Skip to main content
Log in

MusaATAF2-like protein regulates shoot development and multiplication by inducing cytokinin hypersensitivity and flavonoid accumulation in banana plants

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Senescence-associated transcription factor ATAF2 regulates cytokinin signalling and in vitro shoot multiplication in banana plants.

Abstract

MusaATAF2-like protein is a stress-related NAC transcription factor of banana. It regulates senescence in rooted banana plants. During the early stages of plant development under in vitro conditions, the presence of 6-benzylaminopurine leads to vigorous shoot multiplication. The major contributor to plant shoot multiplication is auxin to cytokinin ratio and their signalling components. The LC–MS analysis of transgenic banana plants overexpressing MusaATAF2 indicated significantly higher cytokinin content and remarkably lower auxin content. Auxin transport has been reported to be inhibited by flavonoids. Their significantly higher abundance in the shoot tissues in transgenic lines suggested potential negative regulation of auxin signalling in transgenic plants. Enhanced shoot multiplication in transgenic lines was further corroborated by reduced transcript abundance of type-A Arabidopsis response regulator-like genes (inhibitors of cytokinin signalling pathway) and higher expression of Arabidopsis histidine kinase-like genes and type-B Arabidopsis response regulator-like genes (positive regulators of cytokinin signalling pathway) in transgenic lines. Altogether, the data concludes that MusaATAF2 induces cytokinin hypersensitivity in banana shoots by modulating/regulating the cytokinin signalling components and flavonoids content.

Graphical abstract

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

Similar content being viewed by others

Data availability

The complete coding sequence of MusaATAF2 has been deposited in NCBI database as a gene bank accession: MZ467048.

References

  • Bhakta S, Negi S, Tak H, Singh S, Ganapathi TR (2021) MusaATAF2 like protein, a stress-related transcription factor, induces leaf senescence by regulating chlorophyll catabolism and H2O2 accumulation. Physiol Plant. https://doi.org/10.1111/ppl.13593

    Article  PubMed  Google Scholar 

  • Brown DE, Rashotte AM, Murphy AS, Normanly J, Tague BW, Peer WA, Taiz L, Muday GK (2001) Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol 126:524–535

    Article  CAS  Google Scholar 

  • Cerbantez-Bueno VE, Zúñiga-Mayo VM, Reyes-Olalde JI, Lozano-Sotomayor P, Herrera-Ubaldo H, Marsch-Martinez N, de Folter S (2020) Redundant and non-redundant functions of the AHK cytokinin receptors during gynoecium development. Front Plant Sci 11:1534

    Article  Google Scholar 

  • Chapman JM, Muday GK (2021) Flavonols modulate lateral root emergence by scavenging reactive oxygen species in Arabidopsis thaliana. J Biol Chem. https://doi.org/10.1074/jbc.RA120.014543

    Article  PubMed  PubMed Central  Google Scholar 

  • Daimon Y, Takabe K, Tasaka M (2003) The CUP-SHAPED COTYLEDON genes promote adventitious shoot formation on calli. Plant Cell Physiol 44:113–121

    Article  CAS  Google Scholar 

  • Ganapathi TR, Higgs NS, Balint-Kurti PJ, Arntzen CJ, May GD, Van Eck JM (2001) Agrobacterium -mediated transformation of embryogenic cell suspensions of the banana cultivar Rasthali (AAB). Plant Cell Rep 20:157–162

    Article  CAS  Google Scholar 

  • Hejátko J, Ryu H, Kim G-T, Dobešová R, Choi S, Choi SM, Soucek P, Horák J, Pekárová B, Palme K (2009) The histidine kinases CYTOKININ-INDEPENDENT1 and ARABIDOPSIS HISTIDINE KINASE2 and 3 regulate vascular tissue development in Arabidopsis shoots. Plant Cell 21:2008–2021

    Article  Google Scholar 

  • Hernández I, Munné-Bosch S (2012) Naringenin inhibits seed germination and seedling root growth through a salicylic acid-independent mechanism in Arabidopsis thaliana. Plant Physiol Biochem 61:24–28

    Article  Google Scholar 

  • Heyl A, Schmülling T (2003) Cytokinin signal perception and transduction. Curr Opin Plant Biol 6:480–488

    Article  CAS  Google Scholar 

  • Hill K, Schaller GE (2013) Enhancing plant regeneration in tissue culture: a molecular approach through manipulation of cytokinin sensitivity. Plant Signal Behav 8:212–224

    Article  Google Scholar 

  • Hutchison CE, Kieber JJ (2002) Cytokinin signaling in Arabidopsis. Plant Cell 14:S47–S59

    Article  CAS  Google Scholar 

  • Hwang I, Sheen J (2001) Two-component circuitry in Arabidopsis cytokinin signal transduction. Nature 413:383–389

    Article  CAS  Google Scholar 

  • Kim HJ, Ryu H, Hong SH, Woo HR, Lim PO, Lee IC, Sheen J, Nam HG, Hwang I (2006) Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. Proc Natl Acad Sci 103:814–819

    Article  CAS  Google Scholar 

  • Leyser O (2009) The control of shoot branching: an example of plant information processing. Plant, Cell Environ 32:694–703

    Article  CAS  Google Scholar 

  • Liscum E, Reed JW (2002) Genetics of Aux/IAA and ARF action in plant growth and development. Plant Mol Biol 49:387–400

