Table 2.
The conserved heat-responsive miRNAs in different plant species.
| Family | miRNAa | Heat treatment | Regulation | Validationc | Target proteins |
|---|---|---|---|---|---|
| 156 | ath-miR156h | ATb | Up-regulation | Yes | SPL transcription factor |
| ath-miR156g,h | Grown at 30°C | Up-regulation | No | ||
| bra-miR156g,h | 46°C for 1 h | Up-regulation | Yes | BracSPL2 | |
| osa-miR156a,g,h | 42°C day/36°C night for 24 h | Down-regulation in roots and shoots | Yes | SPL transcription factor | |
| tae-miR156a-g | 40°C for 2 h | Up-regulation | Yes | SPL transcription factor | |
| tae-miR156 | 42°C for 2 h | Up-regulation | Yes | Heat shock protein 90 | |
| mes-miR156a | 37°C for 24 h | Down-regulation | Yes | SPL transcription factor | |
| 159 | ath-miR159a,b | Grown at 30°C | Down-regulation | No | MYB and TCP transcription factors |
| tae-miR159 | 40°C for 2 h | Down-regulation | Yes | GAMYB1 and GAMYB2 | |
| tae-miR159a,b | 42°C for 2 h | Down-regulation | Yes | WRKY transcription factor; MYB3; alkaline phosphatase family protein, cytochrome P450, cobalamine adenosyl transferase, Mob1-like protein and TLD family protein | |
| mes-miR159a | 37°C for 24 h | Down-regulation | Yes | myb-like HTH transcriptional regulators | |
| 160 | ath-miR160a-c | Grown at 30°C | Up-regulation | No | Auxin response factors |
| osa-miR160a | 42°C day/36°C night for 24 h | Down-regulation in roots, up-regulation in shoots | Yes | ||
| pto-miR160a-d | 37°C for 8 h | Down-regulation | No | ||
| tae-miR160 | 40°C for 2 h | Up-regulation | No | Heat shock protein 70; ARF; tetratricopeptide repeat (TPR) | |
| tae-miR160 | 42°C for 2 h | Down-regulation | Yes | ||
| hvu-miR160a | 35.5°C for 24 h | Up-regulation | Yes | ARF17 and ARF13 | |
| mes-miR160a | 37°C for 24 h | Down-regulation | Yes | Auxin response factor | |
| celery-miR160 | 38°C for 1 h | Up-regulation | Yes | Auxin response factor | |
| 162 | osa-miR162a | 42°C day/36°C night for 24 h | Down-regulation in both roots and shoots | Yes | Endoribonuclease DCL1 |
| 164 | ath-miR164a-c | Grown at 30°C | Up-regulation | No | NAC domain containing transcription factors |
| tae-miR164 | 42°C for 2 h | Down-regulation | Yes | Small heat shock proteins 17; NAC transcription factor; target genes involved in mitogen-activated protein kinase (MAPK) signaling pathways | |
| celery-miR164 | 38°C for 1 h | Up-regulation | Yes | NAC domain containing transcription factors | |
| 166 | ath-miR166a | Grown at 30°C | Up-regulation | No | HD-Zip transcription factors including PHV and REVOLUTA |
| tae-miR166a-d | 40°C for 2 h | Up-regulation | Yes | Unknown | |
| hvu-miR166a | 35.5°C for 24 h | Up-regulation | Yes | HD-Zip transcription factors including PHV and REVOLUTA; a homeoboxleucine zipper protein HOX9-like gene | |
| 167 | ath-miR167c,d | Grown at 30°C | Up-regulation | No | HD-Zip transcription factors including PHV and PHB |
| ath-miR167d | ATb | Down-regulation | No | ||
| bra-miR167 | 42°C for 3 h per day for 7 days | Up-regulation | No | TOM1-like protein 2; Tudor domain-containing protein 3 | |
| bra-miR167∗ | 42°C for 3 h per day for 7 days | Up-regulation | No | GDSL esterase/lipase; Ribulose bisphosphate carboxylase/oxygenase activase | |
| bra-miR167 | 46°C for 1 h | Up-regulation | No | BracARF6 | |
| osa-miR167a,c,d | 42°C day/36°C night for 24 h | Down-regulation in both roots and shoots | Yes | Class III HD-Zip protein 4; heat repeat family protein | |
| sja-miR167a | 20°C for 3h | Down-regulation | No | Unknown | |
| pto-miR167c,d,f,g | 37°C for 8 h | Up-regulation | Yes | Unknown | |
