Crop plants with improved culture and quality traits for food, feed and other uses

Abstract

The large French research project GENIUS (2012–2019, https://www6.inra.genius-project_eng/) provides a good showcase of current genome editing techniques applied to crop plants. It addresses a large variety of agricultural species (rice, wheat, maize, tomato, potato, oilseed rape, poplar, apple and rose) together with some models (Arabidopsis, Brachypodium, Physcomitrella). Using targeted mutagenesis as its work horse, the project is limited to proof of concept under confined conditions. It mainly covers traits linked to crop culture, such as disease resistance to viruses and fungi, flowering time, plant architecture, tolerance to salinity and plant reproduction but also addresses traits improving the quality of agricultural products for industrial purposes. Examples include virus resistant tomato, early flowering apple and low-amylose starch potato. The wide range of traits illustrates the potential of genome editing towards a more sustainable agriculture through the reduction of pesticides and to the emergence of innovative bio-economy sectors based on custom tailored quality traits.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Altpeter F, Springer NM, Bartley LE, Blechl AE, Brutnell TP, Citovsky V, Conrad LJ, Gelvin SB, Jackson DP, Kausch AP, Lemaux PG, Medford JI, Orozco-Cardenas ML, Tricoli DM, Van Eck J, Voytas DF, Walbot V, Wang K, Zhang ZJ, Stewart CN Jr (2016) Advancing crop transformation in the era of genome editing. Plant Cell 28:1510–1520

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Andersson M, Turesson H, Nicolia A, Falt AS, Samuelsson M, Hofvander P (2017) Efficient targeted multiallelic mutagenesis in tetraploid potato (Solanum tuberosum) by transient CRISPR-Cas9 expression in protoplasts. Plant Cell Rep 36:117–128

    Article  CAS  PubMed  Google Scholar 

  3. Bettembourg M, Dal-Soglio M, Bureau C, Vernet A, Dardoux A, Portefaix M, Bes M, Meynard D, Mieulet D, Cayrol B, Perin C, Courtois B, Ma JF and Dievart A (2017) Root cone angle is enlarged in docs1 LRR-RLK mutants in rice. Rice 10:50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Chandrasekaran J, Brumin M, Wolf D, Leibman D, Klap C, Pearlsman M, Sherman A, Arazi T, Gal-On A (2016) Development of broad virus resistance in non-transgenic cucumber using CRISPR/Cas9 technology. Mol Plant Pathol 17:1140–1153

    Article  CAS  PubMed  Google Scholar 

  5. Cigan AM, Gadlage MJ, Gao H, Meeley RB, Young JK, Becker JE (2017). WAXY CORN. WO/2017/132239 and PCT/US2017/014903

  6. Collonnier C, Guyon-Debast A, Maclot F, Mara K, Charlot F, Nogue F (2017a) Towards mastering CRISPR-induced gene knock-in in plants: survey of key features and focus on the model physcomitrella patens. Methods 121–122:103–117

    Article  CAS  PubMed  Google Scholar 

  7. Collonnier C, Epert A, Mara K, Maclot F, Guyon-Debast A, Charlot F, White C, Schaefer DG, Nogue F (2017b) CRISPR-Cas9-mediated efficient directed mutagenesis and RAD51-dependent and RAD51-independent gene targeting in the moss physcomitrella patens. Plant Biotechnol J 15:122–131

    Article  CAS  PubMed  Google Scholar 

  8. Dahan-Meir T, Filler-Hayut S, Melamed-Bessudo C, Bocobza S, Czosnek H, Aharoni A, Levy AA (2018) Efficient in planta gene targeting in tomato using geminiviral replicons and the CRISPR/Cas9 system. Plant J 95:5–16

    Article  CAS  PubMed  Google Scholar 

  9. Danilo B, Perrot L, Botton E, Nogué F, Mazier M. (2018) The DFR locus: A smart landing pad for targeted transgene insertion in tomato. PLoS One 13:e0208395

    Article  PubMed  PubMed Central  Google Scholar 

  10. d’Erfurth I, Jolivet S, Froger N, Catrice O, Novatchkova M, Mercier R (2009) Turning meiosis into mitosis. PLoS Biol 7:e1000124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Feng Z, Zhang B, Ding W, Liu X, Yang DL, Wei P, Cao F, Zhu S, Zhang F, Mao Y, Zhu JK (2013) Efficient genome editing in plants using a CRISPR/Cas system. Cell Res 23:1229–1232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Gilles LM, Khaled A, Laffaire JB, Chaignon S, Gendrot G, Laplaige J, Berges H, Beydon G, Bayle V, Barret P, Comadran J, Martinant JP, Rogowsky PM, Widiez T (2017) Loss of pollen-specific phospholipase NOT LIKE DAD triggers gynogenesis in maize. EMBO J 36:707–717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Hua K, Tao X, Yuan F, Wang D, Zhu JK (2018) Precise A.T to G.C base editing in the rice genome. Mol Plant 11:627–630

