Review Article

miRNAomic Approach to Plant Nitrogen Starvation

Table 1

Differentially expressed miRNAs under nitrogen starvation condition.

miRNATarget/functionMode of regulationReferences

miR156Squamosa promoter binding protein-like (SPL) transcription factorsUp[119128]
miR159MYB, TCP transcription factors/peptidase C48, SUMO/sentrin/Ubl1Up[119, 124126, 129134]
miR160Serine carboxypeptidase; transcription factor; auxin-responsive factors (ARF10)Up[119, 120, 123, 125, 135137]
miR162Dicer-like proteinsUp[138, 139]
miR164NAC transcription factorsUp[119, 135, 136, 140]
miR166HD-ZIP transcription factorsDown[135, 138, 141, 142]
miR166a-3pKinesin-1-like protein PSS1; transport[129]
miR167Auxin-responsive factors (ARF8)/cation/H+ exchangerUp/down[125, 126, 130, 136140, 143]
miR167c-5pSCF ubiquitin ligase complex[129]
miR167f-3p_L-1R+1Ubiquitin ligase complex; lysosomal alpha-mannosidase[129]
miR168ARGONAUTE1 (AGO1)Up/down[119, 125, 136, 138, 140]
miR168a-5pWRKY; Cul4-RINGE3 ubiquitin ligase[129]
miR168a-3p-L-3Ubiquitin domain containing protein DSK2b[129]
miR169HAP2 transcription factors CAAT-binding factor/NFYA/MDIS1-interacting receptor-like kinase 1/protein high chlorophyll fluorescent 107Up/down[117, 119, 124126, 130, 136, 137, 139, 141, 142, 144, 145]
miR169oNF-YA1, NF-YA4, NF-YA10, NF-YA11, and TRA[146]
miR169d-5pProtein serine/threonine kinase; ABC transporter; C family member 13[129]
miR169d-3p-L-2R+2Galactinol-sucrose galactosyltransferase 2; E3 ubiquitin-protein ligase[129]
miR169f-5pNF-YA2[119]
miR169(n, o)-5pNF-YA4/NF-YA10[119]
miR169r-5pNF-YA1/NF-YA3[119]
miR170NSP2 transcription factor protein[147]
miR171Scarecrow-like transcription factors (SCL)/GAGA binding-likeUp/down[121, 123, 125, 126, 130, 138]
miR171aDELLA proteins RGL2; malate dehydrogenase[129]
miR171a-3pGRAS transcription factor/similar to scarecrow-like 6[119]
miR171i-3pGRAS transcription factor[119]
miR171e-5p_2ss2GA21AGProtein binding[129]
miR172AP2 like transcription factorsUp[136138]
miR172b-5p[129]
miR172(a, d)-3pAP2/EREBP family transcription factor[119]
miR262F-box/kelch-repeat proteinDown[120]
miR319TCP transcription factors/MYB transcription factor; Dnaj proteinUp/down[125, 126, 129, 133, 136, 143]
miR319a-3p.2-3p_R+1SCF ubiquitin ligase complex; MYB[129]
miR319(a-3p.2,b)-3pOsPCF6/TCP21[119]
miR393(a, b)-5pAuxin signaling F-box 2/OsTIR1[119]
miR393-5p_L-1R+1Auxin-activated signalling; protein transport inhibitor response 1; LRR kinase[129]
miR393Auxin receptors (TIR1/F-box AFB)/cyclin-like F-boxUp[125, 126, 130, 133, 137, 138, 147]
miR394F-box proteinUp/down[139]
miR394-5pSCF ubiquitin ligase complex; glutathione transferase activity[129]
miR395ATP sulfurylase; sulfate transporters (APS/AST)Up/down[120, 123, 125, 133, 136, 146]
miR396Growth regulating factor (GRF)Up/down[121, 125, 138, 143, 148]
miR396a-5pPhosphatidylinositol 4-phosphate 5-kinase 1; glutamate dehydrogenase; response to GA[129]
miR396(a, b)-5pOsGRF7[119]
miR396c-5pGTPase activity; HSP protein; RPM1[129]
miR396e-5pTranscription factor TFIID; ribonuclease P activity[129]
miR396efs growth-regulating factors (OsGRFs)[149]
miR397Laccases, beta-6-tubulin/L-ascorbate oxidase/LAC17Up/down[120, 125, 127, 133, 136, 139, 147, 148]
miR398COX5b-1; CCS1 COX (CSD)/IAA-amino acid hydrolase ILR1/GATA31Up[121, 123, 126, 136, 139, 147, 148, 150153]
miR399Ubiquitin conjugase E2/UBC24Up/down[123, 125, 129, 131, 136, 138, 143, 154, 155]
miR399aOxidoreductase; transcription factor[129]
miR408Plantacyanin laccases/superoxide dismutase [Cu–Zn]1A/SOD1AUp/down[120, 123, 125, 128, 131, 133, 136, 139, 147]
miR408_L-1L-ascorbate oxidase; LPEAT1-like[129]
miR408-p5_1ss20GABrassinosteroid insensitive 1[129]
miR414bZIP transcription factorDown[120]
miR419Organic anion transporter[147]
miR1425-5pPPR domain-containing protein[119]
miR444MADS-boxUp[119]
miR528POD, SODUp[136, 139, 140]
miR528-5pLectin-rich repeat receptor kinase[129]
