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A translatome-transcriptome multi-omics gene regulatory network reveals the complicated functional landscape of maize

BACKGROUND: Maize (Zea mays L.) is one of the most important crops worldwide. Although sophisticated maize gene regulatory networks (GRNs) have been constructed for functional genomics and phenotypic dissection, a multi-omics GRN connecting the translatome and transcriptome is lacking, hampering our...

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Autores principales: Zhu, Wanchao, Miao, Xinxin, Qian, Jia, Chen, Sijia, Jin, Qixiao, Li, Mingzhu, Han, Linqian, Zhong, Wanshun, Xie, Dan, Shang, Xiaoyang, Li, Lin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10053466/
https://www.ncbi.nlm.nih.gov/pubmed/36991439
http://dx.doi.org/10.1186/s13059-023-02890-4
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author Zhu, Wanchao
Miao, Xinxin
Qian, Jia
Chen, Sijia
Jin, Qixiao
Li, Mingzhu
Han, Linqian
Zhong, Wanshun
Xie, Dan
Shang, Xiaoyang
Li, Lin
author_facet Zhu, Wanchao
Miao, Xinxin
Qian, Jia
Chen, Sijia
Jin, Qixiao
Li, Mingzhu
Han, Linqian
Zhong, Wanshun
Xie, Dan
Shang, Xiaoyang
Li, Lin
author_sort Zhu, Wanchao
collection PubMed
description BACKGROUND: Maize (Zea mays L.) is one of the most important crops worldwide. Although sophisticated maize gene regulatory networks (GRNs) have been constructed for functional genomics and phenotypic dissection, a multi-omics GRN connecting the translatome and transcriptome is lacking, hampering our understanding and exploration of the maize regulatome. RESULTS: We collect spatio-temporal translatome and transcriptome data and systematically explore the landscape of gene transcription and translation across 33 tissues or developmental stages of maize. Using this comprehensive transcriptome and translatome atlas, we construct a multi-omics GRN integrating mRNAs and translated mRNAs, demonstrating that translatome-related GRNs outperform GRNs solely using transcriptomic data and inter-omics GRNs outperform intra-omics GRNs in most cases. With the aid of the multi-omics GRN, we reconcile some known regulatory networks. We identify a novel transcription factor, ZmGRF6, which is associated with growth. Furthermore, we characterize a function related to drought response for the classic transcription factor ZmMYB31. CONCLUSIONS: Our findings provide insights into spatio-temporal changes across maize development at both the transcriptome and translatome levels. Multi-omics GRNs represent a useful resource for dissection of the regulatory mechanisms underlying phenotypic variation. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13059-023-02890-4.
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spelling pubmed-100534662023-03-30 A translatome-transcriptome multi-omics gene regulatory network reveals the complicated functional landscape of maize Zhu, Wanchao Miao, Xinxin Qian, Jia Chen, Sijia Jin, Qixiao Li, Mingzhu Han, Linqian Zhong, Wanshun Xie, Dan Shang, Xiaoyang Li, Lin Genome Biol Research BACKGROUND: Maize (Zea mays L.) is one of the most important crops worldwide. Although sophisticated maize gene regulatory networks (GRNs) have been constructed for functional genomics and phenotypic dissection, a multi-omics GRN connecting the translatome and transcriptome is lacking, hampering our understanding and exploration of the maize regulatome. RESULTS: We collect spatio-temporal translatome and transcriptome data and systematically explore the landscape of gene transcription and translation across 33 tissues or developmental stages of maize. Using this comprehensive transcriptome and translatome atlas, we construct a multi-omics GRN integrating mRNAs and translated mRNAs, demonstrating that translatome-related GRNs outperform GRNs solely using transcriptomic data and inter-omics GRNs outperform intra-omics GRNs in most cases. With the aid of the multi-omics GRN, we reconcile some known regulatory networks. We identify a novel transcription factor, ZmGRF6, which is associated with growth. Furthermore, we characterize a function related to drought response for the classic transcription factor ZmMYB31. CONCLUSIONS: Our findings provide insights into spatio-temporal changes across maize development at both the transcriptome and translatome levels. Multi-omics GRNs represent a useful resource for dissection of the regulatory mechanisms underlying phenotypic variation. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s13059-023-02890-4. BioMed Central 2023-03-29 /pmc/articles/PMC10053466/ /pubmed/36991439 http://dx.doi.org/10.1186/s13059-023-02890-4 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Zhu, Wanchao
Miao, Xinxin
Qian, Jia
Chen, Sijia
Jin, Qixiao
Li, Mingzhu
Han, Linqian
Zhong, Wanshun
Xie, Dan
Shang, Xiaoyang
Li, Lin
A translatome-transcriptome multi-omics gene regulatory network reveals the complicated functional landscape of maize
title A translatome-transcriptome multi-omics gene regulatory network reveals the complicated functional landscape of maize
title_full A translatome-transcriptome multi-omics gene regulatory network reveals the complicated functional landscape of maize
title_fullStr A translatome-transcriptome multi-omics gene regulatory network reveals the complicated functional landscape of maize
title_full_unstemmed A translatome-transcriptome multi-omics gene regulatory network reveals the complicated functional landscape of maize
title_short A translatome-transcriptome multi-omics gene regulatory network reveals the complicated functional landscape of maize
title_sort translatome-transcriptome multi-omics gene regulatory network reveals the complicated functional landscape of maize
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10053466/
https://www.ncbi.nlm.nih.gov/pubmed/36991439
http://dx.doi.org/10.1186/s13059-023-02890-4
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