Abstract
Key message
A point mutation of RPM1 triggers persistent immune response that induces leaf premature senescence in wheat, providing novel information of immune responses and leaf senescence.
Abstract
Leaf premature senescence in wheat (Triticum aestivum L.) is one of the most common factors affecting the plant's development and yield. In this study, we identified a novel wheat mutant, yellow leaf and premature senescence (ylp), which exhibits yellow leaves and premature senescence at the heading and flowering stages. Consistent with the yellow leaves phenotype, ylp had damaged and collapsed chloroplasts. Map-based cloning revealed that the phenotype of ylp was caused by a point mutation from Arg to His at amino acid 790 in a plasma membrane–localized protein resistance to Pseudomonas syringae pv. maculicola 1 (RPM1). The point mutation triggered excessive immune responses and the upregulation of senescence- and autophagy-associated genes. This work provided the information for understanding the molecular regulatory mechanism of leaf senescence, and the results would be important to analyze which mutations of RPM1 could enable plants to obtain immune activation without negative effects on plant growth.
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Acknowledgements
We thank Dr. Zhiyong Liu (Institute of Genetics and Developmental Biology, Chinese Academy of Sciences) for providing the EMS-mutagenized population. We thank Drs. Huaizhi Zhang and Guanghao Guo (Institute of Genetics and Developmental Biology, Chinese Academy of Sciences) for stripe rust resistance phenotyping at the adult plant stage.
Funding
This work was supported by National Natural Science Foundation of China (grant no. 32125030), National Key Research and Development Program of China (2020YFE0202300), and Pinduoduo-China Agricultural University Research Fund (PC2023A01003).
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Yingyin Yao and Jinkun Du conceived the project; Wenjia Zhang performed the experiments; Zhaoheng Zhang, Zihao Wang and Wanjun Song performed bioinformatics analysis; Qian Chen and Kai Yang provided technological assistance; Mingming Xin, Zhaorong Hu, Jie Liu, Huiru Peng, Jinsheng Lai, Weilong Guo, Zhongfu Ni, and Oixin Sun provided theoretical contributions to the project; Wenjia Zhang, Yingyin Yao and Jinkun Du contributed to article writing and revision.
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Supplementary Information
Fig. S1 Phenotypic and genetic analysis of F1 and F2 progenies. (a) Phenotypic of the WT, ylp and the F1 from cross between ylp mutant and WT at anthesis stage. Bar, 10 cm. (b) Phenotypic of the Baofeng104 (BF104), ylp and the F1 from cross between ylp and BF104 at anthesis stage. Bar, 10 cm. (c) The segregation ratio of F2 progeny derived from self-pollination of BF104 × ylp.
Fig. S2 Heatmap representing the transcriptional changes of the YLP fine localization region genes in ylp mutants relative to WT. Only four genes were expressed in the fine localization region of YLP. TraesCSC2D01G059100 and TraesCSC2D01G060500 were expressed in the leaves of seedling stage (a) and heading stage (b), while TraesCSC2D01G059400 was only expressed at seedling stage (a) and TraesCSC2D01G059300 was only expressed at heading stage (b). Heat map illustrating the FPKM-based expression patterns of genes in seedling stage (a) and heading stage (b) leaf of the WT and ylp. For each gene, the average value of FPKM values of three biological replicates. Red text indicates the expressed genes.
Fig. S3 Foliar tissues of the WT and the ylp mutants post-inoculated with the Pst races CYR34 were photographed at 20 dpi. Bar, 5 cm.
Fig. S4 Nicotiana benthamiana leaves were agro-infiltrated with constructs expressing heterozygous allele (co-expressed RPM1-H-GFP and RPM1-R-GFP), RPM1-R from WT and RPM1-H from ylp, respectively. Representative leaves were imaged 2, 3, and 4 d after agro-infiltration.
Fig. S5 Heatmap representing the transcriptional changes of plant-type hypersensitive response (HR) genes in ylp mutants relative to WT. Heat map illustrating the FPKM-based expression patterns of HR response gene in seedling stage leaf of the WT and ylp. For each gene, the average value of FPKM values of three biological replicates for each sample was normalized by R and reported as a heatmap.
Fig. S6 Heatmap representing the transcriptional changes of reactive oxygen species (ROS) responsive genes in ylp mutant relative to WT. Heat map illustrating the FPKM-based expression patterns of ROS responsive genes in seedling stage leaf of the WT and ylp. For each gene, the average value of FPKM values of three biological replicates for each sample was normalized by R and reported as a heatmap.
Fig. S7 Heatmap representing the transcriptional changes of pathogenesis-related (PR) defense response marker genes in ylp mutant relative to WT. Heatmap representing the transcriptional changes of pathogenesis-related (PR) defense response marker genes in ylp mutants relative to WT. Heat map illustrating the FPKM-based expression patterns of pathogenesis-related (PR) defense response marker genes in seedling stage leaf of the WT and ylp. For each gene, the average value of FPKM values of three biological replicates for each sample was normalized by R and reported as a heatmap.
Fig. S8 Subcellular localization of RPM1-R and its mutant form RPM1-H. Transient expression of 35S::TaRPM1-R-GFP, 35S::TaRPM1-H-GFP and 35S::PIP2-RFP (OD600 = 0.2) was performed in Nicotiana benthamiana leaves. Images were collected at the time 28 h after agrobacteria infiltration. 35S:PIP2-RFP (OD600 = 0.2) was used as a plasma membrane marker.
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Zhang, W., Zhang, Z., Chen, Q. et al. Mutation of a highly conserved amino acid in RPM1 causes leaf yellowing and premature senescence in wheat. Theor Appl Genet 136, 254 (2023). https://doi.org/10.1007/s00122-023-04499-4
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DOI: https://doi.org/10.1007/s00122-023-04499-4