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Stress-responsive miRNAome of Glycine max (L.) Merrill: molecular insights and way forward

Abstract

Main conclusion

Analysis of stress-associated miRNAs of Glycine max (L.) Merrill reveals wider ramifications of small RNA-mediated (conserved and legume-specific miRNAs) gene regulatory foot prints in molecular adaptive responses.

MicroRNAs (miRNAs) are indispensable components of gene regulatory mechanism of plants. Soybean is a crop of immense commercial potential grown worldwide for its edible oil and soy meal. Intensive research efforts, using the next generation sequencing and bioinformatics techniques, have led to the identification and characterization of numerous small RNAs, especially microRNAs (miRNAs), in soybean. Furthermore, studies have unequivocally demonstrated the significance of miRNAs during the developmental processes and various stresses in soybean. In this review, we summarize the current state of understanding of miRNA-based abiotic and biotic stress responses in soybean. In addition, the molecular insights gained from the stress-related soybean miRNAs have been compared to the miRNAs of other crops, especially legumes, and the core commonalities have been highlighted, though differences among them were not ignored. Nature of response of soybean-derived conserved miRNAs during various stresses was also analyzed to gain deeper insights regarding sRNAome-based defense responses. This review further provides way forward in legume small RNA transcriptomics based on the adaptive responses of soybean and other legume-derived miRNAs.

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Abbreviations

AGO:

Argonaute

AM:

Arbuscular mycorrhiza

AP2:

APETALA 2

ARF:

Auxin response factor

ASR:

Asian soybean rust

DCL-1:

Dicer-like-1

DRE:

Dehydration responsive element

ENOD93:

Early nodulin 93

GSS:

Genome survey sequence

hc-siRNAs:

Heterochromatic siRNAs

HEN 1:

HUA enhancer 1

HESO1:

HEN1 SUPPRESSOR1

HST1:

HASTY 1

HYL1:

HYPONASTIC LEAVES1

miRNAs:

MicroRNAs

nat-siRNAs:

Natural antisense transcript siRNAs

NGS:

Next generation sequencing

PEGs:

Protein encoding genes

PTGS:

Post transcriptional gene silencing

RBPs:

dsRNA-binding proteins

RdDM:

RNA-dependent DNA methylation

RISC:

RNA-induced silencing complex

SCN:

Soybean cyst nematode

SE:

SERRATE

siRNAs:

Small interfering RNAs

SMV:

Soybean mosaic virus

sncRNAs:

Small non-coding RNAs

SNF:

Symbiotic nitrogen fixation

TFs:

Transcriptional factors

TGS:

Transcriptional gene silencing

References

  • Abdel-Ghany SE, Pilon M (2008) MicroRNA-mediated systemic downregulation of copper protein expression in response to low copper availability in Arabidopsis. J Biol Chem 283:15932–15945

    CAS  PubMed  PubMed Central  Google Scholar 

  • Akdogan G, Tufekci ED, Uranbey S, Unver T (2016) miRNA-based drought regulation in wheat. Funct Integr Genom 16(3):221–233

    CAS  Google Scholar 

  • Akpinar BA, Budak H (2016) Dissecting miRNAs in wheat D genome progenitor, Aegilops tauschii. Front Plant Sci 7:606

    PubMed  PubMed Central  Google Scholar 

  • Akpinar BA, Kantar M, Budak H (2015) Root precursors of microRNAs in wild emmer and modern wheats show major differences in response to drought stress. Funct Integr Genom 15(5):587–598

    CAS  Google Scholar 

  • Allen RS, Li J, Stahle MI, Dubroue A, Gubler F, Millar AA (2007) Genetic analysis reveals functional redundancy and the major target genes of the Arabidopsis miR159 family. Proc Natl Acad Sci USA 104:16371–16376

    CAS  PubMed  Google Scholar 

  • Alptekin B, Langridge P, Budak H (2017) Abiotic stress miRNomes in the Triticeae. Funct Integr Genom 17(2–3):145–170

    CAS  Google Scholar 

  • Arenas-Huertero C, Pérez B, Rabanal F, Blanco-Melo D, De la Rosa C, Estrada-Navarrete G, Sanchez F, Covarrubias AA, Reyes JL (2009) Conserved and novel miRNAs in the legume Phaseolus vulgaris in response to stress. Plant Mol Biol 70:385–401

    CAS  PubMed  Google Scholar 

  • Arikit S, Xia R, Kakrana A, Huang K, Zhai J, Yan Z, Valdés-López O, Prince S, Musket TA, Nguyen HT, Stacey G, Meyers BC (2014) An atlas of soybean small RNAs identifies phased siRNAs from hundreds of coding genes. Plant Cell 26:4584–4601

    CAS  PubMed  PubMed Central  Google Scholar 

  • Axtell MJ, Snyder JA, Bartell DP (2007) Common functions for diverse small RNAs of land plants. Plant Cell 19:1750–1769

    CAS  PubMed  PubMed Central  Google Scholar 

  • Babu M, Gagarinova AG, Brandle JE, Wang A (2008) Association of the transcriptional response of soybean plants with Soybean Mosaic Virus systemic infection. J Gen Virol 89:1069–1080

