Skip to main content
SpringerLink
Log in

Histological evaluation of pineapple transgenic plants following 8 years of field growth

  • Published:
Euphytica Aims and scope Submit manuscript

Abstract

Pineapple is among the most important fruits worldwide. However, the narrow genetic base of current commercial cultivars renders the industry at risk from environmental and other biological threats. Hence, there is a need to develop improved cultivars with tolerance to biotic and abiotic stresses. Our prior research resulted in the establishment of a method for genetic transformation of pineapple. The genetically modified pineapple plants generated were characterized following acclimatization and during the subsequent 8 years under field conditions. The current work highlights the results obtained for histological characterization of roots and leaves of transgenic pineapple plants. The four treatments investigated were macropropagated control plants (untransformed), micropropagated control plants (untransformed), and micropropagated genetically transformed plants (clones 90 and 98). Twenty indicators were measured in plants: two of them did not show statistically significant differences among the four groups of plants (2/20 = 10.0%); six showed “Low” overall coefficients of variation (OCV) (6/20 = 30.0%); 12 showed “Medium” OCVs (12/20 = 60.0%); and only two indicators showed “High” OCVs (2/20 = 10.0%). Consideration of medium OCVs showed that the biomass of transgenic plants was slightly greater than those of the non-transgenic controls. Statistically significant differences between the lines were recorded except in the central cylinder diameter of roots and the D leaf adaxial cuticle thickness. “High” OCVs were observed for root exo- and endodermis thickness where transgenic clones showed statistically significantly higher values. In terms of the roots, five out of nine histological indicators showed “Medium” OCVs: cortex, rhyzodermis, and parenchyma thicknesses, pith diameter, and thickness of the transversal root ratio. Again, genetically transformed materials showed statistically significantly higher averages. Only three out of seven histological indicators showed “Medium” OCVs in the leaves: D leaf abaxial cuticle thickness, chlorophyll parenchyma thickness, and D leaf aquifer parenchyma thickness. As noted above, statistically significantly higher values were recorded in the transgenic pineapple plants. Since the differences observed did not ultimately affect fruit yield (as shown in our previous work), they do not appear to be consequences of genetic transformation that impact on reproductive yield.

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

Similar content being viewed by others

References

  • Aragón C, Carvalho L, González J, Escalona M, Amâncio S (2012) The physiology of ex vitro pineapple (Ananas comosus L. Merr. var MD-2) as CAM or C3 is regulated by the environmental conditions. Plant Cell Rep 31:757–769

    Article  Google Scholar 

  • Bayer (2005) Technical information Bayer CropScience. Monheim, Germany

    Google Scholar 

  • Bewley JD, Black M (1995) Seeds: physiology of development and germination. Plenum Press, New York

    Google Scholar 

  • Chen H, Hu B, Zhao L, Shi D, She Z, Huang X, Priyadarshani S, Niu X, Qin Y (2019) Differential expression analysis of reference genes in pineapple (Ananas comosus L.) during reproductive development and response to abiotic stress. Trop Plant Biol 22:1–11

    Google Scholar 

  • Codex (2003) Codex Alimentarius Commission Joint FAO/WHO Food Standard Programme Codex ad hoc intergovernmental task force on foods derived from biotechnology. FAO/WHO. http://www.fao.org/fileadmin/user_upload/gmfp/docs/CAC.GL_45_2003.pdf http://www.who.int/fsf/GMfood/codex_index.htm, http://www.fao.org/fao-who-codexalimentarius/codex-home/en/. Accessed 15 May 2017

  • Coppens d´Eeckenbrugge G, Leal F (2003) Morphology, anatomy and taxonomy. In: Bartholomew DP, Paull RE, Rohrbach KG (eds) The pineapple: botany, production and uses. CAB International, Honolulu, pp 13–32

    Chapter  Google Scholar 

  • DellaPenna D (2015) Plant metabolic engineering. Plant Physiol 125:160–163

    Article  Google Scholar 

  • EFSA (2010) Statistical considerations for the safety evaluation of GMOs. EFSA J 8:59

    Google Scholar 

  • EFSA (2011) Guidance on selection of comparators for the risk assessment of genetically modified plants and derived food and feed. EFSA J 9:1–20

    Google Scholar 

  • Espinosa P, Lorenzo JC, Iglesias A, Yabor L, Menéndez E, Borroto J, Hernández L, Arencibia A (2002) Production of pineapple transgenic plants assisted by temporary immersion bioreactors. Plant Cell Rep 21:136–140

    Article  CAS  Google Scholar 

  • FAOSTAT (2015) http://faostat3.fao.org/browse/Q/*/E

  • Firoozabady E, Heckert M, Gutterson N (2006) Transformation and regeneration of pineapple. Plant Cell Rep 84:1–16

