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Novel insights into expansion and functional diversification of MIR169 family in tomato

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Abstract

Main conclusion

Expansion of MIR169 members by duplication and new mature forms, acquisition of new promoters, differential precursor-miRNA processivity and engaging novel targets increase the functional diversification of MIR169 in tomato.

Abstract

MIR169 family is an evolutionarily conserved miRNA family in plants. A systematic in-depth analysis of MIR169 family in tomato is lacking. We report 18 miR169 precursors, annotating new loci for MIR169a, b and d, as well as 3 novel mature isoforms (MIR169f/g/h). The family has expanded by both tandem- and segmental-duplication events during evolution. A tandem-pair MIR169b/b-1 and MIR169b-2/h is polycistronic in nature coding for three MIR169b isoforms and a new variant miR169h, that is evidently absent in the wild relatives S. pennellii and S. pimpinellifolium. Seven novel miR169 targets including RNA-binding protein, protein-phosphatase, aminotransferase, chaperone, tetratricopeptide-repeat-protein, and transcription factors ARF-9B and SEPELLATA-3 were established by efficient target cleavage in the presence of specific precursors as well as increased target abundance upon miR169 chelation by short-tandem-target-mimic construct in transient assays. Comparative antagonistic expression profiles of MIR169:target pairs suggest MIR169 family as ubiquitous regulator of various abiotic stresses (heat, cold, dehydration and salt) and developmental pathways. This regulation is partly brought about by acquisition of new promoters as demonstrated by promoter MIR169:GUS reporter assays as well as differential processivity of different precursors and miRNA cleavage efficiencies. Thus, the current study augments the functional horizon of MIR169 family with applications for stress tolerance in crops.

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References

  • Abrouk M, Zhang R, Murat F, Li A, Pont C, Mao L, Salse J (2012) Grass microRNA gene paleo history unveils new insights into gene dosage balance in sub-genome partitioning after whole-genome duplication. Plant Cell 24:1776–1792

    CAS  PubMed  PubMed Central  Google Scholar 

  • Addo-Quaye C, Miller W, Axtell MJ (2008) CleaveLand: a pipeline for using degradome data to find cleaved small RNA targets. Bioinformatics 25(1):130–131

    PubMed  PubMed Central  Google Scholar 

  • Altuvia Y, Landgraf P, Lithwick G, Elefant N (2005) Clustering and conservation patterns of human microRNAs. Nucleic Acids Res 33:2697–2706

    CAS  PubMed  PubMed Central  Google Scholar 

  • Axtell MJ, Bartel DP (2005) Antiquity of microRNAs and their targets in land plants. Plant Cell 17:1658–1673

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bai Q, Wang X, Chen X, Shi G, Liu Z, Guo C, Xiao K (2018) Wheat miRNA TaemiR408 acts as an essential mediator in plant tolerance to Pi deprivation and salt stress via modulating stress-associated physiological processes. Frontier Plant Sci 9:499. https://doi.org/10.3389/fpls.2018.00499

    Article  Google Scholar 

  • Baker CC, Sieber P, Wellmer F, Meyerowitz EM (2005) The early extra petals1 mutant uncovers a role for microRNA miR164c in regulating petal number in Arabidopsis. Curr Biol 15:303–315

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Bhan B, Koul A, Sharma D, Manzoor MM, Kaul S, Gupta S, Dhar MK (2019) Identification and expression profiling of miRNAs in two color variants of carrot (Daucus carota L.) using deep sequencing. PLoS ONE 14(3):e0212746. https://doi.org/10.1371/journal.pone.0212746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bologna NG, Schapire AL, Zhai J, Chorostecki U, Boisbouvier J, Meyers BC, Palatnik JF (2013) Multiple RNA recognition patterns during microRNA biogenesis in plants. Genome Res 23:1675–1689

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bouzroud S, Gouiaa S, Hu N, Bernadac A, Mila I, Bendaou N, Smouni A, Bouzayen M, Zouine M (2018) Auxin response factors (ARFs) are potential mediators of auxin action in tomato response to biotic and abiotic stress (Solanum lycopersicum). PLoS ONE 13(2):e0193517. https://doi.org/10.1371/journal.pone.0193517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buhtz A, Pieritz J, Springer F, Kehr J (2010) Phloem small RNAs, nutrient stress responses, and systemic mobility. BMC Plant Biol 10:64. https://doi.org/10.1186/1471-2229-10-64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calviño M, Messing J (2013) Discovery of MicroRNA169 gene copies in genomes of flowering plants through positional information. Genome Biol Evol 5:402–417

