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Abstract: MicroRNAs (miRNAs) are endogenous small non-coding RNAs that play an important role in post-transcriptional gene regulation in plants and animals by targeting messenger RNAs (mRNAs) for cleavage or repressing translation of specific mRNAs. The first miRNA identified in plants, miRNA156 (miR156), targets the SQUAMOSA promoter-binding protein-like (SPL) transcription factors, which play critical roles in plant phase transition, flower and plant architecture, and fruit development. We identified multiple copies of MIR156 and SPL in the rice, Brachypodium, sorghum, maize, and foxtail millet genomes. Sequence and chromosomal synteny analysis showed that both MIR156s and SPLs are conserved across species in the grass family. Analysis of expression data of the SPLs in eleven juvenile and adult rice tissues revealed that four non-miR156-targeted genes were highly expressed and three miR156-targeted genes were only slightly expressed in all tissues/developmental stages. The remaining SPLs were highly expressed in the juvenile stage, but their expression was lower in the adult stage. It has been proposed that under strong selective pressure, non-miR156-targeted mRNA may be able to re-structure to form a miRNA-responsive element. In our analysis, some non-miR156-targeted SPLs (SPL5/8/10) had gene structure and gene expression patterns similar to those of miR156-targeted genes, suggesting that they could diversify into miR156-targeted genes. DNA methylation profiles of SPLs and MIR156s in different rice tissues showed diverse methylation patterns, and hypomethylation of non-CG sites was observed in rice endosperm. Our findings suggested that MIR156s and SPLs had different origination and evolutionary mechanisms: the SPLs appear to have resulted from vertical evolution, whereas MIR156s appear to have resulted from strong evolutionary selection on mature sequences.

禾本科microRNA156及其靶基因SPL转录因子的全基因组分析

[1]AgarwalG, GargV, KudapaH, et al., 2016. Genome-wide dissection of AP2/ERF and HSP90 gene families in five legumes and expression profiles in chickpea and pigeonpea. Plant Biotechnol J, 14(7):1563-1577.

[2]AxtellMJ, MeyersBC, 2018. Revisiting criteria for plant microRNA annotation in the era of big data. Plant Cell, 30(2):272-284.

[3]AxtellMJ, SnyderJA, BartelDP, 2007. Common functions for diverse small RNAs of land plants. Plant Cell, 19(6):1750-1769.

[4]BarrettT, TroupDB, WilhiteSE, et al., 2011. NCBI GEO: archive for functional genomics data sets—10 years on. Nucleic Acids Res, 39(S1):D1005-D1010.

[5]BartelDP, 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116(2):281-297.

[6]BennetzenJL, SchmutzJ, WangH, et al., 2012. Reference genome sequence of the model plant setaria. Nat Biotechnol, 30(6):555-561.

[7]BirkenbihlRP, JachG, SaedlerH, et al., 2005. Functional dissection of the plant-specific SBP-domain: overlap of the DNA-binding and nuclear localization domains. J Mol Biol, 352(3):585-596.

[8]BonnetE, HeY, BilliauK, et al., 2010. TAPIR, a web server for the prediction of plant microRNA targets, including target mimics. Bioinformatics, 26(12):1566-1568.

[9]CardonG, HöhmannS, KleinJ, et al., 1999. Molecular characterisation of the Arabidopsis SBP-box genes. Gene, 237(1):91-104.

[10]ChangJZ, YanFX, QiaoLY, et al., 2016. Genome-wide identification and expression analysis of SBP-box gene family in Sorghum bicolor L. Hereditas (Beijing), 38(6):569-580 (in Chinese).

[11]CuperusJT, FahlgrenN, CarringtonJC, 2011. Evolution and functional diversification of MIRNA genes. Plant Cell, 23(2):431-442.

[12]DaiXB, ZhaoPX, 2011. PsRNATarget: a plant small RNA target analysis server. Nucleic Acids Res, 39(S2):W155-W159.

[13]EdgarRC, 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res, 32(5):1792-1797.

[14]FengSH, JacobsenSE, ReikW, 2010. Epigenetic reprogramming in plant and animal development. Science, 330(6004):622-627.

[15]FornaraF, CouplandG, 2009. Plant phase transitions make a SPLash. Cell, 138(4):625-627.

[16]Franco-ZorrillaJM, ValliA, TodescoM, et al., 2007. Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet, 39(8):1033-1037.

[17]GautBS, le Thierry D'EnnequinM, PeekAS, et al., 2000. Maize as a model for the evolution of plant nuclear genomes. Proc Natl Acad Sci USA, 97(13):7008-7015.

[18]GielenH, RemansT, VangronsveldJ, et al., 2016. Toxicity responses of Cu and Cd: the involvement of miRNAs and the transcription factor SPL7. BMC Plant Biol, 16:145.

[19]GouJY, FelippesFF, LiuCJ, et al., 2011. Negative regulation of anthocyanin biosynthesis in Arabidopsis by a miR156-targeted SPL transcription factor. Plant Cell, 23(4):1512-1522.

[20]GuoAY, HeK, LiuD, et al., 2005. DATF: a database of Arabidopsis transcription factors. Bioinformatics, 21(10):2568-2569.