    Google Scholar 

  • Gambino G, Gribaudo I (2012) Genetic transformation of fruit trees: current status and remaining challenges. Transgenic Res 21:1163–1181

    Article  CAS  Google Scholar 

  • Goedhart PW, van der Voet H, Baldacchino F, Arpaia S (2014) A statistical simulation model for field testing of non-target organisms in environmental risk assessment of genetically modified plants. Ecol Evol 4:1267–1283

    Article  Google Scholar 

  • González R, Serrato R, Molina J, Aragón C, Olalde V, Pulido L, Dibut B, Lorenzo JC (2013) Biochemical and physiological changes produced by Azotobacter chroococcum (INIFAT5 strain) on pineapple in vitro-plantlets during acclimatization. Acta Physiol Plant 35:3483–3487

    Article  Google Scholar 

  • Hossain MF (2016) World pineapple production: an overview. Afric J Food Agric Nutr Dev 16:11443–11456

    Article  Google Scholar 

  • Johansen DA (1940) Plant microtechnique. McGraw-Hill, New York, p 528

    Google Scholar 

  • Kamoun S (2001) Non-host resistance to Phytophthora: novel prospects for a classical problem. Plant Biol 4:295–300

    CAS  Google Scholar 

  • Kuiper HA, Kleter GA, Noteborn HP, Kok M (2001) Assessment of the food safety issues related to genetically modified foods. Plant J 27:503–528

    Article  CAS  Google Scholar 

  • Leal F, d’Eckenbrugge GC (2018) History, distribution and world production. In: Sanewski G, Bartholomew DP, Paull RE (eds) The pineapple: botany production and uses. CAB International, Wallingford, pp 1–10

    Google Scholar 

  • Lorenzo JC, Yabor L, Medina N, Quintana N, Wells V (2015) Coefficient of variation can identify the most important effects of experimental treatments. Not Bot Hortic Agrobo Cluj-Nap 43:287–291

    Article  Google Scholar 

  • Ming R, Van Buren R, Wai CM, Tang H, Schatz MC, Bowers JE, Lyons E, Wang ML, Chen J, Biggers E, Zhang J, Huang L, Zhang L, Miao W, Zhang J, Ye Z, Miao C, Lin Z, Wang H, Zhou H, Yim WC, Priest HD, Zheng C, Woodhous M, Edger P (2015) The pineapple genome and the evolution of CAM photosynthesis. Nat Genet 47:1435–1442

    Article  CAS  Google Scholar 

  • Mohammed A, Abalaka ME (2011) Agrobacterium transformation: a boost to agricultural biotechnology. J Med Gen Genom 3:126–130

    CAS  Google Scholar 

  • Nagendra-Pradra D, Sudhakar N, Murugesan K, Mohan N (2007) Application of ozone on induction of resistance in Vigna unguiculata cv. Co 6, against Fusarium wilt. Arch Phytopathol Plant Prot 3:1–10

    Google Scholar 

  • Nath V, Kumar G, Pandey S, Pandey S (2019) Impact of climate change on tropical fruit production systems and its mitigation strategies. In: Sheraz Mahdi S (ed) Climate change and agriculture in India: impact and adaptation. Springer, Berlin, pp 129–146

    Chapter  Google Scholar 

  • Osmond CB, Austin MP, Berry JA, Billings WD, Boyer JS, Dacey JWH, Nobel PS, Smith SD, Winner WE (1987) Stress physiology and the distribution of plants. Bioscience 37:38–48

    Article  Google Scholar 

  • Pérez G, Yanes-Paz E, Mbogholi A, Valle B, Sagarra F, Yabor L, Aragón C, González J, Isidrón M, Lorenzo JC (2012) New pineapple somaclonal variants: P3R5 and Dwarf. Am J Plant Sci 3:1–11

    Article  Google Scholar 

  • Punja Z (2001) Genetic engineering of plant to enhance resistance to fungal pathogens: a review of progress and future prospects. Chin J Plant Pathol 23:216–235

    CAS  Google Scholar 

  • Py C, Lacoeuilhe JJ, Teisson C (1987) The pineapple: cultivation and uses. Maisonneuve & Larose, Paris

    Google Scholar 

  • Taira T, Toma N, Ishihara M (2005) Purification, characterization, and antifungal activity of chitinases from pineapple (Ananas comosus) leaf. Biochemistry 69:189–196

    CAS  Google Scholar 

  • Thompson CJ, Movva NR, Tizard R, Crameri R, Davies JE, Lauwereys M, Botterman J (1987) Characterization of the herbicide-resistance gene bar from Streptomyces higroscopicus. EMBO J 6:2523–2527

