Skip to main content
SpringerLink
Log in

Identification of a novel promoter region responsible for the embryo-specific expression of SERK1 in pineapple

  • Research Report
  • Published:
Horticulture, Environment, and Biotechnology Aims and scope Submit manuscript

Abstract

Somatic embryogenesis (SE) is a key regeneration process in plant. AcSERK1 is a gene specifically expressed in the early stage of SE in pineapple (Ananas comosus), suggesting that the promoter of SERK1 might contain specific cis-acting element regulating SE. To identify embryonic cell-specific element in the SERK1 promoter, a series of binary plant transformation vectors with GUS (β-glucuronidase) reporter gene were systematically analyzed by transient gene expression system in wild-type and transgenic pineapple embryogenic callus. Histochemical and quantitative GUS assays demonstrated that the activity of the AcSERK1 upstream regulatory sequence lacking − 921 to -911 or -910 to -880 was significantly reduced in the embryonic callus of the pineapple, and these two regions were needed for the embryonic cell-specific. Besides, a promoter lacking − 943 to -922 was shown to significantly increase GUS activity in embryogenic callus, suggesting repressive elements exist in this region. Our data of stable transformation assays confirmed again the 5’ upstream regulatory sequence (-921 to -880) of the AcSERK1 gene is an essential functional region. Our findings lay the basis for better understanding of the molecular mechanisms of AcSERK1 gene in the regulation in early stage of SE.

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

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

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this published article.

References

  • Allen RD, Bernier F, Lessard PA, Beachy RN (1989) Nuclear factors interact with a soybean -conglycinin enhancer. Plant Cell 1:623–631

    PubMed  PubMed Central  Google Scholar 

  • Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208

    PubMed  PubMed Central  Google Scholar 

  • Bhuria M, Goel P, Kumar S, Singh AK (2016) The promoter of AtUSP is cco-regulated by phytohormones and abiotic stresses in arabidopsis thaliana. Front Plant Sci 7:1957

    PubMed  PubMed Central  Google Scholar 

  • Boutilier K, Offringa R, Sharma VK, Kieft H, Ouellet T, Zhang L, Hattori J, Liu CM, van Lammeren AA, Miki BL, Custers JB, van Lookeren Campagne MM (2002) Ectopic expression of BABY BOOM triggers a conversion from vegetative to embryonic growth. Plant Cell 14:1737–1749

    PubMed  PubMed Central  Google Scholar 

  • Braybrook SA, Harada JJ (2008) LECs go crazy in embryo development. Trends Plant Sci 13:624–630

    PubMed  Google Scholar 

  • Calheiros MBP, Vieira LGE, Fuentes SRL (1994) Effects of exogenous polyamines on direct somatic embryogenesis in coffee. Bras Fisiol Veg 6:109–114

    Google Scholar 

  • Ciolkowski I, Wanke D, Birkenbihl RP, Somssich IE (2008) Studies on DNA-binding selectivity of WRKY transcription factors lend structural clues into WRKY-domain function. Plant Mol Biol 68:81–92

    PubMed  PubMed Central  Google Scholar 

  • de Silva KK, Dunwell JM, Wickramasuriya AM (2022) Weighted gene correlation Network Analysis (WGCNA) of Arabidopsis somatic embryogenesis (SE) and identification of key gene modules to uncover SE-associated hub genes

  • Elhiti M, Stasolla C (2013) Wang A.M. Molecular regulation of plant somatic embryogenesis. In Vitro Cell Dev Biol Plant 49:631–642

    Google Scholar 

  • Elmayan T, Tepfer M (1995) Evaluation in tobacco of the organ specificity and strength of the rolD promoter, domain a of the 35S promoter and the 35S2 promoter. Transgenic Res 4:388–396

    PubMed  Google Scholar 

  • Fatihi A, Boulard C, Bouyer D, Baud S, Dubreucq B, Lepiniec L (2016) Deciphering and modifying LAFL transcriptional regulatory network in seed for improving yield and quality of storage compounds. Plant Sci 250:198–204

