Multi-omics strategies uncover the molecular mechanisms of nitrogen, phosphorus and potassium deficiency responses in Brassica napus
Abstract Background Nitrogen (N), phosphorus (P) and potassium (K) are critical macronutrients in crops, such that deficiency in any of N, P or K has substantial effects on crop growth. However, the specific commonalities of plant responses to different macronutrient deficiencies remain largely unkn...
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| Format: | Article |
| Language: | English |
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BMC
2023-08-01
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| Series: | Cellular & Molecular Biology Letters |
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| Online Access: | https://doi.org/10.1186/s11658-023-00479-0 |
| _version_ | 1797452090354696192 |
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| author | Ying Fu Annaliese S. Mason Maolin Song Xiyuan Ni Lei Liu Jianghua Shi Tanliu Wang Meili Xiao Yaofeng Zhang Donghui Fu Huasheng Yu |
| author_facet | Ying Fu Annaliese S. Mason Maolin Song Xiyuan Ni Lei Liu Jianghua Shi Tanliu Wang Meili Xiao Yaofeng Zhang Donghui Fu Huasheng Yu |
| author_sort | Ying Fu |
| collection | DOAJ |
| description | Abstract Background Nitrogen (N), phosphorus (P) and potassium (K) are critical macronutrients in crops, such that deficiency in any of N, P or K has substantial effects on crop growth. However, the specific commonalities of plant responses to different macronutrient deficiencies remain largely unknown. Methods Here, we assessed the phenotypic and physiological performances along with whole transcriptome and metabolomic profiles of rapeseed seedlings exposed to N, P and K deficiency stresses. Results Quantities of reactive oxygen species were significantly increased by all macronutrient deficiencies. N and K deficiencies resulted in more severe root development responses than P deficiency, as well as greater chlorophyll content reduction in leaves (associated with disrupted chloroplast structure). Transcriptome and metabolome analyses validated the macronutrient-specific responses, with more pronounced effects of N and P deficiencies on mRNAs, microRNAs (miRNAs), circular RNAs (circRNAs) and metabolites relative to K deficiency. Tissue-specific responses also occurred, with greater effects of macronutrient deficiencies on roots compared with shoots. We further uncovered a set of common responders with simultaneous roles in all three macronutrient deficiencies, including 112 mRNAs and 10 miRNAs involved in hormonal signaling, ion transport and oxidative stress in the root, and 33 mRNAs and 6 miRNAs with roles in abiotic stress response and photosynthesis in the shoot. 27 and seven common miRNA-mRNA pairs with role in miRNA-mediated regulation of oxidoreduction processes and ion transmembrane transport were identified in all three macronutrient deficiencies. No circRNA was responsive to three macronutrient deficiency stresses, but two common circRNAs were identified for two macronutrient deficiencies. Combined analysis of circRNAs, miRNAs and mRNAs suggested that two circRNAs act as decoys for miR156 and participate in oxidoreduction processes and transmembrane transport in both N- and P-deprived roots. Simultaneously, dramatic alterations of metabolites also occurred. Associations of RNAs with metabolites were observed, and suggested potential positive regulatory roles for tricarboxylic acids, azoles, carbohydrates, sterols and auxins, and negative regulatory roles for aromatic and aspartate amino acids, glucosamine-containing compounds, cinnamic acid, and nicotianamine in plant adaptation to macronutrient deficiency. Conclusions Our findings revealed strategies to rescue rapeseed from macronutrient deficiency stress, including reducing the expression of non-essential genes and activating or enhancing the expression of anti-stress genes, aided by plant hormones, ion transporters and stress responders. The common responders to different macronutrient deficiencies identified could be targeted to enhance nutrient use efficiency in rapeseed. |
| first_indexed | 2024-03-09T15:03:45Z |
| format | Article |
| id | doaj.art-2f20904f688f4a34a8d74d5514680939 |
| institution | Directory Open Access Journal |
| issn | 1689-1392 |
| language | English |
| last_indexed | 2024-03-09T15:03:45Z |
| publishDate | 2023-08-01 |
| publisher | BMC |
| record_format | Article |
| series | Cellular & Molecular Biology Letters |
