Simultaneous modification of three homoeologs of Ta EDR 1 by genome editing enhances powdery mildew resistance in wheat
Open accessAbstract
Wheat (Triticum aestivum L.) incurs significant yield losses from powdery mildew, a major fungal disease caused by Blumeria graminis f. sp. tritici (Bgt). enhanced disease resistance1 (EDR1) plays a negative role in the defense response against powdery mildew in Arabidopsis thaliana; however, the edr1 mutant does not show constitutively activated defense responses. This makes EDR1 an ideal target for approaches using new genome-editing tools to improve resistance to powdery mildew. We cloned TaEDR1 from hexaploid wheat and found high similarity among the three homoeologs of EDR1. Knock-down of TaEDR1 by virus-induced gene silencing or RNA interference enhanced resistance to powdery mildew, indicating that TaEDR1 negatively regulates powdery mildew resistance in wheat. We used CRISPR/Cas9 technology to generate Taedr1 wheat plants by simultaneous modification of the three homoeologs of wheat EDR1. No off-target mutations were detected in the Taedr1 mutant plants. The Taedr1 plants were resistant to powdery mildew and did not show mildew-induced cell death. Our study represents the successful generation of a potentially valuable trait using genome-editing technology in wheat and provides germplasm for disease resistance breeding.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
CRISPR variants Cas12 and Cas13 offered improvements in specificity and reduced off-target effects compared to Cas9.
“The CRISPR variants Cas12 and Cas13 offered improvements in specificity and reduced off-target effects compared to Cas9 and proved to be a highly efficient gene editing tool with complementary properties and functionality to Cas9 (Zetsche et al., 2017; Zhang et al., 2017).”
From Emerging applications of gene editing technologies for the development of climate-resilient crops (2025) · cites this paper as Zhang et al., 2017
The section on knocking out TaEDR1 with CRISPR/Cas9 reports no mutations at seven predicted off-target sites in its Cas9-edited wheat plants. Our copy does not address Cas12 or Cas13 or compare their specificity and off-target effects with Cas9 (searched: Cas12, Cas13, Cpf1, and complementary properties). (LLM, conf=0.78)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
A Programmable Dual-RNA–Guided DNA Endonuclease in Adaptive Bacterial Immunity
Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J. A., & Charpentier, E. (2012) · Science · doi:10.1126/science.1225829 · Cited by 17,116 · see citing works
Wang, Y., Cheng, X., Shan, Q., Zhang, Y., Liu, J., Gao, C., & Qiu, J.-L. (2014) · Nature Biotechnology · doi:10.1038/nbt.2969 · Cited by 2,072 · see citing works
Self-citationTargeted genome modification of crop plants using a CRISPR-Cas system
Shan, Q., Wang, Y., Li, J., Zhang, Y., Chen, K., Liang, Z., Zhang, K., Liu, J., Xi, J., Qiu, J., et al. (2013) · Nature Biotechnology · doi:10.1038/nbt.2650 · Cited by 1,965 · see citing works
Self-citationDouble-Strand Break End Resection and Repair Pathway Choice
Symington, L. S., & Gautier, J. (2011) · Annual Review of Genetics · doi:10.1146/annurev-genet-110410-132435 · Cited by 1,481 · see citing works
Zhang, Y., Liang, Z., Zong, Y., Wang, Y., Liu, J., Chen, K., Qiu, J., & Gao, C. (2016) · Nature Communications · doi:10.1038/ncomms12617 · Cited by 906 · see citing works
Self-citationCosts and benefits of priming for defense in Arabidopsis
van Hulten, M. H. A., Pelser, M., van Loon, L. C., Pieterse, C. M. J., & Ton, J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510213103 · Cited by 860 · see citing works
Genome editing in maize directed by CRISPR–Cas9 ribonucleoprotein complexes
Svitashev, S. K., Schwartz, C., Lenderts, B., Young, J. K., & Cigan, A. M. (2016) · Nature Communications · doi:10.1038/ncomms13274 · Cited by 826 · see citing works