    PubMed  Google Scholar 

  • Gaj MD, Zhang S, Harada JJ, Lemaux PG (2005) Leafy cotyledon genes are essential for induction of somatic embryogenesis of Arabidopsis. Planta 222:977–988

    PubMed  Google Scholar 

  • Gao Y, Zan XL, Wu XF, Yao L, Chen YL, Jia SW, Zhao KJ (2014) Identification of fungus-responsive cis-acting element in the promoter of Brassica juncea chitinase gene, BjCHI1. Plant Sci 215:190–198

    PubMed  Google Scholar 

  • Grosveld F, van Staalduinen J, Stadhouders R (2021) Transcriptional regulation by (Super) Enhancers: from Discovery to Mechanisms. Annu Rev Genom Hum Genet 22

  • He YH, Luo J, Wu HT, Wang RX, Gao AP, Zhao CX, Yu XL, Ye ZX, Wang ZH, Han JZ, Liu HP (2007) Somatic embryogenesis from leaf base callus of Ananas comosus. Fruit Sci 24:59–63

    Google Scholar 

  • Hecht V, Vielle-Calzada JP, Hartog MV, Schmidt ED, Boutilier K, Grossniklaus U, de Vries SC (2001) The Arabidopsis SOMATIC EMBRYOGENESIS RECEPTOR KINASE 1 gene is expressed in developing ovules and embryos and enhances embryogenic competence in culture. Plant physiol 127:803–816

    PubMed  PubMed Central  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300

    PubMed  PubMed Central  Google Scholar 

  • Horstman A, Li MF, Heidmann I, Weemen MK, Chen BJ, Muino JM, Angenent GC, Boutilier K (2017) The BABY BOOM transcription factor activates the LEC1-ABI3-FUS3-LEC2 network to induce somatic embryogenesis. Plant Physiol 175:848–857

    PubMed  PubMed Central  Google Scholar 

  • Ikeda M, Mitsuda N, Ohme-Takagi M (2009) Arabidopsis WUSCHEL is a bifunctional transcription factor that acts as a repressor in stem cell regulation and as an activator in floral patterning. Plant Cell 21:3493–3505

    PubMed  PubMed Central  Google Scholar 

  • Ikeda M, Takahashi M, Fujiwara S, Mitsuda N, Ohme-Takagi M (2020) Improving the efficiency of adventitious shoot induction and somatic embryogenesis via modification of WUSCHEL and LEAFY COTYLEDON 1. Plants 9:1434

    PubMed  PubMed Central  Google Scholar 

  • Ikeuchi M, Sugimoto K, Iwase A (2013) Plant callus: mechanisms of induction and repression. Plant Cell 25:3159–3173

    PubMed  PubMed Central  Google Scholar 

  • Jiménez-Guillen D, Pérez-Pascual D, Souza-Perera R, Godoy-Hernández G, Zúñiga-Aguilar JJ (2018) Cloning of the Coffea canephora SERK1 promoter and its molecular analysis during the cell-to-embryo transition. Electron J Biotechnol 36:34–46

    Google Scholar 

  • Kithmee KDS, Jim MD, Anushka MW (2022) Weighted Gene Correlation Network Analysis (WGCNA) of Arabidopsis Somatic Embryogenesis (SE) and Identification of Key Gene Modules to Uncover SE-Associated Hub Genes”, International Journal of Genomics, vol. 2022, Article ID 7471063, 24 pages

  • Lescot M, De’hais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouz P, Rombauts S (2002) Plant CARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327

    PubMed  PubMed Central  Google Scholar 

  • Li MF, Wrobel-Marek J?Heidmann I, Horstman A, Chen BJ, 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

  • Liu ZZ, Wang JL, Huang X, Xu WH, Liu ZM, Fang RX (2003) The promoter of a rice glycine-rich protein gene, Osgrp-2, confers vascular-specific expression in transgenic plants. Planta 216:824–833

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Lotan T, Ohto M, Yee KM, West MAL, Lo R, Kwong RW, Yamagishi K, Fischer RL, Goldberg RB, Harada JJ (1998) Arabidopsis LEAFY COTYLEDON1 is sufficient to induce embryo development in vegetative cells. Cell 93:1195–1205

