Transcriptome analysis reveals regulatory framework for salt and osmotic tolerance in a succulent xerophyte

Abstract Background Zygophyllum xanthoxylum is a succulent xerophyte with remarkable tolerance to diverse abiotic stresses. Previous studies have revealed important physiological mechanisms and identified functional genes associated with stress tolerance. However, knowledge of the regulatory genes c...

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Main Authors: Hongju Yin, Mengzhan Li, Dingding Li, Sardar-Ali Khan, Shelley R. Hepworth, Suo-Min Wang
Format: Article
Language:English
Published: BMC 2019-02-01
Series:BMC Plant Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12870-019-1686-1
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author Hongju Yin
Mengzhan Li
Dingding Li
Sardar-Ali Khan
Shelley R. Hepworth
Suo-Min Wang
author_facet Hongju Yin
Mengzhan Li
Dingding Li
Sardar-Ali Khan
Shelley R. Hepworth
Suo-Min Wang
author_sort Hongju Yin
collection DOAJ
description Abstract Background Zygophyllum xanthoxylum is a succulent xerophyte with remarkable tolerance to diverse abiotic stresses. Previous studies have revealed important physiological mechanisms and identified functional genes associated with stress tolerance. However, knowledge of the regulatory genes conferring stress tolerance in this species is poorly understood. Results Here, we present a comprehensive analysis of regulatory genes based on the transcriptome of Z. xanthoxylum roots exposed to osmotic stress and salt treatments. Significant changes were observed in transcripts related to known and obscure stress-related hormone signaling pathways, in particular abscisic acid and auxin. Significant changes were also found among key classes of early response regulatory genes encoding protein kinases, transcription factors, and ubiquitin-mediated proteolysis machinery. Network analysis shows a highly integrated matrix formed by these conserved and novel gene products associated with osmotic stress and salt in Z. xanthoxylum. Among them, two previously uncharacterized NAC (NAM/ATAF/CUC) transcription factor genes, ZxNAC083 (Unigene16368_All) and ZxNAC035 (CL6534.Contig1_All), conferred tolerance to salt and drought stress when constitutively overexpressed in Arabidopsis plants. Conclusions This study provides a unique framework for understanding osmotic stress and salt adaptation in Z. xanthoxylum including novel gene targets for engineering stress tolerance in susceptible crop species.
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spelling doaj.art-762ed3a90f5d4a33a519ad77455580352022-12-22T03:15:42ZengBMCBMC Plant Biology1471-22292019-02-0119111510.1186/s12870-019-1686-1Transcriptome analysis reveals regulatory framework for salt and osmotic tolerance in a succulent xerophyteHongju Yin0Mengzhan Li1Dingding Li2Sardar-Ali Khan3Shelley R. Hepworth4Suo-Min Wang5State Key Laboratory of Grassland Agro-ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs; College of Pastoral Agriculture Science and Technology, Lanzhou UniversityState Key Laboratory of Grassland Agro-ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs; College of Pastoral Agriculture Science and Technology, Lanzhou UniversityState Key Laboratory of Grassland Agro-ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs; College of Pastoral Agriculture Science and Technology, Lanzhou UniversityState Key Laboratory of Grassland Agro-ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs; College of Pastoral Agriculture Science and Technology, Lanzhou UniversityState Key Laboratory of Grassland Agro-ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs; College of Pastoral Agriculture Science and Technology, Lanzhou UniversityState Key Laboratory of Grassland Agro-ecosystems; Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs; College of Pastoral Agriculture Science and Technology, Lanzhou UniversityAbstract Background Zygophyllum xanthoxylum is a succulent xerophyte with remarkable tolerance to diverse abiotic stresses. Previous studies have revealed important physiological mechanisms and identified functional genes associated with stress tolerance. However, knowledge of the regulatory genes conferring stress tolerance in this species is poorly understood. Results Here, we present a comprehensive analysis of regulatory genes based on the transcriptome of Z. xanthoxylum roots exposed to osmotic stress and salt treatments. Significant changes were observed in transcripts related to known and obscure stress-related hormone signaling pathways, in particular abscisic acid and auxin. Significant changes were also found among key classes of early response regulatory genes encoding protein kinases, transcription factors, and ubiquitin-mediated proteolysis machinery. Network analysis shows a highly integrated matrix formed by these conserved and novel gene products associated with osmotic stress and salt in Z. xanthoxylum. Among them, two previously uncharacterized NAC (NAM/ATAF/CUC) transcription factor genes, ZxNAC083 (Unigene16368_All) and ZxNAC035 (CL6534.Contig1_All), conferred tolerance to salt and drought stress when constitutively overexpressed in Arabidopsis plants. Conclusions This study provides a unique framework for understanding osmotic stress and salt adaptation in Z. xanthoxylum including novel gene targets for engineering stress tolerance in susceptible crop species.http://link.springer.com/article/10.1186/s12870-019-1686-1RNA-sequencingOsmotic stressSaltProtein kinasesTranscription factorsProteolysis
spellingShingle Hongju Yin
Mengzhan Li
Dingding Li
Sardar-Ali Khan
Shelley R. Hepworth
Suo-Min Wang
Transcriptome analysis reveals regulatory framework for salt and osmotic tolerance in a succulent xerophyte
BMC Plant Biology
RNA-sequencing
Osmotic stress
Salt
Protein kinases
Transcription factors
Proteolysis
title Transcriptome analysis reveals regulatory framework for salt and osmotic tolerance in a succulent xerophyte
title_full Transcriptome analysis reveals regulatory framework for salt and osmotic tolerance in a succulent xerophyte
title_fullStr Transcriptome analysis reveals regulatory framework for salt and osmotic tolerance in a succulent xerophyte
title_full_unstemmed Transcriptome analysis reveals regulatory framework for salt and osmotic tolerance in a succulent xerophyte
title_short Transcriptome analysis reveals regulatory framework for salt and osmotic tolerance in a succulent xerophyte
title_sort transcriptome analysis reveals regulatory framework for salt and osmotic tolerance in a succulent xerophyte
topic RNA-sequencing
Osmotic stress
Salt
Protein kinases
Transcription factors
Proteolysis
url http://link.springer.com/article/10.1186/s12870-019-1686-1
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AT sardaralikhan transcriptomeanalysisrevealsregulatoryframeworkforsaltandosmotictoleranceinasucculentxerophyte
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