The miRNAs and cDNA-microarrays are powerful tools to enhance abiotic stress tolerance in plants through multiple advanced sequencing and bioinformatics techniques, including miRNA-regulated network, miRNA target prediction, miRNA identification, expression profile, features (disease or stress, biomarkers) association, tools based on machine learning algorithms, NGS, and tools specific for plants. Such technologies were established to identify miRNA and their target gene network prediction, emphasizing current achievements, impediments, and future perspectives.
Stress Condition |
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Stress Condition | Plant Species | Inducible Genes | Known Responsive miRNAs | Functions | Plant Species | References | ||
---|---|---|---|---|---|---|---|---|
miRNA | ||||||||
Drought stress | Arabidopsis thaliana | Rd29A (At5g52310) | CCAAT-binding | transcription factors | miR164, miR169, miR389, miR393, miR396, miR397, miR402 |
Pathogen immune response Drought tolerance Oxidative stress tolerance Pathogen immunity response Syncytium formation response to parasitic nematodes |
[13][14][ | |
miR156, miR158, miR159, miR397, miR398, miR482.2, miR530a, miR1445 | ||||||||
Drought tolerance | ||||||||
Pathogen immune response | ||||||||
[ | ||||||||
15 | ] | [ | 18 | ] |
Phenotype of Mutants | Genes | Function | AGI Code | Coded Proteins | Microarrays | |||||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Key Functions | Response | References | ||||||||||||||||||||||
Salt/drought/cold/oxidative | osmotic-stress responses | 15 | ] | [16 | ||||||||||||||||||||
Increased tolerance to drought |
AtPARP2 | ] | DNA repair | At2g31320 | [ | Poly (ADPribose) polymerase16,17,18,19] | ||||||||||||||||||
Phosphate-deficiency response | 24K | Affymetrix | [ | 30 | ] | Up-regulated | [20][44][45][46][47][31][32] | [32,33,34] | Medicago truncatula | CCAAT Binding Factor (CBF) | Growth Regulating Factor (GRF) | |||||||||||||
miR398b,c miR2111u,v miR5274b miR1510a-3p, 5p miR1510aCu/Zn superoxide dismutases (CSD1, CSD2) | TIR-NBS-LRR domain protein | miR169, miR396 miR398, miR2118 |
Drought tolerance Syncytium formation response to parasitic nematodes Oxidative stress tolerance Photoperiod-sensitive male sterility |
[13 | Drought tolerance Heat stress tolerance |
|||||||||||||||||||
Hypersensitive to drought stress |
AHK1/ | ATHK1 | ][17] | [16,20] | ||||||||||||||||||||
Heat stress tolerance | positive regulator of drought and salt stress responses | At2g17820 | Histidine kinase | Drought responsive Oxidative-stress tolerance triggering phasiRNA production from numerous NB-LRRs |
Down-regulated | [44][46 | 22K Agilent | ][30][33][34] | [32,35,36] | [47 | Oryza sativa | SalT (LOC_Os01g24710) | TIR1 | OsLEA3 (LOC_Os05g46480) |
miR393 miR402 |
Salt/cold tolerance | [18][[19] | [6 | 14][15] | ,17,18,21] | ||||
] | 22K Agilent | [ | 31 | ] | [ | 35][36] | [33,37,38] | Cold stress | [13 | |||||||||||||||
Increased tolerance to salt stress |
AtbZIP60 | ] | encodes a predicted protein of 295 aa | At1g42990 | [ | bZIP TF | 14] | [16,17] | ||||||||||||||||
44K Agilent | [ | 35 | ] | [ | 37 | ] | [37,39] | Oryza Sativa | OsWRKY71 | (LOC_Os02g08440) | ||||||||||||||
Increased tolerance to drought stress | OsMAPK2 | (LOC_Os03g17700) |
AtMYB60 | regulates stomatal movements and plant drought tolerance | At1g08810 | MYB TF | 7K cDNA | |||||||||||||||||
Drought stress | Medicago truncatula | miR398a,b miR408 miR399k miR2089 miR2111a-f,h-s miR2111g miR4414a |
Oxidative stress tolerance |
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Glycine max | miR5554a-c | Drought responsive | [46] | |||||||||||||||||||||
Salinity stress | Glycine max | miR169d miR395a miR395b,c miR1510a-5p miR1520d,e,l,n,q |
Drought tolerance Sulfate-deficiency response triggering phasiRNA production from numerous NB-LRRs |