    Article  Google Scholar 

  • Wali N (2019) Pineapple (Ananas comosus). Nonvitamin and nonmineral nutritional supplements. Elsevier, Amsterdam, pp 367–373

    Book  Google Scholar 

  • Wang M-L, Uruu G, Xiong L, He X, Nagai C, Cheah K, Hu J, Nan G-L, Sipes B, Atkinson H (2009) Production of transgenic pineapple (Ananas comosus (L.) Merr.) plants via adventitious bud regeneration. Vitro Cell Dev Biol Plant 45:112–121

    Article  CAS  Google Scholar 

  • Yabor L, Arzola M, Aragón C, Hernández M, Arencibia A, Lorenzo JC (2006) Biochemical side effects of genetic transformation of pineapple. Plant Cell Tissue Organ Cult 86:63–67

    Article  CAS  Google Scholar 

  • Yabor L, Aragón C, Hernández M, Arencibia A, Lorenzo JC (2008) Biochemical side effects of the herbicide FINALE on bar gene-containing transgenic pineapple plantlets. Euphytica 164:515–520

    Article  CAS  Google Scholar 

  • Yabor L, Valle B, Carvajal C, Aragón C, Hernández M, González J, Daquinta M, Arencibia A, Lorenzo JC (2010) Characterization of a field-grown transgenic pineapple clone containing the genes chitinase, AP24, and bar. Vitro Cell Dev Biol Plant 46:1–7

    Article  CAS  Google Scholar 

  • Yabor L, Valle B, Rodríguez RC, Aragón C, Papenbrock J, Tebbe CC, Lorenzo JC (2016) The third vegetative generation of a field-grown transgenic pineapple clone shows minor side effects of transformation on plant physiological parameters. Plant Cell Tissue Organ Cult. https://doi.org/10.1007/s11240-016-0950-4

    Article  Google Scholar 

  • Yabor L, Rumlow A, Gómez D, Tebbe CC, Papenbrock J, Lorenzo JC (2017) Mineral composition of a transgenic pineapple clone grown in the field for 8 yr. Vitro Cell Dev Biol Plant 53:489–493

    Article  CAS  Google Scholar 

  • Yanes-Paz E, González J, Sánchez R (2000) A technology of acclimatization of pineapple vitroplants. Pineapple News 7:24

    Google Scholar 

Download references

Acknowledgements

This research was supported by the Technological Institute of Costa Rica, the Plant Improvement Division of the ARC-Tropical and Subtropical Crops (South Africa), and the Bioplant Centre (University of Ciego de Ávila, Cuba). The authors are grateful to Mr. José Laguna for his skilled technical assistance.

Author information

Authors and Affiliations

  1. Laboratory for Plant Breeding and Conservation of Genetic Resources, Bioplant Center, University of Ciego de Avila, 69450, Ciego de Ávila, Cuba

    Lourdes Yabor, Lisbet Pérez, Daviel Gómez, Ariel Villalobos-Olivera, José Ramón Mendoza, Julia Martínez, Doris Escalante & José Carlos Lorenzo

  2. Biology School, Technological Institute of Costa Rica, Cartago, 25525333, Costa Rica

    Giovanni Garro

  3. Plant Improvement, Agricultural Research Council-Tropical and Subtropical Crops, Private Bag X11208, Nelspruit, 1200, South Africa

    Elliosha Hajari

Authors
  1. Lourdes Yabor
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lisbet Pérez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Daviel Gómez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ariel Villalobos-Olivera
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. José Ramón Mendoza
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Julia Martínez
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Doris Escalante
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Giovanni Garro
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Elliosha Hajari
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. José Carlos Lorenzo
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

LY, LP, DG, AVO, JRM, JM, DE, GG, EH, and JCL designed the research; LY, LP, DG, AVO, JRM, JM, and DE conducted the experiment; LY, DG, GG, EH, and JCL wrote the paper; and JCL had primary responsibility for the final content. All authors have read and approved the final manuscript.

Corresponding author

Correspondence to José Carlos Lorenzo.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Human and animal rights

This research did not involve experiments with human or animal participants.

Informed consent

Informed consent was obtained from all individual participants included in the study. Additional informed consent was obtained from all individual participants for whom identifying information is included in this article.

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

Yabor, L., Pérez, L., Gómez, D. et al. Histological evaluation of pineapple transgenic plants following 8 years of field growth. Euphytica 216, 23 (2020). https://doi.org/10.1007/s10681-020-2555-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10681-020-2555-6

Keywords

Search

Navigation