Skip to main content
Log in

Association genetics in Populus reveals the interactions between Pto-miR160a and its target Pto-ARF16

  • Original Article
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

MicroRNAs (miRNAs) play important roles in the regulation of gene expression in various biological processes. However, the interactions between miRNAs and their targets are largely unknown in plants. As a powerful tool for identification of variation associated with traits, association genetics provides another strategy for exploration of interactions between miRNAs and their targets. Here, we conducted expression analysis and association mapping to evaluate the interaction between Pto-miR160a and its target Pto-ARF16 in Populus tomentosa. By examining the expression patterns of Pto-MIR160a and Pto-ARF16, we identified a significant, negative correlation between their expression levels, indicating that Pto-miR160a may affect the expression of Pto-ARF16. Among the single nucleotide polymorphisms (SNPs) identified in this study, one common SNP in the pre-miRNA region of Pto-miR160a altered its predicted secondary structure while another common SNP in the predicted miRNA target site changed the binding affinity of Pto-miR160a. Linkage disequilibrium (LD) analysis revealed low LD levels of Pto-MIR160a and Pto-ARF16, indicating that they are suitable for candidate gene-based association analysis. Single SNP-based association analysis identified 19 SNPs (false discovery rate Q < 0.05) in Pto-MIR160a and Pto-ARF16 associated with three phenotypic traits. Epistasis analysis further identified 36 SNP–SNP interactions between SNPs in Pto-MIR160a and SNPs in Pto-ARF16, reflecting the possible genetic interaction of Pto-miR160a and Pto-ARF16. Taking these results together, our study identified SNPs in Pto-MIR160a and Pto-ARF16 associated with tree growth and wood properties, providing SNPs with potential applications in marker-assisted breeding and evidence for the genetic interaction of Pto-miR160a and Pto-ARF16.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abdurakhmonov IY, Abdukarimov A (2008) Application of association mapping to understanding the genetic diversity of plan germplasm resources. Int J Plant Genom 2008:1–18

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635

    Article  PubMed  CAS  Google Scholar 

  • Brennecke J, Stark A, Russell RB, Cohen SM (2005) Principles of microRNA-target recognition. PLoS Biol 3:e85

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Carlborg O, Haley CS (2004) Epistasis: too often neglected in complex trait studies? Nat Rev Genet 5:618–625

    Article  PubMed  CAS  Google Scholar 

  • Chamary JV, Hurst LD (2009) The price of silent mutations. Sci Am 300(6):46–53

    Article  PubMed  CAS  Google Scholar 

  • Clop A, Marcq F, Takeda H, Pirottin D, Tordoir X, Bibe B, Bouix J, Caiment F, Elsen JM, Eychenne F, Larzul C, Laville E, Meish F, Milenkovic D, Tobin J, Charlier C, Georges M (2006) A mutation creating a potential illegitimate microRNA target site in the myostatin gene affects muscularity in sheep. Nat Genet 38:813–818

    Article  PubMed  CAS  Google Scholar 

  • Collins RL, Hu T, Wejse C, Sirugo G, Williams SM, Moore JH (2013) Multifactor dimensionality reduction reveals a three-locus epistatic interaction associated with susceptibility to pulmonary tuberculosis. BioData Min 6:4

    Article  PubMed  PubMed Central  Google Scholar 

  • Cordell HJ (2002) Epistasis: what it means, what it doesn’t mean, and statistical methods to detect it in humans. Hum Mol Genet 11:2463–2468

    Article  PubMed  CAS  Google Scholar 

  • Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:W155–W159

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Djerbi S, Aspeborg H, Nilsson P, Sundberg B, Mellerowicz E, Blomqvistn K, Teeri TT (2004) Identification and expression analysis of genes encoding putative cellulose synthases (CesA) in the hybrid aspen, Populus tremula (L.) × P. tremuloides (Michx.). Cellulose 11:301–312

    Article  CAS  Google Scholar 

  • Du Q, Xu B, Pan W, Gong C, Wang Q, Tian J, Li B, Zhang D (2013) Allelic variation in a cellulose synthase gene (PtoCesA4) associated with growth and wood properties in Populus tomentosa. G3 3:2069–2084

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Du Q, Xu B, Gong C, Yang X, Pan W, Tian J, Li B, Zhang D (2014) Variation in growth, leaf and wood-property traits of Chinese white poplar (Populus tomentosa Carr.), a major industrial tree species in Northern China. Can J Forest Res 44:326–339