Up-regulated | [20][48][49] | Os05g47550, Os03g42280 Os01g73250, Os12g16350 Os03g19380 |
miR319 | , | miR389 | , | miR393 | , miR1320, miR1435 miR1884b, CHY1 CP12-2 |
Drought/salt tolerance Cold tolerance | |||||||||||
Heat stress tolerance | ||||||||||||||||||||||||
[ | 20 | ] | ] | [22 | ||||||||||||||||||||
Increased tolerance to drought stress |
AREB1/ | ABF2 | regulate the ABRE-dependent expression | At1g45249 | bZIP TF | Arabidopsis thaliana | Rd29A | (At5g52310) | CBF3 | (At4g25480) | miR165 | , | miR172 | , | miR169 | , | miR396 | , | miR397 | , | miR402 | Drought/cold tolerance Pathogen immunity response |
[ |
Stress Condition | Plant Species | miRNA | Key Functions | Response | References | ||
---|---|---|---|---|---|---|---|
Drought stress | Medicago truncatula | miR398a,b miR408 miR399k miR2089 miR2111a-f,h-s miR2111g miR4414a |
Oxidative stress tolerance Salt/drought/cold/oxidative osmotic-stress responses Phosphate-deficiency response |
Up-regulated | [ | ||
14 | |||||||
] | |||||||
[ | [ | 21 | ] | [ | 38 | ] | [40] |
Pathogen immune response Drought/Salt tolerance |
Down-regulated | [82] | |||||
Phaseolus vulgaris | pvu-miR159.2 | Plant–nematode interaction | [31] | ||||
Cold stress | Phaseolus vulgaris | pvu-miR2118 | regulate the expression of genes encoding the TIR-NBS-LRR resistance protein | Up-regulated |
Software and Tools | Function | Website | Reference | Accessed | ||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
20 | , | 77 | , | |||||||||||||||||
Software and tools used for detection of plant miRNA and data analysis | 78 | , | 79 | ,80] | ||||||||||||||||
miR398b,c miR2111u,v miR5274b miR1510a-3p, 5p miR1510a |
Heat stress tolerance Drought responsive Oxidative-stress tolerance triggering phasiRNA production from numerous NB-LRRs |
Down-regulated | [77,79,80] | |||||||||||||||||
MiPred | Random forest (RF)-based miRNA predictor, which can distinguish between real and pseudo-miRNA precursors | http://server.malab.cn/MiPred/ | [45] | [72] | 5 November 2021 | Glycine max | miR5554a-c | Drought responsive | [79] | |||||||||||
Salinity stress | ||||||||||||||||||||
miBridge | Algorithm and database | http://sitemaker.umich.edu/mibridge/home | [46] | [148] | 5 November 2021 | Glycine max | miR169d miR395a miR395b,c miR1510a-5p miR1520d,e,l,n,q |
Drought tolerance Sulfate-deficiency response triggering phasiRNA production from numerous NB-LRRs |
Up-regulated | [20 | ||||||||||
miRTar | A novel rule-based model learning method for cell line specific microRNA target prediction | http://miRTar.mbc.nctu.edu.tw | [45] | [72 | ,81,82] | gma-miR159b,c | ||||||||||||||
] | 5 November 2021 | gma-miR169b,c gma-miR1520c |
gma-miR159b,c gma-miR169b,c gma-miR1520c | Pathogen immune response | ||||||||||||||||
PolymiRTS | Drought/Salt tolerance | Linking polymorphisms in microRNAs and their target sites | http://compbio.uthsc.edu/miRSNP | [47] | [149][17 | 19][20] | Down-regulated | ,21,22,23] | ||||||||||||
[ | 49 | ] | 25 November 2021 | Salinity stress | Increased sensitivity to drought stress | Arabidopsis thaliana | Rd29A | (At5g52310) | COR15A | (At2g42540) | AtMYB41miR389 | , | miR393 | , | Oxidative stress tolerance Heat stress tolerance |
[22] | control of primary metabolism and negative regulation[24] | |||
At4g28110 | MYB TF | 24K | Affymetrix | [ | 39][40] | |||||||||||||||
Phaseolus vulgaris | [ | 41 | pvu-miR159.2 | ,42] | ||||||||||||||||
Plant–nematode interaction | [ | |||||||||||||||||||
miRGator | 31 | ] | microRNA portal for deep sequencing, expression profiling and mRNA targeting | http://mirgator.kobic.re.kr | [48] | [150] | 10 November 2021 | Populus trichocarpa | Dihydropyrimidinase | miR162, miR164, miR166, miR167, miR168, miR172, miR395, miR396 | Pathogen immune response Drought tolerance Drought/cold tolerance Sulfate-deficiency response |