| tae-miR167 | 42°C for 2 h | Up-regulation | Yes | Dnaj heat shock n-terminal domain-containing protein | |
| hvu-miR167h | 35.5°C for 24 h | Up-regulation | Yes | ARF8 and a serine/threonine-protein kinase Nek5-like gene | |
| 168 | bra-miR168 | 42°C for 3h per day for 7 days | Up-regulation | Yes | BraAGO1 |
| osa-miR168a | 42°C day /36°C night for 24 h | Down-regulation in shoots, no expression in roots | Yes | AGO1 | |
| sja-miR168a | 20°C for 3 h | Down-regulation | No | Unknown | |
| pto-miR168a,b | 37°C for 8 h | Down-regulation | Yes | Unknown | |
| tae-miR168 | 40°C for 2 h | Up-regulation | No | Unknown | |
| celery-miR168 | 38°C for 1 h | Up-regulation | Yes | Unknown | |
| 169 | ath-miR169a,d-n | Grown at 30°C | Down-regulation | No | CCAAT Binding Factor (CBF) and HAP2-like transcription factors |
| ath-miR169d,e,k,i,m | ATb | Down-regulation | No | ||
| ath-miR169b,c | Grown at 30°C | Up-regulation | No | ||
| osa-miR169a,b,g | 42°C day/36°C night for 24 h | Down-regulation in roots, up-regulation in shoots | Yes | Nuclear transcription factor Y subunit | |
| pto-miR169j-m | 37°C for 8 h | Up-regulation | No | Unknown | |
| pto-miR169n-t | 37°C for 8 h | Down-regulation | No | Unknown | |
| tae-miR169a-d | 40°C for 2 h | Up-regulation | No | Unknown | |
| 171 | ath-miR171a-c | Grown at 30°C | Up-regulation | No | Scarecrow-like transcription factors |
| ath-miR171b,c | ATb | Up-regulation | No | ||
| bra-miR171a-1 | 42°C for 3 h per day for 7 days | Up-regulation | No | 26S protease regulatory subunit 6A homolog | |
| pto-miR171a-i | 37°C for 8 h | Down-regulation | No | Unknown | |
| tae-miR171a | 42°C for 2 h | Down-regulation | Yes | Scarecrow-like protein | |
| ptc-miR171l-n | 37°C for 24 h | Down-regulation | Yes | SCL, clathrin assembly protein | |
| 172 | ath-miR172b∗ | Grown at 30°C | Down-regulation | No | Eukaryotic translation initiation factor 5, putative; calcium-transporting ATPase |
| ath-miR172c,d,e | Grown at 30°C | Up-regulation | No | AP2 transcription factors | |
| ath-miR172a,e | ATb | Up-regulation | No | ||
| tae-miR172a,b | 40°C for 2 h | Down-regulation | Yes | AP2 transcription factors; floral homeotic protein | |
| 319 | ath-miR319a,b | Grown at 30°C | Up-regulation | No | MYB and TCP transcription factors |
| ath-miR319a,c | ATb | Up-regulation | No | ||
| ath-miR319c | Grown at 30°C | Down-regulation | No | ||
| tae-miR319 | 42°C for 2 h | Down-regulation | Yes | MYB3; histone protein-associated genes | |
| 393 | ath-miR393a,b | Grown at 30°C | Down-regulation | No | F-box proteins and bHLH transcription factors |
| tae-miR393 | 40°C for 2 h | Up-regulation | Yes | Genes involved in auxin signaling pathway and basal defense | |
| 394 | ath-miR394a,b | Grown at 30°C | Down-regulation | No | F-box proteins |
| celery-miR394 | 38°C for 1 h | Up-regulation | Yes | Unknown | |
| pto-miR394a,b | 37°C for 8 h | Down-regulation | No | Unknown | |
| 395 | ath-miR395a-f | Grown at 30°C | Up-regulation | No | ATP sulphurylases; leucine-rich repeat family protein |
| ath-miR395d | ATb | Up-regulation | No | ||
| pto-miR395a-j | 37°C for 8 h | Down-regulation | Yes | Unknown | |
| sja-miR395x | 20°C for 3 h | Up-regulation | No | Unknown | |
| tae-miR395b | 42°C for 2 h | Up-regulation | No | sulfur transporters and ATP sulphurylases | |
| celery-miR395 | 38°C for 1 h | Up-regulation | Yes | Unknown | |
| 396 | ath-miR396a | Grown at 30°C | Up-regulation | No | Growth-regulating factor (GRF) transcription factors; rhodenase-like proteins; kinesin-like protein B |
| han-miR396 | 37°C for 24 h | Down-regulation | Yes | HaWRKY6 | |
