skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Identification of Ice Plant (Mesembryanthemum crystallinum L.) MicroRNAs Using RNA-Seq and Their Putative Roles in High Salinity Responses in Seedlings

Abstract

The halophyte Mesembryanthemum crystallinum (common or crystalline ice plant) is a useful model for studying molecular mechanisms of salt tolerance. The morphology, physiology, metabolism, and gene expression of ice plant have been studied and large-scale analyses of gene expression profiling have drawn an outline of salt tolerance in ice plant. A rapid root growth to a sudden increase in salinity was observed in ice plant seedlings. Using a fluorescent dye to detect Na+, we found that ice plant roots respond to an increased flux of Na+ by either secreting or storing Na+ in specialized cells. High-throughput sequencing was used to identify small RNA profiles in 3-day-old seedlings treated with or without 200 mM NaCl. In total, 135 conserved miRNAs belonging to 21 families were found. The hairpin precursor of 19 conserved mcr-miRNAs and 12 novel mcr-miRNAs were identified. After 6 h of salt stress, the expression of most mcr-miRNAs showed decreased relative abundance, whereas the expression of their corresponding target genes showed increased mRNA relative abundance. The cognate target genes are involved in a broad range of biological processes: transcription factors that regulate growth and development, enzymes that catalyze miRNA biogenesis for the most conserved mcr-miRNA, and proteins that aremore » involved in ion homeostasis and drought-stress responses for some novel mcr-miRNAs. Analyses of the functions of target genes revealed that cellular processes, including growth and development, metabolism, and ion transport activity are likely to be enhanced in roots under salt stress. The expression of eleven conserved miRNAs and two novel miRNAs were correlated reciprocally with predicted targets within hours after salt stress exposure. Several conserved miRNAs have been known to regulate root elongation, root apical meristem activity, and lateral root formation. Based upon the expression pattern of miRNA and target genes in combination with the observation of Na+ distribution, ice plant likely responds to increased salinity by using Na+ as an osmoticum for cell expansion and guard cell opening. Excessive Na+ could either be secreted through the root epidermis or stored in specialized leaf epidermal cells. These responses are regulated in part at the miRNA-mediated post-transcriptional level.« less

Authors:
 [1];  [2];  [3];  [4];  [4];  [2];  [1]
  1. National Chung Hsing Univ., Taichung (Taiwan). Dept. of Life Sciences
  2. Univ. of Nevada, Reno, NV (United States). Dept. of Biochemistry and Molecular Biology
  3. National Chung Hsing Univ., Taichung (Taiwan). Dept. of Forestry
  4. Kobe Univ., Kobe (Japan). Graduate School of Science
Publication Date:
Research Org.:
Univ. of Nevada, Reno, NV (United States)
Sponsoring Org.:
Ministry of Science and Technology, Taiwan; USDOE Office of Science (SC); National Science Foundation (NSF)
OSTI Identifier:
1326672
Grant/Contract Number:  
SC0008834; MOST 103-2311- B-005-003; IOS-084373
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Frontiers in Plant Science
Additional Journal Information:
Journal Volume: 7; Journal ID: ISSN 1664-462X
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; small RNA profile; halophyte; ice plant; miRNA; root growth; salinity responses