    Article  Google Scholar 

  • Du Q, Tian J, Yang X, Pan W, Xu B, Li B, Ingvarsson PK, Zhang D (2015) Identification of additive, dominant, and epistatic variation conferred by key genes in cellulose biosynthesis pathway in Populus tomentosa. DNA Res 22:53–67

    Article  PubMed  PubMed Central  Google Scholar 

  • Duan R, Pak C, Jin P (2007) Single nucleotide polymorphism associated with mature miR-125a alters the processing of pri-miRNA. Hum Mol Genet 16:1124–1131

    Article  PubMed  CAS  Google Scholar 

  • Ehrenreich IM, Purugganan MD (2008) Sequence variation of microRNAs and their binding sites in Arabidopsis. Plant Physiol 146:1974–1982

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Far RKK, Sczakiel G (2003) The activity of siRNA in mammalian cells is related to structural target accessibility: a comparison with antisense oligonucleotides. Nucleic Acids Res 31:4417–4424

    Article  CAS  Google Scholar 

  • Gong J, Tong Y, Zhang HM, Wang K, Hu T, Shan G, Sun J, Guo AY (2012) Genome-wide identification of SNPs in microRNA genes and the SNP effects on microRNA target binding and biogenesis. Hum Mutat 33:254–263

    Article  PubMed  CAS  Google Scholar 

  • Hahn LW, Ritchie MD, Moore JH (2003) Multifactor dimensionality reduction software for detecting gene-gene and geneenvironment interactions. Bioinformatics 19:376–382

    Article  PubMed  CAS  Google Scholar 

  • Han J, Lee Y, Yeom KH, Nam JW, Heo I, Rhee JK, Sohn SY, Cho Y, Zhang BT, Kim VN (2006) Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell 125:887–901

    Article  PubMed  CAS  Google Scholar 

  • Hardy OJ, Vekemans X (2002) spagedi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620

    Article  CAS  Google Scholar 

  • Hu Z, Liang J, Wang Z, Tian T, Zhou X, Chen J, Miao R, Wang Y, Wang X, Shen H (2009) Common genetic variants in pre-microRNAs were associated with increased risk of breast cancer in Chinese women. Hum Mutat 30:79–84

    Article  PubMed  CAS  Google Scholar 

  • Hung PS, Chang KW, Kao SY, Chu TH, Liu CJ, Lin SC (2012) Association between the rs2910164 polymorphism in pre-mir-146a and oral carcinoma progression. Oral Oncol 48:404–408

    Article  PubMed  CAS  Google Scholar 

  • Ingvarsson PK (2005) Nucleotide polymorphism and linkage disequilibrium within and among natural populations of European aspen (Populus tremula L., Salicaceae). Genetics 169:945–953

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ingvarsson PK, Garcia MV, Luquez V, Hall D, Jansson S (2008) Nucleotide polymorphism and phenotypic associations within and around the phytochrome B2 locus in European aspen (Populus tremula, Salicaceae). Genetics 178:2217–2226

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ismail M, Soolanayakanahally RY, Ingvarsson PK, Guy RD, Jansson S, Silim SN, EI-Kassaby YA (2012) Comparative nucleotide diversity across North American and European Populus species. J Mol Evol 74:257–272

    Article  PubMed  CAS  Google Scholar 

  • Jiao Y, Wang Y, Xue D, Wang J, Yan M, Liu G, Dong G, Zeng D, Lu Z, Zhu X, Qian Q, Li J (2010) Regulation of OsSPL14 by OsmiR156 defines ideal plant architecture in rice. Nat Genet 42:541–544

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Kachanovsky DE, Filler S, Isaacson T, Hirschberg J (2012) Epistasis in tomato color mutations involves regulation of phytoene synthase 1 expression by cis-carotenoids. Proc Natl Acad Sci USA 109:19021–19026

    Article  PubMed  PubMed Central  Google Scholar 

  • Kalluri UC, DiFazio SP, Brunner AM, Tuskan GA (2007) Genome-wide analysis of Aux/IAA and ARF gene families in Populus trichocarpa. BMC Plant Biol 7:59

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kasschau KD, Xie Z, Allen E, Llave C, Chapman EJ, Krizan KA, Carrington JC (2003) P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA function. Dev Cell 4:205–217

    Article  PubMed  CAS  Google Scholar 

  • Kertesz M, Iovino N, Unnerstall U, Gaul U, Segal E (2007) The role of site accessibility in microRNA target recognition. Nat Genet 39:1278–1284

