maruyama K, Yoshida T, Ishiyama K, Kobayashi M, Shinozaki K, Yamaguchi-Shinozaki K (2009) Three Arabidopsis SnRK2 protein kinases, SRK2D/SnRK2.2, SRK2E/SnRK2.6/OST1 and SRK2I/SnRK2.3, involved in ABA signaling are essential for the control of seed development and dormancy. Plant Cell Physiol 50:1345–1363

    Article  CAS  PubMed  Google Scholar 

  • Nee G, Kramer K, Nakabayashi K, Yuan B, **ang Y, Miatton E, Finkemeier I, Soppe W (2017) DELAY OF GERMINATION1 requires PP2C phosphatases of the ABA signalling pathway to control seed dormancy. Nat Commun 8:72

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nonogaki H (2019) Seed germination and dormancy: the classic story, new puzzles, and evolution. J Integr Plant Biol 61:541–563

    Article  PubMed  Google Scholar 

  • Park J, Lee N, Kim W, Lim S, Choi G (2011) ABI3 and PIL5 collaboratively activate the expression of SOMNUS by directly binding to its promoter in imbibed Arabidopsis seeds. Plant Cell 23:1404–1415

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pellizzaro A, Neveu M, Lalanne D, Ly VB, Kanno Y, Seo M, Leprince O, Buitink J (2020) A role for auxin signaling in the acquisition of longevity during seed maturation. New Phytol 225:284–296

    Article  CAS  PubMed  Google Scholar 

  • Piskurewicz U, Jikumaru Y, Kinoshita N, Nambara E, Kamiya Y, Lopez-Molina L (2008) The gibberellic acid signaling repressor RGL2 inhibits Arabidopsis seed germination by stimulating abscisic acid synthesis and ABI5 activity. Plant Cell 20:2729–2745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rajjou L, Duval M, Gallardo K, Catusse J, Bally J, Job C, Job D (2012) Seed germination and vigor. Annu Rev Plant Biol 63:507–533

    Article  CAS  PubMed  Google Scholar 

  • Sajeev N, Bai B, Bentsink L (2019) Seeds: a unique system to study translational regulation. Trends Plant Sci 24:487–495

    Article  CAS  PubMed  Google Scholar 

  • Sanchez-Montesino R, Bouza-Morcillo L, Marquez J, Ghita M, Duran-Nebreda S, Gomez L, Holdsworth MJ, Bassel G, Onate-Sanchez L (2019) A regulatory module controlling GA-mediated endosperm cell expansion is critical for seed germination in Arabidopsis. Mol Plant 12:71–85

    Article  CAS  PubMed  Google Scholar 

  • Schmidt GW, Delaney SK (2010) Stable internal reference genes for normalization of real-time RT-PCR in tobacco (Nicotiana tabacum) during development and abiotic stress. Mol Genet Genomics 283:233–241

    Article  CAS  PubMed  Google Scholar 

  • Shu K, Liu XD, **e Q, He ZH (2016) Two faces of one seed: hormonal regulation of dormancy and germination. Mol Plant 9:34–45

    Article  CAS  PubMed  Google Scholar 

  • Siriwardana CL, Kumimoto RW, Jones DS, Holt BR (2014) Gene family analysis of the Arabidopsis NF-YA transcription factors reveals opposing abscisic acid responses during seed germination. Plant Mol Biol Report 32:971–986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Subbiah V, Reddy KJ (2010) Interactions between ethylene, abscisic acid and cytokinin during germination and seedling establishment in Arabidopsis. J Biosci 35:451–458

    Article  CAS  PubMed  Google Scholar 

  • Tang W, Ji Q, Huang Y, Jiang Z, Bao M, Wang H, Lin R (2013) FAR-RED ELONGATED HYPOCOTYL3 and FAR-RED IMPAIRED RESPONSE1 transcription factors integrate light and abscisic acid signaling in Arabidopsis. Plant Physiol 163:857–866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tognacca RS, Servi L, Hernando CE, Saura-Sanchez M, Yanovsky MJ, Petrillo E, Botto JF (2019) Alternative splicing regulation during light-induced germination of Arabidopsis thaliana seeds. Front Plant Sci 10:1076

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Li L, Ye T, Zhao S, Liu Z, Feng YQ, Wu Y (2011) Cytokinin antagonizes ABA suppression to seed germination of Arabidopsis by downregulating ABI5 expression. Plant J 68:249–261