    CAS  PubMed  Google Scholar 

  • Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism and function. Cell 116:281–297

    CAS  Google Scholar 

  • Bazin J, Khan GA, Combier JP, Bustos-Sanmamed P, Debernardi JM, Rodriguez R, Sorin C, Palatnik J, Hartmann C, Crespi M, Lelandais-Brière C (2013) miR396 affects mycorrhization and root meristem activity in the legume Medicago truncatula. Plant J 74(6):920–934

    CAS  PubMed  Google Scholar 

  • Brant EJ, Budak H (2018) Plant small non-coding RNAs and their roles in biotic stresses. Front Plant Sci 9:1038. https://doi.org/10.3389/fpls.2018.01038

    Article  PubMed  PubMed Central  Google Scholar 

  • Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O (2008) Widespread translational inhibition by plant miRNAs and siRNAs. Science 320:1185–1190

    CAS  PubMed  Google Scholar 

  • Budak H, Akpinar A (2011) Dehydration stress-responsive miRNA in Brachypodium distachyon: evident by genome-wide screening of microRNAs expression. Omics J Integr Biol 15(11):791–799

    CAS  Google Scholar 

  • Budak H, Akpinar BA (2015) Plant miRNAs: biogenesis, organization and origins. Funct Integr Genom 15(5):523–531

    CAS  Google Scholar 

  • Budak H, Khan Z, Kantar M (2014) History and current status of wheat miRNAs using next-generation sequencing and their roles in development and stress. Brief Funct Genom 14(3):189–198

    Google Scholar 

  • Budak H, Kantar M, Bulut R, Akpinar BA (2015a) Stress responsive miRNAs and isomiRs in cereals. Plant Sci 235:1–13

    CAS  PubMed  Google Scholar 

  • Budak H, Hussain B, Khan Z, Ozturk NZ, Ullah N (2015b) From genetics to functional genomics: improvement in drought signaling and tolerance in wheat. Front. Plant Sci 6:1012. https://doi.org/10.3389/fpls.2015.01012

    Article  PubMed  PubMed Central  Google Scholar 

  • Cagirici HB, Alptekin B, Budak H (2017a) RNA sequencing and co-expressed long non-coding RNA in modern and wild wheats. Sci Rep 7(1):10670

    PubMed  PubMed Central  Google Scholar 

  • Cagirici HB, Biyiklioglu S, Budak H (2017b) Assembly and annotation of transcriptome provided evidence of miRNA mobility between wheat and wheat stem sawfly. Front Plant Sci 8:1653

    PubMed  PubMed Central  Google Scholar 

  • Cai Z, Wang Y, Zhu L, Tian Y, Chen L, Sun Z, Ullah I, Li X (2017) GmTIR1/GmAFB3-based auxin perception regulated by miR393 modulates soybean nodulation. New Phytol 215:672–686

    CAS  PubMed  Google Scholar 

  • Carrington JC, Ambros V (2003) Role of microRNAs in plant and animal development. Science 301:336–338

    CAS  Google Scholar 

  • Cervantes-Gámez RG, Bueno-Ibarra MA, Cruz-Mendívil A, Calderón-Vázquez CL, Ramírez-Douriet CM, Maldonado-Mendoza IE, Villalobos-López MÁ, Valdez-Ortíz Á, López-Meyer M (2016) Arbuscular mycorrhizal symbiosis-induced expression changes in Solanum lycopersicum leaves revealed by RNA-seq analysis. Plant Mol Bio Rep 34(1):89–102

    Google Scholar 

  • Chen X (2009) Small RNAs and their roles in plant development. Annu Rev Cell Dev Biol 25:21–44

    PubMed  PubMed Central  Google Scholar 

  • Chen L, Wang T, Zhao M, Tian Q, Zhang WH (2012) Identification of aluminum responsive microRNAs in Medicago truncatula by genome-wide high-throughput sequencing. Planta 235:375–386

    CAS  PubMed  Google Scholar 

  • Chen H, Zhang L, Yu K, Wang A (2015) Pathogenesis of soybean mosaic virus in soybean carrying Rsv1 gene is associated with miRNA and siRNA pathways, and breakdown of AGO1 homeostasis. Virology 476:395–404

    CAS  PubMed  Google Scholar 

  • Chen H, Arsovski AA, Yu K, Wang A (2016) Genome-wide investigation using sRNA-Seq, degradome-Seq and transcriptome-Seq reveals regulatory networks of microRNAs and their target genes in soybean during soybean mosaic virus infection. PLoS One 11:e0150582

    PubMed  PubMed Central  Google Scholar 

  • Chen L, Shi S, Jiang N, Khanzada H, Wassan GM, Zhu C, Peng X, Xu J, Chen Y, Yu Q, He X (2018) Genome-wide analysis of long non-coding RNAs affecting roots development at an early stage in the rice response to cadmium stress. BMC Genom 19(1):460