miR530-5p-R+1Fructose-bisphosphate adolase; HSP70[129]
miR530-5p_R+1_1ss20AG[129]
miR530-5p-L+1Fructose-bisphosphate aldolase; SCF ubiquitin ligase complex[129]
miR531_L-4R+1-1ss5CTNAD(P)H dehydrogenase; ABC transporter[129]
miR780Na+/H+ antiporterUp[123]
miR815c-p5_2ss6CT21CTUDP-arabinose 4-epimerase 1-like; transcription factor TGA2-like; Dnaj[129]
miR826Alkenyl hydroxyalkyl producing 2Up[123]
miR827Ubiquitin E3 ligase with RING and spx-domain-contain; phenylalanyl-tRNA synthetase; WPP domain-interacting protein 2; BTB/POZ domain-containing proteinDown[123, 129, 136, 139, 147]
miR829AP2 domain ethylene responseUp[123, 133, 156]
miR839Up[123]
miR840Basic helix-loop-helix (bHLH) DNA-binding protein[147]
miR846Jacalin lectin family proteinUp[123, 156]
miR850Down[123]
miR854UDP-glucuronic acid decarboxylase 2/ethylene-responsive transcription factor/GRAS transcription factor[147]
miR857LaccaseDown[123]
miR858Myb transcription factor[130]
miR863Transducin/WD40 repeat-like other RNAUp
miR1040Acylsphingosine kinase/hypersensitive-induced response protein 1Down[120]
miR1074LRR receptor-like serine/threonine-protein kinase[147]
miR1088CoA ligase-like 3[147]
miR1127b-3p-1ss12TCUDP-glucuronate decarboxylase; SCF ubiquitin ligase complex[129]
miR1127b-p5-1ss3TC[129]
miR1133bZIP transcription factor superfamily protein[147]
miR1137a-p3_1ss9CT[129]
miR1137a-p5_2ss9GA20GCDNA mismatch repair protein MSH6[129]
miR1214Peroxidase 2-like/F-box domain containing protein[147]
miR2097Translation initiation factor eIF-2B subunit delta[147]
miR2199MDIS1-interacting receptor-like kinase 1[147]
miR2275-p5LRR receptor-like serine/threonine-protein kinase FLS2; brassinosteroid insensitive 1/stress response gene TaPRP/signal transduction-associated genes TaWRK and TaSPK/trafficking genes TaAAT, TaNTA, and TaIM[129, 157]
miR2630Leucine-rich repeat receptor-like serine/threonine-protein kinase[147]
miR2864Sphingosine kinase 1[147]
miR2916-p3-2ss2TC17CAFructose-bisphosphate aldolase; PRM1; peroxidase[129]
miR2916-p5-2ss2AG17TGProtein serine/threonine kinase; glutathione S-transferase (GSTF) 1; DELLA[129]
miR2919F-box protein[147]
miR2948LRR receptor-like serine/threonine-protein kinaseDown[120]
miR3454Protein kinase family protein[147]
PC-5p-3645-2157Metalloendopeptidase; SCF ubiquitin ligase[129]
miR3706Pentatricopeptide repeat-containing protein[147]
miR3946ABC transporter G family member 41/SBP-transcription factor 5[147]
miR3979-3pPPR domain-containing protein[119]
miR4350Cyclin-A2/putative ubiquitin-like-specific protease 1B[147]
PC-3p-4780_1750Aspartic endopeptidase; transcription factor[129]
miR5059Glycosyltransferase family 61 protein[147]
miR5070Transport inhibitor response 1 protein[147]
miR5262F-box/kelch-repeat proteinDown[120]
miR5301Harbinger transposase-derived nucleaseDown[120]
miR5384-p5UDP-glycosyltransferase 83A1-like; ethylene-responsive transcription factor 1B[129]
miR5721Auxilin-related protein 2Down[119]
miR6148Hydroxycinnamoyl transferaseDown[119]
miR6224RNA-directed RNA polymeraseDown[119]
miR6300-p5Protein RPM1; response to nitrate[129]
miR9652-5pRetrograde transport[129]
miR9653b-p3Protein binding[129]
miR9655-p5Transcription factor; oxidation-reduction[129]
miR9657a-3pSerine-type endopeptidase inhibitor activity; amino acid transport; WRKY[129]
miR9658-3pSCF ubiquitin ligase complex; RPM1[129]
miR9664–3p-L-1RPM1 protein; zinc finger CCCH domain-containing glucosidase[129]
miR9666a-3pAlternative splicing regulator; regulator protein NPR5[129]
miR9666b-3pDNA-directed RNA polymerase II subunit I/stress response[129]
miR9672a-3p-L+2R-2Replication factor C subunit 1[129]
miR9672b-p5LRR receptor-like serine/threonine-protein kinase FLS2-like[129]
miR9674b-5pSCF ubiquitin ligase complex; calcium-dependent protein kinase 20-like[129]
miR9772a-5p-L-2R+2SCF ubiquitin ligase complex[129]
miR9776-L-1R+1-1ss18AGCell division; O-methyltransferase[129]
miR9779-p3Hexose transmembrane transport[129]