European Journal of Plant Pathology

, Volume 152, Issue 4, pp 977–986 | Cite as

Transgenic crops and beyond: how can biotechnology contribute to the sustainable control of plant diseases?

Biotechnology for plant disease control: GMOs and beyond
  • David B. Collinge
SI: Plant Pathology for Innovative Agroecology


Disease resistance is without argument the best technological approach to control diseases in plants since no management input is required by the grower once the resistant variety has been planted. The biggest problems in using disease resistance lie in the facts that effective sources of resistance are not available for many important diseases, especially those caused by necrotrophic pathogens; and that pathogen populations adapt to the utilisation of novel sources of resistance, most notably for air-borne biotrophic pathogens. Several biotechnological approaches have been developed to produce disease resistant plants, the most recent known as NBT – New Breeding Technologies. This review focuses on recent advances in those technologies which adapt the knowledge obtained using molecular genetic approaches for the study of plant-microbe interactions to combat plant diseases.


New breeding technologies Gene editing HIGS Gene editing CRISPR-Cas Disease resistance GMO Marker-assisted selection Cisgenic New breeding technologies 



I am grateful to my colleagues Solveig K Christiansen, Rosanna C. Hennessy, Christian S. Jensen, Athina Koutouleas, Edward C. Rojas Tayo and Jeppe Thulin Østerberg for valuable comments and input.

Compliance with ethical standards

Conflict of interest

No external funding is involved in this study therefore I cannot envisage any potential conflicts of interest (financial or non-financial).

Human and animals studies

This review article does not contain any studies with human participants or animals performed by any of the authors.