    Google Scholar 

  • Combier JP, Frugier F, de Billy F, Boualem A, El-Yahyaoui F, Moreau S, Vernie T, Ott T, Gamas P, Crespi M, Niebel A (2006) MtHAP2-1 is a key transcriptional regulator of symbiotic nodule development regulated by microRNA169 in Medicago truncatula. Genes Dev 20:3084–3088

    CAS  PubMed  PubMed Central  Google Scholar 

  • Couzigou JM, André O, Guillotin B, Alexandre M, Combier JP (2016) Use of microRNA-encoded peptide miPEP172c to stimulate nodulation in soybean. New Phytol 211:379–381

    CAS  PubMed  Google Scholar 

  • Crespi MD, Jurkevitch E, Poiret M, d’Aubenton-Carafa Y, Petrovics G, Kondorosi E, Kondorosi A (1994) enod40, a gene expressed during nodule organogenesis, codes for a non-translatable RNA involved in plant growth. EMBO J 13:5099–5112

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cui X, Yan Q, Gan S, Xue D, Dou D, Guo N, Xing H (2017) Overexpression of gma-miR1510a/b suppresses the expression of a NB-LRR domain gene and reduces resistance to Phytophthora sojae. Gene 20(621):32–39

    Google Scholar 

  • Devers EA, Branscheid A, May P, Krajinski F (2011) Stars and symbiosis: microRNA-and microRNA*-mediated transcript cleavage involved in arbuscular mycorrhizal symbiosis. Plant Physiol 156:111

    Google Scholar 

  • Dezulian T, Remmert M, Palatnik JF, Weigel D, Huson DH (2006) Identification of plant microRNA homologs. Bioinformatics 22:359–360

    CAS  PubMed  Google Scholar 

  • Ding D, Zhang L, Wang H, Liu Z, Zhang Z, Zheng Y (2009) Differential expression of miRNAs in response to salt stress in maize roots. Ann Bot 103:29–38

    CAS  PubMed  Google Scholar 

  • Ding X, Zhang H, Ruan H, Li Y, Chen L, Wang T, Jin L, Li X, Yang S, Gai J (2019) Exploration of miRNA-mediated fertility regulation network of cytoplasmic male sterility during flower bud development in soybean. 3 Biotech 9:22. https://doi.org/10.1007/s13205-018-1543-1

    Article  PubMed  Google Scholar 

  • Dong Z, Shi L, Chen L, Wang Y, Cai Z, Wang Y, Jin J, Li X (2013) Identification and dynamic regulation of microRNAs involved in salt stress responses in functional soybean nodules by high-throughput sequencing. Int J Mol Sci 14:2717–2738

    CAS  PubMed  PubMed Central  Google Scholar 

  • EI Yahyaoui F, Kuster H, Amor BB, Hohnjec N, Puhler A, Becker A, Gouzy J, Vernie T, Gough C, Niebel A, Godiard L, Gamas P (2004) Expression profiling in Medicago truncatula identifies more than 750 genes differentially expressed during nodulation, including many potential regulators of the symbiotic program. Plant Physiol 136:3159–3176

    Google Scholar 

  • Eldem V, Akcay UC, Ozhuner E, Bakır Y, Uranbey S, Unver T (2012) Genome-wide identification of miRNAs responsive to drought in peach (Prunus persica) by high-throughput deep sequencing. PLoS One 7(12):e50298

    CAS  PubMed  PubMed Central  Google Scholar 

  • Eren H, Pekmezci MY, Okay S, Turktas M, Inal B, Ilhan E, Atak M, Erayman M, Unver T (2015) Hexaploid wheat (Triticum aestivum) root miRNome analysis in response to salt stress. Ann Appl Biol 167(2):208–216

    CAS  Google Scholar 

  • Fang X, Zhao Y, Ma Q, Huang Y, Wang P, Zhang J, Nian H, Yang C (2013) Identification and comparative analysis of cadmium tolerance-associated miRNAs and their targets in two soybean genotypes. PLoS One 8:e81471

    PubMed  PubMed Central  Google Scholar 

  • Fei Q, Xia R, Meyers BC (2013) Phased, secondary, small interfering RNAs in posttranscriptional regulatory networks. Plant Cell 25:2400–2415

    CAS  PubMed  PubMed Central  Google Scholar 

  • Formey D, Iñiguez LP, Peláez P, Li YF, Sunkar R, Sánchez F, Reyes JL, Hernández G (2015) Genome-wide identification of the Phaseolus vulgaris sRNAome using small RNA and degradome sequencing. BMC Genom 16:423

    Google Scholar 

  • Fu D, Ma B, Mason AS, Xiao M, Wei L, An Z (2013) Micro RNA-based molecular markers: a novel PCR-based genotyping technique in Brassica species. Plant Breed 132(4):375–381

    CAS  Google Scholar 

  • Gao P, Bai X, Yang L, Lv D, Pan X, Li Y, Cai H, Ji W, Chen Q, Zhu Y (2011) osa-MIR393: a salinity- and alkaline stress related microRNA gene. Mol Biol Rep 38:237–242