    Article  CAS  Google Scholar 

  • Mao C, He J, Liu L, Deng Q, Yao X, Liu C, Qiao Y, Li P, Ming F (2020) OsNAC2 integrates auxin and cytokinin pathways to modulate rice root development. Plant Biotechnol J 18:429–442

    Article  CAS  Google Scholar 

  • Mao C, Lu S, Lv B, Zhang B, Shen J, He J, Luo L, Xi D, Chen X, Ming F (2017) A rice NAC transcription factor promotes leaf senescence via ABA biosynthesis. Plant Physiol 174(3):1747–1763

    Article  CAS  Google Scholar 

  • Morishita T, Kojima Y, Maruta T, Nishizawa-Yokoi A, Yabuta Y, Shigeoka S (2009) Arabidopsis NAC transcription factor, ANAC078, regulates flavonoid biosynthesis under high-light. Plant Cell Physiol 50:2210–2222

    Article  CAS  Google Scholar 

  • Negi S, Tak H, Ganapathi TR (2015) In vitro xylem vessel elements formation from banana embryogenic cells and expression analysis of vessel development-related genes. Plant Biotechnol Rep 9:47–54

    Article  Google Scholar 

  • Negi S, Tak H, Ganapathi TR (2016) Expression analysis of MusaNAC68 transcription factor and its functional analysis by overexpression in transgenic banana plants. Plant Cell Tiss Organ Cult (PCTOC) 125:59–70

    Article  CAS  Google Scholar 

  • Negi S, Tak H, Ganapathi TR (2019) Overexpression of MusaNAC68 reduces secondary wall thickness of xylem tissue in banana. Plant Biotechnol Rep 13:151–160

    Article  Google Scholar 

  • Negi S, Tak H, Ganapathi TR (2021) Overexpression of MusaSNAC1 improves shoot proliferation in transgenic banana lines. 3 BIotech 11:1–9

    Article  Google Scholar 

  • Nguyen KH, Van Ha C, Nishiyama R, Watanabe Y, Leyva-González MA, Fujita Y, Tran UT, Li W, Tanaka M, Seki M (2016) Arabidopsis type B cytokinin response regulators ARR1, ARR10, and ARR12 negatively regulate plant responses to drought. Proc Natl Acad Sci 113:3090–3095

    Article  CAS  Google Scholar 

  • Patra B, Schluttenhofer C, Wu Y, Pattanaik S, Yuan L (2013) Transcriptional regulation of secondary metabolite biosynthesis in plants. Biochem Biophys Acta 1829:1236–1247

    CAS  PubMed  Google Scholar 

  • Riefler M, Novak O, Strnad M, Schmülling T (2006) Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18:40–54

    Article  CAS  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108

    Article  CAS  Google Scholar 

  • Tan X, Calderon-Villalobos LIA, Sharon M, Zheng C, Robinson CV, Estelle M, Zheng N (2007) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446:640–645

    Article  CAS  Google Scholar 

  • To JPC, Deruère J, Maxwell BB, Morris VF, Hutchison CE, Ferreira FJ, Schaller GE, Kieber JJ (2007) Cytokinin regulates type-A Arabidopsis response regulator activity and protein stability via two-component phosphorelay. Plant Cell 19:3901–3914

    Article  CAS  Google Scholar 

  • Wang J, Lian W, Cao Y, Wang X, Wang G, Qi C, Liu L, Qin S, Yuan X, Li X, Ren S, Guo Y-D (2018) Overexpression of BoNAC019, a NAC transcription factor from Brassica oleracea, negatively regulates the dehydration response and anthocyanin biosynthesis in Arabidopsis. Sci Rep 8:13349

    Article  Google Scholar 

  • Xie Q, Frugis G, Colgan D, Chua N-H (2000) Arabidopsis NAC1 transduces auxin signal downstream of TIR1 to promote lateral root development. Genes Dev 14:3024–3036

    Article  CAS  Google Scholar 

  • Yildiz M (2012) The prerequisite of the success in plant tissue culture: high frequency shoot regeneration. Recent advances in plant in vitro culture. Intech, Rijeka, pp 63–90

    Google Scholar 

Download references

Acknowledgements

The work was supported from the funding of Department of Atomic Energy, Government of India. SN thanks “Department of Science and Technology” (DST), New Delhi for DST INSPIRE faculty award.

Funding

The work was supported from the funding of Department of Atomic Energy, Government of India. SN thanks “Department of Science and Technology” (DST), New Delhi for DST INSPIRE faculty award.

Author information

Authors and Affiliations

Authors

Contributions

SB, SN, HT, SS and TG planned and designed the experiments. SB, SN and HT performed the experiments and analysed the data. SB, HT, SS and TG wrote the manuscript. All the authors have read and approved the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to T. R. Ganapathi.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Additional information

Communicated by Xian Sheng Zhang.

Publisher's Note

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

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 16 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bhakta, S., Negi, S., Tak, H. et al. MusaATAF2-like protein regulates shoot development and multiplication by inducing cytokinin hypersensitivity and flavonoid accumulation in banana plants. Plant Cell Rep 41, 1197–1208 (2022). https://doi.org/10.1007/s00299-022-02849-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-022-02849-y

Keywords

Navigation