Genome editing in rice and wheat using the CRISPR/Cas system
Shan, Q., Wang, Y., Li, J., & Gao, C. (2014) · Nature Protocols · doi:10.1038/nprot.2014.157 · Cited by 758 · see citing works
Self-citationDraft genome of the wheat A-genome progenitor Triticum urartu
Ling, H., Zhao, S., Liu, D., Wang, J., Sun, H., Zhang, C., 范华杰, Dong, L., Dong, L., Gao, C., et al. (2013) · Nature · doi:10.1038/nature11997 · Cited by 736 · see citing works
Self-citationAegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation
Jia, J., Zhao, S., Kong, X., Li, Y., Zhao, G., He, W., Appels, R., Pfeifer, M., Tao, Y., Zhang, X., et al. (2013) · Nature · doi:10.1038/nature12028 · Cited by 725 · see citing works
Self-citationTargeted Mutagenesis in Zea mays Using TALENs and the CRISPR/Cas System
Liang, Z., Zhang, K., Chen, K., & Gao, C. (2013) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2013.12.001 · Cited by 662 · see citing works
Self-citationBarley stripe mosaic virus ‐induced gene silencing in a monocot plant
Holzberg, S., Brosio, P., Gross, C., & Pogue, G. P. (2002) · The Plant Journal · doi:10.1046/j.1365-313x.2002.01291.x · Cited by 651 · see citing works
A reverse genetic, nontransgenic approach to wheat crop improvement by TILLING
Slade, A. J., Fuerstenberg, S. I., Loeffler, D., Steine, M. N., & Facciotti, D. (2004) · Nature Biotechnology · doi:10.1038/nbt1043 · Cited by 601 · see citing works
Large chromosomal deletions and heritable small genetic changes induced by CRISPR/Cas9 in rice
Zhou, H., Liu, B., Weeks, D. P., Spalding, M. H., & Yang, B. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku806 · Cited by 592 · see citing works
Lawrenson, T., Shorinola, O., Stacey, N., Li, C., Østergaard, L., Patron, N., Uauy, C., & Harwood, W. (2015) · Genome Biology · doi:10.1186/s13059-015-0826-7 · Cited by 551 · see citing works
Jia, H., Zhang, Y., Orbović, V., Xu, J. H., White, F. F., Jones, J. B., & Wang, N. (2016) · Plant Biotechnology Journal · doi:10.1111/pbi.12677 · Cited by 495 · see citing works
Self-citationDisease Impact on Wheat Yield Potential and Prospects of Genetic Control
Singh, R. P., Singh, P. K., Rutkoski, J. E., et al. (2016) · Annual Review of Phytopathology · doi:10.1146/annurev-phyto-080615-095835 · Cited by 484 · see citing works
Scofield, S. R., Huang, L., Brandt, A. S., & Gill, B. S. (2005) · PLANT PHYSIOLOGY · doi:10.1104/pp.105.061861 · Cited by 480 · see citing works
Plant genetic resources: What can they contribute toward increased crop productivity?
Hoisington, D. A., Khairallah, M., Reeves, T. G., Ribaut, J., Skovmand, B., Taba, S., & Warburton, M. L. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.11.5937 · Cited by 473 · see citing works
MATRILINEAL, a sperm-specific phospholipase, triggers maize haploid induction
Kelliher, T., Starr, D., Richbourg, L., Chintamanani, S., Delzer, B., Nuccio, M. L., Green, J., Chen, Z., McCuiston, J., Wang, W., et al. (2017) · Nature · doi:10.1038/nature20827 · Cited by 473 · see citing works
Variation in the flowering gene SELF PRUNING 5G promotes day-neutrality and early yield in tomato
Soyk, S., Müller, N. A., Park, S. J., Schmalenbach, I., Jiang, K., Hayama, R., Zhang, L., Eck, J. M. V., Jiménez‐Gómez, J. M., & Lippman, Z. B. (2016) · Nature Genetics · doi:10.1038/ng.3733 · Cited by 465 · see citing works
Plant Genome Engineering with Sequence-Specific Nucleases
Voytas, D. F. (2013) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-042811-105552 · Cited by 447 · see citing works
Yahiaoui, N., Srichumpa, P., Dudler, R., & Keller, B. (2004) · The Plant Journal · doi:10.1046/j.1365-313x.2003.01977.x · Cited by 436 · see citing works
Gene replacements and insertions in rice by intron targeting using CRISPR–Cas9
Li, J., Meng, X., Zong, Y., Chen, K., Zhang, H., Li, J., Li, J., & Gao, C. (2016) · Nature Plants · doi:10.1038/nplants.2016.139 · Cited by 431 · see citing works
