Skip to main content
SpringerLink
Log in

microRNA 166: an evolutionarily conserved stress biomarker in land plants targeting HD-ZIP family

  • Review Article
  • Published:
Physiology and Molecular Biology of Plants Aims and scope Submit manuscript

Abstract

MicroRNAs (miRNAs) are significant class of noncoding RNAs having analytical investigating and modulatory roles in various signaling mechanisms in plants related to growth, development and environmental stress. Conserved miRNAs are an affirmation of land plants evolution and adaptation. They are a proof of indispensable roles of endogenous gene modulators that mediate plant survival on land. Out of such conserved miRNA families, is one core miRNA known as miR166 that is highly conserved among land plants. This particular miRNA is known to primarily target HD ZIP-III transcription factors. miR166 has roles in various developmental processes, as well as regulatory roles against biotic and abiotic stresses in major crop plants. Major developmental roles indirectly modulated by miR166 include shoot apical meristem and vascular differentiation, leaf and root development. In terms of abiotic stress, it has decisive regulatory roles under drought, salinity, and temperature along with biotic stress management. miR166 and its target genes are also known for their beneficial synergy with microorganisms in leguminous crops in relation to lateral roots and nodule development. Hence it is important to study the roles of miR166 in different crop plants to understand its defensive roles against environmental stresses and improve plant productivity by reprogramming several gene functions at molecular levels. This review is hence a summary of different regulatory roles of miR166 with its target HD-ZIP III and its modulatory and fine tuning against different environmental stresses in various plants.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aravin A et al (2003) The small RNA profile during Drosophila melanogaster development. Dev Cell 5:337–350

    Article  CAS  PubMed  Google Scholar 

  • Ariel FD, Manavella PA, Dezar CA, Chan RL (2007) The true story of the HD-Zip family. Trends Plant Sci 12:419–426

    Article  CAS  PubMed  Google Scholar 

  • Asha S, Nisha J, Soniya EV (2003) In silico characterisation and phylogenetic analysis of two evolutionarily conserved miRNAs (miR166 and miR171) from black pepper (Piper nigrum L.). Plant Mol Biol Rep 31:707–718

    Article  Google Scholar 

  • Barik S et al (2014) Phylogenetic analysis reveals conservation and diversification of micro RNA166 genes among diverse plant species. Genomics 103:114–121

    Article  CAS  PubMed  Google Scholar 

  • Berruezo F et al (2017) Sequencing of small RNAs of the fern Pleopeltis minima (Polypodiaceae) offers insight into the evolution of the microrna repertoire in land plants. PLoS ONE 12:0177573

    Article  Google Scholar 

  • Bita C, Gerats T (2013) Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Front Plant Sci 4:273

    Article  PubMed  PubMed Central  Google Scholar 

  • Boke H, Ozhuner E, Turktas M, Parmaksiz I, Ozcan S, Unver T (2015) Regulation of the alkaloid biosynthesis by mi RNA in opium poppy. Plant Biotechnol J 13:409–420

    Article  CAS  PubMed  Google Scholar 

  • Boualem A et al (2008) MicroRNA166 controls root and nodule development in Medicago truncatula. The Plant J 54:876–887

    Article  CAS  PubMed  Google Scholar 

  • Brodersen P et al (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320:1185–1190

    Article  CAS  PubMed  Google Scholar 

  • Casadevall R, Rodriguez RE, Debernardi JM, Palatnik JF, Casati P (2013) Repression of growth regulating factors by the microRNA396 inhibits cell proliferation by UV-B radiation in Arabidopsis leaves. Plant Cell 25:3570–3583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaves I, Lin YC, Pinto-Ricardo C, Van de Peer Y, Miguel C (2014) miRNA profiling in leaf and cork tissues of Quercus suber reveals novel miRNAs and tissue-specific expression patterns. Tree Genet Genomes 10:721–737

    Article  Google Scholar 

  • Chen X et al (2014) Genome-wide analysis of soybean HD-Zip gene family and expression profiling under salinity and drought treatments. PLoS ONE 9:87156

    Article  Google Scholar 

  • Chi X et al (2011) Identification and characterization of microRNAs from peanut (Arachis hypogaea L.) by high-throughput sequencing. PLoS ONE 6:27530

