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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:
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. Tue . "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},
journal = {Frontiers in Plant Science},
number = ,
volume = 7,
place = {United States},
year = {Tue Aug 09 00:00:00 EDT 2016},
month = {Tue Aug 09 00:00:00 EDT 2016}
}

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Balanced activity of microRNA166/165 and its target transcripts from the class III homeodomain-leucine zipper family regulates root growth in Arabidopsis thaliana
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Methylation Protects miRNAs and siRNAs from a 3′-End Uridylation Activity in Arabidopsis
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microRNA biogenesis and function in plants
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Characterisation of the ATP-dependent phosphofructokinase gene family from Arabidopsis thaliana
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Plant MicroRNAs and Development
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Cytosine methylation changes in the ice plant Ppc1 promoter during transition from C3 to Crassulacean acid metabolism
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RING-type ubiquitin ligase McCPN1 catalyzes UBC8-dependent protein ubiquitination and interacts with Argonaute 4 in halophyte ice plant
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Arabidopsis endogenous small RNAs: highways and byways
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Evolution of plant microRNAs and their targets
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Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana
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CleaveLand: a pipeline for using degradome data to find cleaved small RNA targets
journal, November 2008


Salt tolerance, salt accumulation, and ionic homeostasis in an epidermal bladder-cell-less mutant of the common ice plant Mesembryanthemum crystallinum
journal, April 2007

  • Agarie, Sakae; Shimoda, Toshifumi; Shimizu, Yumi
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Large-scale mRNA expression profiling in the common ice plant, Mesembryanthemum crystallinum, performing C3 photosynthesis and Crassulacean acid metabolism (CAM)
journal, March 2008

  • Cushman, John C.; Tillett, Richard L.; Wood, Joshua A.
  • Journal of Experimental Botany, Vol. 59, Issue 7
  • DOI: 10.1093/jxb/ern008

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

  • Wang, Long; Mai, Yan-Xia; Zhang, Yan-Chun
  • Molecular Plant, Vol. 3, Issue 5
  • DOI: 10.1093/mp/ssq042

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

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  • DOI: 10.1093/nar/gkr319

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

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  • Genome Research, Vol. 18, Issue 4
  • DOI: 10.1101/gr.6897308

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


Nucleotide Sequence of a Root-Specific Transcript Encoding a Germin-Like Protein from the Halophyte Mesembryanthemum crystallinum
journal, September 1992

  • Michalowski, Christine B.; Bohnert, Hans J.
  • Plant Physiology, Vol. 100, Issue 1
  • DOI: 10.1104/pp.100.1.537

A Copper Chaperone for Superoxide Dismutase That Confers Three Types of Copper/Zinc Superoxide Dismutase Activity in Arabidopsis
journal, August 2005

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Tonoplast Na+/H+ Antiport Activity and Its Energization by the Vacuolar H+-ATPase in the Halophytic Plant Mesembryanthemum crystallinum L
journal, October 1995

  • Barkla, B. J.; Zingarelli, L.; Blumwald, E.
  • Plant Physiology, Vol. 109, Issue 2
  • DOI: 10.1104/pp.109.2.549

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

  • Meyers, Blake C.; Axtell, Michael J.; Bartel, Bonnie
  • The Plant Cell, Vol. 20, Issue 12
  • DOI: 10.1105/tpc.108.064311

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

  • Liu, Tzu-Yin; Huang, Teng-Kuei; Tseng, Ching-Ying
  • The Plant Cell, Vol. 24, Issue 5
  • DOI: 10.1105/tpc.112.096636

Adaptation of the tonoplast V-type H+-ATPase of Mesembryanthemum crystallinum to salt stress, C3-CAM transition and plant age
journal, October 1994


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

  • Oh, Dong-Ha; Barkla, Bronwyn J.; Vera-Estrella, Rosario
  • New Phytologist, Vol. 207, Issue 3
  • DOI: 10.1111/nph.13414

Elucidation of the Small RNA Component of the Transcriptome
journal, September 2005


Identification and characterization of maize microRNAs involved in the very early stage of seed germination
journal, March 2011


Genome-wide identification of Thellungiella salsuginea microRNAs with putative roles in the salt stress response
journal, January 2013


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


High-throughput deep sequencing reveals that microRNAs play important roles in salt tolerance of euhalophyte Salicornia europaea
journal, January 2015


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

  • Shi, Rui; Chiang, Vincent L.
  • BioTechniques, Vol. 39, Issue 4
  • DOI: 10.2144/000112010

Salt Stress Leads to Differential Expression of Two Isogenes of Phosphoenolpyruvate Carboxylase during Crassulacean Acid Metabolism Induction in the Common Ice Plant
journal, July 1989

  • Cushman, John C.; Meyer, Gabriele; Michalowski, Christine B.
  • The Plant Cell, Vol. 1, Issue 7
  • DOI: 10.2307/3868962

Single cell-type comparative metabolomics of epidermal bladder cells from the halophyte Mesembryanthemum crystallinum
journal, June 2015


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

  • Motameny, Susanne; Wolters, Stefanie; Nürnberg, Peter
  • Genes, Vol. 1, Issue 1
  • DOI: 10.3390/genes1010070

New insights into miR398 functions in Arabidopsis
journal, June 2010


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

  • Caliskan, Mahmut
  • Abiotic Stress Response in Plants - Physiological, Biochemical and Genetic Perspectives
  • DOI: 10.5772/23313

Works referencing / citing this record:

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


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Making Plants Break a Sweat: the Structure, Function, and Evolution of Plant Salt Glands
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Halophyte Common Ice Plants: A Future Solution to Arable Land Salinization
journal, November 2019

  • Loconsole, Danilo; Murillo-Amador, Bernardo; Cristiano, Giuseppe
  • Sustainability, Vol. 11, Issue 21
  • DOI: 10.3390/su11216076

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