[21]GuoAY, ZhuQH, GuXC, et al., 2008. Genome-wide identification and evolutionary analysis of the plant specific SBP-box transcription factor family. Gene, 418(1-2):1-8.

[22]HuijserP, SchmidM, 2011. The control of developmental phase transitions in plants. Development, 138(19):4117-4129.

[23]International Rice Genome Sequencing Project, SasakiT, 2005. The map-based sequence of the rice genome. Nature, 436(7052):793-800.

[24]JeongDH, ParkS, ZhaiJX, et al., 2011. Massive analysis of rice small RNAs: mechanistic implications of regulated microRNAs and variants for differential target RNA cleavage. Plant Cell, 23(12):4185-4207.

[25]JiaoYP, SongWB, ZhangM, et al., 2011. Identification of novel maize miRNAs by measuring the precision of precursor processing. BMC Plant Biol, 11:141.

[26]JiaoYQ, WangYH, XueDW, et al., 2010. Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet, 42(6):541-544.

[27]JinJH, WangM, ZhangHX, et al., 2018. Genome-wide identification of the AP2/ERF transcription factor family in pepper (Capsicum annuum L.). Genome, 61(9):663-674.

[28]KimuraM, 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol, 16(2):111-120.

[29]KozomaraA, Griffiths-JonesS, 2011. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res, 39(S1):D152-D157.

[30]KropatJ, TotteyS, BirkenbihlRP, et al., 2005. A regulator of nutritional copper signaling in Chlamydomonas is an SBP domain protein that recognizes the GTAC core of copper response element. Proc Natl Acad Sci USA, 102(51):18730-18735.

[31]KumarS, StecherG, LiM, et al., 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol, 35(6):1547-1549.

[32]LalS, PacisLB, SmithHMS, 2011. Regulation of the SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE genes/microRNA156 module by the homeodomain proteins PENNYWISE and POUND-FOOLISH in Arabidopsis. Mol Plant, 4(6):1123-1132.

[33]LangmeadB, TrapnellC, PopM, et al., 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol, 10(3):R25.

[34]LarkinMA, BlackshieldsG, BrownNP, et al., 2007. Clustal W and Clustal X version 2.0. Bioinformatics, 23(21):2947-2948.

[35]LawJA, JacobsenSE, 2010. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet, 11(3):204-220.

[36]LeiKJ, LiuH, 2016. Research advances in plant regulatory hub miR156 and targeted SPL family. Chem Life, 36(1):13-20 (in Chinese).

[37]LiuMM, ShiZY, ZhangXH, et al., 2019. Inducible overexpression of Ideal Plant Architecture1 improves both yield and disease resistance in rice. Nat Plants, 5(4):389-400.

[38]LlaveC, XieZX, KasschauKD, et al., 2002. Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science, 297(5589):2053-2056.

[39]ManningK, TörM, PooleM, et al., 2006. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nat Genet, 38(8):948-952.

[40]MartinRC, LiuPP, GolovizninaNA, et al., 2010. microRNA, seeds, and darwin?: diverse function of miRNA in seed biology and plant responses to stress. J Exp Bot, 61(9):2229-2234.

[41]MeyersBC, AxtellMJ, BartelB, et al., 2008. Criteria for annotation of plant microRNAs. Plant Cell, 20(12):3186-3190.

[42]MiaoCB, WangZ, ZhangL, et al., 2019. The grain yield modulator miR156 regulates seed dormancy through the gibberellin pathway in rice. Nat Commun, 10:3822.

[43]MiuraK, IkedaM, MatsubaraA, et al., 2010. OsSPL14 promotes panicle branching and higher grain productivity in rice. Nat Genet, 42(6):545-549.

[44]MoreaEGO, da SilvaEM, GFFESilva, et al., 2016. Functional and evolutionary analyses of the miR156 and miR529 families in land plants. BMC Plant Biol, 16:40.

[45]Moreno-RisuenoMA, MartínezM, Vicente-CarbajosaJ, et al., 2007. The family of DOF transcription factors: from green unicellular algae to vascular plants. Mol Genet Genomics, 277(4):379-390.

[46]NozawaM, MiuraS, NeiM, 2012. Origins and evolution of microRNA genes in plant species. Genome Biol Evol, 4(3):230-239.

[47]PalatnikJF, AllenE, WuXL, et al., 2003. Control of leaf morphogenesis by microRNAs. Nature, 425(6955):257-263.

[48]PatersonAH, BowersJE, BruggmannR, et al., 2009. The Sorghum bicolor genome and the diversification of grasses. Nature, 457(7229):551-556.

[49]PengH, HeXJ, GaoJ, et al., 2016. Genome-wide identification and function analysis of SBP gene family in maize. Acta Agron Sin, 42(2):201-211 (in Chinese).

[50]RamamurthyRK, XiangQY, HsiehEJ, et al., 2018. New aspects of iron-copper crosstalk uncovered by transcriptomic characterization of Col-0 and the copper uptake mutant spl7 in Arabidopsis thaliana. Metallomics, 10(12):1824-1840.