    Article  Google Scholar 

  • Chuck G, O’Connor D (2010) Small RNAs going the distance during plant development. Current Opin Plant Biol 13:40–45

    Article  CAS  Google Scholar 

  • Ciarbelli AR et al (2008) The Arabidopsis homeodomain-leucine zipper II gene family: diversity and redundancy. Plant Mol Biol 68:465–478

    Article  CAS  PubMed  Google Scholar 

  • Ding Y et al (2018) MicroRNA166 modulates cadmium tolerance and accumulation in rice. Plant Physiol 177:1691–1703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ding Y, Chen Z, Zhu C (2011) Microarray-based analysis of cadmium-responsive microRNAs in rice (Oryza sativa). J Exp Bot 62:3563–3573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du Q, Wang H (2015) The role of HD-ZIP III transcription factors and miR165/166 in vascular development and secondary cell wall formation. Plant Signal Behav 10:1078955

    Article  Google Scholar 

  • Dubey S, Saxena S, Chauhan AS, Mathur P, Rani V, Chakrabaroty D (2020) Identification and expression analysis of conserved microRNAs during short and prolonged chromium stress in rice (Oryza sativa). Environ Sci Pollut Res 27:380–390

    Article  CAS  Google Scholar 

  • Elhiti M, Stasolla C (2009) Structure and function of homodomain-leucine zipper (HD-Zip) proteins. Plant Signal Behav 4:86–88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Emery JF et al (2003) Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Curr Biol 13:1768–1774

    Article  CAS  PubMed  Google Scholar 

  • Fileccia V et al (2017) Identification and characterization of durum wheat microRNAs in leaf and root tissues. Funct Integr Genomic 17:583–598

    Article  CAS  Google Scholar 

  • Floyd SK, Zalewski CS, Bowman JL (2006) Evolution of class III homeodomain–leucine zipper genes in streptophytes. Genetics 173:373–438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galdino JH, Eguiluz M, Guzman F, Margis R (2019) Novel and conserved miRNAs among Brazilian pine and other gymnosperms. Front Genet 10:222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grigg SP, Canales C, Hay A, Tsiantis M (2005) SERRATE coordinates shoot meristem function and leaf axial patterning in Arabidopsis. Nature 437:1022–1026

    Article  CAS  PubMed  Google Scholar 

  • Guo Y et al (2017) Identification of drought-responsive miRNAs and physiological characterization of tea plant (Camellia sinensis L.) under drought stress. BMC Plant Biol 17:211

    Article  PubMed  PubMed Central  Google Scholar 

  • Hamza NB, Sharma N, Tripathi A, Sanan-Mishra N (2016) MicroRNA expression profiles in response to drought stress in Sorghum bicolor. Gene Expr Patterns 20:88–98

    Article  CAS  PubMed  Google Scholar 

  • Huang D, Koh C, Feurtado JA, Tsang EW, Cutler AJ (2013) MicroRNAs and their putative targets in Brassica napus seed maturation. BMC Genomics 14:140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang T et al (2014) Arabidopsis KANADI1 acts as a transcriptional repressor by interacting with a specific cis-element and regulates auxin biosynthesis, transport, and signaling in opposition to HD-ZIPIII factors. Plant Cell 26:246–262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Husbands AY, Chitwood DH, Plavskin Y, Timmermans MC (2009) Signals and prepatterns: new insights into organ polarity in plants. Genes Dev 23:1986–1997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jatan R, Charu L (2019) Role of MicroRNAs in abiotic and biotic stress resistance in plants. Proc Indian National Sci Acad 85:553–567

    Google Scholar 

  • Jatan R, Tiwari S, Asif MH, Lata C (2019) Genome-wide profiling reveals extensive alterations in Pseudomonas putida-mediated miRNAs expression during drought stress in chickpea (Cicer arietinum L.). Environ Exp Bot 157:217–227

    Article  CAS  Google Scholar 

  • Jia X et al (2015) Functional plasticity of miR165/166 in plant development revealed by small tandem target mimic. Plant Sci 233:11–21

    Article  CAS  PubMed  Google Scholar 

  • Jia X, Ren L, Chen QJ, Li R, Tang G (2009) UV-B-responsive microRNAs in Populus tremula. J Plant Physiol 166:2046–2057

