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Genome-edited powdery mildew resistance in wheat without growth penalties

Author

Listed:
  • Shengnan Li

    (Chinese Academy of Sciences)

  • Dexing Lin

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Yunwei Zhang

    (Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Min Deng

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Yongxing Chen

    (Chinese Academy of Sciences)

  • Bin Lv

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Boshu Li

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Yuan Lei

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Yanpeng Wang

    (Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Long Zhao

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Yueting Liang

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Jinxing Liu

    (Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Kunling Chen

    (Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Zhiyong Liu

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Jun Xiao

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences
    Chinese Academy of Sciences)

  • Jin-Long Qiu

    (Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

  • Caixia Gao

    (Chinese Academy of Sciences
    Chinese Academy of Sciences
    University of Chinese Academy of Sciences)

Abstract

Disruption of susceptibility (S) genes in crops is an attractive breeding strategy for conferring disease resistance1,2. However, S genes are implicated in many essential biological functions and deletion of these genes typically results in undesired pleiotropic effects1. Loss-of-function mutations in one such S gene, Mildew resistance locus O (MLO), confers durable and broad-spectrum resistance to powdery mildew in various plant species2,3. However, mlo-associated resistance is also accompanied by growth penalties and yield losses3,4, thereby limiting its widespread use in agriculture. Here we describe Tamlo-R32, a mutant with a 304-kilobase pair targeted deletion in the MLO-B1 locus of wheat that retains crop growth and yields while conferring robust powdery mildew resistance. We show that this deletion results in an altered local chromatin landscape, leading to the ectopic activation of Tonoplast monosaccharide transporter 3 (TaTMT3B), and that this activation alleviates growth and yield penalties associated with MLO disruption. Notably, the function of TMT3 is conserved in other plant species such as Arabidopsis thaliana. Moreover, precision genome editing facilitates the rapid introduction of this mlo resistance allele (Tamlo-R32) into elite wheat varieties. This work demonstrates the ability to stack genetic changes to rescue growth defects caused by recessive alleles, which is critical for developing high-yielding crop varieties with robust and durable disease resistance.

Suggested Citation

  • Shengnan Li & Dexing Lin & Yunwei Zhang & Min Deng & Yongxing Chen & Bin Lv & Boshu Li & Yuan Lei & Yanpeng Wang & Long Zhao & Yueting Liang & Jinxing Liu & Kunling Chen & Zhiyong Liu & Jun Xiao & Jin, 2022. "Genome-edited powdery mildew resistance in wheat without growth penalties," Nature, Nature, vol. 602(7897), pages 455-460, February.
  • Handle: RePEc:nat:nature:v:602:y:2022:i:7897:d:10.1038_s41586-022-04395-9
    DOI: 10.1038/s41586-022-04395-9
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    Citations

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    Cited by:

    1. Mengmeng Li & Zige Yang & Cheng Chang, 2022. "Susceptibility Is New Resistance: Wheat Susceptibility Genes and Exploitation in Resistance Breeding," Agriculture, MDPI, vol. 12(9), pages 1-13, September.
    2. Michelle L. Johnson & Bruce A. Hay & Maciej Maselko, 2024. "Altering traits and fates of wild populations with Mendelian DNA sequence modifying Allele Sails," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    3. Tianye Zhang & Chaonan Shi & Haichao Hu & Zhuo Zhang & Ziqiong Wang & Zhiqing Chen & Huimin Feng & Peng Liu & Jun Guo & Qisen Lu & Kaili Zhong & ZhiHui Chen & Jiaqian Liu & Jiancheng Yu & Jianping Che, 2022. "N6-methyladenosine RNA modification promotes viral genomic RNA stability and infection," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    4. Rongrong Zhang & Yu Wu & Xiangru Qu & Wenjuan Yang & Qin Wu & Lin Huang & Qiantao Jiang & Jian Ma & Yazhou Zhang & Pengfei Qi & Guoyue Chen & Yunfeng Jiang & Youliang Zheng & Xiaojie Wang & Yuming Wei, 2024. "The RING-finger ubiquitin E3 ligase TaPIR1 targets TaHRP1 for degradation to suppress chloroplast function," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    5. Fei Shen & Shixiao Xu & Qi Shen & Changwei Bi & Martin A. Lysak, 2023. "The allotetraploid horseradish genome provides insights into subgenome diversification and formation of critical traits," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    6. Taikui Zhang & Weichen Huang & Lin Zhang & De-Zhu Li & Ji Qi & Hong Ma, 2024. "Phylogenomic profiles of whole-genome duplications in Poaceae and landscape of differential duplicate retention and losses among major Poaceae lineages," Nature Communications, Nature, vol. 15(1), pages 1-27, December.
    7. Qichen Yuan & Xue Gao, 2022. "Multiplex base- and prime-editing with drive-and-process CRISPR arrays," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    8. Zhaojiang Guo & Le Guo & Jianying Qin & Fan Ye & Dan Sun & Qingjun Wu & Shaoli Wang & Neil Crickmore & Xuguo Zhou & Alejandra Bravo & Mario SoberĂ³n & Youjun Zhang, 2022. "A single transcription factor facilitates an insect host combating Bacillus thuringiensis infection while maintaining fitness," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    9. Hang Su & Yuanchun Wang & Jin Xu & Ahmad A. Omar & Jude W. Grosser & Milica Calovic & Liyang Zhang & Yu Feng & Christopher A. Vakulskas & Nian Wang, 2023. "Generation of the transgene-free canker-resistant Citrus sinensis using Cas12a/crRNA ribonucleoprotein in the T0 generation," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    10. Yayu Guo & Shufang Wang & Keji Yu & Hou-Ling Wang & Huimin Xu & Chengwei Song & Yuanyuan Zhao & Jialong Wen & Chunxiang Fu & Yu Li & Shuizhong Wang & Xi Zhang & Yan Zhang & Yuan Cao & Fenjuan Shao & X, 2023. "Manipulating microRNA miR408 enhances both biomass yield and saccharification efficiency in poplar," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

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