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 »
- Authors:
-
- National Chung Hsing Univ., Taichung (Taiwan). Dept. of Life Sciences
- Univ. of Nevada, Reno, NV (United States). Dept. of Biochemistry and Molecular Biology
- National Chung Hsing Univ., Taichung (Taiwan). Dept. of Forestry
- 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
- Adams, Patricia; Nelson, Don E.; Yamada, Shigehiro
- New Phytologist, Vol. 138, Issue 2
CleaveLand: a pipeline for using degradome data to find cleaved small RNA targets
journal, November 2008
- Addo-Quaye, C.; Miller, W.; Axtell, M. J.
- Bioinformatics, Vol. 25, Issue 1
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
- Journal of Experimental Botany, Vol. 58, Issue 8
Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana
journal, November 2004
- Allen, Edwards; Xie, Zhixin; Gustafson, Adam M.
- Nature Genetics, Vol. 36, Issue 12
Evolution of plant microRNAs and their targets
journal, July 2008
- Axtell, Michael J.; Bowman, John L.
- Trends in Plant Science, Vol. 13, Issue 7
miR396a-Mediated Basic Helix–Loop–Helix Transcription Factor bHLH74 Repression Acts as a Regulator for Root Growth in Arabidopsis Seedlings
journal, May 2014
- Bao, Maolin; Bian, Hongwu; Zha, Yulong
- Plant and Cell Physiology, Vol. 55, Issue 7
Single cell-type comparative metabolomics of epidermal bladder cells from the halophyte Mesembryanthemum crystallinum
journal, June 2015
- Barkla, Bronwyn J.; Vera-Estrella, Rosario
- Frontiers in Plant Science, Vol. 6
Quantitative Proteomics of the Tonoplast Reveals a Role for Glycolytic Enzymes in Salt Tolerance
journal, December 2009
- Barkla, Bronwyn J.; Vera-Estrella, Rosario; Hernández-Coronado, Marcela
- The Plant Cell, Vol. 21, Issue 12
Protein profiling of epidermal bladder cells from the halophyte Mesembryanthemum crystallinum
journal, August 2012
- Barkla, Bronwyn J.; Vera-Estrella, Rosario; Pantoja, Omar
- PROTEOMICS, Vol. 12, Issue 18
Single-cell-type quantitative proteomic and ionomic analysis of epidermal bladder cells from the halophyte model plant Mesembryanthemum crystallinum to identify salt-responsive proteins
journal, May 2016
- Barkla, Bronwyn J.; Vera-Estrella, Rosario; Raymond, Carolyn
- BMC Plant Biology, Vol. 16, Issue 1
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
The Ice Plant Cometh: Lessons in Abiotic Stress Tolerance
journal, September 2000
- Bohnert, Hans J.; Cushman, John C.
- Journal of Plant Growth Regulation, Vol. 19, Issue 3
Evidence that microRNA precursors, unlike other non-coding RNAs, have lower folding free energies than random sequences
journal, June 2004
- Bonnet, E.; Wuyts, J.; Rouze, P.
- Bioinformatics, Vol. 20, Issue 17
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
Na+/myo-inositol symporters and Na+/H+-antiport in Mesembryanthemum crystallinum
journal, November 2000
- Chauhan, Sanjay; Forsthoefel, Nancy; Ran, Yingquing
- The Plant Journal, Vol. 24, Issue 4
microRNA biogenesis and function in plants
journal, August 2005
- Chen, Xuemei
- FEBS Letters, Vol. 579, Issue 26
Suppressor of K+ transport growth defect 1 (SKD1) interacts with RING-type ubiquitin ligase and sucrose non-fermenting 1-related protein kinase (SnRK1) in the halophyte ice plant
journal, April 2013
- Chiang, Chih-Pin; Li, Chang-Hua; Jou, Yingtzy
- Journal of Experimental Botany, Vol. 64, Issue 8
Regulation of Phosphate Homeostasis by MicroRNA in Arabidopsis
journal, December 2005
- Chiou, Tzyy-Jen; Aung, Kyaw; Lin, Shu-I
- The Plant Cell, Vol. 18, Issue 2
A Copper Chaperone for Superoxide Dismutase That Confers Three Types of Copper/Zinc Superoxide Dismutase Activity in Arabidopsis
journal, August 2005
- Chu, Chiung-Chih; Lee, Wen-Chi; Guo, Wen-Yu
- Plant Physiology, Vol. 139, Issue 1
Crassulacean Acid Metabolism. A Plastic Photosynthetic Adaptation to Arid Environments
journal, December 2001
- Cushman, John C.