    Article  CAS  PubMed  Google Scholar 

  • Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53

    Article  CAS  PubMed  Google Scholar 

  • Juarez MT, Kui JS, Thomas J, Heller BA, Timmermans MC (2004) microRNA-mediated repression of rolled leaf1 specifies maize leaf polarity. Nature 428:84

    Article  CAS  PubMed  Google Scholar 

  • Jung JH, Park CM (2007) MIR166/165 genes exhibit dynamic expression patterns in regulating shoot apical meristem and floral development in Arabidopsis. Planta 225:1327–1338

    Article  CAS  PubMed  Google Scholar 

  • Kantar M, Unver T, Budak H (2010) Regulation of barley miRNAs upon dehydration stress correlated with target gene expression. Funct Int Gen 10:493–507

    Article  CAS  Google Scholar 

  • Kerstetter RA, Bollman K, Taylor RA, Bomblies K, Poethig RS (2008) KANADI regulates organ polarity in Arabidopsis. Nature 411:706–709

    Article  Google Scholar 

  • Khraiwesh B, Zhu JK, Zhu J (2012) Role of miRNAs and siRNAs in biotic and abiotic stress responses of plants. Biochim Biophys Acta Gene Regul Mech 1819:137–148

    Article  CAS  Google Scholar 

  • Kim J et al (2005) microRNA-directed cleavage of ATHB15 mRNA regulates vascular development in Arabidopsis inflorescence stems. The Plant J 42:84–94

    Article  CAS  PubMed  Google Scholar 

  • Kim YS et al (2008) HD-ZIP III activity is modulated by competitive inhibitors via a feedback loop in Arabidopsis shoot apical meristem development. Plant Cell 20:920–933

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kitazumi A, Kawahara Y, Onda TS, De Koeyer D, de los Reyes BG (2015) Implications of miR166 and miR159 induction to the basal response mechanisms of an andigena potato (Solanum tuberosum subsp. andigena) to salinity stress, predicted from network models in Arabidopsis. Genome 58:13–24

    Article  CAS  PubMed  Google Scholar 

  • Ko JH, Prassinos C, Han KH et al (2006) Developmental and seasonal expression of PtaHB1, a Populus gene encoding a class III HD-Zip protein, is closely associated with secondary growth and inversely correlated with the level of microRNA (miR166). New Phytol 169:469–478

    Article  CAS  PubMed  Google Scholar 

  • Kohli D et al (2014) Identification and characterization of wilt and salt stress-responsive microRNAs in chickpea through high-throughput sequencing. PloS One 9:e108851

    Article  PubMed  PubMed Central  Google Scholar 

  • Kouhi F, Sorkheh K, Ercisli S (2020) MicroRNA expression patterns unveil differential expression of conserved miRNAs and target genes against abiotic stress in safflower. PloS One 15:e0228850

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kruszka K et al (2012) Role of microRNAs and other sRNAs of plants in their changing environments. J Plant Physiol 169:1664–1672

    Article  CAS  PubMed  Google Scholar 

  • Kruszka K et al (2014) Transcriptionally and post-transcriptionally regulated microRNAs in heat stress response in barley. J Exp Bot 65:6123–6135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kulcheski FR et al (2011) Identification of novel soybean microRNAs involved in abiotic and biotic stresses. BMC Genomics 12:307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kundu A, Paul S, Dey A, Pal A (2017) High throughput sequencing reveals modulation of microRNAs in Vigna mungo upon Mungbean Yellow Mosaic India Virus inoculation highlighting stress regulation. Plant Sci 257:96–105

    Article  CAS  PubMed  Google Scholar 

  • Lauressergues D et al (2015) Primary transcripts of microRNAs encode regulatory peptides. Nature 520:90–93

    Article  CAS  PubMed  Google Scholar 

  • Lee C, Clark SE (2015) A WUSCHEL-independent stem cell specification pathway is repressed by PHB, PHV and CNA in Arabidopsis. PloS One 10:e0126006

    Article  PubMed  PubMed Central  Google Scholar 

  • Li SG, Li WF, Han SY, Yang WH, Qi LW (2013) Stage-specific regulation of four HD-ZIP III transcription factors during polar pattern formation in Larix leptolepis somatic embryos. Gene 522:177–183

    Article  CAS  PubMed  Google Scholar 

  • Li X et al (2017) Conservation and diversification of the miR166 family in soybean and potential roles of newly identified miR166s. BMC Plant Biol 17:1–18

