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Transcriptomic Profiling of Tomato Leaves Identifies Novel Transcription Factors Responding to Dehydration Stress

Drought is among the most challenging environmental restrictions to tomatoes (Solanum lycopersi-cum), which causes dehydration of the tissues and results in massive loss of yield. Breeding for dehydration-tolerant tomatoes is a pressing issue as a result of global climate change that leads to increa...

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Autores principales: Dong, Shuchao, Ling, Jiayi, Song, Liuxia, Zhao, Liping, Wang, Yinlei, Zhao, Tongmin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10253658/
https://www.ncbi.nlm.nih.gov/pubmed/37298675
http://dx.doi.org/10.3390/ijms24119725
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author Dong, Shuchao
Ling, Jiayi
Song, Liuxia
Zhao, Liping
Wang, Yinlei
Zhao, Tongmin
author_facet Dong, Shuchao
Ling, Jiayi
Song, Liuxia
Zhao, Liping
Wang, Yinlei
Zhao, Tongmin
author_sort Dong, Shuchao
collection PubMed
description Drought is among the most challenging environmental restrictions to tomatoes (Solanum lycopersi-cum), which causes dehydration of the tissues and results in massive loss of yield. Breeding for dehydration-tolerant tomatoes is a pressing issue as a result of global climate change that leads to increased duration and frequency of droughts. However, the key genes involved in dehydration response and tolerance in tomato are not widely known, and genes that can be targeted for dehydration-tolerant tomato breeding remains to be discovered. Here, we compared phenotypes and transcriptomic profiles of tomato leaves between control and dehydration conditions. We show that dehydration decreased the relative water content of tomato leaves after 2 h of dehydration treatment; however, it promoted the malondialdehyde (MDA) content and ion leakage ratio after 4 h and 12 h of dehydration, respectively. Moreover, dehydration stress triggered oxidative stress as we detected significant increases in H(2)O(2) and O(2−) levels. Simultaneously, dehydration enhanced the activities of antioxidant enzymes including peroxidase (POD), superoxide dismutase (SOD), catalase (CAT), and phenylalanine ammonia-lyase (PAL). Genome-wide RNA sequencing of tomato leaves treated with or without dehydration (control) identified 8116 and 5670 differentially expressed genes (DEGs) after 2 h and 4 h of dehydration, respectively. These DEGs included genes involved in translation, photosynthesis, stress response, and cytoplasmic translation. We then focused specifically on DEGs annotated as transcription factors (TFs). RNA-seq analysis identified 742 TFs as DEGs by comparing samples dehydrated for 2 h with 0 h control, while among all the DEGs detected after 4 h of dehydration, only 499 of them were TFs. Furthermore, we performed real-time quantitative PCR analyses and validated expression patterns of 31 differentially expressed TFs of NAC, AP2/ERF, MYB, bHLH, bZIP, WRKY, and HB families. In addition, the transcriptomic data revealed that expression levels of six drought-responsive marker genes were upregulated by de-hydration treatment. Collectively, our findings not only provide a solid foundation for further functional characterization of dehydration-responsive TFs in tomatoes but may also benefit the improvement of dehydration/drought tolerance in tomatoes in the future.
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spelling pubmed-102536582023-06-10 Transcriptomic Profiling of Tomato Leaves Identifies Novel Transcription Factors Responding to Dehydration Stress Dong, Shuchao Ling, Jiayi Song, Liuxia Zhao, Liping Wang, Yinlei Zhao, Tongmin Int J Mol Sci Article Drought is among the most challenging environmental restrictions to tomatoes (Solanum lycopersi-cum), which causes dehydration of the tissues and results in massive loss of yield. Breeding for dehydration-tolerant tomatoes is a pressing issue as a result of global climate change that leads to increased duration and frequency of droughts. However, the key genes involved in dehydration response and tolerance in tomato are not widely known, and genes that can be targeted for dehydration-tolerant tomato breeding remains to be discovered. Here, we compared phenotypes and transcriptomic profiles of tomato leaves between control and dehydration conditions. We show that dehydration decreased the relative water content of tomato leaves after 2 h of dehydration treatment; however, it promoted the malondialdehyde (MDA) content and ion leakage ratio after 4 h and 12 h of dehydration, respectively. Moreover, dehydration stress triggered oxidative stress as we detected significant increases in H(2)O(2) and O(2−) levels. Simultaneously, dehydration enhanced the activities of antioxidant enzymes including peroxidase (POD), superoxide dismutase (SOD), catalase (CAT), and phenylalanine ammonia-lyase (PAL). Genome-wide RNA sequencing of tomato leaves treated with or without dehydration (control) identified 8116 and 5670 differentially expressed genes (DEGs) after 2 h and 4 h of dehydration, respectively. These DEGs included genes involved in translation, photosynthesis, stress response, and cytoplasmic translation. We then focused specifically on DEGs annotated as transcription factors (TFs). RNA-seq analysis identified 742 TFs as DEGs by comparing samples dehydrated for 2 h with 0 h control, while among all the DEGs detected after 4 h of dehydration, only 499 of them were TFs. Furthermore, we performed real-time quantitative PCR analyses and validated expression patterns of 31 differentially expressed TFs of NAC, AP2/ERF, MYB, bHLH, bZIP, WRKY, and HB families. In addition, the transcriptomic data revealed that expression levels of six drought-responsive marker genes were upregulated by de-hydration treatment. Collectively, our findings not only provide a solid foundation for further functional characterization of dehydration-responsive TFs in tomatoes but may also benefit the improvement of dehydration/drought tolerance in tomatoes in the future. MDPI 2023-06-03 /pmc/articles/PMC10253658/ /pubmed/37298675 http://dx.doi.org/10.3390/ijms24119725 Text en © 2023 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Dong, Shuchao
Ling, Jiayi
Song, Liuxia
Zhao, Liping
Wang, Yinlei
Zhao, Tongmin
Transcriptomic Profiling of Tomato Leaves Identifies Novel Transcription Factors Responding to Dehydration Stress
title Transcriptomic Profiling of Tomato Leaves Identifies Novel Transcription Factors Responding to Dehydration Stress
title_full Transcriptomic Profiling of Tomato Leaves Identifies Novel Transcription Factors Responding to Dehydration Stress
title_fullStr Transcriptomic Profiling of Tomato Leaves Identifies Novel Transcription Factors Responding to Dehydration Stress
title_full_unstemmed Transcriptomic Profiling of Tomato Leaves Identifies Novel Transcription Factors Responding to Dehydration Stress
title_short Transcriptomic Profiling of Tomato Leaves Identifies Novel Transcription Factors Responding to Dehydration Stress
title_sort transcriptomic profiling of tomato leaves identifies novel transcription factors responding to dehydration stress
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10253658/
https://www.ncbi.nlm.nih.gov/pubmed/37298675
http://dx.doi.org/10.3390/ijms24119725
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