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Comparative analysis of Cd-responsive maize and rice transcriptomes highlights Cd co-modulated orthologs

BACKGROUND: Metal tolerance is often an integrative result of metal uptake and distribution, which are fine-tuned by a network of signaling cascades and metal transporters. Thus, with the goal of advancing the molecular understanding of such metal homeostatic mechanisms, comparative RNAseq-based tra...

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Autores principales: Cheng, Dan, Tan, Mingpu, Yu, Haijuan, Li, Liang, Zhu, Dandan, Chen, Yahua, Jiang, Mingyi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6158873/
https://www.ncbi.nlm.nih.gov/pubmed/30257650
http://dx.doi.org/10.1186/s12864-018-5109-8
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author Cheng, Dan
Tan, Mingpu
Yu, Haijuan
Li, Liang
Zhu, Dandan
Chen, Yahua
Jiang, Mingyi
author_facet Cheng, Dan
Tan, Mingpu
Yu, Haijuan
Li, Liang
Zhu, Dandan
Chen, Yahua
Jiang, Mingyi
author_sort Cheng, Dan
collection PubMed
description BACKGROUND: Metal tolerance is often an integrative result of metal uptake and distribution, which are fine-tuned by a network of signaling cascades and metal transporters. Thus, with the goal of advancing the molecular understanding of such metal homeostatic mechanisms, comparative RNAseq-based transcriptome analysis was conducted to dissect differentially expressed genes (DEGs) in maize roots exposed to cadmium (Cd) stress. RESULTS: To unveil conserved Cd-responsive genes in cereal plants, the obtained 5166 maize DEGs were compared with 2567 Cd-regulated orthologs in rice roots, and this comparison generated 880 universal Cd-responsive orthologs groups composed of 1074 maize DEGs and 981 rice counterparts. More importantly, most of the orthologous DEGs showed coordinated expression pattern between Cd-treated maize and rice, and these include one large orthologs group of pleiotropic drug resistance (PDR)-type ABC transporters, two clusters of amino acid transporters, and 3 blocks of multidrug and toxic compound extrusion (MATE) efflux family transporters, and 3 clusters of heavy metal-associated domain (HMAD) isoprenylated plant proteins (HIPPs), as well as all 4 groups of zinc/iron regulated transporter protein (ZIPs). Additionally, several blocks of tandem maize paralogs, such as germin-like proteins (GLPs), phenylalanine ammonia-lyases (PALs) and several enzymes involved in JA biosynthesis, displayed consistent co-expression pattern under Cd stress. Out of the 1074 maize DEGs, approximately 30 maize Cd-responsive genes such as ZmHIPP27, stress-responsive NAC transcription factor (ZmSNAC1) and 9-cis-epoxycarotenoid dioxygenase (NCED, vp14) were also common stress-responsive genes reported to be uniformly regulated by multiple abiotic stresses. Moreover, the aforementioned three promising Cd-upregulated genes with rice counterparts were identified to be novel Cd-responsive genes in maize. Meanwhile, one maize glutamate decarboxylase (ZmGAD1) with Cd co-modulated rice ortholog was selected for further analysis of Cd tolerance via heterologous expression, and the results suggest that ZmGAD1 can confer Cd tolerance in yeast and tobacco leaves. CONCLUSIONS: These novel findings revealed the conserved function of Cd-responsive orthologs and paralogs, which would be valuable for elucidating the genetic basis of the plant response to Cd stress and unraveling Cd tolerance genes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-5109-8) contains supplementary material, which is available to authorized users.
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spelling pubmed-61588732018-10-01 Comparative analysis of Cd-responsive maize and rice transcriptomes highlights Cd co-modulated orthologs Cheng, Dan Tan, Mingpu Yu, Haijuan Li, Liang Zhu, Dandan Chen, Yahua Jiang, Mingyi BMC Genomics Research Article BACKGROUND: Metal tolerance is often an integrative result of metal uptake and distribution, which are fine-tuned by a network of signaling cascades and metal transporters. Thus, with the goal of advancing the molecular understanding of such metal homeostatic mechanisms, comparative RNAseq-based transcriptome analysis was conducted to dissect differentially expressed genes (DEGs) in maize roots exposed to cadmium (Cd) stress. RESULTS: To unveil conserved Cd-responsive genes in cereal plants, the obtained 5166 maize DEGs were compared with 2567 Cd-regulated orthologs in rice roots, and this comparison generated 880 universal Cd-responsive orthologs groups composed of 1074 maize DEGs and 981 rice counterparts. More importantly, most of the orthologous DEGs showed coordinated expression pattern between Cd-treated maize and rice, and these include one large orthologs group of pleiotropic drug resistance (PDR)-type ABC transporters, two clusters of amino acid transporters, and 3 blocks of multidrug and toxic compound extrusion (MATE) efflux family transporters, and 3 clusters of heavy metal-associated domain (HMAD) isoprenylated plant proteins (HIPPs), as well as all 4 groups of zinc/iron regulated transporter protein (ZIPs). Additionally, several blocks of tandem maize paralogs, such as germin-like proteins (GLPs), phenylalanine ammonia-lyases (PALs) and several enzymes involved in JA biosynthesis, displayed consistent co-expression pattern under Cd stress. Out of the 1074 maize DEGs, approximately 30 maize Cd-responsive genes such as ZmHIPP27, stress-responsive NAC transcription factor (ZmSNAC1) and 9-cis-epoxycarotenoid dioxygenase (NCED, vp14) were also common stress-responsive genes reported to be uniformly regulated by multiple abiotic stresses. Moreover, the aforementioned three promising Cd-upregulated genes with rice counterparts were identified to be novel Cd-responsive genes in maize. Meanwhile, one maize glutamate decarboxylase (ZmGAD1) with Cd co-modulated rice ortholog was selected for further analysis of Cd tolerance via heterologous expression, and the results suggest that ZmGAD1 can confer Cd tolerance in yeast and tobacco leaves. CONCLUSIONS: These novel findings revealed the conserved function of Cd-responsive orthologs and paralogs, which would be valuable for elucidating the genetic basis of the plant response to Cd stress and unraveling Cd tolerance genes. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-5109-8) contains supplementary material, which is available to authorized users. BioMed Central 2018-09-26 /pmc/articles/PMC6158873/ /pubmed/30257650 http://dx.doi.org/10.1186/s12864-018-5109-8 Text en © The Author(s). 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Cheng, Dan
Tan, Mingpu
Yu, Haijuan
Li, Liang
Zhu, Dandan
Chen, Yahua
Jiang, Mingyi
Comparative analysis of Cd-responsive maize and rice transcriptomes highlights Cd co-modulated orthologs
title Comparative analysis of Cd-responsive maize and rice transcriptomes highlights Cd co-modulated orthologs
title_full Comparative analysis of Cd-responsive maize and rice transcriptomes highlights Cd co-modulated orthologs
title_fullStr Comparative analysis of Cd-responsive maize and rice transcriptomes highlights Cd co-modulated orthologs
title_full_unstemmed Comparative analysis of Cd-responsive maize and rice transcriptomes highlights Cd co-modulated orthologs
title_short Comparative analysis of Cd-responsive maize and rice transcriptomes highlights Cd co-modulated orthologs
title_sort comparative analysis of cd-responsive maize and rice transcriptomes highlights cd co-modulated orthologs
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6158873/
https://www.ncbi.nlm.nih.gov/pubmed/30257650
http://dx.doi.org/10.1186/s12864-018-5109-8
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