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Physiological and transcriptomic analyses reveal the molecular networks of responses induced by exogenous trehalose in plant

It is well known that exogenous trehalose can improve resistances of plants to some abiotic and biotic stresses. Nonetheless, information respecting the molecular responses of tobacco leaves to Tre treatment is limited. Here we show that exogenous Tre can rapidly reduce stomatal aperture, up-regulat...

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Autores principales: Shi, Yongchun, Sun, Hui, Wang, Xiaoran, Jin, Weihuan, Chen, Qianyi, Yuan, Zhengdong, Yu, Haidong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6530874/
https://www.ncbi.nlm.nih.gov/pubmed/31116769
http://dx.doi.org/10.1371/journal.pone.0217204
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author Shi, Yongchun
Sun, Hui
Wang, Xiaoran
Jin, Weihuan
Chen, Qianyi
Yuan, Zhengdong
Yu, Haidong
author_facet Shi, Yongchun
Sun, Hui
Wang, Xiaoran
Jin, Weihuan
Chen, Qianyi
Yuan, Zhengdong
Yu, Haidong
author_sort Shi, Yongchun
collection PubMed
description It is well known that exogenous trehalose can improve resistances of plants to some abiotic and biotic stresses. Nonetheless, information respecting the molecular responses of tobacco leaves to Tre treatment is limited. Here we show that exogenous Tre can rapidly reduce stomatal aperture, up-regulate NADPH oxidase genes and increase O(2)(•-)andH(2)O(2) on tobacco leaves at 2 h after treatment. We further demonstrated that imidazole and DPI, inhibitors of NADPH oxidase, can promote recovery of stomatal aperture of tobacco leaves upon trehalose treatment. Exogenous trehalose increased tobacco leaf resistance to tobacco mosaic disease significantly in a concentration-dependent way. To elucidate the molecular mechanisms in response to exogenous trehalose, the transcriptomic responses of tobacco leaves with 10 (low concentration) or 50 (high concentration) mM of trehalose treatment at 2 or 24h were investigated through RNA-seq approach. In total, 1288 differentially expressed genes (DEGs) were found with different conditions of trehalose treatments relative to control. Among them, 1075 (83.5%) were triggered by low concentration of trehalose (10mM), indicating that low concentration of Tre is a better elicitor. Functional annotations with KEGG pathway analysis revealed that the DEGs are involved in metabolic pathway, biosynthesis of secondary metabolites, plant hormone signal transduction, plant-pathogen interaction, protein processing in ER, flavonoid synthesis and circadian rhythm and so on. The protein-protein interaction networks generated from the core DEGs regulated by all conditions strikingly revealed that eight proteins, including ClpB1, HSP70, DnaJB1-like protein, universal stress protein (USP) A-like protein, two FTSH6 proteins, GolS1-like protein and chloroplastics HSP, play a core role in responses to exogenous trehalose in tobacco leaves. Our data suggest that trehalose triggers a signal transduction pathway which involves calcium and ROS-mediated signalings. These core components could lead to partial resistance or tolerance to abiotic and biotic stresses. Moreover, 19 DEGs were chosen for analysis of quantitative real-time polymerase chain reaction (qRT-PCR). The qRT-PCR for the 19 candidate genes coincided with the DEGs identified via the RNA-seq analysis, sustaining the reliability of our RNA-seq data.
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spelling pubmed-65308742019-05-31 Physiological and transcriptomic analyses reveal the molecular networks of responses induced by exogenous trehalose in plant Shi, Yongchun Sun, Hui Wang, Xiaoran Jin, Weihuan Chen, Qianyi Yuan, Zhengdong Yu, Haidong PLoS One Research Article It is well known that exogenous trehalose can improve resistances of plants to some abiotic and biotic stresses. Nonetheless, information respecting the molecular responses of tobacco leaves to Tre treatment is limited. Here we show that exogenous Tre can rapidly reduce stomatal aperture, up-regulate NADPH oxidase genes and increase O(2)(•-)andH(2)O(2) on tobacco leaves at 2 h after treatment. We further demonstrated that imidazole and DPI, inhibitors of NADPH oxidase, can promote recovery of stomatal aperture of tobacco leaves upon trehalose treatment. Exogenous trehalose increased tobacco leaf resistance to tobacco mosaic disease significantly in a concentration-dependent way. To elucidate the molecular mechanisms in response to exogenous trehalose, the transcriptomic responses of tobacco leaves with 10 (low concentration) or 50 (high concentration) mM of trehalose treatment at 2 or 24h were investigated through RNA-seq approach. In total, 1288 differentially expressed genes (DEGs) were found with different conditions of trehalose treatments relative to control. Among them, 1075 (83.5%) were triggered by low concentration of trehalose (10mM), indicating that low concentration of Tre is a better elicitor. Functional annotations with KEGG pathway analysis revealed that the DEGs are involved in metabolic pathway, biosynthesis of secondary metabolites, plant hormone signal transduction, plant-pathogen interaction, protein processing in ER, flavonoid synthesis and circadian rhythm and so on. The protein-protein interaction networks generated from the core DEGs regulated by all conditions strikingly revealed that eight proteins, including ClpB1, HSP70, DnaJB1-like protein, universal stress protein (USP) A-like protein, two FTSH6 proteins, GolS1-like protein and chloroplastics HSP, play a core role in responses to exogenous trehalose in tobacco leaves. Our data suggest that trehalose triggers a signal transduction pathway which involves calcium and ROS-mediated signalings. These core components could lead to partial resistance or tolerance to abiotic and biotic stresses. Moreover, 19 DEGs were chosen for analysis of quantitative real-time polymerase chain reaction (qRT-PCR). The qRT-PCR for the 19 candidate genes coincided with the DEGs identified via the RNA-seq analysis, sustaining the reliability of our RNA-seq data. Public Library of Science 2019-05-22 /pmc/articles/PMC6530874/ /pubmed/31116769 http://dx.doi.org/10.1371/journal.pone.0217204 Text en © 2019 Shi et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Shi, Yongchun
Sun, Hui
Wang, Xiaoran
Jin, Weihuan
Chen, Qianyi
Yuan, Zhengdong
Yu, Haidong
Physiological and transcriptomic analyses reveal the molecular networks of responses induced by exogenous trehalose in plant
title Physiological and transcriptomic analyses reveal the molecular networks of responses induced by exogenous trehalose in plant
title_full Physiological and transcriptomic analyses reveal the molecular networks of responses induced by exogenous trehalose in plant
title_fullStr Physiological and transcriptomic analyses reveal the molecular networks of responses induced by exogenous trehalose in plant
title_full_unstemmed Physiological and transcriptomic analyses reveal the molecular networks of responses induced by exogenous trehalose in plant
title_short Physiological and transcriptomic analyses reveal the molecular networks of responses induced by exogenous trehalose in plant
title_sort physiological and transcriptomic analyses reveal the molecular networks of responses induced by exogenous trehalose in plant
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6530874/
https://www.ncbi.nlm.nih.gov/pubmed/31116769
http://dx.doi.org/10.1371/journal.pone.0217204
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