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Engineering disease-resistant plants with alternative translation efficiency by switching uORF types through CRISPR

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Abstract

Engineering disease-resistant plants can be a powerful solution to the issue of food security. However, it requires addressing two fundamental questions: what genes to express and how to control their expressions. To find a solution, we screen CRISPR-edited upstream open reading frame (uORF) variants in rice, aiming to optimize translational control of disease-related genes. By switching uORF types of the 5′-leader from Arabidopsis TBF1, we modulate the ribosome accessibility to the downstream firefly luciferase. We assume that by switching uORF types using CRISPR, we could generate uORF variants with alternative translation efficiency (CRISPR-aTrE-uORF). These variants, capable of boosting translation for resistance-associated genes and dampening it for susceptible ones, can help pinpoint previously unidentified genes with optimal expression levels. To test the assumption, we screened edited uORF variants and found that enhanced translational suppression of the plastic glutamine synthetase 2 can provide broad-spectrum disease resistance in rice with minimal fitness costs. This strategy, which involves modifying uORFs from none to some, or from some to none or different ones, demonstrates how translational agriculture can speed up the development of disease-resistant crops. This is vital for tackling the food security challenges we face due to growing populations and changing climates.

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Data availability

The select Ribo-seq and other NGS sequencing data generated in this study have been deposited in Gene Expression Omnibus under accession numbers PRJNA906650 and PRJNA970919, respectively. Supplementary Tables can be accessed on this website (http://www.rnairport.com:443/public/CRISPR_a-TrE_uORF/).

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Acknowledgement

This study was supported by the National Key Research and Development Program of China (2023ZD04073), the Major Project of Hubei Hongshan Laboratory (2022hszd016), the National Natural Science Foundation of China (32070284, 32172421), the Key Research and Development Program of Hubei Province (2022BFE003) and the Fundamental Research Funds for the Central Universities (2662023PY006).

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Authors and Affiliations

  1. National Key Laboratory of Crop Genetic Improvement, National Centre of Plant Gene Research (Wuhan), Huazhong Agricultural University, Wuhan, 430070, China

    Jingjing Tian, Dan Yang, Dan Chen & Meng Yuan

  2. State Key Laboratory of Hybrid Rice, Institute for Advanced Studies (IAS), Wuhan University, Wuhan, 430072, China

    Zhijuan Tang, Ruixia Niu, Yulu Zhou, Ming Luo, Rui Mou & Guoyong Xu

  3. Hubei Hongshan Laboratory, Wuhan, 430070, China

    Meng Yuan & Guoyong Xu

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  1. Jingjing Tian
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  10. Guoyong Xu
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Correspondence to Meng Yuan or Guoyong Xu.

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A patent (application number: 2024104091412) based on this study has been filed by Wuhan University with G.X., Z.T., R.N. and R.M. as inventors. The author(s) declare that they have no other conflict of interest.

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Tian, J., Tang, Z., Niu, R. et al. Engineering disease-resistant plants with alternative translation efficiency by switching uORF types through CRISPR. Sci. China Life Sci. (2024). https://doi.org/10.1007/s11427-024-2588-9

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