[51]ReinhartBJ, WeinsteinEG, RhoadesMW, et al., 2002. MicroRNAs in plants. Genes Dev, 16(13):1616-1626.

[52]RieseM, HöhmannS, SaedlerH, et al., 2007. Comparative analysis of the SBP-box gene families in P. patens and seed plants. Gene, 401(1-2):28-37.

[53]SaeedAI, BhagabatiNK, BraistedJC, et al., 2006. TM4 microarray software suite. Methods Enzymol, 411:134-193.

[54]SchnablePS, WareD, FultonRS, et al., 2009. The B73 maize genome: complexity, diversity, and dynamics. Science, 326(5956):1112-1115.

[55]SchreiberAW, ShiBJ, HuangCY, et al., 2011. Discovery of barley miRNAs through deep sequencing of short reads. BMC Genomics, 12:129.

[56]ShigyoM, HasebeM, ItoM, 2006. Molecular evolution of the AP2 subfamily. Gene, 366(2):256-265.

[57]SollomeJ, MartinE, SethupathyP, et al., 2016. Environmental contaminants and microRNA regulation: transcription factors as regulators of toxicant-altered microRNA expression. Toxicol Appl Pharmacol, 312:61-66.

[58]SongJ, CaoXN, WangHL, et al., 2020. Genome wide identification and expression analysis of the SBP gene family in foxtail millet. J Nucl Agric Sci, 34(7):1409-1420 (in Chinese).

[59]SunkarR, ZhouXF, ZhengY, et al., 2008. Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biol, 8:25.

[60]TangGL, 2010. Plant microRNAs: an insight into their gene structures and evolution. Semin Cell Dev Biol, 21(8):782-789.

[61]TeixeiraFK, ColotV, 2010. Repeat elements and the Arabidopsis DNA methylation landscape. Heredity (Edinb), 105(1):14-23.

[62]The International Brachypodium Initiative, 2010. Genome sequencing and analysis of the model grass Brachypodium distachyon. Nature, 463(7282):763-768.

[63]VoinnetO, 2009. Origin, biogenesis, and activity of plant microRNAs. Cell, 136(4):669-687.

[64]WangJ, ZhouL, ShiH, et al., 2018. A single transcription factor promotes both yield and immunity in rice. Science, 361(6406):1026-1028.

[65]WillmannMR, PoethigRS, 2007. Conservation and evolution of miRNA regulatory programs in plant development. Curr Opin Plant Biol, 10(5):503-511.

[66]WuL, ZhangQQ, ZhouHY, et al., 2009. Rice microRNA effector complexes and targets. Plant Cell, 21(11):3421-3435.

[67]XieKB, WuCQ, XiongLZ, 2006. Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiol, 142(1):280-293.

[68]XieYR, LiuY, WangH, et al., 2017. Phytochrome-interacting factors directly suppress MIR156 expression to enhance shade-avoidance syndrome in Arabidopsis. Nat Commun, 8:348.

[69]XuL, YuanK, YuanM, et al., 2020. Regulation of rice tillering by RNA-directed DNA methylation at miniature inverted-repeat transposable elements. Mol Plant, 13(6):851-863.

[70]YanJP, ChiaJC, ShengHJ, et al., 2017. Arabidopsis pollen fertility requires the transcription factors CITF1 and SPL7 that regulate copper delivery to anthers and jasmonic acid synthesis. Plant Cell, 29(12):3012-3029.

[71]YangRX, LiPC, MeiHL, et al., 2019. Fine-tuning of miR528 accumulation modulates flowering time in rice. Mol Plant, 12(8):1103-1113.

[72]YaoSZ, YangZR, YangRX, et al., 2019. Transcriptional regulation of miR528 by OsSPL9 orchestrates antiviral response in rice. Mol Plant, 12(8):1114-1122.

[73]YuN, CaiWJ, WangSC, et al., 2010. Temporal control of trichome distribution by microRNA156-targeted SPL genes in Arabidopsis thaliana. Plant Cell, 22(7):2322-2335.

[74]YueEK, LiC, LiY, et al., 2017. MiR529a modulates panicle architecture through regulating SQUAMOSA PROMOTER BINDING-LIKE genes in rice (Oryza sativa). Plant Mol Biol, 94(4-5):469-480.

[75]ZemachA, KimMY, SilvaP, et al., 2010. Local DNA hypomethylation activates genes in rice endosperm. Proc Natl Acad Sci USA, 107(43):18729-18734.

[76]ZhangBH, PanXP, CobbGP, et al., 2006. Plant microRNA: a small regulatory molecule with big impact. Dev Biol, 289(1):3-16.

[77]ZhangGY, LiuX, QuanZW, et al., 2012. Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential. Nat Biotechnol, 30(6):549-554.

[78]ZhangY, SchwarzS, SaedlerH, et al., 2007. SPL8, a local regulator in a subset of gibberellin-mediated developmental processes in Arabidopsis. Plant Mol Biol, 63(3):429-439.

[79]ZilbermanD, GehringM, TranRK, et al., 2007. Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet, 39(1):61-69.

[80]ZukerM, 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res, 31(13):3406-3415.