Photosynthetica 2013, 51(1):22-32 | DOI: 10.1007/s11099-013-0002-9

Unintended effects of genetic transformation on photosynthetic gas exchange, leaf reflectance and plant growth properties in barley (Hordeum vulgare L.)

C. X. Sun1,*, F. Yuan1, Y. L. Zhang2, Z. B. Cui1, Z. H. Chen2, L. J. Chen2, Z. J. Wu2
1 Science College, Northeastern University, Shenyang, P.R. China
2 Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang, P.R. China

Characterization of different component processes of photosynthesis is useful to understand the growth status of plants and to discover possible unintended effects of genetic modification on photosynthesis in transgenic plants. We focused on the changes in photosynthetic gas-exchange properties, reflectance spectra, and plant growth traits among groups of different transgenic barley T1 (TolT1) and its isogenic controls (TolNT1), TolT1, and group of its own transgenic progenies T2 (TolT2), TolNT1 and its wild type (WT), respectively. Gas-exchange measurements showed that only the net photosynthetic rate (P N) and the light-use efficiency (LUE) differed significantly between TolT1 and TolT2 with no obvious changes of other characteristics. Reflectance measurements indicated that the reflectance ratio was sensitive to identify the differences between two barley groups. Differences in reflectance expressed on an index basis depended on barley groups. The relationship between LUE and the photochemical reflectance index (PRI) at a leaf level among different barley groups of WT, TolNT1, TolT1 and TolT2 did not changed obviously. The differences in the total leaf area per plant (LA) between WT and TolNT1 as well as between TolT1 and TolT2 were significant. This study finally provided a plausible complex explanation for the unintended effects of genetic transformation on photosynthesis-related properties in barley at different levels. Furthermore, it was concluded that the photosynthesis-related properties of transgenic plants based on gas exchange, leaf reflectance, and plant growth measurements responded to the same environment in a more different way between two subsequent generations than to the processes of the gene insertion by Agrobacterium and associated tissue culture.

Keywords: genetic modification; leaf area; light-use efficiency; reflectance index; reflectance spectra; stomatal limitation; transgenic plants; water-use efficiency

Received: April 23, 2012; Accepted: November 8, 2012; Published: March 1, 2013Show citation

ACS AIP APA ASA Harvard Chicago IEEE ISO690 MLA NLM Turabian Vancouver
Sun, C.X., Yuan, F., Zhang, Y.L., Cui, Z.B., Chen, Z.H., Chen, L.J., & Wu, Z.J. (2013). Unintended effects of genetic transformation on photosynthetic gas exchange, leaf reflectance and plant growth properties in barley (Hordeum vulgare L.). Photosynthetica, 51(1), 22-32. doi: 10.1007/s11099-013-0002-9.
Download citation
  • BibTeX (.bib)
  • Bookends (.ris)
  • EasyBib (.ris)
  • EndNote (.enw)
  • EndNote 8 (.xml)
  • ISI WoS (.isi)
  • Medlars (.medlars)
  • Mendeley (.ris)
  • MODS (.xml)
  • Papers (.ris)
  • RefWorks (.txt)
  • RefManager (.ris)
  • RIS (.ris)
  • MS Word (.xml)
  • Zotero (.ris)