    CAS  PubMed  Google Scholar 

  • Groszhans H, Filipowicz W (2008) Molecular biology: the expanding world of small RNAs. Nature 451:414–416

    Google Scholar 

  • Guo N, Ye WW, Wu XL, Shen DY, Wang YC, Xing H, Dou DL (2011) Microarray profiling reveals microRNAs involving soybean resistance to Phytophthora sojae. Genome 54(11):954–958

    CAS  PubMed  Google Scholar 

  • Hajyzadeh M, Turktas M, Khawar KM, Unver T (2015) miR408 over-expression causes increased drought tolerance in chickpea. Gene 555(2):186–193

    CAS  PubMed  Google Scholar 

  • Hamilton AJ, Baulcombe DC (1999) A species of small antisense RNA in post-transcriptional gene silencing in plants. Science 286:950–952

    CAS  PubMed  Google Scholar 

  • Han Y, Zheng HU, Zheng D, Gao Y (2014) Analysis of promoters of microRNAs from a Glycine max degradome library. J Zhejiang Univ Sci B (Biomed Biotechnol) 15:125–132

    CAS  Google Scholar 

  • Holt DB, Gupta V, Meyer D, Abel NB, Andersen SU, Stougaard J, Markmann K (2015) Micro RNA 172 (miR172) signals epidermal infection and is expressed in cells primed for bacterial invasion in Lotus japonicus roots and nodules. New Phytopathol 208:241–256

    CAS  Google Scholar 

  • Huang SC, Lu GH, Tang CY, Ji YJ, Tan GS, Hu DQ, Cheng J, Wang GH, Qi JL, Yang YH (2017) Identification and comparative analysis of aluminum-induced microRNAs conferring plant tolerance to aluminum stress in soybean. Biol Plant 62:97–108

    CAS  Google Scholar 

  • Jia X, Mendu V, Tang G (2010) An array platform for identification of stress-responsive microRNAs in plants. Methods Mol Biol 639:253–269

    CAS  PubMed  Google Scholar 

  • Jones-Rhoades MW, Bartel DP (2004) Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol Cell 14(6):787–799

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Kantar M, Lucas SJ, Budak H (2011) miRNA expression patterns of Triticum dicoccoides in response to shock drought stress. Planta 233(3):471–484

    CAS  PubMed  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 1819:137–148

    CAS  PubMed  Google Scholar 

  • Koptekin D, Aktas LY (2016) Identification of conserved miRNAs and their target genes in faba bean by EST based homology analysis. Eur J Sci Technol 5:1–6

    Google Scholar 

  • Kulcheski FR, de Oliveira LF, Molina LG, Almerão MP, Rodrigues FA, Marcolino J, Barbosa JF, Stolf-Moreira R, Nepomuceno AL, Marcelino-Guimarães FC, Abdelnoor RV (2011) Identification of novel soybean microRNAs involved in abiotic and biotic stresses. BMC Genom 12:307

    CAS  Google Scholar 

  • Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854

    CAS  PubMed  Google Scholar 

  • Li WX, Oono Y, Zhu J, He XJ, Wu JM, Iida K, Lu XY, Cui X, Jin H, Zhu JK (2008) The Arabidopsis NFYA5 transcription factor is regulated transcriptionally and post transcriptionally to promote drought resistance. Plant Cell 20:2238–2251

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li T, Li H, Zhang YX, Liu JY (2010) Identification and analysis of seven H2O2-responsive miRNAs and 32 new miRNAs in the seedlings of rice (Oryza sativa L. ssp. indica). Nucleic Acids Res 39:2821–2833

    PubMed  PubMed Central  Google Scholar 

  • Li H, Dong Y, Yin H, Wang N, Yang J, Liu X, Wang Y, Wu J, Li X (2011) Characterization of the stress associated microRNAs in Glycine max by deep sequencing. BMC Plant Biol 11:1–12

    Google Scholar 

  • Li F, Pignatta D, Bendix C, Brunkard JO, Cohn MM, Tung J, Sun H, Kumar P, Baker B (2012a) MicroRNA regulation of plant innate immune receptors. Proc Nat Acad Sci USA 109:1790–1795

    CAS  PubMed  Google Scholar 

  • Li X, Wang X, Zhang S, Liu D, Duan Y, Dong W (2012b) Identification of soybean microRNAs involved in soybean cyst nematode infection by deep sequencing. PLoS One 7:e39650

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu HH, Tian X, Li YJ, Wu CA, Zheng CC (2008) Microarray-based analysis of stress-regulated microRNAs in Arabidopsis thaliana. RNA 14:836–843

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu T, Fang C, Ma Y, Shen Y, Li C, Li Q, Wang M, Liu S, Zhang J, Zhou Z, Yang R (2016) Global investigation of the co-evolution of MIRNA genes and microRNA targets during soybean domestication. Plant J 85:396–409

    CAS  PubMed  Google Scholar 

  • Llave C, Kasschau KD, Rector MA, Carrington JC (2002) Endogenous and silencing-associated small RNAs in plants. Plant Cell 14:1605–1619