| 397 | ath-miR397a,b | Grown at 30°C | Up-regulation | No | Laccases and beta-6 tubulin |
| osa-miR397b.2 | 42°C for 8 h | Up-regulation | Yes | L-ascorbate oxidase | |
| osa-miR397 | 42°C day/36°C night for 24 h | Down-regulation in shoots, no epression in roots | Yes | L-ascorbate oxidase precursor; F-box domain containing protein | |
| mes-miR397a | 37°C for 24 h | Down-regulation | Yes | Laccase/Diphenol oxidase family protein | |
| 398 | ath-miR398b | Grown at 30°C | Up-regulation | No | CSD1, CSD2 and CCS |
| ath-miR398 | 37°C for 4 h | Up-regulation | Yes | ||
| bra-miR398a,b | 46°C for 1 h | Down-regulation | Yes | BracCSD1 | |
| osa-miR398 | 42°C day/36°C night for 24 h | Down-regulation in both roots and shoots | Yes | Superoxide dismutase (SOD) gene family | |
| sja-miR398a-5p | 20°C for 3 h | Up-regulation | No | Unknown | |
| tae-miR398 | 42°C for 2 h | Up-regulation | Yes | Superoxide dismutase (SOD) gene family | |
| 399 | ath-miR399b-d, f | Grown at 30°C | Up-regulation | No | Phosphatase transporter |
| ath-miR399c,d | ATb | Down-regulation | No | ||
| bra-miR399b | 46°C for 1 h | Down-regulation | No | BracPHO2 | |
| 400 | ath-miR400 | 37°C for 12 h | Down-regulation | Yes | Pentatricopeptide (PPR) repeat-containing protein |
| 408 | ath-miR408 | Grown at 30°C | Up-regulation | No | Peptide chain release factor; plantacyanin |
| sja-miR408b-5p | 20°C for 3 h | Down-regulation | Yes | An unknown conserved protein | |
| pto-miR408 | 37°C for 8 h | Down-regulation | Yes | Unknown | |
| mes-miR408 | 37°C for 24 h | Down-regulation | Yes | Plantacyanin | |
| celery-miR408 | 38°C for 1 h | Up-regulation | Yes | Unknown | |
| 472 | ath-miR472 | Grown at 30°C | Down-regulation | No | RFL1 (RPS5-LIKE 1) |
| pto-miR472a,b | 37°C for 8 h | Down-regulation | No | Disease resistance protein; F-box protein | |
| 482 | pto-miR482 | 37°C for 8 h | Down-regulation | Yes | Unknown |
| 827 | ath-miR827 | Grown at 30°C | Down-regulation | No | SPX (SYG1/Pho81/XPR1) domain-containing protein; DNA-binding storekeeper protein-related |
| ath-miR827 | ATb | Down-regulation | No | ||
| bra-miR827 | 46°C for 1 h | Down-regulation | Yes | Unknown | |
| tae-miR827 | 40°C for 2 h | Up-regulation | No | Unknown | |
| ptc-miR827 | 37°C for 24 h | Down-regulation | Yes | Sec14 cytosolic factor family protein | |
| 1117 | tae-miR1117 | 42°C for 2 h | Down-regulation | Yes | Calcium dependent protein kinase 1 |
| 1450 | pto-miR1450 | 37°C for 8 h | Up-regulation | No | Unknown |
| ptc-miR1450 | 37°C for 24 h | Down-regulation | Yes | Leucine-rich repeat transmembrane protein kinase |
The miRNA family, kinds of heat treatment, up or down-regulation, validated by either northern blot or realtime PCR, and their target proteins are presented. aath: Arabidopsis thaliana (Yan et al., 2012; Guan et al., 2013; Zhong et al., 2013; Stief et al., 2014); bra: Brassica rapa (Yu et al., 2012b; Bilichak et al., 2015); celery: Apium graveolens (Li et al., 2014a); han:Helianthus annuus (Giacomelli et al., 2012); hvu: Hordeum vulgare (Kruszka et al., 2014); mes: Manihot esculenta (Ballen-Taborda et al., 2013); osa: Oryza sativa (Jeong et al., 2011; Sailaja et al., 2014); ptc: Populus trichocarpa (Lu et al., 2008); pto: P. tomentosa (Chen et al., 2012); sja: Saccharina japonica (Liu et al., 2014); tae: Triticum aestivum (Xin et al., 2010; Wang et al., 2012b; Kumar et al., 2014). bAT: acquired thermotolerance, pretreated at 37°C for 1 h and returned to 22°C for 1.5 h for recovery, treated at 44°C for 45 min. cvalidated by either northern blot or realtime PCR.