Skip to main content
SpringerLink
Log in

Functional identification of apple Baby Boom in genetic transformation and somatic embryogenesis

  • Biotechnology
  • Published:
In Vitro Cellular & Developmental Biology - Plant Aims and scope Submit manuscript

Abstract 

Agrobacterium-mediated genetic transformation is inefficient in apple, which limits the development of apple-related research and industry. Using molecular methods to create a new and more efficient method of genetic transformation has become the focus of research, and improving the efficiency of the three key steps of transformation, regeneration, and rooting has become an effective means of achieving this goal. Baby Boom (BBM) is widely used in plant biotechnology as an important transcription factor regulating adventitious shoot regeneration and somatic embryogenesis. A homologous gene, MDP0000125317, with high amino acid sequence similarity to AtBBM was cloned in this study, and it was identified from the Royal Gala apple genome (Malus × domestica Borkh.), which was named as MdBBM. The qRT-PCR analysis revealed that MdBBM was expressed at higher levels in the ovary, roots, and seeds. Agrobacterium-mediated transformation of pRI101-MdBBM significantly improved the shoot regeneration efficiency in apples. In the experiment, 33 of the MdBBM-OE transformants were obtained. Compared with the control, only adventitious shoots were formed on the regeneration shoot medium. In vitro leaves of MdBBM-OE transformants were regenerated in three forms: adventitious shoots, adventitious roots, and somatic embryos. Overexpression of MdBBM promoted somatic embryogenesis under 2,4-dichlorophenoxyacetic acid (2,4-D) induction.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Figure 1.
Figure 2.
Figure 3.
Figure 4.
Figure 5.
Figure 6.
Figure 7.
Figure 8.
Figure 9.

Similar content being viewed by others

References 

  • Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh Y-S, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–120

    Article  CAS  PubMed  Google Scholar 

  • Bassuner BM, Lam R, Lukowitz W, Yeung EC (2007) Auxin and root initiation in somatic embryos of Arabidopsis. Plant Cell Rep 26:1–11

    Article  CAS  PubMed  Google Scholar 

  • Boutilier K, Offringa R, Sharma VK, Kieft H, Trs O, Zhang L, Hattori J, Liu C-M, van Lammeren AAM, Miki BLA, Custers JBM, van Lookeren Campagne MM (2002) Ectopic expression of Baby Boom triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bulley S, Malnoy M, Atkinson R, Hs A (2007) Transformed apples: traits of significance to growers and consumers. Transgenic Plant 1:267–279

    Google Scholar 

  • Chen J, Tomes S, Gleave AP, Hall W, Luo Z, Xu J, Yao J-L (2022) Significant improvement of apple (Malus domestica Borkh.) transgenic plant production by pre-transformation with a Baby Boom transcription factor. Hortic Res uhab014

  • de Vries SC, Weijers D (2017) Plant embryogenesis. Curr Biol 27:R870–R873

    Article  PubMed  Google Scholar 

  • Debernardi JM, Tricoli DM, Ercoli MF, Hayta S, Ronald P, Palatnik JF, Dubcovsky J (2020) A GRF–GIF chimeric protein improves the regeneration efficiency of transgenic plants. Nat Biotechnol 38:1274–1279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deng W, Luo K, Li Z, Yang Y (2009) A novel method for induction of plant regeneration via somatic embryogenesis. Plant Sci 177:43–48

    Article  CAS  Google Scholar 

  • El Ouakfaoui S, Schnell J, Abdeen A, Colville A, Labbé H, Han S, Baum B, Laberge S, Miki B (2010) Control of somatic embryogenesis and embryo development by AP2 transcription factors. Plant Mol Biol 74:313–326

    Article  PubMed  PubMed Central  Google Scholar 

  • Elliott RC, Betzner AS, Huttner E, Oakes MP, Tucker WQ, Gerentes D, Perez P, Smyth DR (1996) AINTEGUMENTA, an APETALA2-like gene of Arabidopsis with pleiotropic roles in ovule development and floral organ growth. Plant Cell 8:155–168

    CAS  PubMed  PubMed Central  Google Scholar 

  • Florez SL, Erwin RL, Maximova SN, Guiltinan MJ, Curtis WR (2015) Enhanced somatic embryogenesis in Theobroma cacao using the homologous Baby Boom transcription factor. BMC Plant Biol 15:121

