Physiological, Cytological, and Transcriptomic Analysis of Magnesium Protoporphyrin IX Methyltransferase Mutant Reveal Complex Genetic Regulatory Network Linking Chlorophyll Synthesis and Chloroplast Development in Rice
Functional defects in key genes for chlorophyll synthesis usually cause abnormal chloroplast development, but the genetic regulatory network for these key genes in regulating chloroplast development is still unclear. Magnesium protoporphyrin IX methyltransferase (ChlM) is a key rate-limiting enzyme...
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MDPI AG
2023-11-01
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| Online Access: | https://www.mdpi.com/2223-7747/12/21/3785 |
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| author | Youming Yao Hongyu Zhang Rong Guo Jiangmin Fan Siyi Liu Jianglin Liao Yingjin Huang Zhaohai Wang |
| author_facet | Youming Yao Hongyu Zhang Rong Guo Jiangmin Fan Siyi Liu Jianglin Liao Yingjin Huang Zhaohai Wang |
| author_sort | Youming Yao |
| collection | DOAJ |
| description | Functional defects in key genes for chlorophyll synthesis usually cause abnormal chloroplast development, but the genetic regulatory network for these key genes in regulating chloroplast development is still unclear. Magnesium protoporphyrin IX methyltransferase (ChlM) is a key rate-limiting enzyme in the process of chlorophyll synthesis. Physiological analysis showed that the chlorophyll and carotenoid contents were significantly decreased in the <i>chlm</i> mutant. Transmission electron microscopy demonstrated that the chloroplasts of the <i>chlm</i> mutant were not well developed, with poor, loose, and indistinct thylakoid membranes. Hormone content analysis found that jasmonic acid, salicylic acid, and auxin accumulated in the mutant. A comparative transcriptome profiling identified 1534 differentially expressed genes (DEGs) between <i>chlm</i> and the wild type, including 876 up-regulated genes and 658 down-regulated genes. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis revealed that these DEGs were highly involved in chlorophyll metabolism, chloroplast development, and photosynthesis. Protein−protein interaction network analysis found that protein translation played an essential role in the <i>ChlM</i> gene-regulated process. Specifically, 62 and 6 DEGs were annotated to regulate chlorophyll and carotenoid metabolism, respectively; 278 DEGs were predicted to be involved in regulating chloroplast development; 59 DEGs were found to regulate hormone regulatory pathways; 192 DEGs were annotated to regulate signal pathways; and 49 DEGs were putatively identified as transcription factors. Dozens of these genes have been well studied and reported to play essential roles in chlorophyll accumulation or chloroplast development, providing direct evidence for the reliability of the role of the identified DEGs. These findings suggest that chlorophyll synthesis and chloroplast development are actively regulated by the <i>ChlM</i> gene. And it is suggested that hormones, signal pathways, and transcription regulation were all involved in these regulation processes. The accuracy of transcriptome data was validated by quantitative real-time PCR (qRT-PCR) analysis. This study reveals a complex genetic regulatory network of the <i>ChlM</i> gene regulating chlorophyll synthesis and chloroplast development. The <i>ChlM</i> gene’s role in retrograde signaling was discussed. Jasmonic acid, salicylic acid, or their derivatives in a certain unknown state were proposed as retrograde signaling molecules in one of the signaling pathways from the chloroplast to nucleus. |
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| spelling | doaj.art-3a91cea9b5bd42b3be6d76dccc4c34cc2023-11-10T15:10:31ZengMDPI AGPlants2223-77472023-11-011221378510.3390/plants12213785Physiological, Cytological, and Transcriptomic Analysis of Magnesium Protoporphyrin IX Methyltransferase Mutant Reveal Complex Genetic Regulatory Network Linking Chlorophyll Synthesis and Chloroplast Development in RiceYouming Yao0Hongyu Zhang1Rong Guo2Jiangmin Fan3Siyi Liu4Jianglin Liao5Yingjin Huang6Zhaohai Wang7Key Laboratory of Crop Physiology, Ecology and Genetic Breeding (Jiangxi Agricultural University), Ministry of Education of the P.R. China, Nanchang 330045, ChinaKey Laboratory of Crop Physiology, Ecology and Genetic Breeding (Jiangxi Agricultural University), Ministry of Education of the P.R. China, Nanchang 330045, ChinaKey Laboratory of Crop Physiology, Ecology and Genetic Breeding (Jiangxi Agricultural University), Ministry of Education of the P.R. China, Nanchang 330045, ChinaKey Laboratory of Crop Physiology, Ecology and Genetic Breeding (Jiangxi Agricultural University), Ministry of Education of the P.R. China, Nanchang 330045, ChinaKey Laboratory of Crop Physiology, Ecology and Genetic Breeding (Jiangxi Agricultural University), Ministry of Education of the P.R. China, Nanchang 330045, ChinaKey Laboratory of Crop Physiology, Ecology and Genetic Breeding (Jiangxi Agricultural University), Ministry of Education of the P.R. China, Nanchang 330045, ChinaKey Laboratory of Crop