    Article  PubMed  CAS  Google Scholar 

  • Kimchi-Sarfaty C, Oh JM, Kim IW, Sauna ZE, Calcagno AM, Ambudkar SV, Gottesman MM (2007) A "silent" polymorphism in the MDR1 gene changes substrate specificity. Science 315(5811):525–528

    Article  PubMed  CAS  Google Scholar 

  • Kloosterman WP, Plasterk RHA (2006) The diverse functions of microRNAs in animal development and disease. Dev Cell 11:441–450

    Article  PubMed  CAS  Google Scholar 

  • Kozomara A, Griffiths-Jones S (2014) miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res 42:D68–D73

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liang H, Li WH (2009) Lowly expressed human microRNA genes evolve rapidly. Mol Biol Evol 26:1195–1198

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liu X, Huang J, Wang Y, Khanna K, Xie Z, Owen HA, Zhao D (2010) The role of floral organs in carpels, an Arabidopsis loss-of-function mutation in MicroRNA160a, in organogenesis and the mechanism regulating its expression. Plant J 62:416–428

    Article  PubMed  CAS  Google Scholar 

  • Liu Q, Wang H, Zhu L, Hu H, Sun Y (2013) Genome-wide identification and analysis of miRNA-related single nucleotide polymorphisms (SNPs) in rice. Rice 6:10

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Lu S, Sun Y, 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lu S, Li Q, Wei H, Chang MJ, Tunlaya-Anukit S, Kim H, Liu J, Song J, Sun YH, Yuan L, Yeh TF, Peszlen I, Ralph J, Sederoff RR, Chiang VL (2013) Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa. Proc Natl Acad Sci USA 110:10848–10853

    Article  PubMed  PubMed Central  Google Scholar 

  • Mackay TFC (2014) Epistasis and quantitative traits: using model organisms to study gene-gene interactions. Nat Rev Genet 15:22–33

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mallory AC, Bartel DP, Bartel B (2005) MicroRNA-directed regulation of Arabidopsis AUXIN RESPONSE FACTOR17 is essential for proper development and modulates expression of early auxin response genes. Plant Cell 17:1360–1375

    Article  PubMed  PubMed Central  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Natarajan C, Inoguchi N, Weber RE, Fago A, Moriyama H, Storz JF (2013) Epistasis among adaptive mutations in deer mouse hemoglobin. Science 340:1324–1327

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  PubMed Central  CAS  Google Scholar 

  • Rawlings-Goss RA, Campbell MC, Tishkoff SA (2014) Global population-specific variation in miRNA associated with cancer risk and clinical biomarkers. BMC Med Genomics 7:53

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doebley J, Kresovich S, Goodman MM, Buckler ES IV (2001) Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci USA 98:11479–11484

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP (2002) Prediction of plant microRNA targets. Cell 110:513–520

    Article  PubMed  CAS  Google Scholar 

  • Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  CAS  Google Scholar 

  • Ryan BM, Robles AI, Harris CC (2010) Genetic variation in microRNA networks: the implications for cancer research. Nat Rev Cancer 10:389–402

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Saunders MA, Liang H, Li WH (2007) Human polymorphism at micro-RNAs and microRNA target sites. Proc Natl Acad Sci USA 104:3300–3305

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sethupathy P, Collins FS (2008) MicroRNA target site polymorphisms and human disease. Trends Genet 24:489–497

    Article  PubMed  CAS  Google Scholar 

  • Shastry BS (2009) SNPs: impact on gene function and phenotype. Methods Mol Biol 578:3–22

    Article  PubMed  CAS  Google Scholar 

  • Slavov GT, DiFazio SP, Martin J, Schackwitz W, Muchero W, Rodgers-Melnick E, Lipphardt MF, Pennacchio CP, Hellsten U, Pennacchio LA, Gunter LE, Ranjan P, Vining K, Pomraning KR, Wilhelm LJ, Pellegrini M, Mockler TC, Freitag M, Geraldes A, El-Kassaby YA, Mansfield SD, Cronk QC, Douglas CJ, Strauss SH, Rokhsar D, Tuskan GA (2012) Genome resequencing reveals multiscale geographic structure and extensive linkage disequilibrium in the forest tree Populus trichocarpa. New Phytol 196:713–725

    Article  PubMed  CAS  Google Scholar 

  • Storey JD (2002) A direct approach to false discovery rates. J Roy Stat Soc Ser B 64:479–498

    Article  Google Scholar 

  • Storey JD, Tibshirani R (2003) Statistical significance for genomewide studies. Proc Natl Acad Sci USA 100:9440–9445