- Plant Physiology, Vol. 127, Issue 4
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, J. C.; Meyer, G.; Michalowski, C. B.
- The Plant Cell, Vol. 1, Issue 7
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
psRNATarget: a plant small RNA target analysis server
journal, May 2011
- Dai, Xinbin; Zhao, Patrick Xuechun
- Nucleic Acids Research, Vol. 39, Issue suppl_2
Differential expression of miRNAs in response to salt stress in maize roots
journal, October 2008
- Ding, Dong; Zhang, Lifang; Wang, Hang
- Annals of Botany, Vol. 103, Issue 1
High-throughput deep sequencing reveals that microRNAs play important roles in salt tolerance of euhalophyte Salicornia europaea
journal, January 2015
- Feng, Juanjuan; Wang, Jinhui; Fan, Pengxiang
- BMC Plant Biology, Vol. 15, Issue 1
Construction of Parallel Analysis of RNA Ends (PARE) libraries for the study of cleaved miRNA targets and the RNA degradome
journal, February 2009
- German, Marcelo A.; Luo, Shujun; Schroth, Gary
- Nature Protocols, Vol. 4, Issue 3
Plant tolerance to drought and salinity: stress regulating transcription factors and their functional significance in the cellular transcriptional network
journal, April 2011
- Golldack, Dortje; Lüking, Ines; Yang, Oksoon
- Plant Cell Reports, Vol. 30, Issue 8
MicroRNA Directs mRNA Cleavage of the Transcription Factor NAC1 to Downregulate Auxin Signals for Arabidopsis Lateral Root Development
journal, April 2005
- Guo, Hui-Shan; Xie, Qi; Fei, Ji-Feng
- The Plant Cell, Vol. 17, Issue 5
The Arabidopsis RNA-Directed DNA Methylation Argonautes Functionally Diverge Based on Their Expression and Interaction with Target Loci
journal, February 2010
- Havecker, Ericka R.; Wallbridge, Laura M.; Hardcastle, Thomas J.
- The Plant Cell, Vol. 22, Issue 2
The SHORT-ROOT Gene Controls Radial Patterning of the Arabidopsis Root through Radial Signaling
journal, May 2000
- Helariutta, Yrjo; Fukaki, Hidehiro; Wysocka-Diller, Joanna
- Cell, Vol. 101, Issue 5
Reduced expression of a vesicle trafficking-related ATPase SKD1 decreases salt tolerance in Arabidopsis
journal, January 2010
- Ho, Li-Wei; Yang, Ting-Ting; Shieh, Shyan-Shu
- Functional Plant Biology, Vol. 37, Issue 10
Cytosine methylation changes in the ice plant Ppc1 promoter during transition from C3 to Crassulacean acid metabolism
journal, January 2010
- Huang, Nu-Chuan; Li, Chang-Hua; Lee, Jun-Yi
- Plant Science, Vol. 178, Issue 1
MicroRNAs and Their Cross-Talks in Plant Development
journal, April 2013
- Jin, Danfeng; Wang, Yue; Zhao, Yuhua
- Journal of Genetics and Genomics, Vol. 40, Issue 4
Vacuolar acidity, protein profile, and crystal composition of epidermal bladder cells of the halophyte Mesembryanthemum crystallinum
journal, January 2007
- Jou, Yingtzy; Wang, Ya-Ling; Yen, Hungchen Emilie
- Functional Plant Biology, Vol. 34, Issue 4
Identification and Analysis of Red Sea Mangrove (Avicennia marina) microRNAs by High-Throughput Sequencing and Their Association with Stress Responses
journal, April 2013
- Khraiwesh, Basel; Pugalenthi, Ganesan; Fedoroff, Nina V.