    Article  CAS  PubMed  Google Scholar 

  14. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Kelliher T, Starr D, Richbourg L, Chintamanani S, Delzer B, Nuccio ML, Green J, Chen Z, McCuiston J, Wang W, Liebler T, Bullock P, Martin B (2017) MATRILINEAL, a sperm-specific phospholipase, triggers maize haploid induction. Nature 542:105–109

    Article  CAS  PubMed  Google Scholar 

  16. Li JF, Norville JE, Aach J, McCormack M, Zhang D, Bush J, Church GM, Sheen J (2013) Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nat Biotechnol 31:688–691

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Liu C, Li X, Meng D, Zhong Y, Chen C, Dong X, Xu X, Chen B, Li W, Li L, Tian X, Zhao H, Song W, Luo H, Zhang Q, Lai J, Jin W, Yan J, Chen S (2017) A 4-bp insertion at ZmPLA1 encoding a putative phospholipase a generates haploid induction in Maize. Mol Plant 10:520–522

    Article  CAS  PubMed  Google Scholar 

  18. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, Norville JE, Church GM (2013) RNA-guided human genome engineering via Cas9. Science 339:823–826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Mazier M, Flamain F, Nicolai M, Sarnette V, Caranta C (2011) Knock-down of both eIF4E1 and eIF4E2 genes confers broad-spectrum resistance against potyviruses in tomato. PLoS One 6:e29595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Nekrasov V, Staskawicz B, Weigel D, Jones JD, Kamoun S (2013) Targeted mutagenesis in the model plant nicotiana benthamiana using Cas9 RNA-guided endonuclease. Nat Biotechnol 31:691–693

    Article  CAS  PubMed  Google Scholar 

  21. Nieves-Cordones M, Mohamed S, Tanoi K, Kobayashi NI, Takagi K, Vernet A, Guiderdoni E, Perin C, Sentenac H, Very AA (2017) Production of low-Cs(+) rice plants by inactivation of the K(+) transporter OsHAK1 with the CRISPR-Cas system. Plant J 92:43–56

    Article  CAS  PubMed  Google Scholar 

  22. Puchta H (2017) Applying CRISPR/Cas for genome engineering in plants: the best is yet to come. Curr Opin Plant Biol 36:1–8

    Article  CAS  Google Scholar 

  23. Pyott DE, Sheehan E, Molnar A (2016) Engineering of CRISPR/Cas9-mediated potyvirus resistance in transgene-free Arabidopsis plants. Mol Plant Pathol 17:1276–1288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Shan Q, Wang Y, Li J, Zhang Y, Chen K, Liang Z, Zhang K, Liu J, Xi JJ, Qiu JL, Gao C (2013) Targeted genome modification of crop plants using a CRISPR-Cas system. Nat Biotechnol 31:686–688

    Article  CAS  Google Scholar 

  25. Sun Y, Zhang X, Wu C, He Y, Ma Y, Hou H, Guo X, Du W, Zhao Y, Xia L (2016) Engineering herbicide-resistant rice plants through CRISPR/Cas9-mediated homologous recombination of acetolactate synthase. Mol Plant 9:628–631

    Article  CAS  Google Scholar 

  26. Svitashev S, Young JK, Schwartz C, Gao H, Falco SC, Cigan AM (2015) Targeted mutagenesis, precise gene editing, and site-specific gene insertion in Maize using Cas9 and guide RNA. Plant Physiol 169:931–945

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Veillet F, Chauvin L, Kermarrec M-P, Sevestre F, Merrer M, Terret Z, Szydlowski N, Devaux P, Gallois J-L, Chauvin J-E (2019) The Solanum tuberosum GBSSI gene: a target for assessing gene and base editing in tetraploid potato. Plant Cell Rep. https://doi.org/10.1007/s00299-019-02426-w

    Article  PubMed  Google Scholar 

  28. Xie K, Yang Y (2013) RNA-guided genome editing in plants using a CRISPR-Cas system. Mol Plant 6:1975–1983

    Article  CAS  PubMed  Google Scholar 

  29. Zong Y, Wang Y, Li C, Zhang R, Chen K, Ran Y, Qiu JL, Wang D, Gao C (2017) Precise base editing in rice, wheat and maize with a Cas9-cytidine deaminase fusion. Nat Biotechnol 35:438–440

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was funded by the Investissement d’Avenir program of the French National Agency of Research for the Project GENIUS (ANR-11-BTBR-0001_GENIUS). The IJPB benefits from the support of the LabEx Saclay Plant Sciences-SPS (ANR-10-LABX-0040-SPS).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Peter M. Rogowsky.

Additional information

Publisher's Note

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

Disclaimer: The opinions expressed and arguments employed in this paper are the sole responsibility of the authors and do not necessarily reflect those of the OECD or of the governments of its Member countries.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Nogué, F., Vergne, P., Chèvre, AM. et al. Crop plants with improved culture and quality traits for food, feed and other uses. Transgenic Res 28, 65–73 (2019). https://doi.org/10.1007/s11248-019-00135-4

Download citation

Keywords

  • Agriculture
  • CRISPR-Cas9
  • Genome editing
  • New plant breeding techniques