Citation Formats

Chiang, Chih-Pin, Yim, Won C., Sun, Ying-Hsuan, Ohnishi, Miwa, Mimura, Tetsuro, Cushman, John C., and Yen, Hungchen E. Identification of Ice Plant (Mesembryanthemum crystallinum L.) MicroRNAs Using RNA-Seq and Their Putative Roles in High Salinity Responses in Seedlings. United States: N. p., 2016. Web. doi:10.3389/fpls.2016.01143.
Chiang, Chih-Pin, Yim, Won C., Sun, Ying-Hsuan, Ohnishi, Miwa, Mimura, Tetsuro, Cushman, John C., & Yen, Hungchen E. Identification of Ice Plant (Mesembryanthemum crystallinum L.) MicroRNAs Using RNA-Seq and Their Putative Roles in High Salinity Responses in Seedlings. United States. https://doi.org/10.3389/fpls.2016.01143
Chiang, Chih-Pin, Yim, Won C., Sun, Ying-Hsuan, Ohnishi, Miwa, Mimura, Tetsuro, Cushman, John C., and Yen, Hungchen E. 2016. "Identification of Ice Plant (Mesembryanthemum crystallinum L.) MicroRNAs Using RNA-Seq and Their Putative Roles in High Salinity Responses in Seedlings". United States. https://doi.org/10.3389/fpls.2016.01143. https://www.osti.gov/servlets/purl/1326672.
@article{osti_1326672,
title = {Identification of Ice Plant (Mesembryanthemum crystallinum L.) MicroRNAs Using RNA-Seq and Their Putative Roles in High Salinity Responses in Seedlings},
author = {Chiang, Chih-Pin and Yim, Won C. and Sun, Ying-Hsuan and Ohnishi, Miwa and Mimura, Tetsuro and Cushman, John C. and Yen, Hungchen E.},
abstractNote = {The halophyte Mesembryanthemum crystallinum (common or crystalline ice plant) is a useful model for studying molecular mechanisms of salt tolerance. The morphology, physiology, metabolism, and gene expression of ice plant have been studied and large-scale analyses of gene expression profiling have drawn an outline of salt tolerance in ice plant. A rapid root growth to a sudden increase in salinity was observed in ice plant seedlings. Using a fluorescent dye to detect Na+, we found that ice plant roots respond to an increased flux of Na+ by either secreting or storing Na+ in specialized cells. High-throughput sequencing was used to identify small RNA profiles in 3-day-old seedlings treated with or without 200 mM NaCl. In total, 135 conserved miRNAs belonging to 21 families were found. The hairpin precursor of 19 conserved mcr-miRNAs and 12 novel mcr-miRNAs were identified. After 6 h of salt stress, the expression of most mcr-miRNAs showed decreased relative abundance, whereas the expression of their corresponding target genes showed increased mRNA relative abundance. The cognate target genes are involved in a broad range of biological processes: transcription factors that regulate growth and development, enzymes that catalyze miRNA biogenesis for the most conserved mcr-miRNA, and proteins that are involved in ion homeostasis and drought-stress responses for some novel mcr-miRNAs. Analyses of the functions of target genes revealed that cellular processes, including growth and development, metabolism, and ion transport activity are likely to be enhanced in roots under salt stress. The expression of eleven conserved miRNAs and two novel miRNAs were correlated reciprocally with predicted targets within hours after salt stress exposure. Several conserved miRNAs have been known to regulate root elongation, root apical meristem activity, and lateral root formation. Based upon the expression pattern of miRNA and target genes in combination with the observation of Na+ distribution, ice plant likely responds to increased salinity by using Na+ as an osmoticum for cell expansion and guard cell opening. Excessive Na+ could either be secreted through the root epidermis or stored in specialized leaf epidermal cells. These responses are regulated in part at the miRNA-mediated post-transcriptional level.},
doi = {10.3389/fpls.2016.01143},
url = {https://www.osti.gov/biblio/1326672}, journal = {Frontiers in Plant Science},
issn = {1664-462X},
number = ,
volume = 7,
place = {United States},
year = {Tue Aug 09 00:00:00 EDT 2016},
month = {Tue Aug 09 00:00:00 EDT 2016}
}

Works referenced in this record:

Growth and development of Mesembryanthemum crystallinum (Aizoaceae)
journal, February 1998


CleaveLand: a pipeline for using degradome data to find cleaved small RNA targets
journal, November 2008


Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana
journal, November 2004


Evolution of plant microRNAs and their targets
journal, July 2008


Quantitative Proteomics of the Tonoplast Reveals a Role for Glycolytic Enzymes in Salt Tolerance
journal, December 2009