- PLoS ONE, Vol. 8, Issue 4
Transcript profiling of salinity stress responses by large-scale expressed sequence tag analysis in Mesembryanthemum crystallinum
journal, October 2004
- Kore-eda, Shin; Cushman, Mary Ann; Akselrod, Inna
- Gene, Vol. 341
miRBase: annotating high confidence microRNAs using deep sequencing data
journal, November 2013
- Kozomara, Ana; Griffiths-Jones, Sam
- Nucleic Acids Research, Vol. 42, Issue D1
From The Cover: Arabidopsis micro-RNA biogenesis through Dicer-like 1 protein functions
journal, August 2004
- Kurihara, Y.; Watanabe, Y.
- Proceedings of the National Academy of Sciences, Vol. 101, Issue 34
RING-type ubiquitin ligase McCPN1 catalyzes UBC8-dependent protein ubiquitination and interacts with Argonaute 4 in halophyte ice plant
journal, July 2014
- Li, Chang-Hua; Chiang, Chih-Pin; Yang, Jun-Yi
- Plant Physiology and Biochemistry, Vol. 80
Methylation Protects miRNAs and siRNAs from a 3′-End Uridylation Activity in Arabidopsis
journal, August 2005
- Li, Junjie; Yang, Zhiyong; Yu, Bin
- Current Biology, Vol. 15, Issue 16
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
Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana
journal, March 2008
- Liu, H. -H.; Tian, X.; Li, Y. -J.
- RNA, Vol. 14, Issue 5
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
journal, December 2001
- Livak, Kenneth J.; Schmittgen, Thomas D.
- Methods, Vol. 25, Issue 4
Elucidation of the Small RNA Component of the Transcriptome
journal, September 2005
- Lu, C.
- Science, Vol. 309, Issue 5740
High-Throughput Sequencing, Characterization and Detection of New and Conserved Cucumber miRNAs
journal, May 2011
- Martínez, Germán; Forment, Javier; Llave, Cesar
- PLoS ONE, Vol. 6, Issue 5
Criteria for Annotation of Plant MicroRNAs
journal, December 2008
- Meyers, Blake C.; Axtell, Michael J.; Bartel, Bonnie
- The Plant Cell, Vol. 20, Issue 12
Sorting of Small RNAs into Arabidopsis Argonaute Complexes Is Directed by the 5′ Terminal Nucleotide
journal, April 2008
- Mi, Shijun; Cai, Tao; Hu, Yugang
- Cell, Vol. 133, Issue 1
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
Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa
journal, March 2008
- Morin, R. D.; Aksay, G.; Dolgosheina, E.
- Genome Research, Vol. 18, Issue 4
Next Generation Sequencing of miRNAs – Strategies, Resources and Methods
journal, June 2010
- Motameny, Susanne; Wolters, Stefanie; Nürnberg, Peter
- Genes, Vol. 1, Issue 1
Characterisation of the ATP-dependent phosphofructokinase gene family from Arabidopsis thaliana
journal, April 2007
- Mustroph, Angelika; Sonnewald, Uwe; Biemelt, Sophia
- FEBS Letters, Vol. 581, Issue 13
Myo -Inositol-Dependent Sodium Uptake in Ice Plant
journal, January 1999
- Nelson, Donald E.; Koukoumanos, Michelle; Bohnert, Hans J.
- Plant Physiology, Vol. 119, Issue 1
The regulation of phosphoenolpyruvate carboxylase in CAM plants
journal, February 2000
- Nimmo, Hugh G.
- Trends in Plant Science, Vol. 5, Issue 2
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
Adaptation of the tonoplast V-type H+-ATPase of Mesembryanthemum crystallinum to salt stress, C3-CAM transition and plant age
journal, October 1994
- Ratajczak, R.; Richter, J.; Luttge, U.
- Plant, Cell and Environment, Vol. 17, Issue 10
Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray: Expression profiling under abiotic stresses
journal, August 2002
- Seki, Motoaki; Narusaka, Mari; Ishida, Junko
- The Plant Journal, Vol. 31, Issue 3
Facile means for quantifying microRNA expression by real-time PCR
journal, October 2005
- Shi, Rui; Chiang, Vincent L.