    PubMed  PubMed Central  Google Scholar 

  • Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10. https://doi.org/10.1186/1471-2229-4-10

    Article  PubMed  PubMed Central  Google Scholar 

  • Cardoso TCS, Alves TC, Caneschi CM, Santana DDRG, Fernandes-Brum CN, Reis GLD, Daude MM, Ribeiro THC, Gómez MMD, Lima AA, Gomes LAA, Gomes MS, Gandolfi PE, Amaral LRD, Chalfun-Júnior A, Maluf WR, de Souza Gomes M (2018) New insights into tomato microRNAs. Sci Rep 8(1):16069

    PubMed  PubMed Central  Google Scholar 

  • Castillejo C, Romera-Branchat M, Pelaz S (2005) A new role of the Arabidopsis SEPALLATA3 gene revealed by its constitutive expression. Plant J 43:586–596

    CAS  PubMed  Google Scholar 

  • Chorostecki U, Moro B, Rojas AML, Debernardi JM, Schapire AL, Notredame C, Palatnik JF (2017) Evolutionary footprints reveal insights into plant microRNA biogenesis. Plant Cell 29:1248–1261

    CAS  PubMed  PubMed Central  Google Scholar 

  • Combier JP, Frugier F, de Billy F, Boualem A, El-Yahyaoui F, Moreau S, Vernié 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 

  • Cuperus JT, Carbonell A, Fahlgren N, Garcia-Ruiz H, Burke RT, Takeda A, Sullivan CM, Gilbert SD, Montgomery TA, Carrington JC (2010) Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis. Nature Struct Mol Biol 17:997–1003

    CAS  Google Scholar 

  • de Jong M, Wolters-Arts M, Schimmel BC, Stultiens CL, de Groot PF, Powers SJ, Tikunov YM, Bovy AG, Mariani C, Vriezen WH, Rieu I (2015) Solanum lycopersicum AUXIN RESPONSE FACTOR 9 regulates cell division activity during early tomato fruit development. J Exp Bot 66(11):3405–3416

    PubMed  PubMed Central  Google Scholar 

  • Ding Q, Zeng J, He XQ (2016) MiR169 and its target PagHAP2-6 regulated by ABA are involved in poplar cambium dormancy. J Plant Physiol 198:1–9

    CAS  PubMed  Google Scholar 

  • Du Q, Zhao M, Gao W, Sun S, Li W (2017) microRNA/microRNA* complementarity is important for the regulation pattern of NFYA5 by miR169 under dehydration shock in Arabidopsis. Plant J 91:22–33

    CAS  PubMed  Google Scholar 

  • Gu M, Xu K, Chen A, Zhu Y, Tang G, Xu G (2010) Expression analysis suggests potential roles of microRNAs for phosphate and arbuscular mycorrhizal signaling in Solanum lycopersicum. Physiol Plant 138(2):226–237

    CAS  PubMed  Google Scholar 

  • Guan Q, Lu X, Zeng H, Zhang Y, Zhu J (2013) Heat stress induction of miR398 triggers a regulatory loop that is critical for thermotolerance in Arabidopsis. Plant J 74:840–851

    CAS  PubMed  Google Scholar 

  • Guddeti S, Zhang DC, Li AL, Leseberg CH, Kang H, Li XG, Zhai WX, Johns MA, Mao L (2005) Molecular evolution of the rice miR395 gene family. Cell Res 15:631–638

    CAS  PubMed  Google Scholar 

  • He Z, Wu J, Sun X, Dai M (2019) The maize clade A PP2C phosphatases play critical roles in multiple abiotic stress responses. Int J Mol Sci 20(14):3573. https://doi.org/10.3390/ijms20143573

    Article  CAS  PubMed Central  Google Scholar 

  • Heinnickel M, Kim R, Wittkopp T, Yang W, Walters K, Herbert S (2016) Tetratricopeptide repeat protein protects photosystem I from oxidative disruption during assembly. Proc Natl Acad Sci USA 113:2774–2779. https://doi.org/10.1073/pnas.1524040113

