PI signal transduction and ubiquitination respond to dehydration stress in the red seaweed Gloiopeltis furcata under successive tidal cycles

Abstract Background Intermittent dehydration caused by tidal changes is one of the most important abiotic factors that intertidal seaweeds must cope with in order to retain normal growth and reproduction. However, the underlying molecular mechanisms for the adaptation of red seaweeds to repeated deh...

Full description

Bibliographic Details
Main Authors: Shun Liu, Zi-Min Hu, Quansheng Zhang, Xiaoqi Yang, Alan T. Critchley, Delin Duan
Format: Article
Language:English
Published: BMC 2019-11-01
Series:BMC Plant Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12870-019-2125-z
id doaj-43fa10f8644048d3934b12859eac0398
record_format Article
spelling doaj-43fa10f8644048d3934b12859eac03982020-11-25T02:38:24ZengBMCBMC Plant Biology1471-22292019-11-0119111410.1186/s12870-019-2125-zPI signal transduction and ubiquitination respond to dehydration stress in the red seaweed Gloiopeltis furcata under successive tidal cyclesShun Liu0Zi-Min Hu1Quansheng Zhang2Xiaoqi Yang3Alan T. Critchley4Delin Duan5Key Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of SciencesKey Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of SciencesOcean School, Yantai UniversityKey Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of SciencesVerschuren Centre for Sustainability in Energy and Environment, University of Cape BretonKey Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of SciencesAbstract Background Intermittent dehydration caused by tidal changes is one of the most important abiotic factors that intertidal seaweeds must cope with in order to retain normal growth and reproduction. However, the underlying molecular mechanisms for the adaptation of red seaweeds to repeated dehydration-rehydration cycles remain poorly understood. Results We chose the red seaweed Gloiopeltis furcata as a model and simulated natural tidal changes with two consecutive dehydration-rehydration cycles occurring over 24 h in order to gain insight into key molecular pathways and regulation of genes which are associated with dehydration tolerance. Transcription sequencing assembled 32,681 uni-genes (GC content = 55.32%), of which 12,813 were annotated. Weighted gene co-expression network analysis (WGCNA) divided all transcripts into 20 modules, with Coral2 identified as the key module anchoring dehydration-induced genes. Pathways enriched analysis indicated that the ubiquitin-mediated proteolysis pathway (UPP) and phosphatidylinositol (PI) signaling system were crucial for a successful response in G. furcata. Network-establishing and quantitative reverse transcription PCR (qRT-PCR) suggested that genes encoding ubiquitin-protein ligase E3 (E3–1), SUMO-activating enzyme sub-unit 2 (SAE2), calmodulin (CaM) and inositol-1,3,4-trisphosphate 5/6-kinase (ITPK) were the hub genes which responded positively to two successive dehydration treatments. Network-based interactions with hub genes indicated that transcription factor (e.g. TFIID), RNA modification (e.g. DEAH) and osmotic adjustment (e.g. MIP, ABC1, Bam1) were related to these two pathways. Conclusions RNA sequencing-based evidence from G. furcata enriched the informational database for intertidal red seaweeds which face periodic dehydration stress during the low tide period. This provided insights into an increased understanding of how ubiquitin-mediated proteolysis and the phosphatidylinositol signaling system help seaweeds responding to dehydration-rehydration cycles.http://link.springer.com/article/10.1186/s12870-019-2125-zSeaweedDehydrationUbiquitinationPhosphatidylinositol signaling systemWeighted gene co-expression network analysis
collection DOAJ
language English
format Article
sources DOAJ
author Shun Liu
Zi-Min Hu
Quansheng Zhang
Xiaoqi Yang
Alan T. Critchley
Delin Duan
spellingShingle Shun Liu
Zi-Min Hu
Quansheng Zhang
Xiaoqi Yang
Alan T. Critchley
Delin Duan
PI signal transduction and ubiquitination respond to dehydration stress in the red seaweed Gloiopeltis furcata under successive tidal cycles
BMC Plant Biology
Seaweed
Dehydration
Ubiquitination
Phosphatidylinositol signaling system
Weighted gene co-expression network analysis