    Article  PubMed  PubMed Central  Google Scholar 

  • Heidmann I, Boutilier K (2015) Pepper, sweet (Capsicum annuum). In: Agrobacterium protocols: Volume 1. Wang K (ed.). Springer New York: New York, NY, pp. 321–334

  • Horstman A, Bemer M, Boutilier K (2017) A transcriptional view on somatic embryogenesis. Regeneration 4:201–216

    Article  PubMed  PubMed Central  Google Scholar 

  • Horstman A, Fukuoka H, Muino JM, Nitsch L, Guo C, Passarinho P, Sanchez-Perez G, Immink R, Angenent G, Boutilier K (2015) AIL and HDG proteins act antagonistically to control cell proliferation. Development 142:454–464

    CAS  PubMed  Google Scholar 

  • Horstman A, Willemsen V, Boutilier K, Heidstra R (2014) AINTEGUMENTA-LIKE proteins: hubs in a plethora of networks. Trend Plant Sci 19:146–157

    Article  CAS  Google Scholar 

  • Jha P, Kumar V (2018) Baby Boom (BBM): a candidate transcription factor gene in plant biotechnology. Biotechnol Lett 40:1467–1475

    Article  CAS  PubMed  Google Scholar 

  • Karami O, Rahimi A, Mak P, Horstman A, Boutilier K, Compier M, van der Zaal B, Offringa R (2021) An Arabidopsis AT-hook motif nuclear protein mediates somatic embryogenesis and coinciding genome duplication. Nat Commun 12:2508

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim S, Soltis PS, Wall K, Soltis DE (2006) Phylogeny and domain evolution in the APETALA2-like gene family. Mol Biol Evol 23:107–120

    Article  CAS  PubMed  Google Scholar 

  • Klucher KM, Chow H, Reiser L, Fischer RL (1996) The AINTEGUMENTA gene of Arabidopsis required for ovule and female gametophyte development is related to the floral homeotic gene APETALA2. Plant Cell 8:137–153

    CAS  PubMed  PubMed Central  Google Scholar 

  • Krizek BA (2011) Auxin regulation of Arabidopsis flower development involves members of the AINTEGUMENTA-LIKE/PLETHORA (AIL/PLT) family. J Exp Bot 62:3311–3319

    Article  CAS  PubMed  Google Scholar 

  • Li K-p, Sun X-m, Han H, Zhang S-g (2014) Isolation, characterization and expression analysis of the Baby Boom (BBM) gene from Larix kaempferi×L. olgensis during adventitious rooting. Gene 551:111–118

    Article  CAS  PubMed  Google Scholar 

  • Li M, Wrobel-Marek J, Heidmann I, Horstman A, Chen B, Reis R, Angenent GC, Boutilier K (2022) Auxin biosynthesis maintains embryo identity and growth during Baby Boom-induced somatic embryogenesis. Plant Physiol 188:1095–1110

    Article  CAS  PubMed  Google Scholar 

  • Lowe K, La Rota M, Hoerster G, Hastings C, Wang N, Chamberlin M, Wu E, Jones T, Gordon-Kamm W (2018) Rapid genotype “independent” Zea mays L. (maize) transformation via direct somatic embryogenesis. In Vitro Cell Dev Biol - Plant 54:240–252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lowe K, Wu E, Wang N, Hoerster G, Hastings C, Cho M-J, Scelonge C, Lenderts B, Chamberlin M, Cushatt J, Wang L, Ryan L, Khan T, Chow-Yiu J, Hua W, Yu M, Banh J, Bao Z, Brink K, Igo E, Rudrappa B, Shamseer PM, Bruce W, Newman L, Shen B, Zheng P, Bidney D, Falco C, Register J, Zhao Z-Y, Xu D, Jones T, Gordon-Kamm W (2016) Morphogenic regulators Baby boom and Wuschel improve monocot transformation. Plant Cell 28:1998–2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsuo N, Mase H, Makino M, Takahashi H, Banno H (2009) Identification of ENHANCER OF SHOOT REGENERATION 1-upregulated genes during in vitro shoot regeneration. Plant Biotechnol 26:385–393