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Storey JD, Taylor JE, Siegmund D (2004) Strong control, conservative point estimation and simultaneous conservative consistency of false discovery rates: a unified approach. J Roy Stat Soc Ser B 66:187–205

    Article  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Tian JX, Du QZ, Chang MQ, Zhang DQ (2012) Allelic variation in PtGA20Ox associates with growth and wood properties in Populus spp. PLoS One 7:e53116

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tuominen H, Puech L, Fink S, Sundberg B (1997) A radial concentration gradient of indole-3-acetic acid is related to secondary xylem development in hybrid aspen. Plant Physiol 115:577–585

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wang JW, Wang LJ, Mao YB, Cai WJ, Xue HW, Chen XY (2005) Control of root cap formation by microRNA-targeted auxin response factors in Arabidopsis. Plant Cell 17(8):2204–2216

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang Y, Shen D, Bo S, Chen H, Zheng J, Zhu Q, Cai D, Helliwell C, Fan L (2010) Sequence variation and selection of small RNAs in domesticated rice. BMC Evol Biol 10:119

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang JW, Park MY, Wang LJ, Koo Y, Chen XY, Weigel D, Poethig S (2011) MiRNA control of vegetative phase change in trees. PLoS Genet 7:e1002012

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:188–193

    Article  Google Scholar 

  • Wegrzyn JL, Eckert AJ, Choi M, Lee JM, Stanton BJ, Sykes R, Davis MF, Tsai CJ, Neale DB (2010) Association genetics of traits controlling lignin and cellulose biosynthesis in black cottonwood (Populus trichocarpa, Salicaceae) secondary xylem. New Phytol 188:515–532

    Article  PubMed  CAS  Google Scholar 

  • Woodward AW, Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot 95:707–735

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xie M, Zhang S, Yu B (2015) MiRNA biogenesis, degradation and activity in plants. Cell Mol Life Sci 72:87–99

    Article  PubMed  CAS  Google Scholar 

  • Xu B, Tian J, Du Q, Gong C, Pan W, Zhang D (2014) Single nucleotide polymorphisms in a cellulose synthase gene (PtoCesA3) are associated with growth and wood properties in Populus tomentosa. Planta 240:1269–1286

    Article  PubMed  CAS  Google Scholar 

  • Xu Q, Liu J, Yuan Y (2015) Comprehensive assessment of the association between miRNA polymorphisms and gastric cancer risk. Mutat Res 763:148–160

    Article  CAS  Google Scholar 

  • Yang C, Xu M, Xuan L, Jiang X, Huang M (2014) Identification and expression analysis of twenty ARF genes in Populus. Gene 544:134–144

    Article  PubMed  CAS  Google Scholar 

  • Yu JM, Pressoir G, Briggs WH, Vroh Bi I, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nat Genet 38:203–208

    Article  PubMed  CAS  Google Scholar 

  • Zeng Y, Cullen BR (2004) Structural requirements for pre-microRNA binding and nuclear export by Exportin 5. Nucleic Acids Res 32:4776–4785

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zeng Y, Cullen BR (2005) Efficient processing of primary microRNA hairpins by Drosha requires flanking nonstructured RNA sequences. J Biol Chem 280:27595–27603

    Article  PubMed  CAS  Google Scholar 

  • Zhang DQ, Du QZ, Xu BH, Zhang ZY, Li BL (2010) The actin multigene family in Populus: organization, expression and phylogenetic analysis. Mol Genet Genom 284:105–119

    Article  CAS  Google Scholar 

  • Zhang DQ, Xu BH, Yang XH, Zhang ZY, Li BL (2011) The sucrose synthase gene family in Populus: structure, expression, and evolution. Tree Genet Genomes 7:443–456

    Article  Google Scholar 

Download references

Acknowledgments

This work was supported by the Fundamental Research Funds for the Central Universities (Project No. BLYJ201408), and Shandong Province Agriculture Improved Variety Project (No. 2012213) and the Project of the National Natural Science Foundation of China (No. 31170622).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Deqiang Zhang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Communicated by S. Hohmann.

Sequence data from this article have been deposited in the GenBank Data Library under the accession Nos. KT585479-KT585565.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tian, J., Chen, J., Li, B. et al. Association genetics in Populus reveals the interactions between Pto-miR160a and its target Pto-ARF16 . Mol Genet Genomics 291, 1069–1082 (2016). https://doi.org/10.1007/s00438-015-1165-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-015-1165-9

Keywords

Navigation