    Article  PubMed  PubMed Central  Google Scholar 

  • Li N, Yang T, Guo Z, Wang Q, Chai M, Wu M, Li X, Li W, Li G, Tang J, Tang G (2020) Maize microrna166 inactivation confers plant development and abiotic stress resistance. Int J Mol Sci 21:9506

    Article  CAS  PubMed Central  Google Scholar 

  • Liu Q, Yao X, Pi L, Wang H, Cui X, Huang, H (2009) The ARGONAUTE10 gene modulates shoot apical meristem maintenance and establishment of leaf polarity by repressing miR165/166 in Arabidopsis. Plant J 58:27–40

    Article  CAS  Google Scholar 

  • Mallory AC et al (2004) MicroRNA control of PHABULOSA in leaf development: importance of pairing to the microRNA 5′ region. The EMBO J 23:3356–3364

    Article  CAS  PubMed  Google Scholar 

  • Mandel T et al (2016) Differential regulation of meristem size, morphology and organization by the ERECTA, CLAVATA and class III HD-ZIP pathways. Dev 143:1612–1622

    CAS  Google Scholar 

  • Mao H, Yu L, Li Z, Liu H, Han R (2016) Molecular evolution and gene expression differences within the HD-Zip transcription factor family of Zea mays L. Genetica 144:243–257

    Article  CAS  PubMed  Google Scholar 

  • Mao W, Li Z, Xia X, Li Y, Yu J (2012) A combined approach of high-throughput sequencing and degradome analysis reveals tissue specific expression of microRNAs and their targets in cucumber. PLoS ONE 7:33040

    Article  Google Scholar 

  • Müller CJ et al (2016) PHABULOSA mediates an auxin signaling loop to regulate vascular patterning in Arabidopsis. Plant Physiol 170:956–970

    Article  PubMed  Google Scholar 

  • Nozawa M, Miura S, Nei M (2012) Origins and evolution of microRNA genes in plant species. Genome Biol Evol 4:230–239

    Article  PubMed  PubMed Central  Google Scholar 

  • Ochando I et al (2006) Mutations in the microRNA complementarity site of the INCURVATA4 gene perturb meristem function and adaxialize lateral organs in Arabidopsis. Plant Physiol 141:607–619

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohashi-Ito K, Fukuda H (2003) HD-Zip III homeobox genes that include a novel member, ZeHB-13 (Zinnia)/ATHB-15 (Arabidopsis), are involved in procambium and xylem cell differentiation. Plant Cell Physiol 44:1350–1358

    Article  CAS  PubMed  Google Scholar 

  • Ong SS, Wickneswari R (2012) Characterization of microRNAs expressed during secondary wall biosynthesis in Acacia mangium. PLoS ONE 7:49662

    Article  Google Scholar 

  • Prigge MJ, Clark SE (2006) Evolution of the class III HD-Zip gene family in land plants. Evol Dev 8:350–361

    Article  CAS  PubMed  Google Scholar 

  • Ramachandran P, Carlsbecker A, Etchells JP (2017) Class III HD-ZIPs govern vascular cell fate: an HD view on patterning and differentiation. J Exp Bot 68:55–69

    Article  CAS  PubMed  Google Scholar 

  • Robischon M, Du J, Miura E, Groover A (2011) The Populus class III HD ZIP, popREVOLUTA, influences cambium initiation and patterning of woody stems. Plant Physiol 155:1214–1225

    Article  CAS  PubMed  Google Scholar 

  • Salvador-Guirao R et al (2018) The polycistronic miR166k-166h positively regulates rice immunity via post-transcriptional control of EIN2. Front Plant Sci 9:337

    Article  PubMed  PubMed Central  Google Scholar 

  • Samad AF et al (2017) MicroRNA and transcription factor: key players in plant regulatory network. Front Plant Sci 8:565

    Article  PubMed  PubMed Central  Google Scholar 

  • Saminathan T et al (2016) Genome-wide identification of microRNAs in pomegranate (Punica granatum L.) by high-throughput sequencing. BMC Plant Boil 16:122

    Article  Google Scholar 

  • Sharma A et al (2020) Identification of microRNAs and Their Expression in Leaf Tissues of Guava (Psidium guajava L.) under Salinity Stress. Agronomy 10:1920

