Skip to main content
SpringerLink
Log in

Overexpression of Oil Palm Early Nodulin 93 Protein Gene (EgENOD93) Enhances In Vitro Shoot Regeneration in Arabidopsis thaliana

  • Original Paper
  • Published:
Molecular Biotechnology Aims and scope Submit manuscript

Abstract

EgENOD93 was first identified in a cDNA microarray study of oil palm tissue culture where it was highly expressed in leaf explants with embryogenic potential. Functional characterization via an RNA interference study of its orthologue in Medicago truncatula demonstrated a significant role of this gene in somatic embryo formation. In this study, EgENOD93 was overexpressed in the important model plant Arabidopsis thaliana to investigate the embryogenic potential of EgENOD93 transgenic Arabidopsis explants compared to explants from control plants (pMDC140 and WT). Experiments using leaf explants revealed higher numbers of regenerated shoots at day 27 in all the homozygous transgenic Arabidopsis cultures (Tg01, Tg02 and Tg03) compared to controls. The expression level of EgENOD93 in Arabidopsis cultures was quantified using reverse transcription quantitative real-time PCR (RT-qPCR). The results supported the overexpression of this gene in transgenic Arabidopsis cultures, with 6 and 10 times higher expression of EgENOD93 in callus at Day 9 and Day 20, respectively. Overall, the results support the role of EgENOD93 in the enhancement of shoot regeneration in transgenic Arabidopsis. This together with the previous results observed in oil palm and Medicago truncatula suggests that ENOD93 plays a key role in the induction of somatic embryogenesis. A similarity to early nodulation-like ontogeny is possible.

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
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

Data Availability

The complete CDS of EgENOD93 (accession number MT813427.1) has been submitted to GenBank.

References

  1. Low, E. T. L., Jayanthi, N., Chan, K. L., Mohd, N. S. N., Halim, M. A. A., Rosli, R., Azizi, N., Amiruddin, N., Angel, L. P. L., Ong-Abdullah, M., Singh, R., Abd Manaf, M. A., Sambanthamurthi, R., Parveez, G. K. A., & Kushairi, A. (2017). The oil palm genome revolution. Journal of Oil Palm Research, 29(4), 456–468. https://doi.org/10.21894/jopr.2017.00018

    Article  CAS  Google Scholar 

  2. Parveez, G. K. A., Hishamuddin, E., Loh, S. K., Ong-Abdullah, M., Salleh, K. M., Zanal Bidin, M. N. I., Sundram, S., Azizul Hasan, Z. A., & Idris, Z. (2020). Oil palm economics performance in Malaysia and R&D progress in 2019. Journal of Oil Palm Research, 32(2), 159–190. https://doi.org/10.21894/jopr.2020.0032

    Article  Google Scholar 

  3. Awalludin, M. F., Sulaiman, O., Hashim, R., & Nadhari, W. N. A. W. (2015). An overview of the oil palm industry in Malaysia and its waste utilization through thermochemical conversion, specifically via liquefaction. Renewable and Sustainable Energy Reviews, 50, 1469–1484. https://doi.org/10.1016/j.rser.2015.05.085

    Article  CAS  Google Scholar 

  4. Kushairi, A., Tarmizi, A.H., Zamzuri, I., Ong-Abdullah, M., Samsul Kamal, R., Ooi, S.E., & Rajanaidu, N. (2010). Production, performance and advances in oil palm tissue culture. Proceeding of the International Seminar On Advances In Oil Palm Tissue Culture, Yogyakarta, Indonesia. pp. 1–23.

  5. Chan, P-L., Rose, R. J., Murad, A. M., Zainal, Z., Low, E. T. L., Ooi, L. C. L., Ooi, S. E., Yahya, S., & Singh, R. (2014). Evaluation of reference genes for quantitative real-time PCR in oil palm elite planting materials propagated by tissue culture. PLoS ONE, 9(6), e99774. https://doi.org/10.1371/journal.pone.0110079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Kushairi, A., Singh, R., & Ong-Abdullah, M. (2017). The oil palm industry in Malaysia: Thriving with transformative technologies. Journal of Oil Palm Research, 29(4), 431–439.