Protein profiling of epidermal bladder cells from the halophyte Mesembryanthemum crystallinum
journal, August 2012


MicroRNAs
journal, January 2004


The Ice Plant Cometh: Lessons in Abiotic Stress Tolerance
journal, September 2000


The Roles of Germin Gene Products in Plants Under Salt Stress
book, August 2011


Na+/myo-inositol symporters and Na+/H+-antiport in Mesembryanthemum crystallinum
journal, November 2000


microRNA biogenesis and function in plants
journal, August 2005


Regulation of Phosphate Homeostasis by MicroRNA in Arabidopsis
journal, December 2005


Crassulacean Acid Metabolism. A Plastic Photosynthetic Adaptation to Arid Environments
journal, December 2001


psRNATarget: a plant small RNA target analysis server
journal, May 2011


Differential expression of miRNAs in response to salt stress in maize roots
journal, October 2008


Construction of Parallel Analysis of RNA Ends (PARE) libraries for the study of cleaved miRNA targets and the RNA degradome
journal, February 2009


The Arabidopsis RNA-Directed DNA Methylation Argonautes Functionally Diverge Based on Their Expression and Interaction with Target Loci
journal, February 2010


The SHORT-ROOT Gene Controls Radial Patterning of the Arabidopsis Root through Radial Signaling
journal, May 2000


Reduced expression of a vesicle trafficking-related ATPase SKD1 decreases salt tolerance in Arabidopsis
journal, January 2010


MicroRNAs and Their Cross-Talks in Plant Development
journal, April 2013


Vacuolar acidity, protein profile, and crystal composition of epidermal bladder cells of the halophyte Mesembryanthemum crystallinum
journal, January 2007


miRBase: annotating high confidence microRNAs using deep sequencing data
journal, November 2013


From The Cover: Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions
journal, August 2004


Methylation Protects miRNAs and siRNAs from a 3′-End Uridylation Activity in Arabidopsis
journal, August 2005


PHO2-Dependent Degradation of PHO1 Modulates Phosphate Homeostasis in Arabidopsis
journal, May 2012


Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana
journal, March 2008


Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
journal, December 2001


High-Throughput Sequencing, Characterization and Detection of New and Conserved Cucumber miRNAs
journal, May 2011


Criteria for Annotation of Plant MicroRNAs
journal, December 2008


Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa
journal, March 2008


Next Generation Sequencing of miRNAs – Strategies, Resources and Methods
journal, June 2010


Characterisation of the ATP-dependent phosphofructokinase gene family from Arabidopsis thaliana
journal, April 2007


Myo -Inositol-Dependent Sodium Uptake in Ice Plant
journal, January 1999


The regulation of phosphoenolpyruvate carboxylase in CAM plants
journal, February 2000


Cell type-specific responses to salinity - the epidermal bladder cell transcriptome of Mesembryanthemum crystallinum
journal, May 2015


Facile means for quantifying microRNA expression by real-time PCR
journal, October 2005


Functions of microRNAs in plant stress responses
journal, April 2012


Identification of novel and candidate miRNAs in rice by high throughput sequencing
journal, January 2008


RNA-Seq Analysis of the Response of the Halophyte, Mesembryanthemum crystallinum (Ice Plant) to High Salinity
journal, February 2015


Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs
journal, January 2007


Arabidopsis endogenous small RNAs: highways and byways
journal, September 2006


Control of Root Cap Formation by MicroRNA-Targeted Auxin Response Factors in Arabidopsis
journal, July 2005


MicroRNA171c-Targeted SCL6-II, SCL6-III, and SCL6-IV Genes Regulate Shoot Branching in Arabidopsis
journal, September 2010


Plant MicroRNAs and Development
journal, May 2013


Computational identification of microRNAs and their targets
journal, December 2006


Mfold web server for nucleic acid folding and hybridization prediction
journal, July 2003


