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Transcriptome-wide identification and characterization of microRNAs responsive to phosphate starvation in Populus tomentosa

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Abstract

miRNAs (microRNAs) are ~ 21-nt non-coding small RNAs (sRNAs) that play crucial regulatory roles in plant biotic and abiotic stress responses. Phosphorus (Pi) deficiency constrains plant growth and reduces yields worldwide. To identify tree miRNAs and evaluate their functions in the response to low Pi, we identified 261 known and 31 candidate novel miRNA families from three sRNA libraries constructed from Populus tomentosa subjected to sufficient or Pi deficiency condition or to restoration of a sufficient Pi level after Pi deficiency. Pi deficiency resulted in significant changes in the abundance of TPM (transcript per million) of 65 known and 3 novel miRNAs. Interestingly, four miRNAs responsive to low N—miR167, miR394, miR171, and miR857—were found to be involved in the response to low Pi. Thirty-five known and one novel miRNAs responded dynamically to Pi fluctuations, suggesting their involvement in the response to Pi deficiency. miRNA clusters comprising 36 miRNAs were identified in 10 chromosomes. Intriguingly, nine pairs of sense and antisense miRNAs transcribed from the same loci were detected in P. tomentosa, which is the first such report in woody plants. Moreover, target genes of the known miRNAs and novel miRNA candidates with significantly changed abundance were predicted, and their functions were annotated. Degradome sequencing supported the identified targets of miRNAs in P. tomentosa. These findings will enhance our understanding of universal and specific molecular regulatory mechanisms of trees under nutrition stress and may facilitate improvement of the Pi utilization efficiency of woody plants.

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References

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Addo-Quaye C, Eshoo TW, Bartel DP, Axtell MJ (2008) Endogenous siRNA and miRNA targets identified by sequencing of the Arabidopsis degradome. Curr Biol 18:758–762

    CAS  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 Genomics 15:587–598

    CAS  PubMed  Google Scholar 

  • Allen E, Xie Z, Gustafson AM, Carrington JC (2005) microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121:207–221

    CAS  PubMed  Google Scholar 

  • Alptekin B, Akpinar BA, Budak H (2017) A comprehensive prescription for plant miRNA identification. Front Plant Sci 7:2058

    PubMed  PubMed Central  Google Scholar 

  • Altuvia Y, Landgraf P, Lithwick G, Elefant N, Pfeffer S, Aravin A, Brownstein MJ, Tuschl T, Margalit H (2005) Clustering and conservation patterns of human microRNAs. Nucleic Acids Res 33:2697–2706

    CAS  PubMed  PubMed Central  Google Scholar 

  • Aung K, Lin SI, Wu CC, Huang YT, Su CL, Chiou TJ (2006) pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol 141:1000–1011

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bari R, Datt PB, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999

    CAS  PubMed  PubMed Central  Google Scholar 

  • Barik S, Kumar A, Sarkar DS, Yadav S, Gautam V, Singh A, Singh S, Sarkar AK (2015) Coevolution pattern and functional conservation or divergence of miR167s and their targets across diverse plant species. Sci Rep 5:14611

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Chen L, Ren Y, Zhang Y, Xu J, Sun F, Zhang Z, Wang Y (2012a) Genome-wide identification and expression analysis of heat-responsive and novel microRNAs in Populus tomentosa. Gene 504:160–165

    CAS  PubMed  Google Scholar 

  • Chen L, Ren Y, Zhang Y, Xu J, Zhang Z, Wang Y (2012b) Genome-wide profiling of novel and conserved Populus microRNAs involved in pathogen stress response by deep sequencing. Planta 235:873–883

    CAS  PubMed  Google Scholar 

  • Chen L, Zhang Y, Ren Y, Xu J, Zhang Z, Wang Y (2012c) Genome-wide identification of cold-responsive and new microRNAs in Populus tomentosa by high-throughput sequencing. Biochem Biophys Res Commun 417:892–896

    CAS  PubMed  Google Scholar 

  • Chiou TJ (2007) The role of microRNAs in sensing nutrient stress. Plant Cell Environ 30:323–332

    CAS  PubMed  Google Scholar 

  • Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CL (2006) Regulation of phosphate homeostasis by MicroRNA in Arabidopsis. Plant Cell 18:412–421

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cui X, Xu SM, Mu DS, Yang ZM (2009) Genomic analysis of rice microRNA promoters and clusters. Gene 431:61–66

    CAS  PubMed  Google Scholar 

  • Duan Y, Li W, Wu W, Pan R, Zhou Y, Qi J, Lin L, Chen Z, Mao D, Liu H, Zhang D, Xue Y (2003) Genetic analysis and mapping of gene fzp(t) controlling spikelet differentiation in rice. Sci China C Life Sci 46:328–334