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lu XY, Huang XL (2008) Plant miRNAs and abiotic stress responses. Biochem Biophys Res Commun 368:458–462

    CAS  PubMed  Google Scholar 

  • Mallory AC, Vaucheret H (2006) Functions of microRNAs and related small RNAs in plants. Nat Gen 38:S31–S36

    CAS  Google Scholar 

  • Meyers BC, Axtell MJ, Bartel B, Bartel DP, Baulcombe D, Bowman JL, Cao X, Carrington JC, Chen X, Green PJ, Griffiths-Jones S, Jacobsen SE, Mallory AC, Martienssen RA, Poethig RS, Qi Y, Vaucheret H, Voinnet O, Watanabe Y, Weigel D, Zhu JK (2008) Criteria for annotation of plant microRNAs. Plant Cell 20:3186–3190

    CAS  PubMed  PubMed Central  Google Scholar 

  • Min X, Zhang Z, Liu Y, Wei X, Liu Z, Wang Y, Liu W (2017) Genome-wide development of microRNA-based SSR markers in Medicago truncatula with their transferability analysis and utilization in related legume species. Int J Mol Sci 18(11):2440

    PubMed Central  Google Scholar 

  • Miransari M (2015) Abiotic and biotic stresses in soybean production. Soybean Prod 1:4. https://doi.org/10.1016/b978-0-12-801536-0.00014-1(ISBN: 978-0-12-801536-0)

    Article  Google Scholar 

  • Mitsuda N, Ohme-Takagi M (2009) Functional analysis of transcription factors in Arabidopsis. Plant Cell Physiol 50:1232–1248

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mochida K, Yoshida T, Sakurai T, Yamaguchi-Shinozaki K, Shinozaki K, Tran LSP (2010) LegumeTFDB: an integrative database of Glycine max, Lotus japonicus and Medicago truncatula transcription factors. Bioinformatics 26(2):290–291

    CAS  PubMed  Google Scholar 

  • Nageshbabu R, Usha Jyothi MN, Sharadamma N (2013) Expression of miRNAs confers enhanced tolerance to drought and salt stress in finger millet (Eleusine coracana). J Stress Physiol Biochem 9:220–231

    Google Scholar 

  • Nanjo Y, Maruyama K, Yasue H, Yamaguchi-Shinozaki K, Shinozaki K, Komatsu S (2011) Transcriptional responses to flooding stress in roots including hypocotyl of soybean seedlings. Plant Mol Biol 77:129–144

    CAS  PubMed  Google Scholar 

  • Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439

    CAS  PubMed  Google Scholar 

  • Ng DW, Zhang C, Miller M, Palmer G, Whiteley M, Tholl D, Chen ZJ (2011) cis- and trans-regulation of miR163 and target genes confers natural variation of secondary metabolites in two Arabidopsis species and their allopolyploids. Plant Cell 23:1729–1740

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ni Z, Hu Z, Jiang Q, Zhang H (2012) Over-expression of gma-MIR394a confers tolerance to drought in transgenic Arabidopsis thaliana. Biochem Biophys Res Commun 427:330–335

    CAS  PubMed  Google Scholar 

  • Ni Z, Hu Z, Jiang Q, Zhang H (2013) GmNFYA3, a target gene of miR169, is a positive regulator of plant tolerance to drought stress. Plant Mol Biol 82:113–129

    CAS  PubMed  Google Scholar 

  • Pant BD, Buhtz A, Kehr J, Scheible WR (2008) microRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J 53:731–738

    CAS  PubMed  PubMed Central  Google Scholar 

  • Phillips JR, Dalmay T, Bartels D (2007) The role of small RNAs in abiotic stress. FEBS Lett 581:3592–3597

    CAS  PubMed  Google Scholar 

  • Quach TN, Nguyen HT, Valliyodan B, Joshi T, Xu D, Nguyen HT (2015) Genome-wide expression analysis of soybean NF-Y genes reveals potential function in development and drought response. Mol Genet Genom 290:1095–1115

    CAS  Google Scholar 

  • Ramesh SV, Admane N, Husain SM (2013) Small RNAs landscape (sRNAome) of soybean [Glycine max (L.)]: biogenesis, vital functions and potential applications. Plant Knowl J 2:24–37

    Google Scholar 

  • Ramesh SV, Ratnaparkhe MB, Kumawat G, Gupta GK, Husain SM (2014) Plant miRNAome and antiviral resistance: a retrospective view and prospective challenges. Virus Genes 48:1–14

    CAS  PubMed  Google Scholar 

  • Ramesh SV, Ratnaparkhe MB, Husain SM, Bhatia VS (2015) Viral micro RNA transcriptomics (miRNAomics). Transcriptomics 3:108

    Google Scholar 

  • Ramesh SV, Chouhan BS, Kumar G, Praveen S (2016) Soybean derived miRNAs and Mungbean yellow mosaic India virus resistance. In: 16th biennial conference of the molecular and cellular biology of the soybean conference, Columbus, OH, August 7–10, 2016