    Google Scholar 

  7. Jones, L. H. (1974). Propagation of clonal oil palms by tissue culture. Oil Palm News, 17, 1–8.

    Google Scholar 

  8. Zamzuri, I., Tarmizi, A. H., & Rajinder, S. (2007). Improving the efficiency of oil palm tissue culture. Oil Palm Bulletin, 55, 26–30.

    Google Scholar 

  9. Corley, R.H.V., & Law, I.H. (1997). The future for oil palm clones. Proceedings of the International Planters Conference. Incorporated Society, Kuala Lumpur, Malaysia. pp. 279–289.

  10. Rajanaidu, N., Rohani, O., & Jalani, B. S. (1997). Oil palm clones: Current status and prospects for commercial production. Planter, 73(853), 163–184.

    Google Scholar 

  11. Corley, R. H. V., Lee, C. H., Law, I. M., & Wong, C. Y. (1986). Abnormal flower development in oil palm clones. Planter, 62(723), 233–240.

    Google Scholar 

  12. Ong-Abdullah, M., Ordway, J. M., Jiang, N., Ooi, S. E., Kok, S. Y., Sarpan, N., Azimi, N., Hashim, A. T., Ishak, Z., Rosli, S. K., Malike, F. A., Bakar, N. A., Marjuni, M., Abdullah, N., Yaakub, Z., Amiruddin, M. D., Nookiah, R., Singh, R., Low, E. T., … Martienssen, R. A. (2015). Loss of Karma transposon methylation underlies the mantled somaclonal variant of oil palm. Nature, 525(7570), 533–537. https://doi.org/10.1038/nature15365

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Ong, L.M. (2001). An examination of embryogenic and non-embryogenic cultures of oil palm (Elaeis guineensis). PhD thesis, Universiti Putra Malaysia, Selangor, Malaysia.

  14. Morcillo, F., Gallard, A., Pillot, M., Jouannic, S., Aberlenc-Bertossi, F., Collin, M., Verdeil, J. L., & Tregear, J. W. (2007). EgAP2-1, an AINTEGUMENTA-like (AIL) gene expressed in meristematic and proliferating tissues of embryos in oil palm. Planta, 226(6), 1353–1362. https://doi.org/10.1007/s00425-007-0574-3

    Article  CAS  PubMed  Google Scholar 

  15. Roowi, S. H., Ho, C. L., Alwee, S. S. R. S., Ong-Abdullah, M., & Napis, S. (2010). Isolation and characterization of differentially expressed transcripts from the suspension cells of oil palm (Elaeis guineensis Jacq.) in response to different concentration of auxins. Molecular Biotechnology, 46(1), 1–19. https://doi.org/10.1007/s12033-010-9262-9

    Article  CAS  PubMed  Google Scholar 

  16. Thuc, L. V., Sarpan, N., Ky, H., Ooi, S. E., Napis, S., Ho, C-L., Ong-Abdullah, M., Chin, C-F., & Namasivayam, P. (2011). A novel transcript of oil palm (Elaeis guineensis Jacq.), Eg707, is specifically upregulated in tissues related to totipotency. Molecular Biotechnology, 48, 156–164. https://doi.org/10.1007/s12033-010-9356-4

    Article  CAS  Google Scholar 

  17. Ooi, S-E., Choo, C-N., Ishak, Z., & Ong-Abdullah, M. A. (2012). A candidate auxin responsive expression marker gene, EgIAA9, for somatic embryogenesis in oil palm (Elaeis guineensis Jacq.). Plant Cell, Tissue and Organ Culture, 110(2), 201–212. https://doi.org/10.1007/s11240-012-0143-8

    Article  CAS  Google Scholar 

  18. Ooi, S. E., Low, E. T. L., Chan, P. L., Ooi, C. L. L., Ishak, F., Kadri, F., Singh, R., & Ong-Abdullah, M. (2010). First generation embryogenic markers (GEM) for tissue culture amenity. MPOB information series No. 508, MPOB TT No. 452. MPOB.

