Genome-edited powdery mildew resistance in wheat without growth penalties

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-Long Qiu () and Caixia Gao ()
Additional contact information
Shengnan Li: Chinese Academy of Sciences
Dexing Lin: Chinese Academy of Sciences
Yunwei Zhang: Chinese Academy of Sciences
Min Deng: Chinese Academy of Sciences
Yongxing Chen: Chinese Academy of Sciences
Bin Lv: Chinese Academy of Sciences
Boshu Li: Chinese Academy of Sciences
Yuan Lei: Chinese Academy of Sciences
Yanpeng Wang: Chinese Academy of Sciences
Long Zhao: Chinese Academy of Sciences
Yueting Liang: Chinese Academy of Sciences
Jinxing Liu: Chinese Academy of Sciences
Kunling Chen: Chinese Academy of Sciences
Zhiyong Liu: Chinese Academy of Sciences
Jun Xiao: Chinese Academy of Sciences
Jin-Long Qiu: Chinese Academy of Sciences
Caixia Gao: Chinese Academy of Sciences

Nature, 2022, vol. 602, issue 7897, 455-460

Abstract: 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.

Date: 2022
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DOI: 10.1038/s41586-022-04395-9

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