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Comparative transcriptome and translatome analysis in contrasting rice genotypes reveals differential mRNA translation in salt-tolerant Pokkali under salt stress

BACKGROUND: Soil salinity is one of the primary causes of yield decline in rice. Pokkali (Pok) is a highly salt-tolerant landrace, whereas IR29 is a salt-sensitive but widely cultivated genotype. Comparative analysis of these genotypes may offer a better understanding of the salinity tolerance mecha...

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Autores principales: Li, Yong-Fang, Zheng, Yun, Vemireddy, Lakshminarayana R., Panda, Sanjib Kumar, Jose, Smitha, Ranjan, Alok, Panda, Piyalee, Govindan, Ganesan, Cui, Junxia, Wei, Kangning, Yaish, Mahmoud W., Naidoo, Gnanambal Charmaine, Sunkar, Ramanjulu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6311934/
https://www.ncbi.nlm.nih.gov/pubmed/30598105
http://dx.doi.org/10.1186/s12864-018-5279-4
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author Li, Yong-Fang
Zheng, Yun
Vemireddy, Lakshminarayana R.
Panda, Sanjib Kumar
Jose, Smitha
Ranjan, Alok
Panda, Piyalee
Govindan, Ganesan
Cui, Junxia
Wei, Kangning
Yaish, Mahmoud W.
Naidoo, Gnanambal Charmaine
Sunkar, Ramanjulu
author_facet Li, Yong-Fang
Zheng, Yun
Vemireddy, Lakshminarayana R.
Panda, Sanjib Kumar
Jose, Smitha
Ranjan, Alok
Panda, Piyalee
Govindan, Ganesan
Cui, Junxia
Wei, Kangning
Yaish, Mahmoud W.
Naidoo, Gnanambal Charmaine
Sunkar, Ramanjulu
author_sort Li, Yong-Fang
collection PubMed
description BACKGROUND: Soil salinity is one of the primary causes of yield decline in rice. Pokkali (Pok) is a highly salt-tolerant landrace, whereas IR29 is a salt-sensitive but widely cultivated genotype. Comparative analysis of these genotypes may offer a better understanding of the salinity tolerance mechanisms in rice. Although most stress-responsive genes are regulated at the transcriptional level, in many cases, changes at the transcriptional level are not always accompanied with the changes in protein abundance, which suggests that the transcriptome needs to be studied in conjunction with the proteome to link the phenotype of stress tolerance or sensitivity. Published reports have largely underscored the importance of transcriptional regulation during salt stress in these genotypes, but the regulation at the translational level has been rarely studied. Using RNA-Seq, we simultaneously analyzed the transcriptome and translatome from control and salt-exposed Pok and IR29 seedlings to unravel molecular insights into gene regulatory mechanisms that differ between these genotypes. RESULTS: Clear differences were evident at both transcriptional and translational levels between the two genotypes even under the control condition. In response to salt stress, 57 differentially expressed genes (DEGs) were commonly upregulated at both transcriptional and translational levels in both genotypes; the overall number of up/downregulated DEGs in IR29 was comparable at both transcriptional and translational levels, whereas in Pok, the number of upregulated DEGs was considerably higher at the translational level (544 DEGs) than at the transcriptional level (219 DEGs); in contrast, the number of downregulated DEGs (58) was significantly less at the translational level than at the transcriptional level (397 DEGs). These results imply that Pok stabilizes mRNAs and also efficiently loads mRNAs onto polysomes for translation during salt stress. CONCLUSION: Under salt stress, Pok is more efficient in maintaining cell wall integrity, detoxifying reactive oxygen species (ROS), translocating molecules and maintaining photosynthesis. The present study confirmed the known salt stress-associated genes and also identified a number of putative new salt-responsive genes. Most importantly, the study revealed that the translational regulation under salinity plays an important role in salt-tolerant Pok, but such regulation was less evident in the salt-sensitive IR29. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-5279-4) contains supplementary material, which is available to authorized users.