author_facet Shun Liu
Zi-Min Hu
Quansheng Zhang
Xiaoqi Yang
Alan T. Critchley
Delin Duan
author_sort Shun Liu
title PI signal transduction and ubiquitination respond to dehydration stress in the red seaweed Gloiopeltis furcata under successive tidal cycles
title_short PI signal transduction and ubiquitination respond to dehydration stress in the red seaweed Gloiopeltis furcata under successive tidal cycles
title_full PI signal transduction and ubiquitination respond to dehydration stress in the red seaweed Gloiopeltis furcata under successive tidal cycles
title_fullStr PI signal transduction and ubiquitination respond to dehydration stress in the red seaweed Gloiopeltis furcata under successive tidal cycles
title_full_unstemmed PI signal transduction and ubiquitination respond to dehydration stress in the red seaweed Gloiopeltis furcata under successive tidal cycles
title_sort pi signal transduction and ubiquitination respond to dehydration stress in the red seaweed gloiopeltis furcata under successive tidal cycles
publisher BMC
series BMC Plant Biology
issn 1471-2229
publishDate 2019-11-01
description Abstract Background Intermittent dehydration caused by tidal changes is one of the most important abiotic factors that intertidal seaweeds must cope with in order to retain normal growth and reproduction. However, the underlying molecular mechanisms for the adaptation of red seaweeds to repeated dehydration-rehydration cycles remain poorly understood. Results We chose the red seaweed Gloiopeltis furcata as a model and simulated natural tidal changes with two consecutive dehydration-rehydration cycles occurring over 24 h in order to gain insight into key molecular pathways and regulation of genes which are associated with dehydration tolerance. Transcription sequencing assembled 32,681 uni-genes (GC content = 55.32%), of which 12,813 were annotated. Weighted gene co-expression network analysis (WGCNA) divided all transcripts into 20 modules, with Coral2 identified as the key module anchoring dehydration-induced genes. Pathways enriched analysis indicated that the ubiquitin-mediated proteolysis pathway (UPP) and phosphatidylinositol (PI) signaling system were crucial for a successful response in G. furcata. Network-establishing and quantitative reverse transcription PCR (qRT-PCR) suggested that genes encoding ubiquitin-protein ligase E3 (E3–1), SUMO-activating enzyme sub-unit 2 (SAE2), calmodulin (CaM) and inositol-1,3,4-trisphosphate 5/6-kinase (ITPK) were the hub genes which responded positively to two successive dehydration treatments. Network-based interactions with hub genes indicated that transcription factor (e.g. TFIID), RNA modification (e.g. DEAH) and osmotic adjustment (e.g. MIP, ABC1, Bam1) were related to these two pathways. Conclusions RNA sequencing-based evidence from G. furcata enriched the informational database for intertidal red seaweeds which face periodic dehydration stress during the low tide period. This provided insights into an increased understanding of how ubiquitin-mediated proteolysis and the phosphatidylinositol signaling system help seaweeds responding to dehydration-rehydration cycles.
topic Seaweed
Dehydration
Ubiquitination
Phosphatidylinositol signaling system
Weighted gene co-expression network analysis
url http://link.springer.com/article/10.1186/s12870-019-2125-z
work_keys_str_mv AT shunliu pisignaltransductionandubiquitinationrespondtodehydrationstressintheredseaweedgloiopeltisfurcataundersuccessivetidalcycles
AT ziminhu pisignaltransductionandubiquitinationrespondtodehydrationstressintheredseaweedgloiopeltisfurcataundersuccessivetidalcycles
AT quanshengzhang pisignaltransductionandubiquitinationrespondtodehydrationstressintheredseaweedgloiopeltisfurcataundersuccessivetidalcycles
AT xiaoqiyang pisignaltransductionandubiquitinationrespondtodehydrationstressintheredseaweedgloiopeltisfurcataundersuccessivetidalcycles
AT alantcritchley pisignaltransductionandubiquitinationrespondtodehydrationstressintheredseaweedgloiopeltisfurcataundersuccessivetidalcycles
AT delinduan pisignaltransductionandubiquitinationrespondtodehydrationstressintheredseaweedgloiopeltisfurcataundersuccessivetidalcycles
_version_ 1724791177310371840