Self-citationNegative regulation of defense responses in plants by a conserved MAPKK kinase
Frye, C. A., Tang, D., & Innes, R. W. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.98.1.373 · Cited by 401 · see citing works
Self-citationRNA-Guided Genome Editing for Target Gene Mutations in Wheat
Upadhyay, S. K., Kumar, J., Alok, A., & Tuli, R. (2013) · G3 Genes Genomes Genetics · doi:10.1534/g3.113.008847 · Cited by 392 · see citing works
Creation of fragrant rice by targeted knockout of the Os BADH 2 gene using TALEN technology
Shan, Q., Zhang, Y., Chen, K., Zhang, K., & Gao, C. (2015) · Plant Biotechnology Journal · doi:10.1111/pbi.12312 · Cited by 378 · see citing works
Self-citationWolter, M., Hollricher, K., Salamini, F., et al. (1993) · Molecular and General Genetics MGG · doi:10.1007/bf00281610 · Cited by 336 · see citing works
An Arabidopsis Mutant with Enhanced Resistance to Powdery Mildew
Frye, C. A., & Innes, R. W. (1998) · The Plant Cell · doi:10.1105/tpc.10.6.947 · Cited by 330 · see citing works
Cao, A., Xing, L., Wang, X., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1016981108 · Cited by 319 · see citing works
Rapid gene isolation in barley and wheat by mutant chromosome sequencing
Sánchez‐Martín, J., Steuernagel, B., Ghosh, S., Herren, G., Hurni, S., Adamski, N. M., Vrána, J., Kubaláková, M., Krattinger, S. G., Wicker, T., et al. (2016) · Genome biology · doi:10.1186/s13059-016-1082-1 · Cited by 318 · see citing works
Rapid and Efficient Gene Modification in Rice and Brachypodium Using TALENs
Shan, Q., Wang, Y., Chen, K., Liang, Z., Li, J., Zhang, Y., Zhang, K., Liu, J., Voytas, D. F., Zheng, X., et al. (2013) · Molecular Plant · doi:10.1093/mp/sss162 · Cited by 288 · see citing works
Self-citationTrade-off between growth and immunity: role of brassinosteroids
Lozano‐Durán, R., & Zipfel, C. (2014) · Trends in Plant Science · doi:10.1016/j.tplants.2014.09.003 · Cited by 266 · see citing works
Hurni, S., Brunner, S., Buchmann, G., Herren, G., Jordan, T., Krukowski, P., Wicker, T., Yahiaoui, N., Mago, R., & Keller, B. (2013) · The Plant Journal · doi:10.1111/tpj.12345 · Cited by 229 · see citing works
Acevedo‐Garcia, J., Spencer, D., Thieron, H., et al. (2016) · Plant Biotechnology Journal · doi:10.1111/pbi.12631 · Cited by 225 · see citing works
Peterhänsel, C., Freialdenhoven, A., Kurth, J., et al. (1997) · The Plant Cell · doi:10.1105/tpc.9.8.1397 · Cited by 199 · see citing works
Zhao, C., Nie, H., Shen, Q., et al. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004389 · Cited by 168 · see citing works
The growth–defense pivot: crisis management in plants mediated by LRR-RK surface receptors
Belkhadir, Y., Yang, L., Hetzel, J., Dangl, J. L., & Chory, J. (2014) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2014.06.006 · Cited by 162 · see citing works
Tang, D., Christiansen, K. M., & Innes, R. W. (2005) · PLANT PHYSIOLOGY · doi:10.1104/pp.105.060400 · Cited by 161 · see citing works
Self-citationZhou, H., Li, S., Deng, Z., Wang, X., Chen, T., Zhang, J., Chen, S., Ling, H., Zhang, A., Wang, D., et al. (2007) · The Plant Journal · doi:10.1111/j.1365-313x.2007.03246.x · Cited by 146 · see citing works
OsEDR1 negatively regulates rice bacterial resistance via activation of ethylene biosynthesis
Shen, X., Liu, H., Yuan, B., et al. (2010) · Plant Cell & Environment · doi:10.1111/j.1365-3040.2010.02219.x · Cited by 146 · see citing works
Tang, F., Yang, S., Liu, J., et al. (2015) · PLANT PHYSIOLOGY · doi:10.1104/pp.15.01661 · Cited by 145 · see citing works
Development of wheat near-isogenic lines for powdery mildew resistance
Zhou, R., Zhu, Z., Kong, X., et al. (2005) · Theoretical and Applied Genetics · doi:10.1007/s00122-004-1889-0 · Cited by 128 · see citing works
mlo ‐based powdery mildew immunity: silver bullet or simply non‐host resistance?
