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OsCUL3a-Associated Molecular Switches Have Functions in Cell Metabolism, Cell Death, and Disease Resistance
Zhiqiang Gao1,2,3, Qunen Liu1,2, Yingxin Zhang1,2
1State Key Laboratory of Rice Biology, China National Rice Research Institute, Hangzhou, Zhejiang 310006, People's Republic of China.
Abstract:
This study applies parallel reaction monitoring (PRM) proteomics and CRISPR-Cas9 mutagenesis to identify relationships between cell metabolism, cell death, and disease resistance. In oscul3a (oscullin3a) mutants, OsCUL3a-associated molecular switches are responsible for disrupted cell metabolism that leads to increased total lipid content in rice grain, a late accumulation of H2O2 in leaves, enhanced Xanthomonas oryzae pv. oryzae disease resistance, and suppressed panicle and first internode growth. In oscul3a mutants, PRM-confirmed upregulated molecular switch proteins include lipoxygenases (CM-LOX1 and CM-LOX2), suggesting a novel connection between ferroptosis and rice lesion mimic formation. Rice immunity-associated proteins OsNPR1 and OsNPR3 were shown to interact with each other and have opposing regulatory effects based on the cell death phenotype of osnpr1/oscul3a and osnpr3/oscul3a double mutants. Together, these results describe a network that regulates plant growth, disease resistance, and grain quality that includes the E3 ligase OsCUL3a, cell metabolism-associated molecular switches, and immunity switches OsNPR1 and OsNPR3.
Insights
Rice mutants lacking OsCUL3a show altered metabolism, increased grain lipids, and enhanced disease resistance. This study reveals a network connecting plant growth, immunity, and grain quality.
Area of Science:
- Plant Molecular Biology
- Plant Pathology
- Proteomics
- Genetics
Background:
- Understanding the molecular mechanisms regulating plant growth, disease resistance, and grain quality is crucial for crop improvement.
- The E3 ligase OsCUL3a and its associated proteins play a role in plant development and stress responses, but their precise functions remain largely unelucidated.
Purpose of the Study:
- To investigate the function of OsCUL3a in rice by identifying its interacting proteins and understanding its role in regulating cell metabolism, cell death, and disease resistance.
- To elucidate the molecular network involving OsCUL3a, metabolic switches, and immunity regulators in rice.
Main Methods:
- Utilized parallel reaction monitoring (PRM) proteomics to identify differentially expressed proteins in rice mutants.
- Employed CRISPR-Cas9 mutagenesis to generate and analyze osacul3a mutants and double mutants with immunity-related genes (OsNPR1, OsNPR3).
- Assessed plant growth parameters, grain lipid content, hydrogen peroxide (H2O2) accumulation, and disease resistance against Xanthomonas oryzae pv. oryzae.
Main Results:
- osacul3a mutants exhibited disrupted cell metabolism, increased total lipid content in rice grain, late H2O2 accumulation in leaves, enhanced resistance to Xanthomonas oryzae pv. oryzae, and suppressed growth of panicles and first internodes.
- Proteomics analysis revealed upregulated lipoxygenases (CM-LOX1 and CM-LOX2) in osacul3a mutants, suggesting a link between ferroptosis and lesion mimic formation.
- Rice immunity proteins OsNPR1 and OsNPR3 interacted and showed opposing regulatory effects in osacul3a double mutants, indicating their roles in cell death phenotypes and immunity.
Conclusions:
- The E3 ligase OsCUL3a is a key regulator of a complex network integrating plant growth, disease resistance, and grain quality in rice.
- OsCUL3a influences cell metabolism through associated molecular switches, potentially involving ferroptosis and lesion mimic pathways.
- OsNPR1 and OsNPR3 act as immunity switches with opposing functions, interacting with OsCUL3a to modulate plant defense responses and cell death.
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