Integrative hyperspectral, transcriptomic, and metabolomic analysis reveals the mechanism of tea plants in response to sooty mold disease
Abstract Background Sooty mold (SM), caused by Cladosporium species, is a pervasive threat to tea plant health, affecting both canopy structure and crop yield. Despite its significance, understanding the complex interplay between defense genes and metabolites in tea plants across various SM-infected...
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2024-11-01
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| Series: | BMC Plant Biology |
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| Online Access: | https://doi.org/10.1186/s12870-024-05806-x |
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| author | Shuangshuang Wang Yang Xu Jiazhi Shen Hao Chen Yu Wang Zhaotang Ding |
| author_facet | Shuangshuang Wang Yang Xu Jiazhi Shen Hao Chen Yu Wang Zhaotang Ding |
| author_sort | Shuangshuang Wang |
| collection | DOAJ |
| description | Abstract Background Sooty mold (SM), caused by Cladosporium species, is a pervasive threat to tea plant health, affecting both canopy structure and crop yield. Despite its significance, understanding the complex interplay between defense genes and metabolites in tea plants across various SM-infected canopy layers remains limited. Our study employed hyperspectral imaging, transcriptomic profiling, and metabolomic analysis to decipher the intricate mechanisms underlying the tea plant’s response to SM infection. Results Our hyperspectral imaging identified three critical wavelengths (552, 673, and 800 nm) inflection points associated with varying degrees of SM infection. This non-invasive method allows for the precise assessment of disease progression. Concurrently, transcriptome analysis revealed a wealth of differentially expressed genes (DEGs) enriched in metabolic pathways, secondary metabolite biosynthesis, and plant-pathogen interactions. Cluster analysis highlighted an intensified immune response in A2 and A3 samples. A comprehensive metabolomic profile identified 733 co-changed metabolites in SM-infected leaves, with alcohols, lipids (free fatty acids), hydrocarbons, and amino acids significantly accumulating in A1, while flavonoids were predominantly upregulated in A2 and A3. Weighted Gene Co-Expression Network Analysis (WGCNA) uncovered five hub genes (Dormancy-associated protein, Serine/threonine-protein phosphatase, ABC transporter, and some uncharacterized proteins) and two hub metabolites (D-Mannitol and 17-Hydroxylinolenic Acid) that exhibit significant relationships with DEGs and metabolites. Further co-expression analysis indicated that tea plants mainly employed genes and metabolites related to the biosynthesis of secondary metabolites, plant hormone signal transduction, and plant-pathogen interaction to combat SM. Conclusion This study establishes a foundation for understanding the immune mechanisms of tea plants across different canopy layers in response to SM infection. It not only sheds light on the complex defense strategies employed by tea plants but also identifies candidate genes and metabolites crucial for enhancing tea plant breeding and resistance to SM. |
| format | Article |
| id | doaj-art-2787a4fa57c94d5cad27f6dc2976948b |
| institution | Kabale University |
| issn | 1471-2229 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Plant Biology |
| spelling | doaj-art-2787a4fa57c94d5cad27f6dc2976948b2024-11-17T12:17:55ZengBMCBMC Plant Biology1471-22292024-11-0124111110.1186/s12870-024-05806-xIntegrative hyperspectral, transcriptomic, and metabolomic analysis reveals the mechanism of tea plants in response to sooty mold diseaseShuangshuang Wang0Yang Xu1Jiazhi Shen2Hao Chen3Yu Wang4Zhaotang Ding5Tea Research Institute, Shandong Academy of Agricultural SciencesTea Research Institute, Qingdao Agricultural UniversityTea Research Institute, Shandong Academy of Agricultural SciencesTea Research Institute, Qingdao Agricultural UniversityTea Research Institute, Qingdao Agricultural UniversityTea Research Institute, Shandong Academy of Agricultural SciencesAbstract Background Sooty mold (SM), caused by Cladosporium species, is a pervasive threat to tea plant health, affecting both canopy structure and crop yield. Despite its significance, understanding the complex interplay between defense genes and metabolites in tea plants across various SM-infected canopy layers remains limited. Our study employed hyperspectral imaging, transcriptomic profiling, and metabolomic analysis to decipher the intricate mechanisms underlying the tea plant’s response to SM infection. Results Our hyperspectral imaging identified three critical wavelengths (552, 673, and 800 nm) inflection points associated with varying degrees of SM infection. This non-invasive method allows for the precise assessment of disease progression. Concurrently, transcriptome analysis revealed a wealth of differentially expressed genes (DEGs) enriched in metabolic pathways, secondary metabolite biosynthesis, and plant-pathogen interactions. Cluster analysis highlighted an intensified immune response in A2 and A3 samples. A comprehensive metabolomic profile identified 733 co-changed metabolites in SM-infected leaves, with alcohols, lipids (free fatty acids), hydrocarbons, and amino acids significantly accumulating in A1, while flavonoids were predominantly upregulated in A2 and A3. Weighted Gene Co-Expression Network Analysis (WGCNA) uncovered five hub genes (Dormancy-associated protein, Serine/threonine-protein phosphatase, ABC transporter, and some uncharacterized proteins) and two hub metabolites (D-Mannitol and 17-Hydroxylinolenic Acid) that exhibit significant relationships with DEGs and metabolites. Further co-expression analysis indicated that tea plants mainly employed genes and metabolites related to the biosynthesis of secondary metabolites, plant hormone signal transduction, and plant-pathogen interaction to combat SM. Conclusion This study establishes a foundation for understanding the immune mechanisms of tea plants across different canopy layers in response to SM infection. It not only sheds light on the complex defense strategies employed by tea plants but also identifies candidate genes and metabolites crucial for enhancing tea plant breeding and resistance to SM.https://doi.org/10.1186/s12870-024-05806-xTea plantsSooty mold diseaseResistanceHyperspectralTranscriptomicMetabolomic |
| spellingShingle | Shuangshuang Wang Yang Xu Jiazhi Shen Hao Chen Yu Wang Zhaotang Ding Integrative hyperspectral, transcriptomic, and metabolomic analysis reveals the mechanism of tea plants in response to sooty mold disease BMC Plant Biology Tea plants Sooty mold disease Resistance Hyperspectral Transcriptomic Metabolomic |
| title | Integrative hyperspectral, transcriptomic, and metabolomic analysis reveals the mechanism of tea plants in response to sooty mold disease |
| title_full | Integrative hyperspectral, transcriptomic, and metabolomic analysis reveals the mechanism of tea plants in response to sooty mold disease |
| title_fullStr | Integrative hyperspectral, transcriptomic, and metabolomic analysis reveals the mechanism of tea plants in response to sooty mold disease |
| title_full_unstemmed | Integrative hyperspectral, transcriptomic, and metabolomic analysis reveals the mechanism of tea plants in response to sooty mold disease |
| title_short | Integrative hyperspectral, transcriptomic, and metabolomic analysis reveals the mechanism of tea plants in response to sooty mold disease |
| title_sort | integrative hyperspectral transcriptomic and metabolomic analysis reveals the mechanism of tea plants in response to sooty mold disease |
| topic | Tea plants Sooty mold disease Resistance Hyperspectral Transcriptomic Metabolomic |
| url | https://doi.org/10.1186/s12870-024-05806-x |
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