- BioTechniques, Vol. 39, Issue 4
The isolation and identification of salt-responsive novel microRNAs from Salicornia brachiata, an extreme halophyte
journal, May 2014
- Singh, Dinkar; Jha, Bhavanath
- Plant Biotechnology Reports, Vol. 8, Issue 4
Balanced activity of microRNA166/165 and its target transcripts from the class III homeodomain-leucine zipper family regulates root growth in Arabidopsis thaliana
journal, February 2014
- Singh, Archita; Singh, Sharmila; Panigrahi, Kishore C. S.
- Plant Cell Reports, Vol. 33, Issue 6
The UEA sRNA workbench: a suite of tools for analysing and visualizing next generation sequencing microRNA and small RNA datasets
journal, May 2012
- Stocks, M. B.; Moxon, S.; Mapleson, D.
- Bioinformatics, Vol. 28, Issue 15
Posttranscriptional Induction of Two Cu/Zn Superoxide Dismutase Genes in Arabidopsis Is Mediated by Downregulation of miR398 and Important for Oxidative Stress Tolerance
journal, July 2006
- Sunkar, Ramanjulu; Kapoor, Avnish; Zhu, Jian-Kang
- The Plant Cell, Vol. 18, Issue 8
Functions of microRNAs in plant stress responses
journal, April 2012
- Sunkar, Ramanjulu; Li, Yong-Fang; Jagadeeswaran, Guru
- Trends in Plant Science, Vol. 17, Issue 4
Identification of novel and candidate miRNAs in rice by high throughput sequencing
journal, January 2008
- Sunkar, Ramanjulu; Zhou, Xuefeng; Zheng, Yun
- BMC Plant Biology, Vol. 8, Issue 1
RNA-Seq Analysis of the Response of the Halophyte, Mesembryanthemum crystallinum (Ice Plant) to High Salinity
journal, February 2015
- Tsukagoshi, Hironaka; Suzuki, Takamasa; Nishikawa, Kouki
- PLOS ONE, Vol. 10, Issue 2
Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs
journal, January 2007
- Varkonyi-Gasic, Erika; Wu, Rongmei; Wood, Marion
- Plant Methods, Vol. 3, Issue 1
Arabidopsis endogenous small RNAs: highways and byways
journal, September 2006
- Vazquez, Franck
- Trends in Plant Science, Vol. 11, Issue 9
Control of Root Cap Formation by MicroRNA-Targeted Auxin Response Factors in Arabidopsis
journal, July 2005
- Wang, Jia-Wei; Wang, Ling-Jian; Mao, Ying-Bo
- The Plant Cell, Vol. 17, Issue 8
Identification and characterization of maize microRNAs involved in the very early stage of seed germination
journal, March 2011
- Wang, Liwen; Liu, Huaihua; Li, Detao
- BMC Genomics, Vol. 12, Issue 1
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
Intracellular Localization of Enzymes of Carbon Metabolism in Mesembryanthemum crystallinum Exhibiting C 3 Photosynthetic Characteristics or Performing Crassulacean Acid Metabolism
journal, February 1982
- Winter, Klaus; Foster, Joyce G.; Edwards, Gerald E.
- Plant Physiology, Vol. 69, Issue 2
Environment or Development? Lifetime Net CO 2 Exchange and Control of the Expression of Crassulacean Acid Metabolism in Mesembryanthemum crystallinum
journal, October 2006
- Winter, Klaus; Holtum, Joseph A. M.
- Plant Physiology, Vol. 143, Issue 1
Plant MicroRNAs and Development
journal, May 2013
- Wu, Gang
- Journal of Genetics and Genomics, Vol. 40, Issue 5
Methylation as a Crucial Step in Plant microRNA Biogenesis
journal, February 2005
- Yu, B.
- Science, Vol. 307, Issue 5711
Computational identification of microRNAs and their targets
journal, December 2006
- Zhang, Baohong; Pan, Xiaoping; Wang, Qinglian
- Computational Biology and Chemistry, Vol. 30, Issue 6
Genome-wide identification of Thellungiella salsuginea microRNAs with putative roles in the salt stress response
journal, January 2013
- Zhang, Quan; Zhao, Chuanzhi; Li, Ming
- BMC Plant Biology, Vol. 13, Issue 1
Mfold web server for nucleic acid folding and hybridization prediction
journal, July 2003
- Zuker, M.