    Google Scholar 

  19. Chan, P-L. (2017). Isolation and characterization of genes associated with somatic embryogenesis in oil palm (Elaeis guineensis). PhD, Universiti Kebangsaan Malaysia, Selangor, Malaysia.

  20. Chan, P-L., Rose, R. J., Abdul Murad, A. M., Zainal, Z., Ong, P-W., Ooi, L. C. L., Low, E-T.L., Ishak, Z., Yahya, S., Song, Y., & Singh, R. (2020). Early nodulin 93 protein gene: Essential for induction of somatic embryogenesis in oil palm. Plant Cell Reports, 39, 1395–1413. https://doi.org/10.1007/s00299-020-02571-7

    Article  CAS  PubMed  Google Scholar 

  21. Van Kammen, A. (1984). Suggested nomenclature for plant genes involved in nodulation and symbiosis. Plant Molecular Biology Reporter, 2(2), 43–45. https://doi.org/10.1007/BF03015869

    Article  Google Scholar 

  22. Reddy, P. M., Kouchi, H., & Ladha, J. K. (1998). Isolation, analysis and expression of homologous of the soybean early nodulin gene GmENOD93 (GmN93) from rice. Biochimica et Biophysica Acta, 1443, 386–392. https://doi.org/10.1016/S0167-4781(98)00232-2

    Article  CAS  PubMed  Google Scholar 

  23. Kouchi, H., & Hata, S. (1993). Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Molecular and General Genetics, 238, 106–119. https://doi.org/10.1007/BF00279537

    Article  CAS  PubMed  Google Scholar 

  24. Van De Sande, K., Pawlowski, K., Czaja, I., Wieneke, U., Schell, J., Schmidt, J., Walden, R., Matvienko, M., Wellink, J., Van Kammen, A., Franssen, H., & Bisseling, T. (1996). Modification of phytohormone response by a peptide encoded by ENOD40 of legumes and a nonlegume. Science, 273, 370–373. https://doi.org/10.1126/science.273.5273.370

    Article  PubMed  Google Scholar 

  25. Mashiguchi, K., Asami, T., & Suzuki, Y. (2009). Genome-wide identification, structure and expression studies, and mutant collection of 22 early nodulin-like protein genes in Arabidopsis. Bioscience, Biotechnology and Biochemistry, 73(11), 2452–2459. https://doi.org/10.1271/bbb.90407

    Article  CAS  Google Scholar 

  26. Reddy, P. M., Aggarwal, R. K., Ramos, M. C., Ladha, J. K., Brar, D. S., & Kouchi, H. (1999). Widespread occurrence of the homologues of the early nodulin (ENOD) genes in Oryza species and related grasses. Biochemical and Biophysical Research Communications, 258(1), 148–154. https://doi.org/10.1006/bbrc.1999.0458

    Article  CAS  PubMed  Google Scholar 

  27. Okubara, P. A., Fujishige, N. A., Hirsch, A. M., & Berry, A. M. (2000). Dg93, a nodule abundant mRNA of Datisca glomerata with homology to a soybean early nodulin gene. Plant Physiology, 122(4), 1073–1079. https://doi.org/10.1104/pp.122.4.1073

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Kouchi, H., Takane, K., So, R. B., Ladha, J. K., & Reddy, P. M. (1999). Rice ENOD40: Isolation and expression analysis in rice and transgenic soybean root nodules. The Plant Journal, 18(2), 121–129. https://doi.org/10.1046/j.1365-313x.1999.00432.x