Identification and molecular characterization of miRNAs and their target genes associated with seed development through small RNA sequencing in chickpea
journal, February 2021


Na+/myo-inositol symporters and Na+/H+-antiport in Mesembryanthemum crystallinum: Salinity-induced sodium transporters
journal, November 2000


Protein profiling of epidermal bladder cells from the halophyte Mesembryanthemum crystallinum
journal, August 2012


The Ice Plant Cometh: Lessons in Abiotic Stress Tolerance
journal, September 2000


Regulation mechanism of microRNA in plant response to abiotic stress and breeding
journal, November 2018


Computational identification of microRNAs and their targets
journal, December 2006


Methylation Protects miRNAs and siRNAs from a 3′-End Uridylation Activity in Arabidopsis
journal, August 2005


microRNA biogenesis and function in plants
journal, August 2005


Characterisation of the ATP-dependent phosphofructokinase gene family from Arabidopsis thaliana
journal, April 2007


Plant MicroRNAs and Development
journal, May 2013


Arabidopsis endogenous small RNAs: highways and byways
journal, September 2006


Evolution of plant microRNAs and their targets
journal, July 2008


Functions of microRNAs in plant stress responses
journal, April 2012


Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana
journal, November 2004


Construction of Parallel Analysis of RNA Ends (PARE) libraries for the study of cleaved miRNA targets and the RNA degradome
journal, February 2009


Na+/myo-inositol symporters and Na+/H+-antiport in Mesembryanthemum crystallinum
journal, November 2000


Growth and development of Mesembryanthemum crystallinum (Aizoaceae)
journal, February 1998


CleaveLand: a pipeline for using degradome data to find cleaved small RNA targets
journal, November 2008


MicroRNA171c-Targeted SCL6-II, SCL6-III, and SCL6-IV Genes Regulate Shoot Branching in Arabidopsis
journal, September 2010


psRNATarget: a plant small RNA target analysis server
journal, May 2011


Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa
journal, March 2008


Crassulacean Acid Metabolism. A Plastic Photosynthetic Adaptation to Arid Environments
journal, December 2001


Control of Root Cap Formation by MicroRNA-Targeted Auxin Response Factors in Arabidopsis
journal, July 2005


Regulation of Phosphate Homeostasis by MicroRNA in Arabidopsis
journal, December 2005


Criteria for Annotation of Plant MicroRNAs
journal, December 2008


PHO2-Dependent Degradation of PHO1 Modulates Phosphate Homeostasis in Arabidopsis
journal, May 2012


Cell type-specific responses to salinity - the epidermal bladder cell transcriptome of Mesembryanthemum crystallinum
journal, May 2015


Identification of novel and candidate miRNAs in rice by high throughput sequencing
journal, January 2008


Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs
journal, January 2007


Transcriptome and de novo analysis of Rosa xanthina f. spontanea in response to cold stress
journal, October 2021


Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana
journal, March 2008


High-Throughput Sequencing, Characterization and Detection of New and Conserved Cucumber miRNAs
journal, May 2011


RNA-Seq Analysis of the Response of the Halophyte, Mesembryanthemum crystallinum (Ice Plant) to High Salinity
journal, February 2015


Facile means for quantifying microRNA expression by real-time PCR
journal, October 2005


Next Generation Sequencing of miRNAs – Strategies, Resources and Methods
journal, June 2010


New insights into miR398 functions in Arabidopsis
journal, June 2010


The Roles of Germin Gene Products in Plants Under Salt Stress
book, August 2011


Works referencing / citing this record:

Characterization of Conserved and Novel microRNAs in Lilium lancifolium Thunb. by High-Throughput Sequencing
journal, February 2018


Making Plants Break a Sweat: the Structure, Function, and Evolution of Plant Salt Glands
journal, March 2017


Halophyte Common Ice Plants: A Future Solution to Arable Land Salinization
journal, November 2019


Making Plants Break a Sweat: the Structure, Function, and Evolution of Plant Salt Glands
journal, March 2017