Physiology, Ecology and Genetic Breeding (Jiangxi Agricultural University), Ministry of Education of the P.R. China, Nanchang 330045, ChinaKey Laboratory of Crop Physiology, Ecology and Genetic Breeding (Jiangxi Agricultural University), Ministry of Education of the P.R. China, Nanchang 330045, ChinaFunctional defects in key genes for chlorophyll synthesis usually cause abnormal chloroplast development, but the genetic regulatory network for these key genes in regulating chloroplast development is still unclear. Magnesium protoporphyrin IX methyltransferase (ChlM) is a key rate-limiting enzyme in the process of chlorophyll synthesis. Physiological analysis showed that the chlorophyll and carotenoid contents were significantly decreased in the <i>chlm</i> mutant. Transmission electron microscopy demonstrated that the chloroplasts of the <i>chlm</i> mutant were not well developed, with poor, loose, and indistinct thylakoid membranes. Hormone content analysis found that jasmonic acid, salicylic acid, and auxin accumulated in the mutant. A comparative transcriptome profiling identified 1534 differentially expressed genes (DEGs) between <i>chlm</i> and the wild type, including 876 up-regulated genes and 658 down-regulated genes. Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analysis revealed that these DEGs were highly involved in chlorophyll metabolism, chloroplast development, and photosynthesis. Protein−protein interaction network analysis found that protein translation played an essential role in the <i>ChlM</i> gene-regulated process. Specifically, 62 and 6 DEGs were annotated to regulate chlorophyll and carotenoid metabolism, respectively; 278 DEGs were predicted to be involved in regulating chloroplast development; 59 DEGs were found to regulate hormone regulatory pathways; 192 DEGs were annotated to regulate signal pathways; and 49 DEGs were putatively identified as transcription factors. Dozens of these genes have been well studied and reported to play essential roles in chlorophyll accumulation or chloroplast development, providing direct evidence for the reliability of the role of the identified DEGs. These findings suggest that chlorophyll synthesis and chloroplast development are actively regulated by the <i>ChlM</i> gene. And it is suggested that hormones, signal pathways, and transcription regulation were all involved in these regulation processes. The accuracy of transcriptome data was validated by quantitative real-time PCR (qRT-PCR) analysis. This study reveals a complex genetic regulatory network of the <i>ChlM</i> gene regulating chlorophyll synthesis and chloroplast development. The <i>ChlM</i> gene’s role in retrograde signaling was discussed. Jasmonic acid, salicylic acid, or their derivatives in a certain unknown state were proposed as retrograde signaling molecules in one of the signaling pathways from the chloroplast to nucleus.https://www.mdpi.com/2223-7747/12/21/3785magnesium protoporphyrin IX methyltransferase (ChlM)chlorophyll synthesischloroplast developmenthormonerice |
| spellingShingle | Youming Yao Hongyu Zhang Rong Guo Jiangmin Fan Siyi Liu Jianglin Liao Yingjin Huang Zhaohai Wang Physiological, Cytological, and Transcriptomic Analysis of Magnesium Protoporphyrin IX Methyltransferase Mutant Reveal Complex Genetic Regulatory Network Linking Chlorophyll Synthesis and Chloroplast Development in Rice Plants magnesium protoporphyrin IX methyltransferase (ChlM) chlorophyll synthesis chloroplast development hormone rice |
| title | Physiological, Cytological, and Transcriptomic Analysis of Magnesium Protoporphyrin IX Methyltransferase Mutant Reveal Complex Genetic Regulatory Network Linking Chlorophyll Synthesis and Chloroplast Development in Rice |
| title_full | Physiological, Cytological, and Transcriptomic Analysis of Magnesium Protoporphyrin IX Methyltransferase Mutant Reveal Complex Genetic Regulatory Network Linking Chlorophyll Synthesis and Chloroplast Development in Rice |
| title_fullStr | Physiological, Cytological, and Transcriptomic Analysis of Magnesium Protoporphyrin IX Methyltransferase Mutant Reveal Complex Genetic Regulatory Network Linking Chlorophyll Synthesis and Chloroplast Development in Rice |
| title_full_unstemmed | Physiological, Cytological, and Transcriptomic Analysis of Magnesium Protoporphyrin IX Methyltransferase Mutant Reveal Complex Genetic Regulatory Network Linking Chlorophyll Synthesis and Chloroplast Development in Rice |
| title_short | Physiological, Cytological, and Transcriptomic Analysis of Magnesium Protoporphyrin IX Methyltransferase Mutant Reveal Complex Genetic Regulatory Network Linking Chlorophyll Synthesis and Chloroplast Development in Rice |
| title_sort | physiological cytological and transcriptomic analysis of magnesium protoporphyrin ix methyltransferase mutant reveal complex genetic regulatory network linking chlorophyll synthesis and chloroplast development in rice |
| topic | magnesium protoporphyrin IX methyltransferase (ChlM) chlorophyll synthesis chloroplast development hormone rice |
| url | https://www.mdpi.com/2223-7747/12/21/3785 |
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