    Article  CAS  PubMed  Google Scholar 

  • Hivrale V, Zheng Y, Puli COR, Jagadeeswaran G, Gowdu K, Kakani VG, Barakat A, Sunkar R (2016) Characterization of drought- and heat-responsive microRNAs in switchgrass. Plant Sci 242:214–223

    CAS  PubMed  Google Scholar 

  • Hu Z, Xu F, Guan L, Qian P, Liu Y, Zhang H, Huang Y, Hou S (2014) The tetratricopeptide repeat-containing protein slow green1 is required for chloroplast development in Arabidopsis. J Exp Bot 4:1111–1123

    Google Scholar 

  • Hua W, Hua G, Han B (2009) Genome-wide survey and expression profiling of heat shock proteins and heat shock factors revealed overlapped and stress specific response under abiotic stresses in rice. Plant Sci 176:583–590

    Google Scholar 

  • Jagtap S, Shivaprasad PV (2014) Diversity, expression and mRNA targeting abilities of Argonaute-targeting miRNAs among selected vascular plants. BMC Genomics 15:1049. https://doi.org/10.1186/1471-2164-15-1049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kansal S, Mutum RD, Balyan SC, Arora MK, Singh AK, Mathur S, Raghuvanshi S (2015) Unique miRNome during anthesis in drought-tolerant indica rice var. Nagina 22. Planta 6:1543–1559

    Google Scholar 

  • Kulcheski FR, de Oliveira LF, Molina LG, Almerão MP, Rodrigues FA, Marcolino J, Barbosa JF, Moreira RS, Nepomuceno AL, Marcelino-Guimarães FC, Abdelnoor RV, Nascimento LC, Carazzolle MF, Gonçalo AG, Margis PR (2011) Identification of novel soybean microRNAs involved in abiotic and biotic stresses. BMC Genomics 12:307. https://doi.org/10.1186/1471-2164-12-307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee H, Yoo SJ, Lee JH, Kim W, Yoo SK, Fitzgerald H, Carrington JC, Ahn JH (2010) Genetic framework for flowering-time regulation by ambient temperature-responsive miRNAs in Arabidopsis. Nucleic Acids Res 38:3081–3093

    CAS  PubMed  PubMed Central  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 Y, Fu Y, Ji L, Wu C-A, Zheng C (2010) Characterization and expression analysis of the Arabidopsis mir169 family. Plant Sci 178:271–280

    CAS  Google Scholar 

  • Li S, Li K, Ju Z, Cao D, Fu D, Zhu H, Zhu B, Luo Y (2016) Genome-wide analysis of tomato NF-Y factors and their role in fruit ripening. BMC Genomics 17:36. https://doi.org/10.1186/s12864-015-2334-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Xie X, Li JC, Hou Y, Zhai L, Wang X, Fu Y, Liu R, Bian S (2017a) Conservation and diversification of the miR166 family in soybean and potential roles of newly identified miR166s. BMC Plant Biol 17:32. https://doi.org/10.1186/s12870-017-0983-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Y, Zhao SL, Li JL, Hu XH, Wang H, Cao XL, Xu YJ, Zhao ZX, Xiao ZY, Yang N, Fan J, Huang F, Wang WM (2017b) Osa-miR169 negatively regulates rice immunity against the blast fungus Magnaporthe oryzae. Front Plant Sci 8:2. https://doi.org/10.3389/fpls.2017.00002

    Article  PubMed  PubMed Central  Google Scholar 

  • Liang G, He H, Yu D (2012) Identification of nitrogen starvation responsive microRNAs in Arabidopsis thaliana. PLoS ONE 7(11):e48951. https://doi.org/10.1371/journal.pone.0048951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu Y, Yang X (2010) Computational identification of novel microRNAs and their targets in Vigna unguiculata. Comp Funct Genomics 1531–6912:F1220–1236

    Google Scholar 

  • Luan M, Xu M, Lu Y, Zhang L, Fan Y, Wang L (2015) Expression of zma-miR169 miRNAs and their target ZmNF-YA genes in response to abiotic stress in maize leaves. Gene 555:178–185

