Cargando…

SMRT and Illumina RNA sequencing reveal novel insights into the heat stress response and crosstalk with leaf senescence in tall fescue

BACKGROUND: As a cool-season grass species, tall fescue (Festuca arundinacea) is challenged by increasing temperatures. Heat acclimation or activation of leaf senescence, are two main strategies when tall fescue is exposed to heat stress (HS). However, lacking a genome sequence, the complexity of he...

Descripción completa

Detalles Bibliográficos
Autores principales: Qian, Yiguang, Cao, Liwen, Zhang, Qiang, Amee, Maurice, Chen, Ke, Chen, Liang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7397585/
https://www.ncbi.nlm.nih.gov/pubmed/32746857
http://dx.doi.org/10.1186/s12870-020-02572-4
_version_ 1783565798108823552
author Qian, Yiguang
Cao, Liwen
Zhang, Qiang
Amee, Maurice
Chen, Ke
Chen, Liang
author_facet Qian, Yiguang
Cao, Liwen
Zhang, Qiang
Amee, Maurice
Chen, Ke
Chen, Liang
author_sort Qian, Yiguang
collection PubMed
description BACKGROUND: As a cool-season grass species, tall fescue (Festuca arundinacea) is challenged by increasing temperatures. Heat acclimation or activation of leaf senescence, are two main strategies when tall fescue is exposed to heat stress (HS). However, lacking a genome sequence, the complexity of hexaploidy nature, and the short read of second-generation sequencing hinder a comprehensive understanding of the mechanism. This study aims to characterize the molecular mechanism of heat adaptation and heat-induced senescence at transcriptional and post-transcriptional levels. RESULTS: Transcriptome of heat-treated (1 h and 72 h) and senescent leaves of tall fescue were generated by combining single-molecular real-time and Illumina sequencing. In total, 4076; 6917, and 11,918 differentially expressed genes (DEGs) were induced by short- and long-term heat stress (HS), and senescence, respectively. Venn and bioinformatics analyses of DEGs showed that short-term HS strongly activated heat shock proteins (Hsps) and heat shock factors (Hsfs), as well as specifically activated FK506-binding proteins (FKBPs), calcium signaling genes, glutathione S-transferase genes, photosynthesis-related genes, and phytohormone signaling genes. By contrast, long-term HS shared most of DEGs with senescence, including the up-regulated chlorophyll catabolic genes, phytohormone synthesis/degradation genes, stress-related genes, and NACs, and the down-regulated photosynthesis-related genes, FKBPs, and catalases. Subsequently, transient overexpression in tobacco showed that FaHsfA2a (up-regulated specifically by short-term HS) reduced cell membrane damages caused by HS, but FaNAC029 and FaNAM-B1 (up-regulated by long-term HS and senescence) increased the damages. Besides, alternative splicing was widely observed in HS and senescence responsive genes, including Hsps, Hsfs, and phytohormone signaling/synthesis genes. CONCLUSIONS: The short-term HS can stimulate gene responses and improve thermotolerance, but long-term HS is a damage and may accelerate leaf senescence. These results contribute to our understanding of the molecular mechanism underlying heat adaptation and heat-induced senescence.
format Online
Article
Text
id pubmed-7397585
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-73975852020-08-06 SMRT and Illumina RNA sequencing reveal novel insights into the heat stress response and crosstalk with leaf senescence in tall fescue Qian, Yiguang Cao, Liwen Zhang, Qiang Amee, Maurice Chen, Ke Chen, Liang BMC Plant Biol Research Article BACKGROUND: As a cool-season grass species, tall fescue (Festuca arundinacea) is challenged by increasing temperatures. Heat acclimation or activation of leaf senescence, are two main strategies when tall fescue is exposed to heat stress (HS). However, lacking a genome sequence, the complexity of hexaploidy nature, and the short read of second-generation sequencing hinder a comprehensive understanding of the mechanism. This study aims to characterize the molecular mechanism of heat adaptation