- Nucleic Acids Research, Vol. 31, Issue 13
Morphological and genetic characterization of the first Isospora species (I. lugensae n. sp.) from a Kerguelen petrel (Lugensa brevirostris)
journal, January 2021
- Yang, Rongchang; Brice, Belinda; Liu, Qier
- Parasitology Research, Vol. 120, Issue 3
Identification and molecular characterization of miRNAs and their target genes associated with seed development through small RNA sequencing in chickpea
journal, February 2021
- Pradhan, Seema; Verma, Subodh; Chakraborty, Anirban
- Functional & Integrative Genomics, Vol. 21, Issue 2
Na+/myo-inositol symporters and Na+/H+-antiport in Mesembryanthemum crystallinum: Salinity-induced sodium transporters
journal, November 2000
- Chauhan, Sanjay; Forsthoefel, Nancy; Ran, Yingquing
- The Plant Journal, Vol. 24, Issue 4
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
Protein profiling of epidermal bladder cells from the halophyte Mesembryanthemum crystallinum
journal, August 2012
- Barkla, Bronwyn J.; Vera-Estrella, Rosario; Pantoja, Omar
- PROTEOMICS, Vol. 12, Issue 18
Plant tolerance to drought and salinity: stress regulating transcription factors and their functional significance in the cellular transcriptional network
journal, April 2011
- Golldack, Dortje; Lüking, Ines; Yang, Oksoon
- Plant Cell Reports, Vol. 30, Issue 8
Balanced activity of microRNA166/165 and its target transcripts from the class III homeodomain-leucine zipper family regulates root growth in Arabidopsis thaliana
journal, February 2014
- Singh, Archita; Singh, Sharmila; Panigrahi, Kishore C. S.
- Plant Cell Reports, Vol. 33, Issue 6
The Ice Plant Cometh: Lessons in Abiotic Stress Tolerance
journal, September 2000
- Bohnert, Hans J.; Cushman, John C.
- Journal of Plant Growth Regulation, Vol. 19, Issue 3
Regulation mechanism of microRNA in plant response to abiotic stress and breeding
journal, November 2018
- Sun, Xi; Lin, Lin; Sui, Na
- Molecular Biology Reports, Vol. 46, Issue 1
The isolation and identification of salt-responsive novel microRNAs from Salicornia brachiata, an extreme halophyte
journal, May 2014
- Singh, Dinkar; Jha, Bhavanath
- Plant Biotechnology Reports, Vol. 8, Issue 4
Identification of putative microRNAs in the complete genome of Mycobacterium avium and their possible interaction with human transcripts
journal, October 2021
- Nath, Durbba; Chakraborty, Supriyo
- Journal of Applied Genetics, Vol. 63, Issue 1
Sorting of Small RNAs into Arabidopsis Argonaute Complexes Is Directed by the 5′ Terminal Nucleotide
journal, April 2008
- Mi, Shijun; Cai, Tao; Hu, Yugang
- Cell, Vol. 133, Issue 1
Computational identification of microRNAs and their targets
journal, December 2006
- Zhang, Baohong; Pan, Xiaoping; Wang, Qinglian
- Computational Biology and Chemistry, Vol. 30, Issue 6
Methylation Protects miRNAs and siRNAs from a 3′-End Uridylation Activity in Arabidopsis
journal, August 2005
- Li, Junjie; Yang, Zhiyong; Yu, Bin
- Current Biology, Vol. 15, Issue 16
microRNA biogenesis and function in plants
journal, August 2005
- Chen, Xuemei
- FEBS Letters, Vol. 579, Issue 26
Characterisation of the ATP-dependent phosphofructokinase gene family from Arabidopsis thaliana
journal, April 2007
- Mustroph, Angelika; Sonnewald, Uwe; Biemelt, Sophia
- FEBS Letters, Vol. 581, Issue 13
Transcript profiling of salinity stress responses by large-scale expressed sequence tag analysis in Mesembryanthemum crystallinum
journal, October 2004
- Kore-eda, Shin; Cushman, Mary Ann; Akselrod, Inna
- Gene, Vol. 341
Plant MicroRNAs and Development
journal, May 2013
- Wu, Gang
- Journal of Genetics and Genomics, Vol. 40, Issue 5
Cytosine methylation changes in the ice plant Ppc1 promoter during transition from C3 to Crassulacean acid metabolism
journal, January 2010
- Huang, Nu-Chuan; Li, Chang-Hua; Lee, Jun-Yi
- Plant Science, Vol. 178, Issue 1
RING-type ubiquitin ligase McCPN1 catalyzes UBC8-dependent protein ubiquitination and interacts with Argonaute 4 in halophyte ice plant
journal, July 2014
- Li, Chang-Hua; Chiang, Chih-Pin; Yang, Jun-Yi
- Plant Physiology and Biochemistry, Vol. 80
Arabidopsis endogenous small RNAs: highways and byways
journal, September 2006
- Vazquez, Franck
- Trends in Plant Science, Vol. 11, Issue 9
Evolution of plant microRNAs and their targets
journal, July 2008
- Axtell, Michael J.; Bowman, John L.