    PubMed  Google Scholar 

  • Loyolavargas V, Delapeña C, Galazávalos R, Quirozfigueroa F (2008) Plant tissue culture. In: Walker J, Rapley R (eds) Molecular Biomethods Handbook, 2nd edn. Humana Press, New York, NY, USA, pp 875–904

    Google Scholar 

  • Luan AP, He YH, Lin WQ, Chen CJ, Feng JT, Xie T, Gong X, Xia JX (2016) Identification of transcription start site of AcSERK1 and its embryo specific cell promoter in pineapple. J Hortic 43:2251–2256

    Google Scholar 

  • Luan AP, He YH, Xie T, Chen CJ, Mao Q, Wang XS, Li CH, Ding YQ, Lin WQ, Liu C, Xia JX, He JH (2019) Identification of an embryonic cell-specific region within the pineapple SERK1 promoter. Genes 10:883

    PubMed  PubMed Central  Google Scholar 

  • Luan AP, Chen CJ, Xie T, He JH, He YH (2020) Methylation analysis of CpG islands in pineapple SERK1 promoter. Genes 2020, 11: 425–435

  • Ma J, He Y, Wu C, Liu H, Hu Z, Sun G (2012) Cloning and molecular characterization of a SERK gene transcriptionally induced during somatic embryogenesis in Ananas comosus cv. Shenwan. Plant Mol Biol Rep 30:195–203

    Google Scholar 

  • Ma J, He YH, Hu ZY, Xu WT, Xia JX, Guo CH, Lin SQ, Chen CJ, Wu CH, Zhang JL (2014) Characterization of the third SERK gene in pineapple (Ananas comosus) and analysis of its expression and autophosphorylation activity in vitro. Genet Mol biology 37:530–539

    Google Scholar 

  • Manisha V, Bansal YK (2004) Somatic embryogenesis and plantlet regeneration in semul (Bombax ceiba). Plant Cell Tiss Organ Cult 79:115–118

    Google Scholar 

  • Mariashibu TS, Subramanyam K, Arun M, Mayavan S, Rajesh M, Theboral J, Manickavasagam M, Ganapathi A (2013) Vacuum infiltration enhances the Agrobacterium-mediated genetic transformation in indian soybean cultivars. Acta Physiol Plant 35:41–54

    Google Scholar 

  • Mathew MW, Philip VJ (2003) Somatic embryogenesis versus zygotic embryogenesis in Ensete superbum. Plant Cell Tiss Organ Cult 72:267–275

    Google Scholar 

  • Mozgová I, Muñoz-Viana R, Hennig L (2017) PRC2 represses Hormone-Induced somatic embryogenesis in vegetative tissue of Arabidopsis thaliana. PLoS Genet 13:e1006562

    PubMed  PubMed Central  Google Scholar 

  • Nic-Can GI, Pena C (2014) Epigenetic advances on somatic embryogenesis of agronomical and important crops. In: Alvarez-Venegas R (ed) Epigenetics in plants of agronomic importance: Fundamentals and Applications, 6th edn. Springer International Publishing, Berlin, Germany, pp 91–109

    Google Scholar 

  • Nolan KE, Kurdyukov S, Rose RJ (2009) Expression of the SOMATIC EMBRYOGENESIS RE-CEPTOR-LIKE KINASE1 (SERK1) gene is associated with developmental change in the life cycle of the model legume Medicago truncatula. J Exp Bot 60:1759–1771

    PubMed  PubMed Central  Google Scholar 

  • Pandey DK, Chaudhary B (2014) Oxidative stress responsive SERK1 gene directs the progression of somatic embryogenesis in cotton (Gossypium hirsutum L. cv. Coker 310). Am J Plant Sci 2014:80–102

    Google Scholar 

  • Paul P, Joshi S, Tian R, Junior RD, Manohar Chakrabarti M, Perry SE (2022) The MADS-domain factor AGAMOUS-Like18 promotes somatic embryogenesis. Plant Physiol 188:1617–1631