    CAS  PubMed  Google Scholar 

  • Maher C, Stein L, Ware D (2006) Evolution of Arabidopsis microRNA families through duplication events. Genome Res 16:510–519

    CAS  PubMed  PubMed Central  Google Scholar 

  • Marcinkowska M, Szymanski M, Krzyzosiak WJ, Kozlowski P (2011) Copy number variation of microRNA genes in the human genome. BMC Genomics 12:183. https://doi.org/10.1186/1471-2164-12-183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mateos JL, Bologna NG, Chorostecki U, Palatnik JF (2010) Identification of microRNA processing determinants by random mutagenesis of Arabidopsis MIR172a precursor. Curr Biol 20:49–54

    CAS  PubMed  Google Scholar 

  • Merchan F, Boualem A, Crespi M, Frugier F (2009) Plant poly-cistronic precursors containing non-homologous microRNAs target transcripts encoding functionally related proteins. Genome Biol 10:R136

    PubMed  PubMed Central  Google Scholar 

  • Mi S, Cai T, Hu Y, Chen Y, Hodges E, Ni F, Wu L, Li S, Zhou H, Long C, Chen S, Hannon GJ, Qi YJ (2008) Sorting of small RNAs into Arabidopsis Argonaute complexes is directed by the 5′ terminal nucleotide. Cell 133:116–127

    CAS  PubMed  PubMed Central  Google Scholar 

  • Mica E, Gianfranceschi L, Pè ME (2006) Characterization of five microRNA families in maize. J Exp Bot 57:2601–2612

    CAS  PubMed  Google Scholar 

  • Muoki RC, Paul A, Kumari A, Singh K, Kumar S (2012) An improved protocol for the isolation of RNA from roots of tea (Camellia sinensis (L.) O. Kuntze). Mol Biotechnol 52:82–88

    CAS  PubMed  Google Scholar 

  • Mutum RD, Kumar S, Balyan S, Kansal S, Mathur S, Raghuvanshi S (2016) Identification of novel miRNAs from drought tolerant rice variety Nagina 22. Sci Rep 6:30786

    CAS  PubMed  PubMed Central  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 

  • Pan Y, Niu M, Liang J, Lin E, Tong Z, Zhang J (2017) identification of heat-responsive miRNAs to reveal the miRNA-mediated regulatory network of heat stress response in Betula luminifera. Trees 31:1635–1652

    CAS  Google Scholar 

  • Pant BD, Musialak-Lange M, Nuc P, May P, Buhtz A, Kehr J, Walther D, Scheible WR (2009) Identification of nutrient-responsive Arabidopsis and rapeseed microRNAs by comprehensive real-time polymerase chain reaction profiling and small RNA sequencing. Plant Physiol 150:1541–1555

    PubMed  PubMed Central  Google Scholar 

  • Park S, Khamai P, Garcia-Cerdan JG, Melis A (2007) REP27, a tetratricopeptide repeat nuclear-encoded and chloroplast-localized protein, functions in D1/32-kD reaction center protein turnover and photosystem II repair from photodamage. Plant Physiol 143:1547–1560

    CAS  PubMed  PubMed Central  Google Scholar 

  • Paul A, Rao S, Mathur S (2016) The α-crystallin domain containing genes: Identification, phylogeny and expression profiling in abiotic stress, phytohormone response and development in tomato (Solanum lycopersicum). Front Plant Sci 7:246. https://doi.org/10.3389/fpls.2016.00426

    Article  Google Scholar 

  • Pelaz S, Tapia-López R, Alvarez-Buylla ER, Yanofsky MF (2001) Conversion of leaves into petals in Arabidopsis. Curr Biol 3:182–184

    Google Scholar 

  • Ravichandran S, Ragupathy R, Edwards T, Domaratzki M, Cloutier S (2019) MicroRNA-guided regulation of heat stress response in wheat. BMC Genomics 20(1):488

    PubMed  PubMed Central  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 

  • Salvador-Guirao R, Hsing YI, San Segundo B (2018) The polycistronic miR166k-166h positively regulates rice immunity via post-transcriptional control of EIN2. Front Plant Sci 9:337. https://doi.org/10.3389/fpls.2018.00337