    Article  CAS  PubMed  Google Scholar 

  29. Bi, Y. M., Kant, S., Clark, J., Gidda, S., Ming, F., Xu, J., Rochon, A., Shelp, B. J., Hao, L., Zhao, R., Mullen, R. T., Zhu, T., & Rothstein, S. J. (2009). Increased nitrogen-use efficiency in transgenic rice plants over-expressing a nitrogen-responsive early nodulin gene identified from rice expression profiling. Plant, Cell & Environment, 32(12), 1749–1760. https://doi.org/10.1111/j.1365-3040.2009.02032.x

    Article  CAS  Google Scholar 

  30. Zubaidah, R. (2009). Strategies to dissect the roles of oil palm genes using Arabidopsis as a model plant. PhD, University of Nottingham, United Kingdom.

  31. Weigel, D., & Glazebrook, J. (2002). Arabidopsis: a laboratory manual. CSHL Press.

    Google Scholar 

  32. Jefferson, R. A. (1987). Assaying chimeric genes in plants: The GUS gene fusion system. Plant Molecular Biology Reporter, 5, 387–405. https://doi.org/10.1007/BF02667740

    Article  CAS  Google Scholar 

  33. Bandupriya, H. D. D., Gibbings, J. G., & Dunwell, J. M. (2014). Overexpression of coconut AINTEGUMENTA-like gene, CnANT, promotes in vitro regeneration in transgenic Arabidopsis. Plant Cell, Tissue and Organ Culture, 116(1), 67–79. https://doi.org/10.1007/s11240-013-0383-2

    Article  CAS  Google Scholar 

  34. Rosa, M., Von Harder, M., Cigliano, R. A., Schlögelhofer, P., & Mittelsten Scheid, O. (2013). The Arabidopsis SWR1 chromatin-remodeling complex is important for DNA repair, somatic recombination, and meiosis. The Plant Cell, 25(6), 1990–2001. https://doi.org/10.1105/tpc.112.104067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Yeap, W.C., Lee, F.C., Shan, D.K.S., Hamidah, M., Appleton, D.R., & Kulaveerasingam, H. (2017). WRI1-1, ABI5, NF-YA3 and NF-YC2 increase oil biosynthesis in coordination with hormonal signalling during fruit development in oil palm. The Plant Journal, 91(1), 97-113. https://doi.org/10.1111/tpj.13549

    Article  CAS  PubMed  Google Scholar 

  36. Fones, H., Davis, C.A.R., Rico, A., Fang, F., & Smith, J.A.C. (2010). Metal hyperaccumulation armors plants against disease. PLoS Pathogens, 6(9), e1001093. https://doi.org/10.1371/journal.ppat.1001093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Philippar, K., Geis, T., Ilkavets, I., Oster, U., Schwenkert, S., Meurer, J., & Soll, J. (2007). Chloroplast biogenesis: The use of mutants to study the etioplast–chloroplast transition. Proceedings of the National Academy of Sciences, 104(2), 678–683. https://doi.org/10.1073/pnas.0610062104

    Article  CAS  Google Scholar 

  38. Xie, F., Xiao, P., Chen, D., Xu, L., & Zhang, B. (2012). miRDeepFinder: A miRNA analysis tool for deep sequencing of plant small RNAs. Plant Molecular Biology, 80(1), 75–84. https://doi.org/10.1007/s11103-012-9885-2

    Article  CAS  Google Scholar 

  39. Ruijter, J. M., Ramakers, C., Hoogaars, W. M., Karlen, Y., Bakker, O., Van Den Hoff, M. J., & Moorman, A. F. (2009). Amplification efficiency: Linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Research, 37, e45. https://doi.org/10.1093/nar/gkp045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Research, 18, e45.