- Trends in Plant Science, Vol. 13, Issue 7
Functions of microRNAs in plant stress responses
journal, April 2012
- Sunkar, Ramanjulu; Li, Yong-Fang; Jagadeeswaran, Guru
- Trends in Plant Science, Vol. 17, Issue 4
Evolution of microRNA genes by inverted duplication of target gene sequences in Arabidopsis thaliana
journal, November 2004
- Allen, Edwards; Xie, Zhixin; Gustafson, Adam M.
- Nature Genetics, Vol. 36, Issue 12
Construction of Parallel Analysis of RNA Ends (PARE) libraries for the study of cleaved miRNA targets and the RNA degradome
journal, February 2009
- German, Marcelo A.; Luo, Shujun; Schroth, Gary
- Nature Protocols, Vol. 4, Issue 3
Proteomic analysis of Mesembryanthemum crystallinum leaf microsomal fractions finds an imbalance in V-ATPase stoichiometry during the salt-induced transition from C3 to CAM
journal, February 2013
- Cosentino, Cristian; Di Silvestre, Dario; Fischer-Schliebs, Elke
- Biochemical Journal, Vol. 450, Issue 2
Na+/myo-inositol symporters and Na+/H+-antiport in Mesembryanthemum crystallinum
journal, November 2000
- Chauhan, Sanjay; Forsthoefel, Nancy; Ran, Yingquing
- The Plant Journal, Vol. 24, Issue 4
Growth and development of Mesembryanthemum crystallinum (Aizoaceae)
journal, February 1998
- Adams, Patricia; Nelson, Don E.; Yamada, Shigehiro
- New Phytologist, Vol. 138, Issue 2
CleaveLand: a pipeline for using degradome data to find cleaved small RNA targets
journal, November 2008
- Addo-Quaye, C.; Miller, W.; Axtell, M. J.
- Bioinformatics, Vol. 25, Issue 1
The UEA sRNA workbench: a suite of tools for analysing and visualizing next generation sequencing microRNA and small RNA datasets
journal, May 2012
- Stocks, M. B.; Moxon, S.; Mapleson, D.
- Bioinformatics, Vol. 28, Issue 15
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
- Journal of Experimental Botany, Vol. 58, Issue 8
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
Suppressor of K+ transport growth defect 1 (SKD1) interacts with RING-type ubiquitin ligase and sucrose non-fermenting 1-related protein kinase (SnRK1) in the halophyte ice plant
journal, April 2013
- Chiang, Chih-Pin; Li, Chang-Hua; Jou, Yingtzy
- Journal of Experimental Botany, Vol. 64, Issue 8
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
psRNATarget: a plant small RNA target analysis server
journal, May 2011
- Dai, Xinbin; Zhao, Patrick Xuechun
- Nucleic Acids Research, Vol. 39, Issue suppl_2
Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa
journal, March 2008
- Morin, R. D.; Aksay, G.; Dolgosheina, E.