    Article  PubMed  PubMed Central  Google Scholar 

  • Sarkar KN, Kim YK, Grover A (2009) Rice sHsp genes: genomic organization and expression profiling under stress and development. BMC Genomics 10:393. https://doi.org/10.1186/1471-2164-10-393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schottkowski M, Ratke J, Oster U, Nowaczyk M, Nickelsen J (2009) Pitt, a novel tetratricopeptide repeat protein involved in light-dependent chlorophyll biosynthesis and thylakoid membrane biogenesis in Synechocystis sp. PCC 6803. Mol Plant 2:1289–1297

    CAS  PubMed  Google Scholar 

  • Sheu-Gruttadauria J, Pawlica P, Klum SM, Wang S, Yario TA, Oakdale NTS, Steitz JA, MacRae IJ (2019) Structural basis for target-directed microRNA degradation. Mol Cell 75:1243–1255 (available at SSRN 3318944)

    CAS  PubMed  Google Scholar 

  • Shi T, Wang K, Yang P (2017) The evolution of plant microRNAs: insights from a basal eudicot sacred lotus. Plant J 89(3):442–457

    CAS  PubMed  Google Scholar 

  • Sieber P, Wellmer F, Gheyselinck J, Riechmann JL, Meyerowitz EM (2007) Redundancy and specialization among plant microRNAs: role of the MIR164 family in developmental robustness. Development 134:1051–1060

    CAS  PubMed  Google Scholar 

  • Singh J, Nagaraju J (2008) In silico prediction and characterization of microRNAs from red flour beetle (Tribolium castaneum). Insect Mol Biol 17(4):427–436

    CAS  PubMed  Google Scholar 

  • Song L, Axtell MJ, Fedoroff NV (2010) RNA secondary structural determinants of miRNA precursor processing in Arabidopsis. Curr Biol 20:37–41

    CAS  PubMed  Google Scholar 

  • Song S, Xu Y, Huang D, Ashraf MA, Li J, Hu W, Jin Z, Zeng C, Tang F, Xu B, Zeng H, Li Y, Xie J (2018) Identification and characterization of miRNA169 family members in banana (Musa acuminata L.) that respond to fusarium oxysporum f. sp. cubense infection in banana cultivars. Peer J 6:e6209. https://doi.org/10.7717/peerj.6209

    Article  CAS  PubMed  Google Scholar 

  • Sorin C, Declerck M, Christ A, Blein T, Ma L, Lelandais-Brière C, Njo MF, BeeckmanT CM, Hartmann C (2014) A miR169 isoform regulates specific NF-YA targets and root architecture in Arabidopsis. New Phytol 202:1197–1211

    CAS  PubMed  Google Scholar 

  • Starega-Roslan J, Koscianska E, Kozlowski P, Krzyzosiak WJ (2011) The role of the precursor structure in the biogenesis of microRNA. Cell Mol Life Sci 68:2859–2871

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sunkar R, Jagadeeswaran G (2008) In silico identification of conserved microRNAs in large number of diverse plant species. BMC Plant Biol 8:37. https://doi.org/10.1186/1471-2229-8-37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tanzer A, Stadler PF (2004) Molecular evolution of a microRNA cluster. J Mol Biol 339:327–335

    CAS  Google Scholar 

  • Thakur V, Wanchana S, Xu M, Bruskiewich R, Quick WP, Mosig A, Zhu XG (2011) Characterization of statistical features for plant microRNA prediction. BMC Genomics 12:108. https://doi.org/10.1186/1471-2164-12-108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thiebaut F, Rojas CA, Grativol C, Motta MR, Vieira T, Regulski M (2014) Genome-wide identification of microRNA and siRNA responsive to endophytic beneficial diazotrophic bacteria in maize. BMC Genomics 15:766. https://doi.org/10.1186/1471-2164-15-766

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Heredity 93:77–78

    CAS  Google Scholar 

  • Werner S, Wollmann H, Schneeberger K, Weigel D (2010) Structure determinants for accurate processing of miR172a in Arabidopsis thaliana. Curr Biol 20(1):42–48

    CAS  PubMed  Google Scholar 

  • Xu F, Liu Q, Chen L, Kuang J, Walk T, Wang J, Liao H (2013) Genome wide identification of soybean microRNAs and their targets reveals their organ-specificity and responses to phosphate starvation. BMC Genomics 14:66. https://doi.org/10.1186/1471-2164-14-66