    CAS  PubMed  Google Scholar 

  • Fujii H, Chiou TJ, Lin SI, Aung K, Zhu JK (2005) A miRNA involved in phosphate-starvation response in Arabidopsis. Curr Biol 15:2038–2043

    CAS  PubMed  Google Scholar 

  • German MA, Pillay M, Jeong DH, Hetawal A, Luo S, Janardhanan P, Kannan V, Rymarquis LA, Nobuta K, German R, De Paoli E, Lu C, Schroth G, Meyers BC, Green PJ (2008) Global identification of microRNA-target RNA pairs by parallel analysis of RNA ends. Nat Biotechnol 26:941–946

    CAS  PubMed  Google Scholar 

  • Greb T, Clarenz O, Schafer E, Muller D, Herrero R, Schmitz G, Theres K (2003) Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. Genes Dev 17:1175–1187

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hackenberg M, Shi BJ, Gustafson P, Langridge P (2013) Characterization of phosphorus-regulated miR399 and miR827 and their isomirs in barley under phosphorus-sufficient and phosphorus-deficient conditions. BMC Plant Biol 13:214

    PubMed  PubMed Central  Google Scholar 

  • Hsieh LC, Lin SI, Shih AC, Chen JW, Lin WY, Tseng CY, Li WH, Chiou TJ (2009) Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol 151:2120–2132

    PubMed  PubMed Central  Google Scholar 

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

    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

    CAS  PubMed  Google Scholar 

  • Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:D480–D484

    CAS  PubMed  Google Scholar 

  • Kant S, Peng M, Rothstein SJ (2011) Genetic regulation by NLA and microRNA827 for maintaining nitrate-dependent phosphate homeostasis in Arabidopsis. PLoS Genet 7:e1002021

    CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Kawashima CG, Yoshimoto N, Maruyama-Nakashita A, Tsuchiya YN, Saito K, Takahashi H, Dalmay T (2009) Sulphur starvation induces the expression of microRNA-395 and one of its target genes but in different cell types. Plant J 57:313–321

    CAS  PubMed  Google Scholar 

  • Kurtoglu KY, Kantar M, Lucas SJ, Budak H (2013) Unique and conserved MicroRNAs in wheat chromosome 5D revealed by next-generation sequencing. PLoS One 8:e69801

    CAS  PubMed  PubMed Central  Google Scholar 

  • Laloi C, Apel K, Danon A (2004) Reactive oxygen signalling: the latest news. Curr Opin Plant Biol 7:323–328

    CAS  PubMed  Google Scholar 

  • Leaman D, Chen PY, Fak J, Yalcin A, Pearce M, Unnerstall U, Marks DS, Sander C, Tuschl T, Gaul U (2005) Antisense-mediated depletion reveals essential and specific functions of microRNAs in Drosophila development. Cell 121:1097–1108

    CAS  PubMed  Google Scholar 

  • Li R, Li Y, Kristiansen K, Wang J (2008a) SOAP: short oligonucleotide alignment program. Bioinformatics 24:713–714

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li YF, Zheng Y, Addo-Quaye C, Zhang L, Saini A, Jagadeeswaran G, Axtell MJ, Zhang W, Sunkar R (2010) Transcriptome-wide identification of microRNA targets in rice. Plant J 62:742–759

    CAS  PubMed  Google Scholar 

  • Li B, Qin Y, Duan H, Yin W, Xia X (2011) Genome-wide characterization of new and drought stress responsive microRNAs in Populus euphratica. J Exp Bot 62:3765–3779

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liang G, He H, Yu D (2012) Identification of nitrogen starvation-responsive microRNAs in Arabidopsis thaliana. PLoS One 7:e48951

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lin WY, Huang TK, Chiou TJ (2013) Nitrogen limitation adaptation a target of MicroRNA827, mediates degradation of plasma membrane-localized phosphate transporters to maintain phosphate homeostasis in Arabidopsis. Plant Cell 25:4061–4074

    CAS  PubMed  PubMed Central  Google Scholar 

  • Liu TY, Huang TK, Tseng CY, Lai YS, Lin SI, Lin WY, Chen JW, Chiou TJ (2012) PHO2-dependent degradation of PHO1 modulates phosphate homeostasis in Arabidopsis. Plant Cell 24:2168–2183

    CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408

    CAS  PubMed  Google Scholar 

  • Lu S, Sun YH, Shi R, Clark C, Li L, Chiang VL (2005) Novel and mechanical stress-responsive MicroRNAs in Populus trichocarpa that are absent from Arabidopsis. Plant Cell 17:2186–2203

    CAS  PubMed  PubMed Central  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 