Humphry, M., Consonni, C., & Panstruga, R. (2006) · Molecular Plant Pathology · doi:10.1111/j.1364-3703.2006.00362.x · Cited by 109 · see citing works
Rasco-Gaunt, S., Riley, A., Cannell, M. E., et al. (2001) · Journal of Experimental Botany · doi:10.1093/jexbot/52.357.865 · Cited by 107 · see citing works
Kim, J.-A., Agrawal, G. K., Rakwal, R., Han, K.-S., Kim, K., Yun, C.-H., Heu, S., Park, S., Lee, Y., & Jwa, N. (2003) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(02)02944-3 · Cited by 105 · see citing works
Kusch, S., Pesch, L., & Panstruga, R. (2016) · Genome Biology and Evolution · doi:10.1093/gbe/evw036 · Cited by 104 · see citing works
Wu, G., Liu, S., Zhao, Y., et al. (2015) · The Plant Cell · doi:10.1105/tpc.114.134668 · Cited by 94 · see citing works
Self-citationPeterhänsel, C., Freialdenhoven, A., Kurth, J., et al. (1997) · The Plant Cell · doi:10.2307/3870390 · Cited by 94 · see citing works
RNA Interference in the Age of CRISPR: Will CRISPR Interfere with RNAi?
Unniyampurath, U., Pilankatta, R., & Krishnan, M. N. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17030291 · Cited by 85 · see citing works
Transgenic Pm3b wheat lines show resistance to powdery mildew in the field
Brunner, S., Hurni, S., Herren, G., et al. (2011) · Plant Biotechnology Journal · doi:10.1111/j.1467-7652.2011.00603.x · Cited by 72 · see citing works
Serrano, I., Gu, Y., Qi, D., et al. (2014) · The Plant Cell · doi:10.1105/tpc.114.131540 · Cited by 70 · see citing works
Liu, J., Zhang, T., Jia, J., et al. (2016) · PLANT PHYSIOLOGY · doi:10.1104/pp.15.01784 · Cited by 59 · see citing works
Pan, H., Liu, S., & Tang, D. (2011) · The Plant Journal · doi:10.1111/j.1365-313x.2011.04835.x · Cited by 58 · see citing works
Self-citationLiu, X., Khajuria, C., Li, J., et al. (2013) · Nature Communications · doi:10.1038/ncomms3070 · Cited by 45 · see citing works
Analysis of Nicotiana tabacum PIN genes identifies NtPIN4 as a key regulator of axillary bud growth
Xie, X., Qin, G., Si, P., Luo, Z., Gao, J., Chen, X., Zhang, J., Wei, P., Xia, Q., Lin, F., et al. (2017) · Physiologia Plantarum · doi:10.1111/ppl.12547 · Cited by 40 · see citing works
Xing, L., Qian, C., Cao, A., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0072571 · Cited by 26 · see citing works
Li, J., Zhao, W., Li, Q.-Z., et al. (2005) · PubMed · Cited by 24 · see citing works
Factors Influencing the Growth of Johne's Bacillus
Glavind, J., & Dam, H. (1948) · Physiologia Plantarum · doi:10.1111/j.1399-3054.1948.tb07107.x · Cited by 17 · see citing works
Cloning, characterization and expression of wheat EDR1 (enhanced disease resistance) gene.