  • Pérez-Pascual D, Jiménez‐Guillen D, Villanueva‐Alonzo H, Souza‐Perera R, Godoy‐Hernández G, Zúñiga‐Aguilar JJ (2018) Ectopic expression of the Coffea canephora SERK1 homolog‐induced differential transcription of genes involved in auxin metabolism and in the developmental control of embryogenesis. Physiol Plant 163:530–551

    PubMed  Google Scholar 

  • Reinert J (1958) Under the control of the morphogenes and the induction of adventive embryos into tissues of litres of carrots. Plant 53:318–333

    Google Scholar 

  • Rocha DI, Pinto DL, Vieira LM, Tanaka FA, Dornelas MC, Otoni WC (2016) Cellular and molecular changes associated with competence acquisition during passion fruit somatic embryogenesis: ultrastructural characterization and analysis of SERK gene expression. Protoplasma 253:595–609

    PubMed  Google Scholar 

  • Sakhanokho H, Rajasekaran K (2016) Cotton regeneration in vitro. In: Ramawat KG, Ahuja MR (eds) Fiber plants. Springer, Berlin, Germany, pp 87–110

    Google Scholar 

  • Santos MO, Aragão FJL (2009) Role of SERK genes in plant environmental response. Plant Signal Behav 4:1111–1113

    PubMed  PubMed Central  Google Scholar 

  • Schmidt E, Guzzo F, Toonen MA, De Vries SC (1997) A leucine-rich repeat containing receptor-like kinase marks somatic plant cells competent to form embryos. Development 124:2049–2062

    PubMed  Google Scholar 

  • Serfling E, Jasin M, Schaffner W (1985) Enhancers and eukaryotic gene transcription. Trends Genet 1:224–230

    Google Scholar 

  • Shirsat A, Wilford N, Croy R, Boulter D (1989) Sequences responsible for the tissue specific promoter activity of a pea legumin gene in tobacco. Mol Gen Genet MGG 215:326–331

    PubMed  Google Scholar 

  • Singh A, Khurana P (2017) Ectopic expression of Triticum aestivum SERK genes (TaSERKs) control plant growth and development in Arabidopsis. Sci Rep 7:12368

    PubMed  PubMed Central  Google Scholar 

  • Steiner N, Santa-Catarina C, Guerra MP, Cutri L, Dornelas MC, Floh EI (2012) A gymnosperm homolog of SOMATIC EMBRYOGENESIS RECEPTOR-LIKE KINASE-1 (SERK1) is expressed during somatic embryogenesis. Plant Cell Tiss Organ Cult 109:41–50

    Google Scholar 

  • Steward FC, Mapes MO, Smith J (1958) Growth and organized development of cultured cells I. Growth and division of freely suspended cells. Am J Bot 45:693–703

    Google Scholar 

  • Talukder P, Mitra D (2020) Expression of somatic embryogenesis receptor kinase (SERK) gene and its regulation under the influence of exogenous additives during in vitro somantic embryo development in medicinal plants. Am J Appl Biotechnol Res 1:1–10

    Google Scholar 

  • Vogel G (2005) How does a single somatic cell become a whole plant? Science 309:86

    PubMed  Google Scholar 

  • Wang H, Han J, Kanagarajan S, Lundgren A, Brodelius PE (2013) Trichome-specific expression of the amorpha-4,11-diene 12-hydroxylase (cyp71av1) gene, encoding a key enzyme of artemisinin biosynthesis in Artemisia annua, as reported by a promoter-gus fusion. Plant Mol Biol 81:119–138

    PubMed  Google Scholar 

  • Xiao Y, Chen Y, Ding Y, Wu J, Wang P, Yu Y, Ge X (2018) Effects of GhWUS from upland cotton (Gossypium hirsutum L.) on somatic embryogenesis and shoot regeneration. Plant Sci 270:157–165

    PubMed  Google Scholar 

  • Xie T, Chen CJ, Li CH, Liu JR, Liu CY, He YH (2018) Genome-wide investigation of WRKY gene family in pineapple: evolution and expression profiles during development and stress. BMC Genomics 19:490