  1. Acevedo-García, J., Kusch, S., & Panstruga, R. (2014). Magical mystery tour: MLO proteins in plant immunity and beyond. New Phytologist, 204, 273–281. Scholar
  2. Acevedo-Garcia, J., Spencer, D., Thieron, H., Reinstädler, A., Hammond-Kosack, K., Phillips, A. L., et al. (2017). Mlo-based powdery mildew resistance in hexaploid bread wheat generated by a non-transgenic TILLING approach. Plant Biotechnology Journal, 15(3), 367–378. Scholar
  3. Ahmed, A. A., McLellan, H., Aguilar, G. B., Hein, I., Thordal-Christensen, H., & Birch, P. R. J. (2016a). Engineering barriers to infection by undermining pathogen effector function or by gaining effector recognition. In D. B. Collinge (Ed.), Plant pathogen resistance biotechnology (pp. 23–50). New York: WILEY Blackwell.Google Scholar
  4. Ahmed, A. A., Pedersen, C., & Thordal-Christensen, H. (2016b). The barley powdery mildew effector candidates CSEP0081 and CSEP0254 promote fungal infection success. PLoS One, 11(6).
  5. Andersen, M. M., Landes, X., Xiang, W., Anyshchenko, A., Falhof, J., Østerberg, J. T., et al. (2015). Feasibility of new breeding techniques for organic farming. Trends in Plant Science, 20, 426–434.CrossRefGoogle Scholar
  6. Anon (2013). The regulatory status of plants resulting from New Breeding Technologies. Accessed 25/10–17 2017.
  7. Bai, Y. L., Pavan, S., Zheng, Z., Zappel, N. F., Reinstadler, A., Lotti, C., et al. (2008). Naturally occurring broad-spectrum powdery mildew resistance in a central American tomato accession is caused by loss of Mlo function. Molecular Plant-Microbe Interactions, 21(1), 30–39.CrossRefGoogle Scholar
  8. Belhaj, K., Chaparro-Garcia, A., Kamoun, S., & Nekrasov, V. (2013). Plant genome editing made easy: Targeted mutagenesis in model and crop plants using the CRISPR/Cas system. Plant Methods, 9, 39.
  9. Blomme, G., Dita, M., Jacobsen, K. S., Pérez Vicente, L., Molina, A., Ocimati, W., et al. (2017). Bacterial diseases of bananas and Enset: Current state of knowledge and integrated approaches toward sustainable management. [review]. Frontiers in Plant Science, 8(1290).
  10. Bravo-Almonacid, F. F., & Segretin, M. F. (2016). Status of transgenic crops in Argentina. In D. B. Collinge (Ed.), Biotechnology for plant disease control (pp. 275–283). New York: Wiley Blackwell.Google Scholar
  11. Brennan, J. P., & Martin, P. J. (2007). Returns to investment in new breeding technologies. Euphytica, 157, 337–349.CrossRefGoogle Scholar
  12. Butler, D. (2013). Fungus threatens top banana. Nature, 504, 195–196.CrossRefGoogle Scholar
  13. Camacho, A., Van Deynze, A., Chi-Ham, C., & Bennett, A. B. (2014). Genetically engineered crops that fly under the US regulatory radar. [opinion and comment]. Nature Biotechnology, 32(11), 1087–1091. Scholar
  14. Cantu, D., Roper, M. C., Powell, A. L. T., & Labavitch, J. M. (2016). To long life and good health: untangling the complexity of grape diseases to develop pathogen resistant varieties. In D. B. Collinge (Ed.), Plant Pathogen Resistance Biotechnology (pp. 193-215). New York: Wiley Blackwell.Google Scholar
  15. Chen, Y. J., Lyngkjaer, M. F., & Collinge, D. B. (2012). Future prospects for genetically engineering disease resistance plants. In G. Sessa (Ed.), Molecular plant immunity (pp. 251–275). New York: Wiley.CrossRefGoogle Scholar
  16. Chen, Y. Y., Wang, Z., Ni, H., Xu, Y., Chen, Q. J., & Jiang, L. (2017). CRISPR/Cas9-mediated base-editing system efficiently generates gain-of-function mutations in Arabidopsis. [journal article]. Science China Life Sciences, 60(5), 520–523. Scholar
  17. Coca, M., López-García, B., & Segundo, B. S. (2016). Transgenic crops in Spain. In D. B. Collinge (Ed.), Plant pathogen resistance biotechnology (pp. 295–304). New York: Wiley Blackwell.CrossRefGoogle Scholar
  18. Collinge, D. B. (2016). Biotechnology for plant disease control (first ed.). New York: Wiley Blackwell.Google Scholar
  19. Collinge, D. B., Lund, O. S., & Thordal-Christensen, H. (2008). What are the prospects for genetically engineered, disease resistant plants? European Journal of Plant Pathology, 121(3), 217–231.CrossRefGoogle Scholar