Niu, J., Zhang, L., De-feng, H., et al. (2005) · PubMed · Cited by 4 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Applications of CRISPR–Cas in agriculture and plant biotechnology
Zhu, H., Li, C., & Gao, C. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-020-00288-9 · Cited by 870 · see citing works
Self-citationBiomass for a sustainable bioeconomy: An overview of world biomass production and utilization
Antar, M., Lyu, D., Nazari, M., Shah, A., Zhou, X., & Smith, D. L. (2021) · Renewable and Sustainable Energy Reviews · doi:10.1016/j.rser.2020.110691 · Cited by 878 · see citing works
The CRISPR/Cas9 system and its applications in crop genome editing
Bao, A., Burritt, D. J., Chen, H., Zhou, X., Cao, D., & Tran, L.-S. P. (2019) · Critical Reviews in Biotechnology · doi:10.1080/07388551.2018.1554621 · Cited by 185 · see citing works
CRISPR-based genome editing in wheat: a comprehensive review and future prospects
Kumar, R., Kaur, A., Pandey, A., Mamrutha, H. M., & Singh, G. P. (2019) · Molecular Biology Reports · doi:10.1007/s11033-019-04761-3 · Cited by 70 · see citing works
A CRISPR way for accelerating cereal crop improvement: Progress and challenges
Basu, U., Riaz Ahmed, S., Bhat, B. A., Anwar, Z., Ali, A., Ijaz, A., Gulzar, A., Bibi, A., Tyagi, A., Nebapure, S. M., et al. (2023) · Frontiers in Genetics · doi:10.3389/fgene.2022.866976 · Cited by 51 · see citing works
Tariq, A., Mushtaq, M., Yaqoob, H., Bhat, B. A., Zargar, S. M., Raza, A., Ali, S., Charagh, S., Mubarik, M. S., Zaman, Q. U., et al. (2023) · GM Crops & Food · doi:10.1080/21645698.2023.2219111 · Cited by 45 · see citing works
Emerging applications of gene editing technologies for the development of climate-resilient crops
Chavhan, R. L., Jaybhaye, S. G., Hinge, V. R., Deshmukh, A. S., Shaikh, U. S., Jadhav, P. K., Kadam, U. S., & Hong, J. C. (2025) · Frontiers in Genome Editing · doi:10.3389/fgeed.2025.1524767 · Cited by 43 · see citing works
- Authors
- Zhang, Y., Bai, Y., Wu, G., Zou, S., Chen, Y., Gao, C., & Tang, D.
- Affiliations
- Chinese Academy of Sciences (CN)
- Corresponding author
- Gao, Caixia
- Tang, Dingzhong
- Venue
- The Plant Journal
- Publisher
- Wiley
- Published
- 2017-06-13
- Volume
- 91
- Issue
- 4
- Pages
- 714-724
- ISSN
- 0960-7412 (ISSN-L)
- 1365-313X
- OpenAlex
- W2612614002
- Cited by
- 525
- References
- 60
- Citations by year
- 2026: 35 · 2025: 59 · 2024: 66 · 2023: 75 · 2022: 100 · 2021: 67 · 2020: 59 · 2019: 37 · 2018: 19 · 2017: 6
- FWCI
- 32.56
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The Plant Journal (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Chinese Academy of Sciences (XDB11020100, KFZD‐SW‐107)
- Ministry of Science and Technology of the People's Republic of China (2014DFA31540, 2015CB910202)
- Topics
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Powdery Mildew Fungal Diseases
- Life Sciences › Agricultural and Biological Sciences › Plant Science › Wheat and Barley Genetics and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › CRISPR and Genetic Engineering
- Keywords
- homoeologs, wheat, powdery mildew resistance, Blumeria graminis f. sp. tritici, CRISPR/Cas9 genome editing, disease resistance breeding, virus-induced gene silencing, RNA interference
- MeSH terms
- Gene Editing, Amino Acid Sequence, Ascomycota, Plant Diseases, Polyploidy, Triticum, Sequence Alignment, Plant Leaves, Gene Silencing, Disease Resistance, Clustered Regularly Interspaced Short Palindromic Repeats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review