    • Open full article

    References

    1. Baruah-Wolff, J., Harwood, W.A., Lonsdale, D.A., Harvey, A., Hull, R., Snape, J.W.: Luciferase as a reporter gene for transformation studies in rice (Oryza sativa L.). - Plant Cell Rep. 18: 715-720, 1999. Go to original source...
    2. Bednarek, P.T., Orłowska, R., Koebner, R.M.D., Zimny, J.: Quantification of the tissue-culture induced variation in barley (Hordeum vulgare L.). - BMC Plant Biol. 7: 10-19, 2007. Go to original source...
    3. Bourdon, V., Ladbrooke, Z., Wickham, A. et al.: Homozygous transgenic wheat plants with increased luciferase activity do not maintain their high level of expression in the next generation. - Plant Sci. 163: 297-305, 2002. Go to original source...
    4. Butaye, K.M.J., Cammue, B.P.A., Delauré, S.L., De Bolle, M.F.C.: Approaches to minimize variation of transgene expression in plants. - Mol. Breeding 16: 79-91, 2005. Go to original source...
    5. Carter, G.A.: Primary and secondary effects of water content on the spectral reflectance of leaves. - Amer. J. Bot. 78: 916-924, 1991. Go to original source...
    6. Carter, G.A., Knapp, A.K.: Leaf optical properties in higher plants: linking spectral characteristics to stress and chlorophyll concentration. - Amer. J. Bot. 88: 677-684, 2001. Go to original source...
    7. Cassells, A.C., Curry, R.F.: Oxidative stress and physiological, epigenetic and genetic variability in plant tissue culture: implications for micropropagators and genetic engineers. - Plant Cell Tiss. Org. 64: 145-157, 2001. Go to original source...
    8. Cellini, F.A., Chesson, I., Colquhoun, I. et al.: Unintended effects and their detection in genetically modified crops. - Food Chem. Toxicol. 42: 1089-1125, 2004. Go to original source...
    9. Chow, W.S., Goodchild, D.J., Miller, C., Anderson, J.M.: The influence of high levels of brief or prolonged supplementary far red illumination during growth on the photosynthetic characteristics, composition and morphology of Pisum sativum chloroplasts. - Plant Cell Environ. 13: 135-145, 1990. Go to original source...
    10. Conner, A.J., Jacobs, J.M.E.: Food risks from transgenic crops in perspective. - Nutrition 16: 709-711, 2000. Go to original source...
    11. Cullen, D., Harwood, W.A., Smedley, M.A., Davies, H., Taylor, M.: Comparison of DNA walking methods for isolation of transgene-flanking regions in GM potato. - Mol. Biotechnol. 49: 19-31, 2011. Go to original source...
    12. Curran, P.J., Dungan, J.L., Ghglz, H.L.: Exploring the relationship between reflectance red edge and chlorophyll content in slash pine. - Tree Physiol. 7: 33-48, 1990. Go to original source...
    13. Demmig-Adams, B., Adams, W.W.: Photoprotection in an ecological context: the remarkable complexity of thermal dissipation. - New Phytol. 172: 11-21, 2006. Go to original source...
    14. Dong, H.Z., Li, W.J., Tang, W., Li, Z.H., Zhang, D.M.: Effects of genotypes and plant density on yield, yield components and photosynthesis in Bt transgenic cotton. - J. Agron. Crop Sci. 192: 132-139, 2006. Go to original source...
    15. Downton, W.J., Loveys, B.R., Grant, J.R.: Stomatal closure fully accounts for the inhibition of photosynthesis by abscisic acid. - New Phytol. 108: 263-266, 1988. Go to original source...
    16. Duan, F.P., Zheng, F., Duan, J., et al.: [Resistant inheritance, physiological and agricultural characters of BAR transgenic rice.] - J. Zhejiang Univ. 32: 355-359, 2006. [In Chin.]
    17. Edwards, K., Johnstone, C., Thompson, C.: A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. - Nucleic Acids Res. 19: 1349, 1991. Go to original source...
    18. Frak, E., Roux, X.L., Millard, P., et al.: Spatial distribution of leaf nitrogen and photosynthetic capacity within the foliage of individual trees: disentangling the effects of local light quality, leaf irradiance, and transpiration. - J. Exp. Bot. 53: 2207-2216, 2002. Go to original source...
    19. Gamon, J.A., Field, C.B., Fredeen, A.L., Thayer, S.: Assessing photosynthetic down regulation in sunflower stands with an optically-based model. - Photosynth. Res. 67: 113-125, 2001. Go to original source...
    20. Gamon, J.A., Serrano, L., Surfus, J.S.: The photochemical reflectance index: an optical indicator of photosynthetic radiation use efficiency across species, functional types, and nutrient levels. - Oecologia 112: 492-501, 1997. Go to original source...