  • Morin RD, O'Connor MD, Griffith M, Kuchenbauer F, Delaney A, Prabhu AL, Zhao Y, McDonald H, Zeng T, Hirst M, Eaves CJ, Marra MA (2008) Application of massively parallel sequencing to microRNA profiling and discovery in human embryonic stem cells. Genome Res 18:610–621

    CAS  PubMed  PubMed Central  Google Scholar 

  • Neill SJ, Desikan R, Clarke A, Hurst RD, Hancock JT (2002) Hydrogen peroxide and nitric oxide as signaling molecules in plants. J Exp Bot 53:1237–1247

    CAS  PubMed  Google Scholar 

  • Nguyen GN, Rothstein SJ, Spangenberg G, Kant S (2015) Role of microRNAs involved in plant response to nitrogen and phosphorous limiting conditions. Front Plant Sci 6:629

    PubMed  PubMed Central  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 BS, Seo JS, Chua NH (2014) NITROGEN LIMITATION ADAPTATION recruits PHOSPHATE2 to target the phosphate transporter PT2 for degradation during the regulation of Arabidopsis phosphate homeostasis. Plant Cell 26:454–464

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pei H, Ma N, Chen J, Zheng Y, Tian J, Li J, Zhang S, Fei Z, Gao J (2013) Integrative analysis of miRNA and mRNA profiles in response to ethylene in rose petals during flower opening. PLoS One 8:e64290

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ren Y, Chen L, Zhang Y, Kang X, Zhang Z, Wang Y (2012) Identification of novel and conserved Populus tomentosa microRNA as components of a response to water stress. Funct Integr Genomics 12:327–339

    CAS  PubMed  Google Scholar 

  • Ren Y, Sun F, Hou J, Chen L, Zhang Y, Kang X, Wang Y (2015) Differential profiling analysis of miRNAs reveals a regulatory role in low N stress response of Populus. Funct Integr Genomics 15:93–105

    CAS  PubMed  Google Scholar 

  • Rufty TW, Mackown CT, Israel DW (1990) Phosphorus stress effects on assimilation of nitrate. Plant Physiol 94:328–333

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schwab R, Voinnet O (2009) miRNA processing turned upside down. EMBO J 28:3633–3634

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D (2005) Specific effects of microRNAs on the plant transcriptome. Dev Cell 8:517–527

    CAS  PubMed  Google Scholar 

  • Seitz H, Royo H, Bortolin ML, Lin SP, Ferguson-Smith AC, Cavaille J (2004) A large imprinted microRNA gene cluster at the mouse Dlk1-Gtl2 domain. Genome Res 14:1741–1748

    CAS  PubMed  PubMed Central  Google Scholar 

  • Shin R, Berg RH, Schachtman DP (2005) Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Plant Cell Physiol 46:1350–1357

    CAS  PubMed  Google Scholar 

  • Shuai P, Liang D, Zhang Z, Yin W, Xia X (2013) Identification of drought-responsive and novel Populus trichocarpa microRNAs by high-throughput sequencing and their targets using degradome analysis. BMC Genomics 14:233

    CAS  PubMed  PubMed Central  Google Scholar 

  • Si J, Zhou T, Bo W, Xu F, Wu R (2014) Genome-wide analysis of salt-responsive and novel microRNAs in Populus euphratica by deep sequencing. BMC Genet 15(Suppl 1):S6

    PubMed  PubMed Central  Google Scholar 

  • Song Y, Wang Z, Bo W, Ren Y, Zhang Z, Zhang D (2012) Transcriptional profiling by cDNA-AFLP analysis showed differential transcript abundance in response to water stress in Populus hopeiensis. BMC Genomics 13:286

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sun X, Xie Z, Zhang C, Mu Q, Wu W, Wang B, Fang J (2016) A characterization of grapevine of GRAS domain transcription factor gene family. Funct Integr Genomics 16:347–363

    CAS  PubMed  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 

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

    CAS  PubMed  Google Scholar 

  • Valdes-Lopez O, Arenas-Huertero C, Ramirez M, Girard L, Sanchez F, Vance CP, Luis RJ, Hernandez G (2008) Essential role of MYB transcription factor: PvPHR1 and microRNA: PvmiR399 in phosphorus-deficiency signalling in common bean roots. Plant Cell Environ 31:1834–1843

    CAS  PubMed  Google Scholar 

  • Wang P, Grimm B (2015) Organization of chlorophyll biosynthesis and insertion of chlorophyll into the chlorophyll-binding proteins in chloroplasts. Photosynth Res 126:189–202