[23 | Increased tolerance to drought and salt stress | ][24][25 | AHK2] | positive regulators for cytokinin signaling[ | At5g3575025,26,27] | |||
Histidine kinase | Agilent | [ | 33 | ] | [ | |||||||||||||||
Cold stress | 34 | ] | [ | 35 | ,36] | Glycine max | ||||||||||||||
Phaseolus vulgaris | pvu-miR2118 | regulate the expression of genes encoding the TIR-NBS-LRR resistance protein | Up-regulated | |||||||||||||||||
Bowtie | Aligns efficiently, and short-read aligners | http://bowtie-bio.sourceforge.net | [45] | [72] | 5 November 2021 | Increased tolerance tomiR1507a, miR395 | Sulfate-deficiency response |
drought and salt | ||||||||||||
miRBase | Provides handy and useful ID conversion tools | http://www.mirbase.org/ | [45 | [26] | [28] | |||||||||||||||
stress | AHK3 | perception of cytokinin, downstream signal transduction | At1g27320 | ] | Histidine kinase | 22K Agilent | [72] | [33 | 25 November 2021 | ][34] | [35,36] | Oryza sativa | Increased tolerance to drought and freezing stress | SalT | (LOC_Os01g24710) | OsLEA3 | (LOC_Os05g46480) | [27] | DREB1A/ | |
miRDB | CBF3 | miRNA target databases | http://www.mirdb.org | [49] | [151],29 | [28][29 | ,30,31] | |||||||||||||
stress-inducible transcription factor | ERF/AP2 TF | ERF/AP2 TF | 1.3K cDNA | [ | 41 | ] | [ | 25 November 202143] | Zea mays | |||||||||||
Increased tolerance to | ||||||||||||||||||||
mirDIP | miR402 | drought stress | DREB2A | heat shock-stress responses.Seed germination and seedling growth of Arabidopsis under stress | At5g05410 | ERF/AP2 TF | 22K Agilent 7K cDNA |
[42] | [44] | |||||||||||
Hypersensitive to salt |
HOS10 | coordinating factor for responses to abiotic stress and for growth and development. | At1g35515 | MYB TF | 24K Affymetrix |
[30][43] | [32,45] | |||||||||||||
Increased tolerance to drought stress |
ZFHD1 | mediates all the protein-protein interactions | At1g69600 | Zinc finger HD TF |
22K Agilent | [34][37] | [36,39] |
Integrative database of microRNA target predictions | ||||||||
http://ophid.utoronto.ca/mirDIP | ||||||||
[ | ||||||||
78 | ||||||||
] | ||||||||
[ | ||||||||
152 | ||||||||
] | ||||||||
25 November 2021 | ||||||||
miRanda | Predict or collect miRNA targets | http://34.236.212.39/microrna/home.do | [45] | [72] | 25 November 2021 | |||
RNAhybrid | microRNA target prediction | https://bibiserv.cebitec.uni-bielefeld.de/rnahybrid | [45] | [72] | 8 November 2021 | |||
miTALOS | Analyzes tissue specific microRNA function. | http://mips.helmholtz-muenchen.de/mitalos | [79] | [153] | 5 November 2021 | |||
RNA22 | microRNA target predictions | https://cm.jefferson.edu/rna22 | [80] | [154] | 5 November 2021 | |||
psRNATarget | Small RNA target analysis server | http://plantgrn.noble.org/psRNATarget/ | [81] | [155] | 5 November 2021 | |||
miRandola | Curated knowledge base of non-invasive biomarkers | http://mirandola.iit.cnr.it/ | [81] | [155] | 5 November 2021 | |||
ChIPBase | Decoding transcriptional regulatory networks of non-coding RNAs and protein-coding genes from ChIP-seq data | http://rna.sysu.edu.cn/chipbase/ | [81][82] | [155,156] | 1 October 2021 | |||
MirGeneDB | Curated miRNA gene database | http://mirgenedb.org/ | [83] | [157] | 28 November 2021 | |||
TarHunter | Predicting conserved microRNA targets and target mimics in plants | http://tarhunter.genetics.ac.cn | [84] | [158] | 28 November 2021 | |||
TissueAtlas | Tissue specificity miRNA database | https://ccb-web.cs.uni-saarland.de/tissueatlas/ | [45] | [72] | 28 November 2021 | |||
miRNAme Converter | miRNA ID converter | http://163.172.134.150/miRNAmeConverter-shiny | [85] | [159] | 28 November 2021 | |||
Software and tools used for detection of plant microarray and data analysis | ||||||||