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spelling pubmed-63119342019-01-07 Comparative transcriptome and translatome analysis in contrasting rice genotypes reveals differential mRNA translation in salt-tolerant Pokkali under salt stress Li, Yong-Fang Zheng, Yun Vemireddy, Lakshminarayana R. Panda, Sanjib Kumar Jose, Smitha Ranjan, Alok Panda, Piyalee Govindan, Ganesan Cui, Junxia Wei, Kangning Yaish, Mahmoud W. Naidoo, Gnanambal Charmaine Sunkar, Ramanjulu BMC Genomics Research BACKGROUND: Soil salinity is one of the primary causes of yield decline in rice. Pokkali (Pok) is a highly salt-tolerant landrace, whereas IR29 is a salt-sensitive but widely cultivated genotype. Comparative analysis of these genotypes may offer a better understanding of the salinity tolerance mechanisms in rice. Although most stress-responsive genes are regulated at the transcriptional level, in many cases, changes at the transcriptional level are not always accompanied with the changes in protein abundance, which suggests that the transcriptome needs to be studied in conjunction with the proteome to link the phenotype of stress tolerance or sensitivity. Published reports have largely underscored the importance of transcriptional regulation during salt stress in these genotypes, but the regulation at the translational level has been rarely studied. Using RNA-Seq, we simultaneously analyzed the transcriptome and translatome from control and salt-exposed Pok and IR29 seedlings to unravel molecular insights into gene regulatory mechanisms that differ between these genotypes. RESULTS: Clear differences were evident at both transcriptional and translational levels between the two genotypes even under the control condition. In response to salt stress, 57 differentially expressed genes (DEGs) were commonly upregulated at both transcriptional and translational levels in both genotypes; the overall number of up/downregulated DEGs in IR29 was comparable at both transcriptional and translational levels, whereas in Pok, the number of upregulated DEGs was considerably higher at the translational level (544 DEGs) than at the transcriptional level (219 DEGs); in contrast, the number of downregulated DEGs (58) was significantly less at the translational level than at the transcriptional level (397 DEGs). These results imply that Pok stabilizes mRNAs and also efficiently loads mRNAs onto polysomes for translation during salt stress. CONCLUSION: Under salt stress, Pok is more efficient in maintaining cell wall integrity, detoxifying reactive oxygen species (ROS), translocating molecules and maintaining photosynthesis. The present study confirmed the known salt stress-associated genes and also identified a number of putative new salt-responsive genes. Most importantly, the study revealed that the translational regulation under salinity plays an important role in salt-tolerant Pok, but such regulation was less evident in the salt-sensitive IR29. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-018-5279-4) contains supplementary material, which is available to authorized users. BioMed Central 2018-12-31 /pmc/articles/PMC6311934/ /pubmed/30598105 http://dx.doi.org/10.1186/s12864-018-5279-4 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
Li, Yong-Fang
Zheng, Yun
Vemireddy, Lakshminarayana R.
Panda, Sanjib Kumar
Jose, Smitha
Ranjan, Alok
Panda, Piyalee
Govindan, Ganesan
Cui, Junxia
Wei, Kangning
Yaish, Mahmoud W.
Naidoo, Gnanambal Charmaine
Sunkar, Ramanjulu
Comparative transcriptome and translatome analysis in contrasting rice genotypes reveals differential mRNA translation in salt-tolerant Pokkali under salt stress
title Comparative transcriptome and translatome analysis in contrasting rice genotypes reveals differential mRNA translation in salt-tolerant Pokkali under salt stress
title_full Comparative transcriptome and translatome analysis in contrasting rice genotypes reveals differential mRNA translation in salt-tolerant Pokkali under salt stress
title_fullStr Comparative transcriptome and translatome analysis in contrasting rice genotypes reveals differential mRNA translation in salt-tolerant Pokkali under salt stress
title_full_unstemmed Comparative transcriptome and translatome analysis in contrasting rice genotypes reveals differential mRNA translation in salt-tolerant Pokkali under salt stress
title_short Comparative transcriptome and translatome analysis in contrasting rice genotypes reveals differential mRNA translation in salt-tolerant Pokkali under salt stress
title_sort comparative transcriptome and translatome analysis in contrasting rice genotypes reveals differential mrna translation in salt-tolerant pokkali under salt stress
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6311934/
https://www.ncbi.nlm.nih.gov/pubmed/30598105
http://dx.doi.org/10.1186/s12864-018-5279-4
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