Genome editing of a rice CDP-DAG synthase confers multipathogen resistance

Gan Sha; Peng Sun; Xiaojing Kong; Xinyu Han; Qiping Sun; Laetitia Fouillen; Juan Zhao; Yun Li; Lei Yang; Yin Wang; Qiuwen Gong; Yaru Zhou; Wenqing Zhou; Rashmi Jain; Jie Gao; Renliang Huang; Xiaoyang Chen; Lu Zheng; Wanying Zhang; Ziting Qin; Qi Zhou; Qingdong Zeng; Kabin Xie; Jiandi Xu; Tsan-Yu Chiu; Liang Guo; Jenny C Mortimer; Yohann Boutté; Qiang Li; Zhensheng Kang; Pamela C Ronald; Guotian Li

doi:10.1038/s41586-023-06205-2

Genome editing of a rice CDP-DAG synthase confers multipathogen resistance

Nature. 2023 Jun;618(7967):1017-1023. doi: 10.1038/s41586-023-06205-2. Epub 2023 Jun 14.

Authors

Gan Sha^#^{1

2

3

4}, Peng Sun^#^{1

2

3

4}, Xiaojing Kong^{1

2

3

4}, Xinyu Han^{1

2

3

4}, Qiping Sun^{1

2

3

4}, Laetitia Fouillen⁵, Juan Zhao^{1

2

3

4

6}, Yun Li^{1

2

3

4}, Lei Yang^{1

2

3

4}, Yin Wang^{1

2

3

4}, Qiuwen Gong^{1

2

3

4}, Yaru Zhou^{1

2

3

4}, Wenqing Zhou^{1

2

3

4}, Rashmi Jain^{7

8}, Jie Gao⁹, Renliang Huang¹⁰, Xiaoyang Chen^{1

2

3

4

11}, Lu Zheng^{1

2

3

4}, Wanying Zhang^{1

2

3

4}, Ziting Qin^{1

2

3

4}, Qi Zhou¹², Qingdong Zeng¹³, Kabin Xie⁹, Jiandi Xu¹⁴, Tsan-Yu Chiu¹², Liang Guo⁹, Jenny C Mortimer^{8

15}, Yohann Boutté⁵, Qiang Li⁹, Zhensheng Kang¹³, Pamela C Ronald^{16

17

18}, Guotian Li^{19

20

21

22

23

24}

Affiliations

¹ National Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan, China.
² Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, China.
³ Hubei Key Laboratory of Plant Pathology, Huazhong Agricultural University, Wuhan, China.
⁴ The Center of Crop Nanobiotechnology, Huazhong Agricultural University, Wuhan, China.
⁵ Laboratoire de Biogenèse Membranaire, Université de Bordeaux, CNRS, Villenave-d'Ornon, France.
⁶ College of Chemistry and Life Sciences, Sichuan Provincial Key Laboratory for Development and Utilization of Characteristic Horticultural Biological Resources, Chengdu Normal University, Chengdu, China.
⁷ Department of Plant Pathology and the Genome Center, University of California, Davis, Davis, CA, USA.
⁸ Feedstocks Division, The Joint BioEnergy Institute, Emeryville, CA, USA.
⁹ National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, China.
¹⁰ National Engineering Research Center of Rice (Nanchang), Key Laboratory of Rice Physiology and Genetics of Jiangxi Province, Rice Research Institute, Jiangxi Academy of Agricultural Sciences, Nanchang, China.
¹¹ College of Plant Protection, Anhui Agricultural University, Hefei, China.
¹² BGI-Shenzhen, Shenzhen, China.
¹³ State Key Laboratory of Crop Stress Biology for Arid Areas, Northwest A&F University, Yangling, China.
¹⁴ Institute of Wetland Agriculture and Ecology, Shandong Academy of Agricultural Sciences, Jinan, China.
¹⁵ School of Agriculture, Food and Wine, University of Adelaide, Glen Osmond, South Australia, Australia.
¹⁶ Department of Plant Pathology and the Genome Center, University of California, Davis, Davis, CA, USA. pcronald@ucdavis.edu.
¹⁷ Feedstocks Division, The Joint BioEnergy Institute, Emeryville, CA, USA. pcronald@ucdavis.edu.
¹⁸ Innovative Genomics Institute, University of California, Berkeley, Berkeley, CA, USA. pcronald@ucdavis.edu.
¹⁹ National Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan, China. li4@mail.hzau.edu.cn.
²⁰ Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, China. li4@mail.hzau.edu.cn.
²¹ Hubei Key Laboratory of Plant Pathology, Huazhong Agricultural University, Wuhan, China. li4@mail.hzau.edu.cn.
²² The Center of Crop Nanobiotechnology, Huazhong Agricultural University, Wuhan, China. li4@mail.hzau.edu.cn.
²³ Department of Plant Pathology and the Genome Center, University of California, Davis, Davis, CA, USA. li4@mail.hzau.edu.cn.
²⁴ Feedstocks Division, The Joint BioEnergy Institute, Emeryville, CA, USA. li4@mail.hzau.edu.cn.

^# Contributed equally.

PMID: 37316672
DOI: 10.1038/s41586-023-06205-2

Abstract

The discovery and application of genome editing introduced a new era of plant breeding by giving researchers efficient tools for the precise engineering of crop genomes¹. Here we demonstrate the power of genome editing for engineering broad-spectrum disease resistance in rice (Oryza sativa). We first isolated a lesion mimic mutant (LMM) from a mutagenized rice population. We then demonstrated that a 29-base-pair deletion in a gene we named RESISTANCE TO BLAST1 (RBL1) caused broad-spectrum disease resistance and showed that this mutation caused an approximately 20-fold reduction in yield. RBL1 encodes a cytidine diphosphate diacylglycerol synthase that is required for phospholipid biosynthesis². Mutation of RBL1 results in reduced levels of phosphatidylinositol and its derivative phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P₂). In rice, PtdIns(4,5)P₂ is enriched in cellular structures that are specifically associated with effector secretion and fungal infection, suggesting that it has a role as a disease-susceptibility factor³. By using targeted genome editing, we obtained an allele of RBL1, named RBL1^Δ12, which confers broad-spectrum disease resistance but does not decrease yield in a model rice variety, as assessed in small-scale field trials. Our study has demonstrated the benefits of editing an LMM gene, a strategy relevant to diverse LMM genes and crops.

MeSH terms

Alleles
Diacylglycerol Cholinephosphotransferase* / genetics
Diacylglycerol Cholinephosphotransferase* / metabolism
Disease Resistance* / genetics
Gene Editing* / methods
Genome, Plant / genetics
Oryza* / enzymology
Oryza* / genetics
Oryza* / microbiology
Phosphatidylinositol 4,5-Diphosphate / metabolism
Phosphatidylinositols / metabolism
Plant Breeding* / methods
Plant Diseases* / genetics
Plant Diseases* / microbiology

Substances

Phosphatidylinositols
Phosphatidylinositol 4,5-Diphosphate
Diacylglycerol Cholinephosphotransferase