  • Ramesh SV, Gupta GK, Husain SM (2016b) Soybean (Glycine max) miRNAs display proclivity to repress Begomovirus genomes. Curr Sci 110:424–428

    Google Scholar 

  • Ramesh SV, Chouhan BS, Gaurav K, Praveen S, Chand S (2017) Expression dynamics of Glycine max (L.) Merrill derived microRNAs (miRNAs) and their targets during Mungbean yellow mosaic India virus (MYMIV) infection. Physiol Mol Plant Pathol 100:13–22

    CAS  Google Scholar 

  • Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Genes Dev 16:1616–1626

    CAS  PubMed  PubMed Central  Google Scholar 

  • Reyes JL, Chua NH (2007) ABA induction of miR159 controls transcript levels of two MYB factors during Arabidopsis seed germination. Plant J 49:592–606

    CAS  PubMed  Google Scholar 

  • Rhoades M, Reinhart B, Lim L, Burge C, Bartel B, Bartel D (2002) Prediction of plant microRNA targets. Cell 110:513–520

    CAS  PubMed  Google Scholar 

  • Sahito ZA, Wang L, Sun Z, Yan Q, Zhang X, Jiang Q, Ullah I, Tong Y, Li X (2017) The miR172c-NNC1 module modulates root plastic development in response to salt in soybean. BMC Plant Biol 17(1):229

    PubMed  PubMed Central  Google Scholar 

  • Sattar S, Song Y, Anstead JA, Sunkar R, Thompson GA (2012) Cucumis melo microRNA expression profile during aphid herbivory in a resistant and susceptible interaction. Mol Plant Microbe Interact 25:839–848

    CAS  PubMed  Google Scholar 

  • Shivaprasad PV, Chen HM, Patel K, Bond DM, Santos BA, Baulcombe DC (2012) A microRNA superfamily regulates nucleotide binding site-leucine-rich repeats and other mRNAs. Plant Cell 24:859–874

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shuai P, Liang D, Tang S, Zhang Z, Ye CY, Su Y, Xia X, Yin W (2014) Genome-wide identification and functional prediction of novel and drought-responsive lincRNAs in Populus trichocarpa. J Exp Bot 65(17):4975–4983

    CAS  PubMed  PubMed Central  Google Scholar 

  • Soares-Cavalcanti NM, Belarmino LC, Kido EA, Pandolfi V, Marcelino-Guimarães FC, Rodrigues FA, Pereira GA, Benko-Iseppon AM (2012) Overall picture of expressed Heat Shock Factors in Glycine max, Lotus japonicus and Medicago truncatula. Genet Mol Biol 35(1):247–259

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sosa-Valencia G, Palomar M, Covarrubias AA, Reyes JL (2017) The legume miR1514a modulates a NAC transcription factor transcript to trigger phasiRNA formation in response to drought. J Exp Bot 68:2013–2026

    CAS  PubMed  Google Scholar 

  • Srivastava S, Zheng Y, Kudapa H, Jagadeeswaran G, Hivrale V, Varshney RK, Sunkar R (2015) High throughput sequencing of small RNA component of leaves and inflorescence revealed conserved and novel miRNAs as well as phasiRNA loci in chickpea. Plant Sci 235:46–57

    CAS  PubMed  Google Scholar 

  • Subramanian S, Fu Y, Sunkar R, Barbazuk WB, Zhu JK, Yu O (2008) Novel and nodulation-regulated microRNAs in soybean roots. BMC Genom 9:160

    Google Scholar 

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

    CAS  Google Scholar 

  • Sunkar R, Zhu JK (2004) Novel and stress-regulated microRNAs and other small RNAs from Arabidopsis. Plant Cell 16:2001–2019

    CAS  PubMed  PubMed Central  Google Scholar 

  • Swiezewski S, Liu F, Magusin A, Dean C (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462(7274):799

    CAS  PubMed  Google Scholar 

  • Tian B, Wang S, Todd TC, Johnson CD, Tang G, Trick HN (2017) Genome-wide identification of soybean microRNA responsive to soybean cyst nematodes infection by deep sequencing. BMC Genom 18:572

    Google Scholar 

  • Trindade I, Capitao C, Dalmay T, Fevereiro MP, Santos DM (2010) miR398 and miR408 are upregulated in response to water deficit in Medicago truncatula. Planta 231:705–716

    CAS  PubMed  Google Scholar 

  • Turner M, Yu O, Subramanian S (2012) Genome organization and characteristics of soybean microRNAs. BMC Genom 13:169

    CAS  Google Scholar 

  • Turner M, Nizampatnam NR, Baron M, Coppin S, Damodaran S, Adhikari S, Arunachalam SP, Yu O, Subramanian S (2013) Ectopic expression of miR160 results in auxin hypersensitivity, cytokinin hyposensitivity, and inhibition of symbiotic nodule development in soybean. Plant Physiol 162:2042–2055