    Google Scholar 

  • Yadak JS, Rajam MV (1997) Spatial distribution of free and conjugated polyamines in leaves of Solanum melongena L. associated with differential morphogenetic capacity: efficient somatic embryogenesis with putrescine. J Exp Bot 48:1537–1545

    Google Scholar 

  • Yang F, Xia XR, Ke X, Ye J, Zhu LH (2020a) Somatic embryogenesis in slash pine (Pinus elliottii Engelm): improving initiation of embryogenic tissues and maturation of somatic embryos. Plant Cell Tiss Organ Cult 143:159–171

    Google Scholar 

  • Yang Y, Wang N, Zhao S (2020b) Functional characterization of a WRKY family gene involved in somatic embryogenesis in Panax ginseng. Protoplasma 257:449–458

    PubMed  Google Scholar 

  • Zakizadeh H, Stummann BM, Lutken H, Muller R (2010) Isolation and characterization of four somatic embryogenesis receptor-like kinase (RhSERK) genes from miniature potted rose (Rosa hybrida cv. Linda). Plant Cell Tissue Organ cult 101:331–338

    Google Scholar 

  • Zeng F, Zhang X, Cheng L, Hu L, Zhu L, Cao J, Guo X (2007) A draft gene regulatory network for cellular totipotency reprogramming during plant somatic embryogenesis. Genomics 90:620–628

    PubMed  Google Scholar 

  • Zhang ZL, Xie Z, Zou X, Casaretto J, Ho TH, Shen QJ (2004) A rice WRKY gene encodes a transcriptional repressor of the gibberellin signaling pathway in aleurone cells. Plant Physiol 134:1500–1513

    PubMed  PubMed Central  Google Scholar 

  • Zhao DM, Zheng YX, Yang LG, Yao ZY, Cheng JF, Zhang F, Jiang HY, Liu D (2021) The transcription factor AtGLK1 acts upstream of MYBL2 to genetically regulate sucrose-induced anthocyanin biosynthesis in Arabidopsis. BMC Plant Biol 21:1–14

    Google Scholar 

  • Zuo J, Niu QW, Frugis G, Chua NH (2002) The WUSCHEL gene promotes vegetative-to-embryonic transition in Arabidopsis. Plant J 30:349–359

    PubMed  Google Scholar 

Download references

Acknowledgements

This research was financially supported by the National Natural Science Foundation of China (No. 32101584), Natural Science Foundation of Guangdong Province (2020A1515110331), and Rural Revitalization Strategy Special Fund Seed Industry Revitalization Project of Guangdong Province (2022-NPY-00-031). The authors acknowledge support from National Tropical Plants Germplasm Resource Center.

Author information

Authors and Affiliations

  1. Department of Horticulture, Foshan University, 528231, Foshan, China

    Tao Xie & Jing Zhang

  2. Key Laboratory of Biology and Germplasm Enhancement of Horticultural Crops in South China, Ministry of Agriculture, South China Agricultural University, 510642, Guangzhou, China

    Tao Xie, Wei Zhang, Chengjie Chen, Xiaoshuang Wang & Yehua He

  3. Tropical Crops Genetic Resources Institute of Chinese Academy of Tropical Agricultural Science, 571101, Haikou, China

    Aiping Luan

  4. College of Horticulture, South China Agricultural University, 510642, Guangzhou, China

    Yehua He

Authors
  1. Tao Xie
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chengjie Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Xiaoshuang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jing Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Aiping Luan
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yehua He
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Y.-H.H. and T.X. conceived the research plan and designed the study. T.X. performed most of the experiments and data analysis. A.-P.L., C.-J.C., X.-S.W. and C.-Y.L. carried out part of material preparation. T.X. and Y.-H.H. wrote the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Yehua He.

Ethics declarations

Conflict of interest

There is no conflict of interest between the authors.

Additional information

Communicated by Cecile Segonzac.

Publisher’s Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Material 1

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

Xie, T., Zhang, W., Chen, C. et al. Identification of a novel promoter region responsible for the embryo-specific expression of SERK1 in pineapple. Hortic. Environ. Biotechnol. 64, 1071–1082 (2023). https://doi.org/10.1007/s13580-023-00542-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13580-023-00542-x

Keywords

Search

Navigation