  20. Collinge, D. B., Jørgensen, H. J. L., Lund, O. S., & Lyngkjær, M. F. (2010). Engineering pathogen resistance in crop plants - current trends and future prospects. Annual Review of Phytopathology, 48, 269–291.CrossRefGoogle Scholar
  21. Collinge, D. B., Mullins, E., Jensen, B., & Jørgensen, H. J. L. (2016). The status and prospects for biotechnological approaches to attaining sustainable disease resistance. In D. B. Collinge (Ed.), Biotechnology for plant disease control (pp. 1–20). New York: Wiley Blackwell.Google Scholar
  22. Dale, J. L., James, A., Paul, J.-Y., Khanna, H., Smith, M., Peraza-Echeverria, S., et al. (2017). Transgenic Cavendish bananas with resistance to fusarium wilt tropical race 4. Nature Communications, 8(1), 1496. Scholar
  23. Deschamps, S., Llaca, V., & May, G. D. (2012). Genotyping-by-sequencing in plants. Biology, 1(3), 460.CrossRefGoogle Scholar
  24. Fernandes, J. S., Angelo, P. C. S., Cruz, J. C., Santos, J. M. M., Sousa, N. R., & Silva, G. F. (2016). Post-transcriptional silencing of the SGE1 gene induced by a dsRNA hairpin in Fusarium oxysporum f. sp cubense, the causal agent of Panama disease. Genetics and Molecular Research, 15(2), gmr.15027941. Scholar
  25. Fuchs, M., & Gonsalves, D. (2007). Safety of virus-resistant transgenic plants two decades after their introduction: Lessons from realistic field risk assessment studies. Annual Review of Phytopathology, 45(1), 173–202.CrossRefGoogle Scholar
  26. Ge, X. T., Deng, W. W., Lee, Z. Z., Lopez-Ruiz, F. J., Schweizer, P., & Ellwood, S. R. (2016). Tempered mlo broad-spectrum resistance to barley powdery mildew in an Ethiopian landrace. Scientific Reports, 6.
  27. Ghag, S. B., & Ganapathi, T. R. (2017). Genetically modified bananas: To mitigate food security concerns. Scientia Horticulturae, 214(Supplement C), 91–98. Scholar
  28. Ghag, S. B., Shekhawat, U. K. S., & Ganapathi, T. R. (2014). Host-induced post-transcriptional hairpin RNA-mediated gene silencing of vital fungal genes confers efficient resistance against fusarium wilt in banana. Plant Biotechnology Journal, 12(5), 541–553. Scholar
  29. Glazebrook, J. (2001). Genes controlling expression of defense responses in Arabidopsis-2001 status. Current Opinion in Plant Biology, 4(4), 301–308.CrossRefGoogle Scholar
  30. Groen, S. C., Wamonje, F. O., Murphy, A. M., & Carr, J. P. (2017). Engineering resistance to virus transmission. Current Opinion in Virology, 26(Supplement C), 20–27. Scholar
  31. Holme, I. B., Wendt, T., & Holm, P. B. (2013). Intragenesis and cisgenesis as alternatives to transgenic crop development. Plant Biotechnology Journal, 11(4), 395–407.CrossRefGoogle Scholar
  32. Jarosch, B., Jansen, M., & Schaffrath, U. (2003). Acquired resistance functions in mlo barley, which is hypersusceptible to Magnaporthe grisea. Molecular Plant-Microbe Interactions, 16(2), 107–114.CrossRefGoogle Scholar
  33. Jensen, D. F., Karlsson, M., Sarrocco, S., & Vannacci, G. (2016). Biological control using microorganisms as an alternative to disease resistance. In D. B. Collinge (Ed.), Plant pathogen resistance biotechnology (pp. 341–363). New York: Wiley Blackwell.CrossRefGoogle Scholar
  34. Jia, H., Zhang, Y., Orbović, V., Xu, J., White, F. F., Jones, J. B., et al. (2017). Genome editing of the disease susceptibility gene CsLOB1 in citrus confers resistance to citrus canker. Plant Biotechnology Journal, 15(7), 817–823. Scholar
  35. Jo, K. R., Zhu, S. Z., Bai, Y., Hutten, R. C. B., Kessel, G. J. T., Vleeshouwers, V. G. A. A., et al. (2016). Problematic crops: 1. Potatoes: Towards sustainable potato late blight resistance by Cisgenic R gene pyramiding. In D. B. Collinge (Ed.), Biotechnology for plant disease control (pp. 171–191). New York: Wiley Blackwell.Google Scholar
  36. Jørgensen, J. H. (1992). Discovery, characterization and exploitation of Mlo powdery mildew resistance in barley. Euphytica, 63, 141–152.CrossRefGoogle Scholar
  37. Kaniewski, W. K., & Thomas, P. E. (2004). The potato story. AgBioforum, 7(1&2), 41–46.Google Scholar
  38. Koch, A., Kumar, N., Weber, L., Keller, H., Imani, J., & Kogel, K.-H. (2013). Host-induced gene silencing of cytochrome P450 lanosterol C14α-demethylase–encoding genes confers strong resistance to fusarium species. Proceedings of the National Academy of Sciences, 110(48), 19324–19329. Scholar