    21. Gamon, J.A., Surfus, J.S.: Assessing leaf pigment content and activity with a reflectometer. - New Phytol. 143: 105-117, 1999. Go to original source...
    22. Gitelson, A., Merzlyak, M.N.: Detection of red edge position and chlorophyll content by reflectance measurements near 700 nm. - J. Plant Physiol. 148: 501-508, 1996. Go to original source...
    23. Guo, N., Zhang, Y.J., Jiang, C.J.: [Resistant inheritance and agronomic characters of bar transgenic wheat.] - Chin. Agric. Sci. Bull. 23: 192-192, 2007. [In Chin.]
    24. Harper, B., McClain, S., Ganko, E.W.: Interpreting the biological relevance of bioinformatic analyses with T-DNA sequence for protein allergenicity. - Regul. Toxicol. Pharmacol. 63: 426-432, 2012. Go to original source...
    25. Harwood, W.A., Ross, S.M., Cilento, P., Snape, J.W.: The effect of DNA/gold particle preparation technique, and particle bombardment device, on the transformation of barley (Hordeum vulgare). - Euphytica 111: 67-76, 2000. Go to original source...
    26. Hebbar, K.B., Perumal, N.K., Khadi, B.M.: Photosynthesis and plant growth response of transgenic Bt cotton (Gossypium hirsutum L.) hybrids under field condition. - Photosynthetica 45: 254-258, 2007. Go to original source...
    27. Jordá, L., Vera, P.: Local and systemic induction of two sefense-related subtilisin-like protease promoters in transgenic Arabidopsis plants. Luciferin induction of PR gene expression. - Plant Physiol. 124: 1049-1057, 2000. Go to original source...
    28. Kabouw, P., van Dam, N.M., van der Putten, W.H., Biere, A.: How genetic modification of roots affects rhizosphere processes and plant performance. - J. Exp. Bot. 63: 3475-3483, 2012. Go to original source...
    29. Kaeppler, S.M., Kaepller, H.F., Rhee, Y.: Epigenetic aspects of somaclonal variation in plants. - Plant Mol. Biol. 43: 179-188, 2000. Go to original source...
    30. Kakani, V.G., Reddy, K.R., Zhao, D., Gao, W.: Senescence and hyperspectral reflectance of cotton leaves exposed to ultraviolet-B radiation and carbon dioxide. - Physiol. Plant. 121: 250-257, 2004. Go to original source...
    31. Kier, L.D., Petrick, J.S.: Safety assessment considerations for food and feed derived from plants with genetic modifications that modulate endogenous gene expression and pathways. - Food Chem. Toxicol. 46: 2591-2605, 2008. Go to original source...
    32. Königa, A., Cockburnb, A., Crevelc, R.W.R., et al.: Assessment of the safety of foods derived from genetically modified (GM) crops. - Food Chem. Toxicol. 42: 1047-1088, 2004. Go to original source...
    33. Long, S.P., Baker, N.R., Raines, C.A.: Analyzing the responses of photosynthetic CO2 assimilation to long term elevation of atmospheric CO2 concentration. - Vegetatio 104: 33-45, 1993. Go to original source...
    34. Markwell, J., Osterman, J.C., Mitchell, J.L.: Calibration of the Minolta SPAD-502 leaf chlorophyll meter. - Photosynth. Res. 46: 467-472, 1995. Go to original source...
    35. Miki, B., McHugh, S.: Selectable marker genes in transgenic plants: applications, alternatives and biosafety. - J. Biotech. 107: 193-232, 2004. Go to original source...
    36. Millstone, E., Brunner, E., Mayer, S.: Beyond 'substantial equivalence'. - Nature 401: 525-526, 1999. Go to original source...
    37. Moran, J.A., Mitchell, A.K., Goodmanson, G., Stockburger, K.A.: Differentiation among effects of nitrogen fertilization treatments on conifer seedlings by foliar reflectance: a comparison of methods. - Tree Physiol. 20: 1113-1120, 2000. Go to original source...
    38. Nijs, I., Ferris, R., Blum, H., Hendrey, G., Impens, I.: Stomatal regulation in a changing climate: a field study using Free Air Temperature Increase (FATI) and Free Air CO2 enrichment (FACE). - Plant Cell Environ. 20: 1041-1050, 1997. Go to original source...
    39. Ouakfaoui, S.E., Miki, B.: The stability of the Arabidopsis transcriptome in transgenic plants expressing the marker genes nptII and uidA. - J. Plant 41: 791-800, 2005. Go to original source...
    40. Papazova, N., Windels, P., Depicker, A., Taverniers, I., Roldán-Ruiz, I., Milcamps, A., Van Bockstaele, E., Van Den Eede, G., De Loose, M.: Sequence stability of the T-DNA-plant junctions in tissue culture in Arabidopsis transgenic lines. - Plant Cell Rep. 25: 1362-1368, 2006. Go to original source...
    41. Penũelas, J., Filella, I., Gamon, J.A.: Assessment of photosynthetic radiation-use efficiency with spectral reflectance. - New Phytol. 131: 291-296, 1995.
