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Global leaf and root transcriptome in response to cadmium reveals tolerance mechanisms in Arundo donax L

The expected increase of sustainable energy demand has shifted the attention towards bioenergy crops. Due to their know tolerance against abiotic stress and relatively low nutritional requirements, they have been proposed as election crops to be cultivated in marginal lands without disturbing the pa...

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Autores principales: Santoro, Danilo Fabrizio, Sicilia, Angelo, Testa, Giorgio, Cosentino, Salvatore Luciano, Lo Piero, Angela Roberta
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9175368/
https://www.ncbi.nlm.nih.gov/pubmed/35672691
http://dx.doi.org/10.1186/s12864-022-08605-6
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author Santoro, Danilo Fabrizio
Sicilia, Angelo
Testa, Giorgio
Cosentino, Salvatore Luciano
Lo Piero, Angela Roberta
author_facet Santoro, Danilo Fabrizio
Sicilia, Angelo
Testa, Giorgio
Cosentino, Salvatore Luciano
Lo Piero, Angela Roberta
author_sort Santoro, Danilo Fabrizio
collection PubMed
description The expected increase of sustainable energy demand has shifted the attention towards bioenergy crops. Due to their know tolerance against abiotic stress and relatively low nutritional requirements, they have been proposed as election crops to be cultivated in marginal lands without disturbing the part of lands employed for agricultural purposes. Arundo donax L. is a promising bioenergy crop whose behaviour under water and salt stress has been recently studied at transcriptomic levels. As the anthropogenic activities produced in the last years a worrying increase of cadmium contamination worldwide, the aim of our work was to decipher the global transcriptomic response of A. donax leaf and root in the perspective of its cultivation in contaminated soil. In our study, RNA-seq libraries yielded a total of 416 million clean reads and 10.4 Gb per sample. De novo assembly of clean reads resulted in 378,521 transcripts and 126,668 unigenes with N50 length of 1812 bp and 1555 bp, respectively. Differential gene expression analysis revealed 5,303 deregulated transcripts (3,206 up- and 2,097 down regulated) specifically observed in the Cd-treated roots compared to Cd-treated leaves. Among them, we identified genes related to “Protein biosynthesis”, “Phytohormone action”, “Nutrient uptake”, “Cell wall organisation”, “Polyamine metabolism”, “Reactive oxygen species metabolism” and “Ion membrane transport”. Globally, our results indicate that ethylene biosynthesis and the downstream signal cascade are strongly induced by cadmium stress. In accordance to ethylene role in the interaction with the ROS generation and scavenging machinery, the transcription of several genes (NADPH oxidase 1, superoxide dismutase, ascorbate peroxidase, different glutathione S-transferases and catalase) devoted to cope the oxidative stress is strongly activated. Several small signal peptides belonging to ROTUNDIFOLIA, CLAVATA3, and C-TERMINALLY ENCODED PEPTIDE 1 (CEP) are also among the up-regulated genes in Cd-treated roots functioning as messenger molecules from root to shoot in order to communicate the stressful status to the upper part of the plants. Finally, the main finding of our work is that genes involved in cell wall remodelling and lignification are decisively up-regulated in giant reed roots. This probably represents a mechanism to avoid cadmium uptake which strongly supports the possibility to cultivate giant cane in contaminated soils in the perspective to reserve agricultural soil for food and feed crops. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08605-6.
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spelling pubmed-91753682022-06-09 Global leaf and root transcriptome in response to cadmium reveals tolerance mechanisms in Arundo donax L Santoro, Danilo Fabrizio Sicilia, Angelo Testa, Giorgio Cosentino, Salvatore Luciano Lo Piero, Angela Roberta BMC Genomics Research The expected increase of sustainable energy demand has shifted the attention towards bioenergy crops. Due to their know tolerance against abiotic stress and relatively low nutritional requirements, they have been proposed as election crops to be cultivated in marginal lands without disturbing the part of lands employed for agricultural purposes. Arundo donax L. is a promising bioenergy crop whose behaviour under water and salt stress has been recently studied at transcriptomic levels. As the anthropogenic activities produced in the last years a worrying increase of cadmium contamination worldwide, the aim of our work was to decipher the global transcriptomic response of A. donax leaf and root in the perspective of its cultivation in contaminated soil. In our study, RNA-seq libraries yielded a total of 416 million clean reads and 10.4 Gb per sample. De novo assembly of clean reads resulted in 378,521 transcripts and 126,668 unigenes with N50 length of 1812 bp and 1555 bp, respectively. Differential gene expression analysis revealed 5,303 deregulated transcripts (3,206 up- and 2,097 down regulated) specifically observed in the Cd-treated roots compared to Cd-treated leaves. Among them, we identified genes related to “Protein biosynthesis”, “Phytohormone action”, “Nutrient uptake”, “Cell wall organisation”, “Polyamine metabolism”, “Reactive oxygen species metabolism” and “Ion membrane transport”. Globally, our results indicate that ethylene biosynthesis and the downstream signal cascade are strongly induced by cadmium stress. In accordance to ethylene role in the interaction with the ROS generation and scavenging machinery, the transcription of several genes (NADPH oxidase 1, superoxide dismutase, ascorbate peroxidase, different glutathione S-transferases and catalase) devoted to cope the oxidative stress is strongly activated. Several small signal peptides belonging to ROTUNDIFOLIA, CLAVATA3, and C-TERMINALLY ENCODED PEPTIDE 1 (CEP) are also among the up-regulated genes in Cd-treated roots functioning as messenger molecules from root to shoot in order to communicate the stressful status to the upper part of the plants. Finally, the main finding of our work is that genes involved in cell wall remodelling and lignification are decisively up-regulated in giant reed roots. This probably represents a mechanism to avoid cadmium uptake which strongly supports the possibility to cultivate giant cane in contaminated soils in the perspective to reserve agricultural soil for food and feed crops. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08605-6. BioMed Central 2022-06-08 /pmc/articles/PMC9175368/ /pubmed/35672691 http://dx.doi.org/10.1186/s12864-022-08605-6 Text en © The Author(s) 2022 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
Santoro, Danilo Fabrizio
Sicilia, Angelo
Testa, Giorgio
Cosentino, Salvatore Luciano
Lo Piero, Angela Roberta
Global leaf and root transcriptome in response to cadmium reveals tolerance mechanisms in Arundo donax L
title Global leaf and root transcriptome in response to cadmium reveals tolerance mechanisms in Arundo donax L
title_full Global leaf and root transcriptome in response to cadmium reveals tolerance mechanisms in Arundo donax L
title_fullStr Global leaf and root transcriptome in response to cadmium reveals tolerance mechanisms in Arundo donax L
title_full_unstemmed Global leaf and root transcriptome in response to cadmium reveals tolerance mechanisms in Arundo donax L
title_short Global leaf and root transcriptome in response to cadmium reveals tolerance mechanisms in Arundo donax L
title_sort global leaf and root transcriptome in response to cadmium reveals tolerance mechanisms in arundo donax l
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9175368/
https://www.ncbi.nlm.nih.gov/pubmed/35672691
http://dx.doi.org/10.1186/s12864-022-08605-6
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