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu MY, Zhang L, Li WW, Hu XL, Wang MB, Fan YL, Zhang CY, Wang L (2014) Stress-induced early flowering is mediated by miR169 in Arabidopsis thaliana. J Exp Bot 65(1):89–101

    CAS  PubMed  Google Scholar 

  • Yu C, Chen Y, Cao Y, Chen H, Wang J, Bi Y-M, Tian F, Yang F, Rothstein SJ, Zhou X (2018) Overexpression of miR169o, an overlapping microRNA in response to both nitrogen limitation and bacterial infection, promotes nitrogen use efficiency and susceptibility to bacterial blight in rice. Plant Cell Physiol 59:1234–1247

    CAS  PubMed  Google Scholar 

  • Zhai J, Arikit S, Simon SA, Kingham BF, Meyers BC (2014) Rapid construction of parallel analysis of RNA end (PARE) libraries for Illumina sequencing. Methods 67:84–90

    CAS  PubMed  Google Scholar 

  • Zhang BH, Pan XP, Cox SB, Cobb GP, Anderson TA (2006) Evidence that miRNAs are different from other RNAs. Cell Mol Life Sci 63:246–254

    CAS  PubMed  Google Scholar 

  • Zhang X, Zou Z, Gong P, Zhang J, Ziaf K, Li H, Xiao F, Ye Z (2011) Over-expression of microRNA169 confers enhanced drought tolerance to tomato. Biotechnol Lett 33:403–409

    CAS  PubMed  Google Scholar 

  • Zhao B, Liang R, Ge L, Li W, Xiao H, Lin H, Ruan K, Jin Y (2007) Identification of drought-induced microRNAs in rice. Biochem Biophys Res Comm 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. https://doi.org/10.1186/1471-2199-10-29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao Z, Zhang W, Yan J, Zhang J, Liu Z, Li X, Yi Y (2010) Over-expression of Arabidopsis DnaJ (Hsp40) contributes to NaCl-stress tolerance. African J Biotechnol 9:972–978. https://doi.org/10.5897/AJB09.1450

    Article  CAS  Google Scholar 

  • Zhao M, Ding H, Zhu JK, Zhang F, Li WX (2011) Involvement of miR169 in the nitrogen-starvation responses in Arabidopsis. New Phytol 190:906–915

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao M, Tai H, Sun S, Zhang F, Xu Y, Li WX (2012) Cloning and characterization of maize miRNAs involved in responses to nitrogen deficiency. PLoS ONE 7(1):e29669. https://doi.org/10.1371/journal.pone.0029669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou X, Wang G, Sutoh K, Zhu JK, Zhang W (2008) Identification of cold-inducible microRNAs in plants by transcriptome analysis. Biochim Biophys Acta 11:780–788

    Google Scholar 

  • Zhou R, Wang Q, Jiang F, Cao X, Sun M, Liu M, Wu Z (2016) Identification of miRNAs and their targets in wild tomato at moderately and acutely elevated temperatures by high-throughput sequencing and degradome analysis. Sci Rep 6:33777

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu H, Zhang Y, Tang R, Qu H, Duan X, Jiang Y (2019) Banana sRNAome and degradome identify microRNAs functioning in differential responses to temperature stress. BMC Genomics 20:33. https://doi.org/10.1186/s12864-018-5395-1

    Article  PubMed  PubMed Central  Google Scholar 

  • Zuker M (2003) M fold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 13:3406–3415

    Google Scholar 

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Acknowledgements

The authors acknowledge NIPGR core grant, phytotron facility, CIF and field area. CLN1621L seeds were provided by AVRDC, TAIWAN. SR and SJ acknowledge Department of Biotechnology (DBT) and University Grants Commission (UGC) Govt. of India, respectively, for the award of research fellowships.

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  1. National Institute of Plant Genome Research, Aruna Asaf Ali Marg, PO Box No. 10531, New Delhi, 110 067, India

    Sombir Rao, Sonia Balyan, Sarita Jha & Saloni Mathur

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  1. Sombir Rao
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Rao, S., Balyan, S., Jha, S. et al. Novel insights into expansion and functional diversification of MIR169 family in tomato. Planta 251, 55 (2020). https://doi.org/10.1007/s00425-020-03346-w

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