and heat-induced senescence at transcriptional and post-transcriptional levels. RESULTS: Transcriptome of heat-treated (1 h and 72 h) and senescent leaves of tall fescue were generated by combining single-molecular real-time and Illumina sequencing. In total, 4076; 6917, and 11,918 differentially expressed genes (DEGs) were induced by short- and long-term heat stress (HS), and senescence, respectively. Venn and bioinformatics analyses of DEGs showed that short-term HS strongly activated heat shock proteins (Hsps) and heat shock factors (Hsfs), as well as specifically activated FK506-binding proteins (FKBPs), calcium signaling genes, glutathione S-transferase genes, photosynthesis-related genes, and phytohormone signaling genes. By contrast, long-term HS shared most of DEGs with senescence, including the up-regulated chlorophyll catabolic genes, phytohormone synthesis/degradation genes, stress-related genes, and NACs, and the down-regulated photosynthesis-related genes, FKBPs, and catalases. Subsequently, transient overexpression in tobacco showed that FaHsfA2a (up-regulated specifically by short-term HS) reduced cell membrane damages caused by HS, but FaNAC029 and FaNAM-B1 (up-regulated by long-term HS and senescence) increased the damages. Besides, alternative splicing was widely observed in HS and senescence responsive genes, including Hsps, Hsfs, and phytohormone signaling/synthesis genes. CONCLUSIONS: The short-term HS can stimulate gene responses and improve thermotolerance, but long-term HS is a damage and may accelerate leaf senescence. These results contribute to our understanding of the molecular mechanism underlying heat adaptation and heat-induced senescence. BioMed Central 2020-08-03 /pmc/articles/PMC7397585/ /pubmed/32746857 http://dx.doi.org/10.1186/s12870-020-02572-4 Text en © The Author(s) 2020 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/. 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 in a credit line to the data.
spellingShingle Research Article
Qian, Yiguang
Cao, Liwen
Zhang, Qiang
Amee, Maurice
Chen, Ke
Chen, Liang
SMRT and Illumina RNA sequencing reveal novel insights into the heat stress response and crosstalk with leaf senescence in tall fescue
title SMRT and Illumina RNA sequencing reveal novel insights into the heat stress response and crosstalk with leaf senescence in tall fescue
title_full SMRT and Illumina RNA sequencing reveal novel insights into the heat stress response and crosstalk with leaf senescence in tall fescue
title_fullStr SMRT and Illumina RNA sequencing reveal novel insights into the heat stress response and crosstalk with leaf senescence in tall fescue
title_full_unstemmed SMRT and Illumina RNA sequencing reveal novel insights into the heat stress response and crosstalk with leaf senescence in tall fescue
title_short SMRT and Illumina RNA sequencing reveal novel insights into the heat stress response and crosstalk with leaf senescence in tall fescue
title_sort smrt and illumina rna sequencing reveal novel insights into the heat stress response and crosstalk with leaf senescence in tall fescue
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7397585/
https://www.ncbi.nlm.nih.gov/pubmed/32746857
http://dx.doi.org/10.1186/s12870-020-02572-4
work_keys_str_mv AT qianyiguang smrtandilluminarnasequencingrevealnovelinsightsintotheheatstressresponseandcrosstalkwithleafsenescenceintallfescue
AT caoliwen smrtandilluminarnasequencingrevealnovelinsightsintotheheatstressresponseandcrosstalkwithleafsenescenceintallfescue
AT zhangqiang smrtandilluminarnasequencingrevealnovelinsightsintotheheatstressresponseandcrosstalkwithleafsenescenceintallfescue
AT ameemaurice smrtandilluminarnasequencingrevealnovelinsightsintotheheatstressresponseandcrosstalkwithleafsenescenceintallfescue
AT chenke smrtandilluminarnasequencingrevealnovelinsightsintotheheatstressresponseandcrosstalkwithleafsenescenceintallfescue
AT chenliang smrtandilluminarnasequencingrevealnovelinsightsintotheheatstressresponseandcrosstalkwithleafsenescenceintallfescue