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tworak A, Urbanowicz A, Podkowinski J, Kurzynska-Kokorniak A, Koralewska N, Figlerowicz M (2016) Six Medicago truncatula Dicer-like protein genes are expressed in plant cells and upregulated in nodules. Plant Cell Rep 35:1043–1052

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Li P, Cao X, Wang X, Zhang A, Li X (2009) Identification and expression analysis of miRNAs from nitrogen-fixing soybean nodules. Biochem Biophys Res Commun 378:799–803

    CAS  PubMed  Google Scholar 

  • Wang Y, Zhang C, Hao Q, Sha A, Zhou R, Zhou X, Yuan L (2013) Elucidation of miRNAs-mediated responses to low Nitrogen stress by deep sequencing of two soybean genotypes. PLoS One 8:e67423

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Yu W, Yang Y, Li X, Chen T, Liu T, Ma N, Yang X, Liu R, Zhang B (2015) Genome-wide analysis of tomato long non-coding RNAs and identification as endogenous target mimic for microRNA in response to TYLCV infection. Sci Rep 5:16946

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wei L, Zhang D, Xiang F, Zhang Z (2009) Differentially expressed miRNAs potentially involved in the regulation of defense mechanism to drought stress in maize seedlings. Int J Plant Sci 170:979–989

    CAS  Google Scholar 

  • Wong J, Gao L, Yang Y, Zhai J, Arikit S, Yu Y, Duan S, Chan V, Xiong Q, Yan J, Li S, Liu R, Wang Y, Tang G, Meyers BC, Chen X, Ma W (2014) Roles of small RNAs in soybean defense against Phytophthora sojae infection. Plant J 79:928–940

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu L, Zhou H, Zhang Q, Zhang J, Ni F, Liu C, Qi Y (2010) DNA methylation mediated by a microRNA pathway. Mol Cell 38:465–475

    CAS  PubMed  Google Scholar 

  • Xia K, Wang R, Ou X, Fang Z, Tian C, Duan J, Wang Y, Zhang M (2012) OsTIR1 and OsAFB2 downregulation via OsmiR393 over-expression leads to more tillers, early flowering and less tolerance to salt and drought in rice. PLoS One 7:1–10

    Google Scholar 

  • Xia X, Shao Y, Jiang J, Du X, Sheng L, Chen F, Fang W, Guan Z, Chen S (2015) MicroRNA expression profile during Aphid feeding in Chrysanthemum (Chrysanthemum morifolium). PLoS One 10:e0143720

    PubMed  PubMed Central  Google Scholar 

  • Xin M, Wang Y, Yao Y, Song N, Hu Z, Qin D, Xie C, Peng H, Ni Z, Sun Q (2011) Identification and characterization of wheat long non-protein coding RNAs responsive to powdery mildew infection and heat stress by using microarray analysis and SBS sequencing. BMC Plant Biol 11(1):61

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu MY, Zhang L, Li WW, Hu X, Wang MB, Fan YL, Zhang CY, Wang L (2014) Stress-induced early flowering is mediated by miR169 in Arabidopsis thaliana. J Exp Bot 65:89–101

    CAS  PubMed  Google Scholar 

  • Xu S, Liu N, Mao W, Hu Q, Wang G, Gong Y (2016) Identification of chilling-responsive microRNAs and their targets in vegetable soybean (Glycine max L.). Sci Rep 6:26619

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Y, Zhu S, Liu F, Wang W, Wang X, Han G, Cheng B (2018) Identification of Arbuscular Mycorrhiza fungi responsive microRNAs and their regulatory network in maize. Int J Mol Sci 19:3201

    PubMed Central  Google Scholar 

  • Yan K, Liu P, Wu CA, Yang GD, Xu R, Guo QH, Haung JG, Zheng CC (2012) Stress-induced alternative splicing provides a mechanism for the regulation of microRNA processing in Arabidopsis thaliana. Mol Cell 48:521–531

    CAS  PubMed  Google Scholar 

  • Yan Z, Hossain MS, Wang J, Valdés-López O, Liang Y, Libault M, Qiu L, Stacey G (2013) miR172 regulates soybean nodulation. Mol Plant Microbe Interact 26(12):1371–1377

    CAS  PubMed  Google Scholar 

  • Yan Z, Hossain MS, Arikit S, Valdés-López O, Zhai J, Wang J, Libault M, Ji T, Qiu L, Meyers BC, Stacey G (2015) Identification of microRNAs and their mRNA targets during soybean nodule development: functional analysis of the role of miR393j-3p in soybean nodulation. New Phytol 207:748–759

    CAS  PubMed  Google Scholar 

  • Yang WC, Katinakis P, Hendriks P, Smolders A, de Vries F, Spee J, van Kammen A, Bisseling T, Franssen H (1993) Characterization of GmENOD40, a gene showing novel patterns of cell-specific expression during soybean nodule development. Plant J 3:573–585

    CAS  PubMed  Google Scholar 

  • Yin X, Wang J, Cheng H, Wang X, Yu D (2013) Detection and evolutionary analysis of soybean miRNAs responsive to Soybean Mosaic Virus. Planta 237:1213–1225

