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

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 genomes 1 . Here we demonstrate the power of genome editing for engineering broad-spectrum disease resistance in rice ( Oryza sativa ). We...

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Published inNature (London) Vol. 618; no. 7967; pp. 1017 - 1023
Main Authors Sha, Gan, Sun, Peng, Kong, Xiaojing, Han, Xinyu, Sun, Qiping, Fouillen, Laetitia, Zhao, Juan, Li, Yun, Yang, Lei, Wang, Yin, Gong, Qiuwen, Zhou, Yaru, Zhou, Wenqing, Jain, Rashmi, Gao, Jie, Huang, Renliang, Chen, Xiaoyang, Zheng, Lu, Zhang, Wanying, Qin, Ziting, Zhou, Qi, Zeng, Qingdong, Xie, Kabin, Xu, Jiandi, Chiu, Tsan-Yu, Guo, Liang, Mortimer, Jenny C., Boutté, Yohann, Li, Qiang, Kang, Zhensheng, Ronald, Pamela C., Li, Guotian
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 29.06.2023
Nature Publishing Group
Subjects
38/1
38/23
38/39
45
45/44
45/70
631/1647/1511
631/449/2169
631/449/2661/2666
631/449/448/2024
631/61/447/8
96/35
96/63
Acids
Agricultural production
Alleles
Cellular structure
Diacylglycerol Cholinephosphotransferase - genetics
Diacylglycerol Cholinephosphotransferase - metabolism
Diglycerides
Disease resistance
Disease Resistance - genetics
Editing
Environmental Sciences
Fungal infections
Gene deletion
Gene Editing - methods
Genes
Genome editing
Genome, Plant - genetics
Genomes
Genotype & phenotype
Humanities and Social Sciences
Life Sciences
Medical research
multidisciplinary
Mutation
Oryza - enzymology
Oryza - genetics
Oryza - microbiology
Oryza sativa
Pathogens
Phosphatidylinositol 4,5-diphosphate
Phosphatidylinositol 4,5-Diphosphate - metabolism
Phosphatidylinositols - metabolism
Phospholipids
Plant breeding
Plant Breeding - methods
Plant diseases
Plant Diseases - genetics
Plant Diseases - microbiology
Rice
Science
Science & Technology - Other Topics
Science (multidisciplinary)
Yeast
Protein trafficking in plants
Genetic engineering
Biotic
Agricultural genetics
Plant immunity
Online AccessGet full text
ISSN0028-0836
1476-4687
1476-4687
DOI10.1038/s41586-023-06205-2

