Integration of transcriptomic and proteomic analyses reveals several levels of metabolic regulation in the excess starch and early senescent leaf mutant lses1 in rice
Abstract Background The normal metabolism of transitory starch in leaves plays an important role in ensuring photosynthesis, delaying senescence and maintaining high yield in crops. OsCKI1 (casein kinase I1) plays crucial regulatory roles in multiple important physiological processes, including root...
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| Format: | Article |
| Language: | English |
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BMC
2022-03-01
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| Series: | BMC Plant Biology |
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| Online Access: | https://doi.org/10.1186/s12870-022-03510-2 |
| _version_ | 1818776093741547520 |
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| author | Zhiming Chen Yongsheng Wang Rongyu Huang Zesen Zhang Jinpeng Huang Feng Yu Yaohai Lin Yuchun Guo Kangjing Liang Yuanchang Zhou Fangyu Chen |
| author_facet | Zhiming Chen Yongsheng Wang Rongyu Huang Zesen Zhang Jinpeng Huang Feng Yu Yaohai Lin Yuchun Guo Kangjing Liang Yuanchang Zhou Fangyu Chen |
| author_sort | Zhiming Chen |
| collection | DOAJ |
| description | Abstract Background The normal metabolism of transitory starch in leaves plays an important role in ensuring photosynthesis, delaying senescence and maintaining high yield in crops. OsCKI1 (casein kinase I1) plays crucial regulatory roles in multiple important physiological processes, including root development, hormonal signaling and low temperature-treatment adaptive growth in rice; however, its potential role in regulating temporary starch metabolism or premature leaf senescence remains unclear. To reveal the molecular regulatory mechanism of OsCKI1 in rice leaves, physiological, transcriptomic and proteomic analyses of leaves of osckI1 allele mutant lses1 (leaf starch excess and senescence 1) and its wild-type varieties (WT) were performed. Results Phenotypic identification and physiological measurements showed that the lses1 mutant exhibited starch excess in the leaves and an obvious leaf tip withering phenotype as well as high ROS and MDA contents, low chlorophyll content and protective enzyme activities compared to WT. The correlation analyses between protein and mRNA abundance are weak or limited. However, the changes of several important genes related to carbohydrate metabolism and apoptosis at the mRNA and protein levels were consistent. The protein-protein interaction (PPI) network might play accessory roles in promoting premature senescence of lses1 leaves. Comprehensive transcriptomic and proteomic analysis indicated that multiple key genes/proteins related to starch and sugar metabolism, apoptosis and ABA signaling exhibited significant differential expression. Abnormal increase in temporary starch was highly correlated with the expression of starch biosynthesis-related genes, which might be the main factor that causes premature leaf senescence and changes in multiple metabolic levels in leaves of lses1. In addition, four proteins associated with ABA accumulation and signaling, and three CKI potential target proteins related to starch biosynthesis were up-regulated in the lses1 mutant, suggesting that LSES1 may affect temporary starch accumulation and premature leaf senescence through phosphorylation crosstalk ABA signaling and starch anabolic pathways. Conclusion The current study established the high correlation between the changes in physiological characteristics and mRNA and protein expression profiles in lses1 leaves, and emphasized the positive effect of excessive starch on accelerating premature leaf senescence. The expression patterns of genes/proteins related to starch biosynthesis and ABA signaling were analyzed via transcriptomes and proteomes, which provided a novel direction and research basis for the subsequent exploration of the regulation mechanism of temporary starch and apoptosis via LSES1/OsCKI1 in rice. |
| first_indexed | 2024-12-18T11:07:27Z |
| format | Article |
| id | doaj.art-8137203079204a04802b50248e5efbad |
| institution | Directory Open Access Journal |
| issn | 1471-2229 |
| language | English |
| last_indexed | 2024-12-18T11:07:27Z |
| publishDate | 2022-03-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Plant Biology |
| spelling | doaj.art-8137203079204a04802b50248e5efbad2022-12-21T21:10:04ZengBMCBMC Plant Biology1471-22292022-03-0122111710.1186/s12870-022-03510-2Integration of transcriptomic and proteomic analyses reveals several levels of metabolic regulation in the excess starch and early senescent leaf mutant lses1 in riceZhiming Chen0Yongsheng Wang1Rongyu Huang2Zesen Zhang3Jinpeng Huang4Feng Yu5Yaohai Lin6Yuchun Guo7Kangjing Liang8Yuanchang Zhou9Fangyu Chen10Key Laboratory of Ministry of Education for Genetic Improvement and Comprehensive Utilization of Crops, Fujian Provincial Key Laboratory of Crop Breeding by Design, College of Agriculture, Fujian Agriculture and Forestry UniversityPostdoctoral Station of Biology, School of Life Sciences, Hebei UniversitySchool of Life Sciences, Xiamen UniversitySchool of Life Sciences, Xiamen UniversitySchool of Life Sciences, Xiamen UniversityKey Laboratory of Ministry of Education for Genetic Improvement and Comprehensive Utilization of Crops, Fujian Provincial Key Laboratory of Crop Breeding by Design, College of Agriculture, Fujian Agriculture and Forestry UniversityCollege of Computer and Information Science, Fujian Agriculture