  39. Koch, A., Biedenkopf, D., Furch, A. C. U., Weber, L., Rossbach, O., Abdellatef, E., et al. (2016). An RNAi-based control of fusarium graminearum infections through spraying of long dsRNAs involves a plant passage and is controlled by the fungal silencing machinery. PLoS Pathogens, 12(10), e1005901. Scholar
  40. Kumakech, A., Jørgensen, H. J. L., Collinge, D. B., Edema, R., & Okori, P. (2017). Azadirachta indica reduces black Sigatoka in east African highland banana by direct antimicrobial effects against Mycosphaerella fijiensis without inducing resistance. Journal of Agricultural Science, 9(4).
  41. Laaninen, T. (2016). New plant-breeding techniques: Applicability of GM rules. EPRS, PE, 582, 018.Google Scholar
  42. Langridge, P., & Fleury, D. (2011). Making the most of ‘omics’ for crop breeding. Trends in Biotechnology, 29(1), 33–40. Scholar
  43. Magg, T., Melchinger, A. E., Klein, D., & Bohn, M. (2002). Relationship between European corn borer resistance and concentration of mycotoxins produced by fusarium spp. in grains of transgenic Bt maize hybrids, their isogenic counterparts, and commercial varieties. Plant Breeding, 121(2), 146–154. Scholar
  44. Malnoy, M., Viola, R., Jung, M.-H., Koo, O.-J., Kim, S., Kim, J.-S., et al. (2016). DNA-free genetically edited grapevine and apple protoplast using CRISPR/Cas9 ribonucleoproteins. [original research]. Frontiers in Plant Science, 7(1904).
  45. McGrann, G. R. D., Stavrinides, A., Russell, J., Corbitt, M. M., Booth, A., Chartrain, L., et al. (2014). A trade off between mlo resistance to powdery mildew and increased susceptibility of barley to a newly important disease, Ramularia leaf spot. Journal of Experimental Botany, 65, 1025–1037.
  46. McHale, L., Tan, X. P., Koehl, P., & Michelmore, R. W. (2006). Plant NBS-LRR proteins: Adaptable guards. Genome Biology, 7(4).
  47. Mitter, N., Worrall, E. A., Robinson, K. E., Xu, Z. P., & Carroll, B. J. (2017). Induction of virus resistance by exogenous application of double-stranded RNA. Current Opinion in Virology, 26(Supplement C), 49–55. Scholar
  48. Molina, A. B., Sinohin, V. O., Fabregar, E. G., Ramillete, E. B., Loayan, M. M., & Chao, C. P. (2016). Field resistance of Cavendish somaclonal variants and local banana cultivars to tropical race 4 of fusarium wilt in the Philippines. In International Society for Horticultural Science (ISHS), Leuven, Belgium (1114 ed., pp. 227-230).
  49. Munkvold, G. P., Hellmich, R. L., & Rice, L. G. (1999). Comparison of fumonisin concentrations in kernels of transgenic Bt maize hybrids and nontransgenic hybrids. Plant Disease, 83, 130–138.CrossRefGoogle Scholar
  50. Nekrasov, V., Wang, C., Win, J., Lanz, C., Weigel, D., & Kamoun, S. (2017). Rapid generation of a transgene-free powdery mildew resistant tomato by genome deletion. Scientific Reports, 7(1), 482. Scholar
  51. Niu, J. H., Jiang, H., Xu, J.-M., Guo, Y. D., & Liu, Q. (2010). RNAi technology extends its reach: Engineering plant resistance against harmful eukaryotes. African Journal of Biotechnology, 9(45), 7573–7582.Google Scholar
  52. Nowara, D., Gay, A., Lacomme, C., Shaw, J., Ridout, C., Douchkov, D., et al. (2010). HIGS: Host-induced gene silencing in the obligate biotrophic fungal pathogen Blumeria graminis. Plant Cell, 22(9), 3130–3141.CrossRefGoogle Scholar
  53. Ordonez, N., Seidl, M. F., Waalwijk, C., Drenth, A., Kilian, A., Thomma, B. P. H. J., et al. (2015). Worse comes to worst: Bananas and Panama disease—When plant and pathogen clones meet. PLoS Pathogens, 11(11), e1005197. Scholar
  54. Ortiz, R., & Swennen, R. (2014). From crossbreeding to biotechnology-facilitated improvement of banana and plantain. Biotechnology Advances, 32(1), 158–169.CrossRefGoogle Scholar
  55. Pavan, S., Schiavulli, A., Appiano, M., Marcotrigiano, A. R., Cillo, F., Visser, R. G. F., et al. (2011). Pea powdery mildew er1 resistance is associated to loss-of-function mutations at a MLO homologous locus. [journal article]. Theoretical and Applied Genetics, 123(8), 1425–1431. Scholar
  56. Pessina, S., Lenzi, L., Perazzolli, M., Campa, M., Costa, S. U., Valè, G., et al. (2016). Knockdown of MLO genes reduces susceptibility to powdery mildew in grapevine. Horticulture Research, 3.