    Article  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nelson-Vasilchik K, Hague JP, Tilelli M, Kausch AP (2022) Rapid transformation and plant regeneration of sorghum (Sorghum bicolor L.) mediated by altruistic Baby boom and Wuschel2. In Vitro Cell Dev Biol - Plant 58:331–342

    Article  CAS  Google Scholar 

  • Nole-Wilson S, Tranby TL, Krizek BA (2005) AINTEGUMENTA-like (AIL) genes are expressed in young tissues and may specify meristematic or division-competent states. Plant Mol Biol 57:613–628

    Article  CAS  PubMed  Google Scholar 

  • Passarinho P, Ketelaar T, Xing M, van Arkel J, Maliepaard C, Hendriks MW, Joosen R, Lammers M, Herdies L, den Boer B, van der Geest L, Boutilier K (2008) Baby Boom target genes provide diverse entry points into cell proliferation and cell growth pathways. Plant Mol Biol 68:225–237

    Article  CAS  PubMed  Google Scholar 

  • Rupps A, Raschke J, Rümmler M, Linke B, Zoglauer K (2016) Identification of putative homologs of Larix decidua to Baby Boom (BBM), LEAFY COTYLEDON1 (LEC1), WUSCHEL-related HOMEOBOX2 (WOX2) and SOMATIC EMBRYOGENESIS RECEPTOR-like KINASE (SERK) during somatic embryogenesis. Planta 243:473–488

    Article  CAS  PubMed  Google Scholar 

  • Sánchez-Romero C (2021) Somatic Embryogenesis in Olive. Plants 10:187–202

    Article  Google Scholar 

  • Scheres B, Krizek BA (2018) Coordination of growth in root and shoot apices by AIL/PLT transcription factors. Curr Opin Plant Biol 41:95–101

    Article  CAS  PubMed  Google Scholar 

  • von Arnold S, Sabala I, Bozhkov P, Dyachok J, Filonova L (2002) Developmental pathways of somatic embryogenesis. Plant Cell Tiss Org Cult 69:233–249

    Article  Google Scholar 

  • Wójcik AM, Wójcikowska B, Gaj MD (2020) Current perspectives on the auxin-mediated genetic network that controls the induction of somatic embryogenesis in plants. Int J Mol Sci 21:1333

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang HF, Kou YP, Gao B, Soliman TMA, Xu KD, Ma N, Cao X, Zhao LJ (2014) Identification and functional analysis of Baby Boom genes from Rosa canina. Biol Plant 58:427–435

    Article  CAS  Google Scholar 

  • Zhang C-L, Mao K, Zhou L-J, Wang G-L, Zhang Y-L, Li Y-Y, Hao Y-J (2018) Genome-wide identification and characterization of apple long-chain Acyl-CoA synthetases and expression analysis under different stresses. Plant Physiol Biochem 132:320–332

    Article  CAS  PubMed  Google Scholar 

  • Zhou L-J, Mao K, Qiao Y, Jiang H, Li Y-Y, Hao Y-J (2017) Functional identification of MdPIF1 as a phytochrome interacting factor in apple. Plant Physiol Biochem 119:178–188

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was financially supported by grants from the National Key Research and Development Program (2018YFD1000200), the China Agriculture Research System of MOF and MARA (CARS-27), and the Agricultural Variety Improvement Project of Shandong Province (2019LZGC007).

Author information

Authors and Affiliations

  1. State Key Laboratory of Crop Biology, College of Horticulture Science and Engineering, Shandong Agricultural University, Tai’an, China

    Xu Xiao, Chunling Zhang, Yang Liu, Xiaofei Wang & Chunxiang You

Authors
  1. Xu Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chunling Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaofei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chunxiang You
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chunxiang You.

Supplementary Information

Below is the link to the electronic supplementary material.

ESM 1

(DOCX 459 KB)

Rights and permissions

Springer Nature or its licensor 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

Xiao, X., Zhang, C., Liu, Y. et al. Functional identification of apple Baby Boom in genetic transformation and somatic embryogenesis. In Vitro Cell.Dev.Biol.-Plant 59, 1–13 (2023). https://doi.org/10.1007/s11627-022-10292-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11627-022-10292-7

Keywords

Search

Navigation