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Comparative physiological and transcriptome analysis in cultivated and wild sugarcane species in response to hydrogen peroxide-induced oxidative stress

BACKGROUND: Sugarcane is an important energy crop grown worldwide,supplementing various renewable energy sources. Cultivated and wild sugarcane species respond differently to biotic and abiotic stresses. Generally, wild species are tolerant to various abiotic stresses. In the present study, the phys...

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Autores principales: Manimekalai, R., Selvi, A, Narayanan, Jini, Vannish, Ram, Shalini, R., Gayathri, S, Rabisha, V.P
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10045617/
https://www.ncbi.nlm.nih.gov/pubmed/36973642
http://dx.doi.org/10.1186/s12864-023-09218-3
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author Manimekalai, R.
Selvi, A
Narayanan, Jini
Vannish, Ram
Shalini, R.
Gayathri, S
Rabisha, V.P
author_facet Manimekalai, R.
Selvi, A
Narayanan, Jini
Vannish, Ram
Shalini, R.
Gayathri, S
Rabisha, V.P
author_sort Manimekalai, R.
collection PubMed
description BACKGROUND: Sugarcane is an important energy crop grown worldwide,supplementing various renewable energy sources. Cultivated and wild sugarcane species respond differently to biotic and abiotic stresses. Generally, wild species are tolerant to various abiotic stresses. In the present study, the physiological and molecular responses of cultivated and wild sugarcane species to oxidative stress at the transcriptional levels were compared. Transcriptional responses were determined using RNAseq. The representative RNA-seq transcript values were validated by reverse transcriptase quantitative polymerase chain reaction (RT-qPCR) and confirmed through physiological responses. RESULTS: Oxidative stress causes leaf-rolling and -tip drying in cultivated sugarcane, but the wild species are tolerant. Higher chlorophyll fluorescence was observed in the wild species than that in the cultivated varieties under stress. Wild species can maintain a higher chlorophyll stability index than the cultivated species, which was confirmed by the lower transcripts of the chlorophyllase gene in the wild species than that in the cultivated variety. Transcription factor genes (NAC, MYB, and WRKY) were markedly expressed in response to oxidative stress, revealing their involvement in stress tolerance. The analysis revealed synchronized expression of acetyl-transferase, histone2A, cellulose synthase, and secondary cell wall biosynthetic genes in the wild species. The validation of selected genes and 15 NAC transcription factors using RT-qPCR revealed that their expression profiles were strongly correlated with RNA-seq. To the best of our knowledge, this is the first report on the oxidative stress response in cultivated and wild sugarcane species. CONCLUSION: Physiological and biochemical changes in response to oxidative stress markedly differ between cultivated and wild sugarcane species. The differentially expressed stress-responsive genes are grouped intothe response to oxidative stress, heme-binding, peroxidase activity, and metal ion binding categories. Chlorophyll maintenance is a stress tolerance response enhanced by the differential regulation of the chlorophyllase gene.There is a considerable difference in the chlorophyll stability index between wild and cultivated varieties. We observed a substantial regulation of secondary wall biosynthesis genes in the wild species compared with that in the cultivated variety, suggesting differences in stress tolerance mechanisms. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09218-3.
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spelling pubmed-100456172023-03-29 Comparative physiological and transcriptome analysis in cultivated and wild sugarcane species in response to hydrogen peroxide-induced oxidative stress Manimekalai, R. Selvi, A Narayanan, Jini Vannish, Ram Shalini, R. Gayathri, S Rabisha, V.P BMC Genomics Research BACKGROUND: Sugarcane is an important energy crop grown worldwide,supplementing various renewable energy sources. Cultivated and wild sugarcane species respond differently to biotic and abiotic stresses. Generally, wild species are tolerant to various abiotic stresses. In the present study, the physiological and molecular responses of cultivated and wild sugarcane species to oxidative stress at the transcriptional levels were compared. Transcriptional responses were determined using RNAseq. The representative RNA-seq transcript values were validated by reverse transcriptase quantitative polymerase chain reaction (RT-qPCR) and confirmed through physiological responses. RESULTS: Oxidative stress causes leaf-rolling and -tip drying in cultivated sugarcane, but the wild species are tolerant. Higher chlorophyll fluorescence was observed in the wild species than that in the cultivated varieties under stress. Wild species can maintain a higher chlorophyll stability index than the cultivated species, which was confirmed by the lower transcripts of the chlorophyllase gene in the wild species than that in the cultivated variety. Transcription factor genes (NAC, MYB, and WRKY) were markedly expressed in response to oxidative stress, revealing their involvement in stress tolerance. The analysis revealed synchronized expression of acetyl-transferase, histone2A, cellulose synthase, and secondary cell wall biosynthetic genes in the wild species. The validation of selected genes and 15 NAC transcription factors using RT-qPCR revealed that their expression profiles were strongly correlated with RNA-seq. To the best of our knowledge, this is the first report on the oxidative stress response in cultivated and wild sugarcane species. CONCLUSION: Physiological and biochemical changes in response to oxidative stress markedly differ between cultivated and wild sugarcane species. The differentially expressed stress-responsive genes are grouped intothe response to oxidative stress, heme-binding, peroxidase activity, and metal ion binding categories. Chlorophyll maintenance is a stress tolerance response enhanced by the differential regulation of the chlorophyllase gene.There is a considerable difference in the chlorophyll stability index between wild and cultivated varieties. We observed a substantial regulation of secondary wall biosynthesis genes in the wild species compared with that in the cultivated variety, suggesting differences in stress tolerance mechanisms. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-023-09218-3. BioMed Central 2023-03-27 /pmc/articles/PMC10045617/ /pubmed/36973642 http://dx.doi.org/10.1186/s12864-023-09218-3 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
Manimekalai, R.
Selvi, A
Narayanan, Jini
Vannish, Ram
Shalini, R.
Gayathri, S
Rabisha, V.P
Comparative physiological and transcriptome analysis in cultivated and wild sugarcane species in response to hydrogen peroxide-induced oxidative stress
title Comparative physiological and transcriptome analysis in cultivated and wild sugarcane species in response to hydrogen peroxide-induced oxidative stress
title_full Comparative physiological and transcriptome analysis in cultivated and wild sugarcane species in response to hydrogen peroxide-induced oxidative stress
title_fullStr Comparative physiological and transcriptome analysis in cultivated and wild sugarcane species in response to hydrogen peroxide-induced oxidative stress
title_full_unstemmed Comparative physiological and transcriptome analysis in cultivated and wild sugarcane species in response to hydrogen peroxide-induced oxidative stress
title_short Comparative physiological and transcriptome analysis in cultivated and wild sugarcane species in response to hydrogen peroxide-induced oxidative stress
title_sort comparative physiological and transcriptome analysis in cultivated and wild sugarcane species in response to hydrogen peroxide-induced oxidative stress
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10045617/
https://www.ncbi.nlm.nih.gov/pubmed/36973642
http://dx.doi.org/10.1186/s12864-023-09218-3
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