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Cui Y, Hu G, Wang X, Chen H, Shi Q, **ang J, Zhang Y, Zhu D, Zhang Y (2018) Reduced bioactive gibberellin content in rice seeds under low temperature leads to decreased sugar consumption and low seed germination rates. Plant Physiol Biochem 133:1–10

    Article  PubMed  CAS  Google Scholar 

  • Wu W, Yan Y (2018) Chloroplast proteome analysis of Nicotiana tabacum overexpressing TERF1 under drought stress condition. Bot Stud 59:26 

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xu D, Li J, Gangappa SN, Hettiarachchi C, Lin F, Andersson MX, Jiang Y, Deng XW, Holm M (2014) Convergence of light and ABA signaling on the ABI5 promoter. Plos Genet 10:e1004197

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xu H, Lantzouni O, Bruggink T, Benjamins R, Lanfermeijer F, Denby K, Schwechheimer C, Bassel GW (2020) A molecular signal integration network underpinning arabidopsis seed germination. Curr Biol 30:3703–3712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang L, Liu S, Lin R (2020) The role of light in regulating seed dormancy and germination. J Integr Plant Biol 62:1310–1326

    Article  PubMed  Google Scholar 

  • Yu Y, Wang J, Shi H, Gu J, Dong J, Deng XW, Huang R (2016) Salt stress and ethylene antagonistically regulate nucleocytoplasmic partitioning of COP1 to control seed germination. Plant Physiol 170:2340–2350

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu Y, Zhang Y, Chen X, Chen Y (2019) Plant noncoding RNAs: hidden players in development and stress responses. Annu Rev Cell Dev Bi 35:407–431

    Article  CAS  Google Scholar 

  • Zhang X, Zhang Z, Chen J, Chen Q, Wang XC, Huang R (2005) Expressing TERF1 in tobacco enhances drought tolerance and abscisic acid sensitivity during seedling development. Planta 222:494–501

    Article  CAS  PubMed  Google Scholar 

  • Zhang Q, Zhang X, Wang S, Tan C, Zhou G, Li C (2016) Involvement of alternative splicing in barley seed germination. Plos One 11:e152824

    Google Scholar 

  • Zhang H, Gannon L, Jones PD, Rundle CA, Hassall KL, Gibbs DJ, Holdsworth MJ, Theodoulou FL (2018) Genetic interactions between ABA signalling and the Arg/N-end rule pathway during Arabidopsis seedling establishment. Sci Rep 8:15192

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhao X, Dou L, Gong Z, Wang X, Mao T (2019) BES1 hinders ABSCISIC ACID INSENSITIVE5 and promotes seed germination in Arabidopsis. New Phytol 221:908–918

    Article  CAS  PubMed  Google Scholar 

  • Zhou SF, Sun L, Valdes AE, Engstrom P, Song ZT, Lu SJ, Liu JX (2015) Membrane-associated transcription factor peptidase, site-2 protease, antagonizes ABA signaling in Arabidopsis. New Phytol 208:188–197

    Article  CAS  PubMed  Google Scholar 

  • Zhu L, Bu Q, Xu X, Paik I, Huang X, Hoecker U, Deng XW, Huq E (2015) CUL4 forms an E3 ligase with COP1 and SPA to promote light-induced degradation of PIF1. Nat Commun 6:7245

    Article  CAS  PubMed  Google Scholar 

Download references

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 information

Authors and Affiliations

  1. Graduate School of Chinese Academy of Agricultural Sciences, No.12 Zhongguancun South St., Haidian District, Bei**g, 100081, People’s Republic of China

    Hongzhi Liu & Wei Wu

Authors
  1. Hongzhi Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wei Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

WW and HL designed and preformed the experiments.HL analyzed the data and wrote the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Wei Wu.

Ethics declarations

Conflict of interest

The authors declare that the submitted work was not performed in the presence of any personal, professional or financial relationships that could be constructed as a conflict of interest.

Data availability

The sequencing raw data has been uploaded to the Sequence Read Archive (https://www.ncbi.nlm.nih.gov/sra) under Bioproject PRJNA706111.

Additional information

Publisher's Note

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

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, H., Wu, W. Comparative transcriptome analysis reveals function of TERF1 in promoting seed germination. Physiol Mol Biol Plants 27, 1659–1674 (2021). https://doi.org/10.1007/s12298-021-01049-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12298-021-01049-4

Keywords

Search

Navigation