- Genome Research, Vol. 18, Issue 4
Crassulacean Acid Metabolism. A Plastic Photosynthetic Adaptation to Arid Environments
journal, December 2001
- Cushman, John C.
- Plant Physiology, Vol. 127, Issue 4
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
A Copper Chaperone for Superoxide Dismutase That Confers Three Types of Copper/Zinc Superoxide Dismutase Activity in Arabidopsis
journal, August 2005
- Chu, Chiung-Chih; Lee, Wen-Chi; Guo, Wen-Yu
- Plant Physiology, Vol. 139, Issue 1
Environment or Development? Lifetime Net CO 2 Exchange and Control of the Expression of Crassulacean Acid Metabolism in Mesembryanthemum crystallinum
journal, October 2006
- Winter, Klaus; Holtum, Joseph A. M.
- Plant Physiology, Vol. 143, Issue 1
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
Intracellular Localization of Enzymes of Carbon Metabolism in Mesembryanthemum crystallinum Exhibiting C 3 Photosynthetic Characteristics or Performing Crassulacean Acid Metabolism
journal, February 1982
- Winter, Klaus; Foster, Joyce G.; Edwards, Gerald E.
- Plant Physiology, Vol. 69, Issue 2
Control of Root Cap Formation by MicroRNA-Targeted Auxin Response Factors in Arabidopsis
journal, July 2005
- Wang, Jia-Wei; Wang, Ling-Jian; Mao, Ying-Bo
- The Plant Cell, Vol. 17, Issue 8
Regulation of Phosphate Homeostasis by MicroRNA in Arabidopsis
journal, December 2005
- Chiou, Tzyy-Jen; Aung, Kyaw; Lin, Shu-I
- The Plant Cell, Vol. 18, Issue 2
Posttranscriptional Induction of Two Cu/Zn Superoxide Dismutase Genes in Arabidopsis Is Mediated by Downregulation of miR398 and Important for Oxidative Stress Tolerance
journal, July 2006
- Sunkar, Ramanjulu; Kapoor, Avnish; Zhu, Jian-Kang
- The Plant Cell, Vol. 18, Issue 8
Criteria for Annotation of Plant MicroRNAs
journal, December 2008
- Meyers, Blake C.; Axtell, Michael J.; Bartel, Bonnie
- The Plant Cell, Vol. 20, Issue 12
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
Adaptation of the tonoplast V-type H+-ATPase of Mesembryanthemum crystallinum to salt stress, C3-CAM transition and plant age
journal, October 1994
- Ratajczak, R.; Richter, J.; Luttge, U.
- Plant, Cell and Environment, Vol. 17, Issue 10
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
Elucidation of the Small RNA Component of the Transcriptome
journal, September 2005
- Lu, C.
- Science, Vol. 309, Issue 5740
Identification and characterization of maize microRNAs involved in the very early stage of seed germination
journal, March 2011
- Wang, Liwen; Liu, Huaihua; Li, Detao
- BMC Genomics, Vol. 12, Issue 1
Genome-wide identification of Thellungiella salsuginea microRNAs with putative roles in the salt stress response
journal, January 2013
- Zhang, Quan; Zhao, Chuanzhi; Li, Ming
- BMC Plant Biology, Vol. 13, Issue 1
Identification of novel and candidate miRNAs in rice by high throughput sequencing
journal, January 2008
- Sunkar, Ramanjulu; Zhou, Xuefeng; Zheng, Yun
- BMC Plant Biology, Vol. 8, Issue 1
Protocol: a highly sensitive RT-PCR method for detection and quantification of microRNAs
journal, January 2007
- Varkonyi-Gasic, Erika; Wu, Rongmei; Wood, Marion
- Plant Methods, Vol. 3, Issue 1
High-throughput deep sequencing reveals that microRNAs play important roles in salt tolerance of euhalophyte Salicornia europaea
journal, January 2015
- Feng, Juanjuan; Wang, Jinhui; Fan, Pengxiang
- BMC Plant Biology, Vol. 15, Issue 1
Single-cell-type quantitative proteomic and ionomic analysis of epidermal bladder cells from the halophyte model plant Mesembryanthemum crystallinum to identify salt-responsive proteins
journal, May 2016
- Barkla, Bronwyn J.; Vera-Estrella, Rosario; Raymond, Carolyn
- BMC Plant Biology, Vol. 16, Issue 1
Transcriptome and de novo analysis of Rosa xanthina f. spontanea in response to cold stress
journal, October 2021
- Zhuang, Defeng; Ma, Ce; Xue, Li
- BMC Plant Biology, Vol. 21, Issue 1
Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana
journal, March 2008
- Liu, H. -H.; Tian, X.; Li, Y. -J.