and Forestry UniversityKey Laboratory of Ministry of Education for Genetic Improvement and Comprehensive Utilization of Crops, Fujian Provincial Key Laboratory of Crop Breeding by Design, College of Agriculture, Fujian Agriculture and Forestry UniversityKey Laboratory of Ministry of Education for Genetic Improvement and Comprehensive Utilization of Crops, Fujian Provincial Key Laboratory of Crop Breeding by Design, College of Agriculture, Fujian Agriculture and Forestry UniversityKey Laboratory of Ministry of Education for Genetic Improvement and Comprehensive Utilization of Crops, Fujian Provincial Key Laboratory of Crop Breeding by Design, College of Agriculture, Fujian Agriculture and Forestry UniversityKey Laboratory of Ministry of Education for Genetic Improvement and Comprehensive Utilization of Crops, Fujian Provincial Key Laboratory of Crop Breeding by Design, College of Agriculture, Fujian Agriculture and Forestry UniversityAbstract Background The normal metabolism of transitory starch in leaves plays an important role in ensuring photosynthesis, delaying senescence and maintaining high yield in crops. OsCKI1 (casein kinase I1) plays crucial regulatory roles in multiple important physiological processes, including root development, hormonal signaling and low temperature-treatment adaptive growth in rice; however, its potential role in regulating temporary starch metabolism or premature leaf senescence remains unclear. To reveal the molecular regulatory mechanism of OsCKI1 in rice leaves, physiological, transcriptomic and proteomic analyses of leaves of osckI1 allele mutant lses1 (leaf starch excess and senescence 1) and its wild-type varieties (WT) were performed. Results Phenotypic identification and physiological measurements showed that the lses1 mutant exhibited starch excess in the leaves and an obvious leaf tip withering phenotype as well as high ROS and MDA contents, low chlorophyll content and protective enzyme activities compared to WT. The correlation analyses between protein and mRNA abundance are weak or limited. However, the changes of several important genes related to carbohydrate metabolism and apoptosis at the mRNA and protein levels were consistent. The protein-protein interaction (PPI) network might play accessory roles in promoting premature senescence of lses1 leaves. Comprehensive transcriptomic and proteomic analysis indicated that multiple key genes/proteins related to starch and sugar metabolism, apoptosis and ABA signaling exhibited significant differential expression. Abnormal increase in temporary starch was highly correlated with the expression of starch biosynthesis-related genes, which might be the main factor that causes premature leaf senescence and changes in multiple metabolic levels in leaves of lses1. In addition, four proteins associated with ABA accumulation and signaling, and three CKI potential target proteins related to starch biosynthesis were up-regulated in the lses1 mutant, suggesting that LSES1 may affect temporary starch accumulation and premature leaf senescence through phosphorylation crosstalk ABA signaling and starch anabolic pathways. Conclusion The current study established the high correlation between the changes in physiological characteristics and mRNA and protein expression profiles in lses1 leaves, and emphasized the positive effect of excessive starch on accelerating premature leaf senescence. The expression patterns of genes/proteins related to starch biosynthesis and ABA signaling were analyzed via transcriptomes and proteomes, which provided a novel direction and research basis for the subsequent exploration of the regulation mechanism of temporary starch and apoptosis via LSES1/OsCKI1 in rice.https://doi.org/10.1186/s12870-022-03510-2TranscriptomeProteomelses1Leaf senescenceTransitory starchRice (Oryza sativa L.) |
| spellingShingle | Zhiming Chen Yongsheng Wang Rongyu Huang Zesen Zhang Jinpeng Huang Feng Yu Yaohai Lin Yuchun Guo Kangjing Liang Yuanchang Zhou Fangyu Chen Integration of transcriptomic and proteomic analyses reveals several levels of metabolic regulation in the excess starch and early senescent leaf mutant lses1 in rice BMC Plant Biology Transcriptome Proteome lses1 Leaf senescence Transitory starch Rice (Oryza sativa L.) |
| title | Integration of transcriptomic and proteomic analyses reveals several levels of metabolic regulation in the excess starch and early senescent leaf mutant lses1 in rice |
| title_full | Integration of transcriptomic and proteomic analyses reveals several levels of metabolic regulation in the excess starch and early senescent leaf mutant lses1 in rice |
| title_fullStr | Integration of transcriptomic and proteomic analyses reveals several levels of metabolic regulation in the excess starch and early senescent leaf mutant lses1 in rice |
| title_full_unstemmed | Integration of transcriptomic and proteomic analyses reveals several levels of metabolic regulation in the excess starch and early senescent leaf mutant lses1 in rice |
| title_short | Integration of transcriptomic and proteomic analyses reveals several levels of metabolic regulation in the excess starch and early senescent leaf mutant lses1 in rice |
| title_sort | integration of transcriptomic and proteomic analyses reveals several levels of metabolic regulation in the excess starch and early senescent leaf mutant lses1 in rice |
| topic | Transcriptome Proteome lses1 Leaf senescence Transitory starch Rice (Oryza sativa L.) |
| url | https://doi.org/10.1186/s12870-022-03510-2 |
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