  57. Pliego, C., Nowara, D., Bonciani, G., Gheorghe, D. M., Xu, R., Surana, P., et al. (2013). Host-induced gene silencing in barley powdery mildew reveals a class of ribonuclease-like effectors. Molecular Plant-Microbe Interactions, 26(6), 633–642.CrossRefGoogle Scholar
  58. Ploetz, R. C. (2015). Management of Fusarium wilt of banana: A review with special reference to tropical race 4. Crop Protection, 73(Supplement C), 7–15. Scholar
  59. Poland, J. A., & Rife, T. W. (2012). Genotyping-by-sequencing for plant breeding and genetics. The Plant Genome, 5(3), 92–102. Scholar
  60. Qi, T., Zhu, X., Tan, C., Liu, P., Guo, J., Kang, Z., et al. (2017). Host-induced gene silencing of an important pathogenicity factor PsCPK1 in Puccinia striiformis f. sp. tritici enhances resistance of wheat to stripe rust. Plant Biotechnology Journal.
  61. Ricroch, A. E., & Henard-Damave, M. (2016). Next biotech plants: New traits, crops, developers and technologies for addressing global challenges. Critical Reviews in Biotechnology, 36(4), 675–690.Google Scholar
  62. Salvi, S., & Tuberosa, R. (2015). The crop QTLome comes of age. Current Opinion in Biotechnology, 32(Supplement C), 179–185. Scholar
  63. Sauer, N. J., Mozoruk, J., Miller, R. B., Warburg, Z. J., Walker, K. A., Beetham, P. R., et al. (2016). Oligonucleotide-directed mutagenesis for precision gene editing. Plant Biotechnology Journal, 14(2), 496–502. Scholar
  64. Schaefer, K. A., Wu, W. H., Colgan, D. F., Tsang, S. H., Bassuk, A. G., & Mahajan, V. B. (2017). Unexpected mutations after CRISPR-Cas9 editing in vivo. [correspondence]. Nature Methods, 14(6), 547–548. Scholar
  65. Schulze-Lefert, P., & Vogel, J. (2000). Closing the ranks to attack by powdery mildew. Trends in Plant Science, 5(8), 343–348.CrossRefGoogle Scholar
  66. Songstad, D. D., Petolino, J. F., Voytas, D. F., & Reichert, N. A. (2017). Genome editing of plants. Critical Reviews in Plant Sciences, 36(1), 1–23. Scholar
  67. Subburaj, S., Chung, S. J., Lee, C., Ryu, S.-M., Kim, D. H., Kim, J.-S., et al. (2016). Site-directed mutagenesis in petunia × hybrida protoplast system using direct delivery of purified recombinant Cas9 ribonucleoproteins. [journal article]. Plant Cell Reports, 35(7), 1535–1544. Scholar
  68. Taning, C. N. T., Andrade, E. C., Hunter, W. B., Christiaens, O., & Smagghe, G. (2016). Asian citrus psyllid RNAi pathway–RNAi evidence. [article]. Scientific Reports, 6, 38082. Scholar
  69. Thakare, D., Zhang, J., Wing, R. A., Cotty, P. J., & Schmidt, M. A. (2017). Aflatoxin-free transgenic maize using host-induced gene silencing. Science Advances, 3(3).
  70. van Schie, C. C. N., & Takken, F. L. W. (2014). Susceptibility genes 101: How to be a good host. Annual Review of Phytopathology, 52(1), 551–581. Scholar
  71. Wang, Y. P., Cheng, X., Shan, Q. W., Zhang, Y., Liu, J. X., Gao, C. X., et al. (2014). Simultaneous editing of three homoeoalleles in hexaploid bread wheat confers heritable resistance to powdery mildew. Nature Methods, 32(9), 947–951.Google Scholar
  72. Woo, J. W., Kim, J., Kwon, S. I., Corvalan, C., Cho, S. W., Kim, H., et al. (2015). DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. [research]. Nature Methods, 33(11), 1162–1164. Scholar
  73. Xue, C., Ryan Penton, C., Shen, Z. Z., Zhang, R. F., Huang, Q. W., Li, R., et al. (2015). Manipulating the banana rhizosphere microbiome for biological control of Panama disease. Scientific Reports, 5, 11124.CrossRefGoogle Scholar
  74. Zetterberg, C., & Björnberg, K. E. (2017). Time for a new EU regulatory framework for GM crops? [journal article]. Journal of Agricultural and Environmental Ethics, 30(3), 325–347. Scholar
  75. Zhang, Y., Liang, Z., Zong, Y., Wang, Y., Liu, J., Chen, K., et al. (2016). Efficient and transgene-free genome editing in wheat through transient expression of CRISPR/Cas9 DNA or RNA. [article]. 7, 12617. doi:

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© Koninklijke Nederlandse Planteziektenkundige Vereniging 2018

Authors and Affiliations

  1. 1.Department of Plant and Environmental Sciences and Copenhagen Plant Science CentreUniversity of CopenhagenFrederiksbergDenmark

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