- RNA, Vol. 14, Issue 5
High-Throughput Sequencing, Characterization and Detection of New and Conserved Cucumber miRNAs
journal, May 2011
- Martínez, Germán; Forment, Javier; Llave, Cesar
- PLoS ONE, Vol. 6, Issue 5
Identification and Analysis of Red Sea Mangrove (Avicennia marina) microRNAs by High-Throughput Sequencing and Their Association with Stress Responses
journal, April 2013
- Khraiwesh, Basel; Pugalenthi, Ganesan; Fedoroff, Nina V.
- PLoS ONE, Vol. 8, Issue 4
RNA-Seq Analysis of the Response of the Halophyte, Mesembryanthemum crystallinum (Ice Plant) to High Salinity
journal, February 2015
- Tsukagoshi, Hironaka; Suzuki, Takamasa; Nishikawa, Kouki
- PLOS ONE, Vol. 10, Issue 2
Facile means for quantifying microRNA expression by real-time PCR
journal, October 2005
- Shi, Rui; Chiang, Vincent L.
- BioTechniques, Vol. 39, Issue 4
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
Single cell-type comparative metabolomics of epidermal bladder cells from the halophyte Mesembryanthemum crystallinum
journal, June 2015
- Barkla, Bronwyn J.; Vera-Estrella, Rosario
- Frontiers in Plant Science, Vol. 6
Next Generation Sequencing of miRNAs – Strategies, Resources and Methods
journal, June 2010
- Motameny, Susanne; Wolters, Stefanie; Nürnberg, Peter
- Genes, Vol. 1, Issue 1
New insights into miR398 functions in Arabidopsis
journal, June 2010
- Bouché, Nicolas
- Plant Signaling & Behavior, Vol. 5, Issue 6
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
Works referencing / citing this record:
Characterization of Conserved and Novel microRNAs in Lilium lancifolium Thunb. by High-Throughput Sequencing
journal, February 2018
- He, Xiangfeng; Shenkute, Awraris Getachew; Wang, Wenhe
- Scientific Reports, Vol. 8, Issue 1
A combined small RNA and transcriptome sequencing analysis reveal regulatory roles of miRNAs during anther development of Upland cotton carrying cytoplasmic male sterile Gossypium harknessii (D2) cytoplasm
journal, October 2018
- Zhang, Bingbing; Zhang, Xuexian; Liu, Guoyuan
- BMC Plant Biology, Vol. 18, Issue 1
Effective Agrobacterium-mediated transformation protocols for callus and roots of halophyte ice plant (Mesembryanthemum crystallinum)
journal, January 2019
- Hwang, Hau-Hsuan; Wang, Chih-Hao; Chen, Hsiao-Huei
- Botanical Studies, Vol. 60, Issue 1
Making Plants Break a Sweat: the Structure, Function, and Evolution of Plant Salt Glands
journal, March 2017
- Dassanayake, Maheshi; Larkin, John C.
- Frontiers in Plant Science, Vol. 08
Functional analysis of McSnRK1 (SNF1-related protein kinase 1) in regulating Na/K homeostasis in transgenic cultured cells and roots of halophyte Mesembryanthemum crystallinum
journal, April 2019
- Hwang, Hau-Hsuan; Wang, Chih-Hao; Huang, Hsiao-Wei
- Plant Cell Reports, Vol. 38, Issue 8
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
Making Plants Break a Sweat: the Structure, Function, and Evolution of Plant Salt Glands
journal, March 2017
- Dassanayake, Maheshi; Larkin, John C.
- Frontiers in Plant Science, Vol. 08