    Article  Google Scholar 

  41. Florez, S. L., Erwin, R. L., Maximova, S. N., Guiltinan, M. J., & Curtis, W. R. (2015). Enhanced somatic embryogenesis in Theobroma cacao using the homologous BABY BOOM transcription factor. BMC Plant Biology, 15(1), 121. https://doi.org/10.1186/s12870-015-0479-4

    Article  PubMed  PubMed Central  Google Scholar 

  42. Kim, H. U., Jung, S.-J., Lee, K.-R., Kim, E. H., Lee, S.-M., Roh, K. H., & Kim, J.-B. (2014). Ectopic overexpression of castor bean LEAFY COTYLEDON2 (LEC2) in Arabidopsis triggers the expression of genes that encode regulators of seed maturation and oil body proteins in vegetative tissues. FEBS Open Bio, 4, 25–32. https://doi.org/10.1016/j.fob.2013.11.003

    Article  CAS  Google Scholar 

  43. Zubaidah, R., Nurniwalis, A. W., Siti, N. A. A., & Parveez, G. K. A. (2017). The use of Arabidopsis thaliana model system for testing oil palm promoter: case study on oil palm MT3-A promoter. Journal of Oil Palm Research, 29(2), 189–196. https://doi.org/10.21894/jopr.2017.2902.04

    Article  CAS  Google Scholar 

  44. Lardon, R., & Geelen, D. (2020). Natural variation in plant pluripotency and regeneration. Plants, 9(10), 1261. https://doi.org/10.3390/plants9101261

    Article  CAS  PubMed Central  Google Scholar 

  45. Alagarsamy, K., Pandian, S., & Ramesh, M. (2009). High frequency plant regeneration from embryogenic callus of popular indica rice (Oryza sativa L.). Physiology and Molecular Biology of Plants, 15, 371–375. https://doi.org/10.1007/s12298-009-0042-6

    Article  Google Scholar 

  46. Lee, S.-T., & Huang, W.-L. (2013). Cytokinin, auxin, and abscisic acid affects sucrose metabolism conduce to de novo shoot organogenesis in rice (Oryza sativa L.) callus. Botanical Studies, 54, 5. https://doi.org/10.1186/1999-3110-54-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Kulinska-Lukaszek, K., Tobojka, M., Adamiok, A., & Kurczynska, E. U. (2012). Expression of the BBM gene during somatic embryogenesis of Arabidopsis thaliana. Biologia Plantarum, 56(2), 389–394. https://doi.org/10.1007/s10535-012-0105-3

    Article  CAS  Google Scholar 

  48. Iwase, A., Harashima, H., Ikeuchi, M., Rymen, B., Ohnuma, M., Komaki, S., Morohashi, K., Kurata, T., Nakata, M., Ohme-Takagi, M., Grotewold, E., & Sugimoto, K. (2017). WIND1 promotes shoot regeneration through transcriptional activation of ENHANCER OF SHOOT REGENERATION1 in Arabidopsis. The Plant Cell, 29(1), 54–69. https://doi.org/10.1105/tpc.16.00623

    Article  CAS  PubMed  Google Scholar 

  49. Dai, X., Liu, Z., Qiao, M., Li, J., Li, S., & Xiang, F. (2017). ARR12 promotes de novo shoot regeneration in Arabidopsis thaliana via activation of WUSCHEL expression. Journal of Integrative Plant Biology, 59(10), 747–758. https://doi.org/10.1111/jipb.12567

    Article  CAS  PubMed  Google Scholar 

  50. Wójcikowska, B., & Gaj, M. D. (2017). Expression profiling of AUXIN RESPONSE FACTOR genes during somatic embryogenesis induction in Arabidopsis. Plant Cell Reports, 36, 843–858. https://doi.org/10.1007/s00299-017-2114-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Uddenberg, D., Valladares, S., Abrahamsson, M., Sundström, J. F., Sundås-Larsson, A., & von Arnold, S. (2011). Embryogenic potential and expression of embryogenesis-related genes in conifers are affected by treatment with a histone deacetylase inhibitor. Planta, 234, 527–539. https://doi.org/10.1007/s00425-011-1418-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Yi, S., Lin, Q., Zhang, X., Wang, J., Miao, Y., & Tan, N. (2020). Selection and validation of appropriate reference genes for quantitative RT-PCR analysis in Rubia yunnanensis diels based on transcriptome data. BioMed Research International. https://doi.org/10.1155/2020/5824841