| spelling | doaj.art-2f20904f688f4a34a8d74d55146809392023-11-26T13:46:35ZengBMCCellular & Molecular Biology Letters1689-13922023-08-0128112610.1186/s11658-023-00479-0Multi-omics strategies uncover the molecular mechanisms of nitrogen, phosphorus and potassium deficiency responses in Brassica napusYing Fu0Annaliese S. Mason1Maolin Song2Xiyuan Ni3Lei Liu4Jianghua Shi5Tanliu Wang6Meili Xiao7Yaofeng Zhang8Donghui Fu9Huasheng Yu10Institute of Crop and Nuclear Technology Utilization, Zhejiang Academy of Agricultural SciencesPlant Breeding Department, University of BonnInstitute of Crop and Nuclear Technology Utilization, Zhejiang Academy of Agricultural SciencesInstitute of Crop and Nuclear Technology Utilization, Zhejiang Academy of Agricultural SciencesInstitute of Crop and Nuclear Technology Utilization, Zhejiang Academy of Agricultural SciencesInstitute of Crop and Nuclear Technology Utilization, Zhejiang Academy of Agricultural SciencesInstitute of Crop and Nuclear Technology Utilization, Zhejiang Academy of Agricultural SciencesKey Laboratory of Crop Physiology, Ecology and Genetic Breeding, Ministry of Education, Agronomy College, Jiangxi Agricultural UniversityInstitute of Crop and Nuclear Technology Utilization, Zhejiang Academy of Agricultural SciencesKey Laboratory of Crop Physiology, Ecology and Genetic Breeding, Ministry of Education, Agronomy College, Jiangxi Agricultural UniversityInstitute of Crop and Nuclear Technology Utilization, Zhejiang Academy of Agricultural SciencesAbstract Background Nitrogen (N), phosphorus (P) and potassium (K) are critical macronutrients in crops, such that deficiency in any of N, P or K has substantial effects on crop growth. However, the specific commonalities of plant responses to different macronutrient deficiencies remain largely unknown. Methods Here, we assessed the phenotypic and physiological performances along with whole transcriptome and metabolomic profiles of rapeseed seedlings exposed to N, P and K deficiency stresses. Results Quantities of reactive oxygen species were significantly increased by all macronutrient deficiencies. N and K deficiencies resulted in more severe root development responses than P deficiency, as well as greater chlorophyll content reduction in leaves (associated with disrupted chloroplast structure). Transcriptome and metabolome analyses validated the macronutrient-specific responses, with more pronounced effects of N and P deficiencies on mRNAs, microRNAs (miRNAs), circular RNAs (circRNAs) and metabolites relative to K deficiency. Tissue-specific responses also occurred, with greater effects of macronutrient deficiencies on roots compared with shoots. We further uncovered a set of common responders with simultaneous roles in all three macronutrient deficiencies, including 112 mRNAs and 10 miRNAs involved in hormonal signaling, ion transport and oxidative stress in the root, and 33 mRNAs and 6 miRNAs with roles in abiotic stress response and photosynthesis in the shoot. 27 and seven common miRNA-mRNA pairs with role in miRNA-mediated regulation of oxidoreduction processes and ion transmembrane transport were identified in all three macronutrient deficiencies. No circRNA was responsive to three macronutrient deficiency stresses, but two common circRNAs were identified for two macronutrient deficiencies. Combined analysis of circRNAs, miRNAs and mRNAs suggested that two circRNAs act as decoys for miR156 and participate in oxidoreduction processes and transmembrane transport in both N- and P-deprived roots. Simultaneously, dramatic alterations of metabolites also occurred. Associations of RNAs with metabolites were observed, and suggested potential positive regulatory roles for tricarboxylic acids, azoles, carbohydrates, sterols and auxins, and negative regulatory roles for aromatic and aspartate amino acids, glucosamine-containing compounds, cinnamic acid, and nicotianamine in plant adaptation to macronutrient deficiency. Conclusions Our findings revealed strategies to rescue rapeseed from macronutrient deficiency stress, including reducing the expression of non-essential genes and activating or enhancing the expression of anti-stress genes, aided by plant hormones, ion transporters and stress responders. The common responders to different macronutrient deficiencies identified could be targeted to enhance nutrient use efficiency in rapeseed.https://doi.org/10.1186/s11658-023-00479-0NitrogenPhosphorusPotassiumDeprivationRNAMetabolite |
| spellingShingle | Ying Fu Annaliese S. Mason Maolin Song Xiyuan Ni Lei Liu Jianghua Shi Tanliu Wang Meili Xiao Yaofeng Zhang Donghui Fu Huasheng Yu Multi-omics strategies uncover the molecular mechanisms of nitrogen, phosphorus and potassium deficiency responses in Brassica napus Cellular & Molecular Biology Letters Nitrogen Phosphorus Potassium Deprivation RNA Metabolite |
| title | Multi-omics strategies uncover the molecular mechanisms of nitrogen, phosphorus and potassium deficiency responses in Brassica napus |
| title_full | Multi-omics strategies uncover the molecular mechanisms of nitrogen, phosphorus and potassium deficiency responses in Brassica napus |
| title_fullStr | Multi-omics strategies uncover the molecular mechanisms of nitrogen, phosphorus and potassium deficiency responses in Brassica napus |
| title_full_unstemmed | Multi-omics strategies uncover the molecular mechanisms of nitrogen, phosphorus and potassium deficiency responses in Brassica napus |
| title_short | Multi-omics strategies uncover the molecular mechanisms of nitrogen, phosphorus and potassium deficiency responses in Brassica napus |
| title_sort | multi omics strategies uncover the molecular mechanisms of nitrogen phosphorus and potassium deficiency responses in brassica napus |
| topic | Nitrogen Phosphorus Potassium Deprivation RNA Metabolite |
| url | https://doi.org/10.1186/s11658-023-00479-0 |
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