Ribosome footprint profiling enables elucidating the systemic regulation of fatty acid accumulation in Acer truncatum

Abstract Background The accumulation of fatty acids in plants covers a wide range of functions in plant physiology and thereby affects adaptations and characteristics of species. As the famous woody oilseed crop, Acer truncatum accumulates unsaturated fatty acids and could serve as the model to unde...

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Main Authors: Qiuyue Ma, Yuxiao Wang, Shushun Li, Jing Wen, Lu Zhu, Kunyuan Yan, Yiming Du, Shuxian Li, Liping Yan, Zhijun Xie, Yunzhou Lyu, Fei Shen, Qianzhong Li
Format: Article
Language:English
Published: BMC 2023-04-01
Series:BMC Biology
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Online Access:https://doi.org/10.1186/s12915-023-01564-8
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author Qiuyue Ma
Yuxiao Wang
Shushun Li
Jing Wen
Lu Zhu
Kunyuan Yan
Yiming Du
Shuxian Li
Liping Yan
Zhijun Xie
Yunzhou Lyu
Fei Shen
Qianzhong Li
author_facet Qiuyue Ma
Yuxiao Wang
Shushun Li
Jing Wen
Lu Zhu
Kunyuan Yan
Yiming Du
Shuxian Li
Liping Yan
Zhijun Xie
Yunzhou Lyu
Fei Shen
Qianzhong Li
author_sort Qiuyue Ma
collection DOAJ
description Abstract Background The accumulation of fatty acids in plants covers a wide range of functions in plant physiology and thereby affects adaptations and characteristics of species. As the famous woody oilseed crop, Acer truncatum accumulates unsaturated fatty acids and could serve as the model to understand the regulation and trait formation in oil-accumulation crops. Here, we performed Ribosome footprint profiling combing with a multi-omics strategy towards vital time points during seed development, and finally constructed systematic profiling from transcription to proteomes. Additionally, we characterized the small open reading frames (ORFs) and revealed that the translational efficiencies of focused genes were highly influenced by their sequence features. Results The comprehensive multi-omics analysis of lipid metabolism was conducted in A. truncatum. We applied the Ribo-seq and RNA-seq techniques, and the analyses of transcriptional and translational profiles of seeds collected at 85 and 115 DAF were compared. Key members of biosynthesis-related structural genes (LACS, FAD2, FAD3, and KCS) were characterized fully. More meaningfully, the regulators (MYB, ABI, bZIP, and Dof) were identified and revealed to affect lipid biosynthesis via post-translational regulations. The translational features results showed that translation efficiency tended to be lower for the genes with a translated uORF than for the genes with a non-translated uORF. They provide new insights into the global mechanisms underlying the developmental regulation of lipid metabolism. Conclusions We performed Ribosome footprint profiling combing with a multi-omics strategy in A. truncatum seed development, which provides an example of the use of Ribosome footprint profiling in deciphering the complex regulation network and will be useful for elucidating the metabolism of A. truncatum seed oil and the regulatory mechanisms.
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spelling doaj.art-87e64eae68df44228e7b23480a262c5a2023-04-09T11:26:57ZengBMCBMC Biology1741-70072023-04-0121111410.1186/s12915-023-01564-8Ribosome footprint profiling enables elucidating the systemic regulation of fatty acid accumulation in Acer truncatumQiuyue Ma0Yuxiao Wang1Shushun Li2Jing Wen3Lu Zhu4Kunyuan Yan5Yiming Du6Shuxian Li7Liping Yan8Zhijun Xie9Yunzhou Lyu10Fei Shen11Qianzhong Li12Institute of Leisure Agriculture, Jiangsu Academy of Agricultural Sciences, Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement NanjingNanjing Forestry UniversityInstitute of Leisure Agriculture, Jiangsu Academy of Agricultural Sciences, Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement NanjingInstitute of Leisure Agriculture, Jiangsu Academy of Agricultural Sciences, Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement NanjingInstitute of Leisure Agriculture, Jiangsu Academy of Agricultural Sciences, Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement NanjingInstitute of Leisure Agriculture, Jiangsu Academy of Agricultural Sciences, Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement NanjingInstitute of Leisure Agriculture, Jiangsu Academy of Agricultural Sciences, Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement NanjingNanjing Forestry UniversityShandong Academy of Forestry SciencesXiangyang Forestry Science and Technology Extension StationJiangsu Academy of ForestryInstitute of Biology, Beijing Academy of Agriculture and Forestry SciencesInstitute of Leisure Agriculture, Jiangsu Academy of Agricultural Sciences, Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement NanjingAbstract Background The accumulation of fatty acids in plants covers a wide range of functions in plant physiology and thereby affects adaptations and characteristics of species. As the famous woody oilseed crop, Acer truncatum accumulates unsaturated fatty acids and could serve as the model to understand the regulation and trait formation in oil-accumulation crops. Here, we performed Ribosome footprint profiling combing with a multi-omics strategy towards vital time points during seed development, and finally constructed systematic profiling from transcription to proteomes. Additionally, we characterized the small open reading frames (ORFs) and revealed that the translational efficiencies of focused genes were highly influenced by their sequence features. Results The comprehensive multi-omics analysis of lipid metabolism was conducted in A. truncatum. We applied the Ribo-seq and RNA-seq techniques, and the analyses of transcriptional and translational profiles of seeds collected at 85 and 115 DAF were compared. Key members of biosynthesis-related structural genes (LACS, FAD2, FAD3, and KCS) were characterized fully. More meaningfully, the regulators (MYB, ABI, bZIP, and Dof) were identified and revealed to affect lipid biosynthesis via post-translational regulations. The translational features results showed that translation efficiency tended to be lower for the genes with a translated uORF than for the genes with a non-translated uORF. They provide new insights into the global mechanisms underlying the developmental regulation of lipid metabolism. Conclusions We performed Ribosome footprint profiling combing with a multi-omics strategy in A. truncatum seed development, which provides an example of the use of Ribosome footprint profiling in deciphering the complex regulation network and will be useful for elucidating the metabolism of A. truncatum seed oil and the regulatory mechanisms.https://doi.org/10.1186/s12915-023-01564-8Acer truncatumRibosome profilingTranscriptome
spellingShingle Qiuyue Ma
Yuxiao Wang
Shushun Li
Jing Wen
Lu Zhu
Kunyuan Yan
Yiming Du
Shuxian Li
Liping Yan
Zhijun Xie
Yunzhou Lyu
Fei Shen
Qianzhong Li
Ribosome footprint profiling enables elucidating the systemic regulation of fatty acid accumulation in Acer truncatum
BMC Biology
Acer truncatum
Ribosome profiling
Transcriptome
title Ribosome footprint profiling enables elucidating the systemic regulation of fatty acid accumulation in Acer truncatum
title_full Ribosome footprint profiling enables elucidating the systemic regulation of fatty acid accumulation in Acer truncatum
title_fullStr Ribosome footprint profiling enables elucidating the systemic regulation of fatty acid accumulation in Acer truncatum
title_full_unstemmed Ribosome footprint profiling enables elucidating the systemic regulation of fatty acid accumulation in Acer truncatum
title_short Ribosome footprint profiling enables elucidating the systemic regulation of fatty acid accumulation in Acer truncatum
title_sort ribosome footprint profiling enables elucidating the systemic regulation of fatty acid accumulation in acer truncatum
topic Acer truncatum
Ribosome profiling
Transcriptome
url https://doi.org/10.1186/s12915-023-01564-8
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