    Article  PubMed  PubMed Central  Google Scholar 

  53. Martins, P., Mafra, V., de Souza, W. R., Ribeiro, A. P., Vinecky, F., Basso, M. F., da Cunha, B. A. D. B., Kobayashi, A. K., & Molinari, H. B. C. (2016). Selection of reliable reference genes for RT-qPCR analysis during developmental stages and abiotic stress in Setaria viridis. Scientific Reports, 6, 28348. https://doi.org/10.1038/srep28348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., & Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology, 3(7), research0034-1. https://doi.org/10.1186/gb-2002-3-7-research0034

    Article  Google Scholar 

  55. Andersen, C. L., Jensen, J. L., & Orntoft, T. F. (2004). Normalization of real-time quantitative reverse transcription-PCR data: A model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Research, 64(15), 5245–5250. https://doi.org/10.1158/0008-5472.can-04-0496

    Article  CAS  PubMed  Google Scholar 

  56. Pfaffl, M. W., Tichopad, A., Prgomet, C., & Neuvians, T. P. (2004). Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-excel-based tool using pair-wise correlations. Biotechnology Letters, 26, 509–515. https://doi.org/10.1023/B:BILE.0000019559.84305.47

    Article  CAS  PubMed  Google Scholar 

  57. Silver, N., Best, S., Jiang, J., & Thein, S. L. (2006). Selection of housekeeping genes for gene expression studies in human reticulocytes using real-time PCR. BMC Molecular Biology, 7(1), 33. https://doi.org/10.1186/1471-2199-7-33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Beveridge, C. A., Mathesius, U., Rose, R. J., & Gresshoff, P. M. (2007). Common regulatory themes in meristem development and whole-plant homeostasis. Current Opinion in Plant Biology, 10(1), 44–51. https://doi.org/10.1016/j.pbi.2006.11.011

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors would like to thank the Director General of MPOB, Deputy Director General of MPOB, and Director of ABBC for permission to publish this paper. We appreciate the technical assistance from Madam Hilda Hamzah, Ms Tan Yung Xin, and Ms Eo Shao Yim. We would like to also thank the Functional Biotechnology Unit for providing the facility to carry out the Arabidopsis transformation work. This work was supported by internal funding from MPOB DNA Chip Technology Programme (R000999000).

Author information

Authors and Affiliations

  1. Advanced Biotechnology and Breeding Centre, Malaysian Palm Oil Board, No. 6, Persiaran Institusi, Bandar Baru Bangi, 43000, Kajang, Selangor, Malaysia

    Intan Ernieza Farhana Nizan, Katialisa Kamaruddin, Pei-Wen Ong, Zubaidah Ramli, Rajinder Singh & Pek-Lan Chan

  2. School of Environmental and Life Sciences, The University of Newcastle, Callaghan, NSW, 2308, Australia

    Ray J. Rose

  3. Institute of Plant Biology, National Taiwan University, No. 1, Section 4, Roosevelt Road, 10617, Taipei, Taiwan, ROC

    Pei-Wen Ong

Authors
  1. Intan Ernieza Farhana Nizan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Katialisa Kamaruddin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Pei-Wen Ong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zubaidah Ramli
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Rajinder Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ray J. Rose
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Pek-Lan Chan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pek-Lan Chan.

Ethics declarations

Conflict of interest

The authors declare that there are no conflict of interest regarding the publication of this paper.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nizan, I.E.F., Kamaruddin, K., Ong, PW. et al. Overexpression of Oil Palm Early Nodulin 93 Protein Gene (EgENOD93) Enhances In Vitro Shoot Regeneration in Arabidopsis thaliana. Mol Biotechnol 64, 743–757 (2022). https://doi.org/10.1007/s12033-022-00450-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12033-022-00450-y

Keywords

Search

Navigation