    Article  CAS  Google Scholar 

  • Shen W et al (2019) Genomic and transcriptomic analyses of HD-Zip family transcription factors and their responses to abiotic stress in tea plant (Camellia sinensis). Genomics 111:1142–1151

    Article  CAS  PubMed  Google Scholar 

  • Shi M et al (2017) Genome-wide profiling of small RNAs and degradome revealed conserved regulations of miRNAs on auxin-responsive genes during fruit enlargement in peaches. Int j Mol Sci 18:2599

    Article  PubMed Central  Google Scholar 

  • Shin SJ, Lee JH, Kwon HB (2017) Genome-wide identification and characterization of drought responsive MicroRNAs in Solanum tuberosum L. Genes-Genomics 39:1193–1203

    Article  CAS  Google Scholar 

  • Shinde H et al (2020) Small RNA sequencing reveals the role of pearl millet miRNAs and their targets in salinity stress responses. S Afr J Bot 132:395–402

    Article  CAS  Google Scholar 

  • Singh A et al (2017) Phytohormonal crosstalk modulates the expression of miR166/165s, target Class III HD-ZIPs, and KANADI genes during root growth in Arabidopsis thaliana. Sci Rep 7:3408

    Article  PubMed  PubMed Central  Google Scholar 

  • Subramanian S et al (2008) Novel and nodulation-regulated microRNAs in soybean roots. BMC Genomics 9:160

    Article  PubMed  PubMed Central  Google Scholar 

  • Singh P, Dutta P, Chakrabarty D (2021) miRNAs play critical roles in response to abiotic stress by modulating cross-talk of phytohormone signaling. Plant Cell Rep 40:1–14

    Article  Google Scholar 

  • Sunkar R (2010) MicroRNAs with macro-effects on plant stress responses. Seminars Cell Dev Biol 21:805–811

    Article  CAS  Google Scholar 

  • Tang X et al (2012) MicroRNA–mediated repression of the seed maturation program during vegetative development in Arabidopsis. PLoS Genet 8:1003091

    Article  Google Scholar 

  • Tiwari M, Bhatia S (2020) Expression profiling of miRNAs indicates crosstalk between phytohormonal response and rhizobial infection in chickpea. J Plant Biochem Biot 29:380–394

    Article  CAS  Google Scholar 

  • Tiwari S, Lata C, Chauhan PS, Nautiyal CS (2016) Pseudomonas putida attunes morphophysiological, biochemical and molecular responses in Cicer arietinum L. during drought stress and recovery. Plant Physiol Biochem 99:108–117

    Article  CAS  PubMed  Google Scholar 

  • Tsuzuki M et al (2016) Profiling and characterization of small RNAs in the liverwort, Marchantia polymorpha, belonging to the first diverged land plants. Plant Cell Physiol 57:359–372

    Article  CAS  PubMed  Google Scholar 

  • Turchi L, Baima S, Morelli G, Ruberti I (2015) Interplay of HD-Zip II and III transcription factors in auxin-regulated plant development. J Exp Bot 66:5043–5053

    Article  CAS  PubMed  Google Scholar 

  • Valiollahi E, Farsi M, Kakhki AM (2014) Sly-miR166 and Sly-miR319 are components of the cold stress response in Solanum lycopersicum. Plant Biotechnol Rep 8:349–356

    Article  Google Scholar 

  • Varkonyi-Gasic E, Gould N, Sandanayaka M, Sutherland P, MacDiarmid RM (2010) Characterisation of microRNAs from apple (Malus domestica ’Royal Gala’) vascular tissue and phloem sap. BMC Plant Boil 10:159

    Article  Google Scholar 

  • Wang B et al (2019) Bioinformatic exploration of the targets of xylem sap miRNAs in maize under cadmium stress. Int j Mol Sci 20:1474

    Article  CAS  PubMed Central  Google Scholar 

  • Wang T, Chen L, Zhao M, Tian Q, Zhang WH (2011) Identification of drought-responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. BMC Genomics 12:367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y et al (2016) High-throughput sequencing revealed that microRNAs were involved in the development of superior and inferior grains in bread wheat. Sci Rep 8:1–18