    42. Penũelas, J., Filella, I.: Visible and near-infrared reflectance techniques for diagnosing plant physiological status. - Trends Plant Sci. 3: 151-156, 1998.
    43. Pieruschkaa, R., Hubera, G., Berry, J.A.: Control of transpiration by radiation. - Proc. Natr. Acad. Sci. 107: 13372-13377, 2010. Go to original source...
    44. Richardson, A.D., Berlyn, G.P.: Spectral reflectance and photosynthetic properties of betulapapyrifera (Betulaceae) leaves alongan elevational gradient on MT. Mansfield, Vermont, USA. - Amer. J. Bot. 89: 88-94, 2002. Go to original source...
    45. Richardson, A.D., Duigan, S.P., Berlyn, G.P.: An evaluation of noninvasive methods to estimate foliar chlorophyll content. - New Phytol. 153: 185-194, 2002. Go to original source...
    46. Rosati, A., DeJong, T.M.: Estimating photosynthetic radiation use efficiency using incident light and photosynthesis of individual leaves. - Ann. Bot. 91: 869-877, 2003. Go to original source...
    47. Rosati, A., Esparza, G., DeJong, T.M., Pearcy, R.W.: Influence of canopy light environment and nitrogen availability on leaf photosynthetic characteristics and photosynthetic nitrogen-use effciency of field-grown nectarine trees. - Tree Physiol. 19: 173-180, 1999. Go to original source...
    48. Salvo-Garrido, H., Travella, S., Bilham, L.J., et al.: The distribution of transgene insertion sites in barley determined by physical and genetic mapping. - Genetics 167: 1371-1379, 2004. Go to original source...
    49. Saxena, D., Stotzky, G.: Bt corn has a higher lignin content than non-Bt corn. - Amer. J. Bot. 88: 1704-1706, 2001. Go to original source...
    50. Shrawat, A.K., Lörz, H.: Agrobacterium-mediated transformation of cereals: a promising approach crossing barriers. - Plant Biotech. J. 4: 575-603, 2006. Go to original source...
    51. Sims, D.A., Gamon, J.A.: Relationships between leaf pigment content and spectral reflectance across a wide range of species, leaf structures and developmental stages. - Remote Sens. Environ. 81: 337-354, 2002. Go to original source...
    52. Slaton, M.R., Hunt, E.R., Smith, W.K.: Estimating near IR leaf reflectance from leaf structural characteristics. - Amer. J. Bot. 88: 278-284, 2001. Go to original source...
    53. Stirling, C.M., Rodrigo, V.H., Emberru, J.: Chilling and photosynthetic productivity of field-grown maize (Zea mays) - changes in the parameters of the light-response curve, canopy leaf CO2 assimilation rate and crop radiation-use efficiency. - Photosynth. Res. 38: 125-133, 1993. Go to original source...
    54. Sun, C.X., Qi, H., Hao, J.J., et al.: Single leaves photosynthetic characteristics of two insect-resistant transgenic cotton (Gossypium hirsutum L.) varieties in response to light. - Photosynthetica 47: 399-408, 2009. Go to original source...
    55. Sun, C.X., Qi, H., Sun, J.Q., et al.: [Photosynthetic characteristics of Bt or CpTI+Bt transgenic cotton at seedling stage.] - Acta Agron. Sin. 33: 469-475, 2007 [In Chin.].
    56. Sun, C.X., Wu, X.F., Wang, J., Chen, Z.H.: [Lignin content and related characteristics of transgenic barley stems.] - J. NEU 33: 1060-1064, 2012. [In Chin.]
    57. Terashima, I., Saeki, T.: A new model for leaf photosynthesis incorporating the gradients of light environment and of photosynthetic properties of chloroplasts within a leaf. - Ann. Bot. 56: 489-499, 1985. Go to original source...
    58. Tian, S.L., Yang, P.Z.: [Study on the relationship between source and sink of Bt transgenic cotton.] - Acta Gossypii Sin. 11: 151-156, 1999. [In Chin.]
    59. Zhao, H. Z., Liang, Z. J., Qi, H. L.: [Research on biology traits of Bt cotton.] - Chin. Cotton 29: 10-11, 2002. [In Chin.]
    60. Zaidi, M.A., Cheng, X.Y., Altosaar, I.: Characterization of leftborder flanking sequences of T-DNA integration in transgenic rice (Oryza sativa L.) expressing cry1Ab. - Cereal Res. Commun. 35: 1375-1383, 2007. Go to original source...
    61. Zolla, L., Rinalducci, S., Antonioli, P., Righetti, P.G.: Proteomics as a complementary tool for identifying unintended side effects occurring in transgenic maize seeds as a result of genetic modifications. - J. Proteome Res. 7: 1850-1861, 2008.
    62. Zu, Y.G., Pang, H.H., Yu, J.H., Li, D.W., Wei, X.X., Gao, Y.X., Tong, L.: Responses in the morphology, physiology and biochemistry of Taxus chinensis var. mairei grown under supplementary UV-B radiation. - J. Photochem. Photobiol. B: Biol. 98: 152-158, 2010. Go to original source...

    Return to the content