Array Designer | Design primers and probes for oligo and cDNA expression microarrays. | http://www.premierbiosoft.com/dnamicroarray/index.html | [86] | [160] | 1 November 2021 | |||
Stanford Microarray Database SMD | Stores raw and normalized data from microarray experiments | http://smd-www.stanford.edu//download/ | [87] | [161] | 1 November 2021 | |||
eArray | Designing Agilent arrays | http://earray.chem.agilent.com/earray/login.do | [86] | [160] | 1 November 2021 | |||
Significance Analysis of Microarrays | Adjustments for multiple testing, statistical analysis for discrete, quantitative, and time series data, gene set enrichment analysis | http://www-stat.stanford.edu/~tibs/SAM/ | [88] | [162] | 5 November 2021 | |||
Visual OMP | Design software for RNA, DNA, single or multiple probe design, microarrays, Taq Manassays, genotyping, single and multiplex PCR, secondary structure simulation, sequencing, genotyping. | http://www.dnasoftware.com/Products/VisualOMP | [86] | [160] | 5 November 2021 | |||
caArray | Open-source, web and programmatically accessible microarray data management system that supports the annotation of microarray | http://caarray.nci.nih.gov/ | 5 November 2021 | |||||
Gene Expression Model Selector | Diagnostic models and biomarker discovery | http://www.gems-system.org/ | [89] | [163] | 18 November 2021 | |||
Gene index | Gene Index Project is to use the available EST and gene sequences, along with the reference genomes, to provide an inventory of likely genes and variants. | http://compbio.dfci.harvard.edu/tgi/plant.html | [86] | [160] | 5 November 2021 | |||
Genesis | Java package of tools to simultaneously visualize and analyze a whole set of gene expression experiments | http://genome.tugraz.at/genesisclient/genesisclient_description.shtml | 18 November 2021 | |||||
RMA Express | Standalone GUI program for Windows, OS X and Linux to compute gene expression summary values for Affymetrix | http://rmaexpress.bmbolstad.com | http://www.r-project.org | http://www.bioconductor.org | 18 November 2021 | |||
dCHIP | Model-based expression analysis for Affymetrix gene expression arrays | http://www.dchip.org | [90] | [164] | 18 November 2021 | |||
TM4 | Microarray Data Manager (MADAM), TIGR Spotfinder, Microarray Data Analysis System (MIDAS), and Multi experiment Viewer (MeV) | http://www.tm4.org/ | [90] | [164] | 18 November 2021 | |||
Able Image Analyser | Software for image analysis. It enables dimensional measurements: distance, area, angle in digital images | http://able.mulabs.com | [86] | [160] | 18 November 2021 | |||
ImaGene | Unique, robust, room-temperature preservation solutions for nucleic acids, biospecimens and bioreagents for in the living ectors | http://www.biodiscovery.com/index/imagene | [86] | [160] | 13 November 2021 | |||
Spotfinder | Custom-designed cDNA array, the chips are scanned using a microarray scanner | http://www.tm4.org/spotfinder.html | [90] | [164] | 18 November 2021 | |||
SNOMAD | Web-based tool and has various normalization options for two-channel and single-channel experiments | http://pevsnerlab.kennedykrieger.org/snomadinput.html | [90] | [164] | 18 November 2021 | |||
Multiexperimet Viewer | Cloud-based application supporting analysis, visualization, and stratification of large genomic data | http://www.tm4.org/mev.html | 18 November 2021 | |||||
Onto-Express and Pathway-Express | Automatically translates DE gene transcripts from microarray experiments into functional profiles characterizing the impact of the condition studied | http://vortex.cs.wayne.edu/projects.htm | [90] | [164] | 13 November 2021 | |||
DAVID/EASE | Database for annotation, visualization and integrated discovery (DAVID) is an online tool for annotation and functional analysis. Expression analysis systematic sxplorer (EASE) | http://david.abcc.ncifcrf.gov | [90] | [164] | 13 November 2021 |