    Google Scholar 

  • Wen M et al (2016) Expression variations of miRNAs and mRNAs in rice (Oryza sativa). Genome Biol Evol 8:3529–3544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williams L, Grigg SP, Xie M, Christensen S, Fletcher JC (2005) Regulation of Arabidopsis shoot apical meristem and lateral organ formation by microRNA miR166g and its AtHD-ZIP target genes. Dev 132:3657–3668

    Article  CAS  Google Scholar 

  • Wójcik AM, Nodine MD, Gaj MD (2017) miR160 and miR166/165 contribute to the LEC2-mediated auxin response involved in the somatic embryogenesis induction in Arabidopsis. Front Plant Sci 8:2024

    Article  PubMed  PubMed Central  Google Scholar 

  • Xie F et al (2014) High-throughput deep sequencing shows that microRNA s play important roles in switchgrass responses to drought and salinity stress. Plant Biotech 12:354–366

    Article  CAS  Google Scholar 

  • Xin M et al (2010) Diverse set of microRNAs are responsive to powdery mildew infection and heat stress in wheat (Triticum aestivum L.). BMC Plant Biol 10:123

    Article  PubMed  PubMed Central  Google Scholar 

  • Yadav A, Sanyal I, Rai SP, Lata C (2021) An overview on miRNA-encoded peptides in plant biology research. Genomics 113:2385–2391

    Article  CAS  PubMed  Google Scholar 

  • Yang Y et al (2020) Dynamic changes of miR166s at both the transcriptional and post-transcriptional levels during somatic embryogenesis in Lilium. Sci Hortic 261:108928

    Article  CAS  Google Scholar 

  • Yip HK, Floyd SK, Sakakibara K, Bowman JL (2016) Class III HD-Zip activity coordinates leaf development in Physcomitrella patens. Dev Biol 419:184–197

    Article  CAS  PubMed  Google Scholar 

  • Yu X et al (2012) Identification of conserved and novel microRNAs that are responsive to heat stress in Brassica rapa. J Exp Bot 63:1025–1038

    Article  CAS  PubMed  Google Scholar 

  • Yu Y, Jia T, Chen X (2017) The ‘how’ and ‘where’ of plant microRNAs. New Phytol 216:1002–1017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao JP, Jiang XL, Zhang BY, Su XH (2012) Involvement of microRNA-mediated gene expression regulation in the pathological development of stem canker disease in Populus trichocarpa. PLoS ONE 7:44968

    Article  Google Scholar 

  • Zhou X, Wang G, Zhang W (2007) UV-B responsive microRNA genes in Arabidopsis thaliana. Mol Syst Biol 3:103

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The study was supported by the CSIR Niche Creating High Science Project “Genome-wide editing for enhanced yield and quality traits” (MLP 0026) from the Council of Scientific and Industrial Research (CSIR), New Delhi, India. AY acknowledges Junior Research Fellowship [IF180146] from Department of Science and Technology, Government of India and SPR for Centre of Advance Study (CAS) faculty, Department of Botany, BHU, Varanasi.

Author information

Authors and Affiliations

  1. CSIR-National Botanical Research Institute, Rana Pratap Marg, Lucknow, 226001, India

    Ankita Yadav, Sanoj Kumar, Rita Verma & Indraneel Sanyal

  2. Laboratory of Morphogenesis, Department of Botany, Institute of Science, Banaras Hindu University, Varanasi, 221005, India

    Ankita Yadav & Shashi Pandey Rai

  3. Institute of Environment and Sustainable Development, Banaras Hindu University, Varanasi, 221005, India

    Sanoj Kumar

  4. CSIR-National Institute of Science Communication and Information Resources, 14 Satsang Vihar Marg, New Delhi, 110067, India

    Charu Lata

Authors
  1. Ankita Yadav
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sanoj Kumar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rita Verma
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Charu Lata
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Indraneel Sanyal
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shashi Pandey Rai
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AY wrote the manuscript, SK, RV, IS, CL and SPR reviewed the manuscript.

Corresponding author

Correspondence to Shashi Pandey Rai.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yadav, A., Kumar, S., Verma, R. et al. microRNA 166: an evolutionarily conserved stress biomarker in land plants targeting HD-ZIP family. Physiol Mol Biol Plants 27, 2471–2485 (2021). https://doi.org/10.1007/s12298-021-01096-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12298-021-01096-x

Keywords

Search

Navigation