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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 genomes 1 . 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 biosynthesis 2 . Mutation of RBL1 results in reduced levels of phosphatidylinositol and its derivative phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P 2 ). In rice, PtdIns(4,5)P 2 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 factor 3 . 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. Editing of a rice gene that has a role in phospholipid synthesis has endowed rice plants with broad-spectrum resistance to disease, including protection from common bacterial and fungal pathogens, without decreasing the yield.
AbstractList Not provided.
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 genomes . 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 biosynthesis . Mutation of RBL1 results in reduced levels of phosphatidylinositol and its derivative phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P ). In rice, PtdIns(4,5)P 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 factor . By using targeted genome editing, we obtained an allele of RBL1, named RBL1 , 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.
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 RBL1Δ12, 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.
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 genomes 1 . 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 biosynthesis 2 . Mutation of RBL1 results in reduced levels of phosphatidylinositol and its derivative phosphatidylinositol 4,5-bisphosphate (PtdIns(4,5)P 2 ). In rice, PtdIns(4,5)P 2 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 factor 3 . 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. Editing of a rice gene that has a role in phospholipid synthesis has endowed rice plants with broad-spectrum resistance to disease, including protection from common bacterial and fungal pathogens, without decreasing the yield.
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 RBL1Δ12, 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.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 RBL1Δ12, 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.
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 TOBLAST1 (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 RBL1Δ12, 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.
Author Zeng, Qingdong
Zhou, Qi
Li, Yun
Sun, Qiping
Ronald, Pamela C.
Zhang, Wanying
Wang, Yin
Zhao, Juan
Gao, Jie
Xie, Kabin
Jain, Rashmi
Gong, Qiuwen
Zhou, Wenqing
Kong, Xiaojing
Li, Guotian
Chiu, Tsan-Yu
Qin, Ziting
Mortimer, Jenny C.
Han, Xinyu
Chen, Xiaoyang
Xu, Jiandi
Kang, Zhensheng
Boutté, Yohann
Sun, Peng
Zhou, Yaru
Huang, Renliang
Li, Qiang
Yang, Lei
Fouillen, Laetitia
Guo, Liang
Zheng, Lu
Sha, Gan
AuthorAffiliation 5 Laboratoire de Biogenèse Membranaire, Université de Bordeaux, CNRS, Villenave-d’Ornon, France
6 Department of Plant Pathology and the Genome Center, University of California, Davis, Davis, CA, USA
1 National Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan, China
7 Feedstocks Division, The Joint BioEnergy Institute, Emeryville, CA, USA
13 School of Agriculture, Food and Wine, University of Adelaide, Glen Osmond, South Australia, Australia
16 Present address: College of Plant Protection, Anhui Agricultural University, Hefei, China
15 Present address: College of Chemistry and Life Sciences, Sichuan Provincial Key Laboratory for Development and Utilization of Characteristic Horticultural Biological Resources, Chengdu Normal University, Chengdu, China
4 The Center of Crop Nanobiotechnology, Huazhong Agricultural University, Wuhan, China
14 Innovative Genomics Institute, University of California, Berkeley, Berkeley, CA, USA
11 State Key Laboratory of Crop Stress
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– name: 16 Present address: College of Plant Protection, Anhui Agricultural University, Hefei, China
– name: 2 Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, China
– name: 14 Innovative Genomics Institute, University of California, Berkeley, Berkeley, CA, USA
– name: 17 These authors contributed equally: Gan Sha, Peng Sun
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  organization: National Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Hubei Hongshan Laboratory, Huazhong Agricultural University, Hubei Key Laboratory of Plant Pathology, Huazhong Agricultural University, The Center of Crop Nanobiotechnology, Huazhong Agricultural University, Department of Plant Pathology and the Genome Center, University of California, Davis, Feedstocks Division, The Joint BioEnergy Institute
BackLink https://www.ncbi.nlm.nih.gov/pubmed/37316672$$D View this record in MEDLINE/PubMed
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https://www.osti.gov/biblio/2422796$$D View this record in Osti.gov
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Keywords Protein trafficking in plants
Genetic engineering
Biotic
Agricultural genetics
Plant immunity
Language English
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USDOE
AC02-05CH11231
Author contributions G.L., G.S., P.S. and P.C.R. designed the experiments. G.L. and R.J. screened and analysed the genomic data of the rbl1 mutant. G.S., P.S., X.K., X.H., Y.L., Y.W., Q.G., X.C. and L.Z. performed plant infection assays. G.S., X.K., X.H. and Y.W. performed DAB, ROS, salicylic acid, subcellular localization, RT–qPCR and GUS histochemical analyses. L.Y. and Z.Q. performed bioinformatics analysis. G.S., J.G., L.F., L.G., J.C.M., Y.B. and Q.L. performed lipidomics assays. Y.Z. and Y.W. performed chemical supplementation analyses of rbl1. G.S., Q.S., Q.G., Q. Zhou and T.-Y.C. performed yeast mutant complementation analyses. J.Z. and K.X. generated the CRISPR constructs. X.K., X.H., Y.L., W. Zhou, W. Zhang, Q. Zeng and Z.K. screened the edited lines. G.S., Y.W., R.H. and J.X. performed field trials and agronomic trait analyses. G.L. and G.S. drafted the manuscript and G.L., G.S., P.S., L.F., L.Z., L.G., K.X., J.C.M., Q.L., Y.B., Z.K. and P.C.R. revised the manuscript. All authors read and approved the final manuscript.
ORCID 0000-0001-9848-5496
0000-0002-7856-2340
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SSID ssj0005174
Score 2.681414
Snippet The discovery and application of genome editing introduced a new era of plant breeding by giving researchers efficient tools for the precise engineering of...
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631/449/2169
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Acids
Agricultural production
Alleles
Cellular structure
Diacylglycerol Cholinephosphotransferase - genetics
Diacylglycerol Cholinephosphotransferase - metabolism
Diglycerides
Disease resistance
Disease Resistance - genetics
Editing
Environmental Sciences
Fungal infections
Gene deletion
Gene Editing - methods
Genes
Genome editing
Genome, Plant - genetics
Genomes
Genotype & phenotype
Humanities and Social Sciences
Life Sciences
Medical research
multidisciplinary
Mutation
Oryza - enzymology
Oryza - genetics
Oryza - microbiology
Oryza sativa
Pathogens
Phosphatidylinositol 4,5-diphosphate
Phosphatidylinositol 4,5-Diphosphate - metabolism
Phosphatidylinositols - metabolism
Phospholipids
Plant breeding
Plant Breeding - methods
Plant diseases
Plant Diseases - genetics
Plant Diseases - microbiology
Rice
Science
Science & Technology - Other Topics
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Title Genome editing of a rice CDP-DAG synthase confers multipathogen resistance
URI https://link.springer.com/article/10.1038/s41586-023-06205-2
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https://pubmed.ncbi.nlm.nih.gov/PMC11575942
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