    CAS  PubMed  Google Scholar 

  • Zeng HQ, Zhu YY, Huang SQ, Yang ZM (2010) Analysis of phosphorus-deficient responsive miRNAs and cis-elements from soybean (Glycine max L.). J Plant Physiol 167:1289–1297

    CAS  PubMed  Google Scholar 

  • Zeng QY, Yang CY, Ma QB, Li XP, Dong WW, Nian H (2012) Identification of wild soybean miRNAs and their target genes responsive to aluminum stress. BMC Plant Biol 12:1

    Google Scholar 

  • Zhai J, Jeong DH, De Paoli E, Park S, Rosen BD, Li Y, González AJ, Yan Z, Kitto SL, Grusak MA, Jackson S (2011) MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev 25:2540–2553

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang YC, Chen YQ (2013) Long noncoding RNAs: new regulators in plant development. Biochem Biophys Res Commun 436:111–114

    CAS  PubMed  Google Scholar 

  • Zhang B, Wang Q (2016) MicroRNA, a new target for engineering new crop varieties. Bioengineered 7:7–10

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang BH, Pan XP, Wang QL, Cobb GP, Anderson TA (2005) Identification and characterization of new plant microRNAs using EST analysis. Cell Res 15:336–360

    PubMed  Google Scholar 

  • Zhang Z, Wei L, Zou X, Tao Y, Liu Z, Zheng Y (2008) Submergence-responsive MicroRNAs are potentially involved in the regulation of morphological and metabolic adaptations in maize root cells. Ann Bot 102:509–519

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Chia JM, Kumari S, Stein JC, Liu Z, Narechania A, Maher CA, Guill K, McMullen MD, Ware D (2009) A genome-wide characterization of microRNA genes in maize. PLoS Genet 5:e1000716

    PubMed  PubMed Central  Google Scholar 

  • Zhang S, Wang Y, Li K, Zou Y, Chen L, Li X (2014) Identification of cold-responsive miRNAs and their target genes in nitrogen-fixing nodules of soybean. Int J Mol Sci 15:13596–13614

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao BT, Liang RQ, Ge LF, Li W, Xiao HS, Lin HX, Ruan KC, Jin YX (2007) Identification of drought-induced microRNAs in rice. Biochem Biophys Res Commun 354:585–590

    CAS  PubMed  Google Scholar 

  • Zhao B, Ge L, Liang R, Li W, Ruan K, Lin H, Jin Y (2009) Members of miR-169 family are induced by high salinity and transiently inhibit the NF-YA transcription factor. BMC Mol Biol 10:29

    PubMed  PubMed Central  Google Scholar 

  • Zhao Y, Yu Y, Zhai J, Ramachandran V, Dinh TT, Meyers BC, Mo B, Chen X (2012) The Arabidopsis nucleotidyl transferase HESO1 uridylates unmethylated small RNAs to trigger their degradation. Curr Biol 22:689–694

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao M, Cai C, Zhai J, Lin F, Li L, Shreve J, Thimmapuram J, Hughes TJ, Meyers BC, Ma J (2015a) Coordination of microRNAs, phasiRNAs, and NBS-LRR Genes in response to a plant pathogen: insights from analyses of a set of soybean Rps gene near-isogenic lines. Plant Genome 8:1

    Google Scholar 

  • Zhao M, Meyers BC, Cai C, Xu W, Ma J (2015b) Evolutionary patterns and co-evolutionary consequences of MIRNA genes and microRNA targets triggered by multiple mechanisms of genomic duplications in soybean. Plant Cell 27:546–562

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng Y, Hivrale V, Zhang X, Valliyodan B, Lelandais-Brière C, Farmer AD, May GD, Crespi M, Nguyen HT, Sunkar R (2016) Small RNA profiles in soybean primary root tips under water deficit. BMC Syst Biol 10:126

    PubMed  PubMed Central  Google Scholar 

  • Zhou L, Liu Y, Liu Z, Kong D, Duan M, Luo L (2010) Genome-wide identification and analysis of drought-responsive microRNAs in Oryza sativa. J Exp Bot 61:4157–4168

    CAS  PubMed  Google Scholar 

  • Zhou J, Deng K, Cheng Y, Zhong Z, Tian L, Tang X, Tang A, Zheng X, Zhang T, Qi Y, Zhang Y (2017) CRISPR-Cas9 based genome editing reveals new insights into microRNA function and regulation in rice. Front Plant Sci 8:1598

    PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This study was funded by Indian Council of Agricultural Research (ICAR)-Indian Institute of Soybean Research (ICAR-IISR) sponsored project (Grant no.: 1.24/12).

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Ramesh, S.V., Govindasamy, V., Rajesh, M.K. et al. Stress-responsive miRNAome of Glycine max (L.) Merrill: molecular insights and way forward. Planta 249, 1267–1284 (2019). https://doi.org/10.1007/s00425-019-03114-5

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Keywords

  • Conserved miRNAs
  • Gene regulation
  • Legumes
  • miRNA evolution
  • Non-coding RNAs
  • Soybean
  • Stressors