    CAS  PubMed  Google Scholar 

  • Wang C, Shangguan L, Kibet KN, Wang X, Han J, Song C, Fang J (2011) Characterization of microRNAs identified in a table grapevine cultivar with validation of computationally predicted grapevine miRNAs by miR-RACE. PLoS One 6:e21259

    CAS  PubMed  PubMed Central  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 

  • Xu J, Wong C (2008) A computational screen for mouse signaling pathways targeted by microRNA clusters. RNA 14:1276–1283

    CAS  PubMed  PubMed Central  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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yamasaki H, Hayashi M, Fukazawa M, Kobayashi Y, Shikanai T (2009) SQUAMOSA promoter binding protein-Like7 is a central regulator for copper homeostasis in Arabidopsis. Plant Cell 21:347–361

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yu J, Wang F, Yang GH, Wang FL, Ma YN, Du ZW, Zhang JW (2006) Human microRNA clusters: genomic organization and expression profile in leukemia cell lines. Biochem Biophys Res Commun 349:59–68

    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 

  • Zhang B, Pan X, Stellwag EJ (2008) Identification of soybean microRNAs and their targets. Planta 229:161–182

    CAS  PubMed  Google Scholar 

  • Zhang Y, Zhang R, Su B (2009) Diversity and evolution of MicroRNA gene clusters. Sci China C Life Sci 52:261–266

    CAS  PubMed  Google Scholar 

  • Zhang D, Song H, Cheng H, Hao D, Wang H, Kan G, Jin H, Yu D (2014) The acid phosphatase-encoding gene GmACP1 contributes to soybean tolerance to low-phosphorus stress. PLoS Genet 10:e1004061

    PubMed  PubMed Central  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 Commun 354:585–590

    CAS  PubMed  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:e29669

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou L, Chen J, Li Z, Li X, Hu X, Huang Y, Zhao X, Liang C, Wang Y, Sun L, Shi M, Xu X, Shen F, Chen M, Han Z, Peng Z, Zhai Q, Chen J, Zhang Z, Yang R, Ye J, Guan Z, Yang H, Gui Y, Wang J, Cai Z, Zhang X (2010) Integrated profiling of microRNAs and mRNAs: microRNAs located on Xq27.3 associate with clear cell renal cell carcinoma. PLoS One 5:e15224

    CAS  PubMed  PubMed Central  Google Scholar 

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Data archiving statement

The raw sequence data can be available at the NIH Short Read Archive database (http://www.ncbi.nlm.nih.gov/sra) under the BioProject ID PRJNA430018 (small RNA sequences) and PRJNA430019 (degradome sequences).

Funding

This work was supported by the Fundamental Research Funds for Central Universities (No.2015ZCQ-SW-01), National Natural Science Foundation of China (No. 31670671, 31470668).

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Authors and Affiliations

  1. Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Biotechnology, Beijing Forestry University, Beijing, 100083, People’s Republic of China

    Hai Bao, Hui Chen, Min Chen, Xiaowei Huo, Qianhui Xu & Yanwei Wang

  2. College of Life Sciences, Peking University, Beijing, 100871, People’s Republic of China

    Huimin Xu

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  1. Hai Bao
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  2. Hui Chen
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  3. Min Chen
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Correspondence to Yanwei Wang.

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Suppl. Fig. S1

Mature and precursor sequences and predicted stem-loop structures of novel miRNAs from Populous tomentosa. The sequences indicated in red color are miRNAs sequences, and sequences in green color are miRNA* sequences (PDF 3467 kb)

Suppl. Fig. S2

Target plots (t-plots) of miRNA targets in different categories confirmed by degradome sequencing. The normalized signature abundance throughout the length of the indicated transcripts is shown. Representative t-plots for class 0 (a), class 1 (b), class 2 (c), class 3 (d), and class 4 (e) categories are shown. Red peaks indicate signatures consistent with miRNA-directed cleavage. The solid lines and dot in miRNA:mRNA alignments indicate matched RNA base pairs and GU mismatch, respectively. On the left of the t-plots, the cleavage sites and raw tags are shown in the left and right column, respectively (PDF 210 kb)

Suppl. Fig. S3

GO enrichment analysis for the target genes of miRNAs with altered expression in P. tomentosa under Pi starvation stress. (a) GO enrichment of targets genes of miRNAs with altered expression in DP/KK. (b) GO enrichment of targets genes of miRNAs with altered expression in HF/DP (PDF 151 kb)

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Bao, H., Chen, H., Chen, M. et al. Transcriptome-wide identification and characterization of microRNAs responsive to phosphate starvation in Populus tomentosa. Funct Integr Genomics 19, 953–972 (2019). https://doi.org/10.1007/s10142-019-00692-1

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  • DOI: https://doi.org/10.1007/s10142-019-00692-1

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