Genetic variations and miRNA-target interactions contribute to natural phenotypic variations in Populus.

Variation in regulatory factors, including microRNAs (miRNAs), contributes to variation in quantitative and complex traits. However, in plants, variants in miRNAs and their target genes that contribute to natural phenotypic variation, and the underlying regulatory networks, remain poorly characterized. We investigated the associations and interactions of single-nucleotide polymorphisms (SNPs) in miRNAs and their target genes with phenotypes in 435 individuals from a natural population of Populus. We used RNA-seq to identify 217 miRNAs differentially expressed in a tension wood system, and identified 1196 candidate target genes; degradome sequencing confirmed 60 of the target sites. In addition, 72 miRNA-target pairs showed significant co-expression. Gene ontology (GO) term analysis showed that most of the genes in the co-regulated pairs participate in biological regulation. Genome resequencing found 5383 common SNPs (frequency ≥ 0.05) in 139 miRNAs and 31 037 SNPs in 819 target genes. Single-SNP association analyses identified 232 significant associations between wood traits (P ≤ 0.05) and SNPs in 102 miRNAs and 1387 associations with 478 target genes. Among these, 102 miRNA-target pairs associated with the same traits. Multi-SNP associations found 102 epistatic pairs associated with traits. Furthermore, a reconstructed regulatory network contained 12 significantly co-expressed pairs, including eight miRNAs and nine targets associated with traits. Lastly, both expression and genetic association showed that miR156i, miR156j, miR396a and miR6445b were involved in the formation of tension wood. This study shows that variants in miRNAs and target genes contribute to natural phenotypic variation and annotated roles and interactions of miRNAs and their target genes by genetic association analysis.

[1]  Heng-fu Yin,et al.  Integration of small RNAs, degradome and transcriptome sequencing in hyperaccumulator Sedum alfredii uncovers a complex regulatory network and provides insights into cadmium phytoremediation , 2016, Plant biotechnology journal.

[2]  Z. Cao,et al.  Genome-wide expression profiling of microRNAs in poplar upon infection with the foliar rust fungus Melampsora larici-populina , 2015, BMC Genomics.

[3]  A. Montagnoli,et al.  MicroRNAs expression patterns in the response of poplar woody root to bending stress , 2015, Planta.

[4]  Beibei Chen,et al.  Transcript profiling of Populus tomentosa genes in normal, tension, and opposite wood by RNA-seq , 2015, BMC Genomics.

[5]  L. Kruglyak,et al.  The role of regulatory variation in complex traits and disease , 2015, Nature Reviews Genetics.

[6]  Andrew D. Johnson,et al.  Genome-wide Identification of microRNA Expression Quantitative Trait Loci , 2015, Nature Communications.

[7]  H. Burbano,et al.  Rapid divergence and high diversity of miRNAs and miRNA targets in the Camelineae. , 2015, The Plant journal : for cell and molecular biology.

[8]  Jason A. Corwin,et al.  An Arabidopsis Gene Regulatory Network for Secondary Cell Wall Synthesis , 2014, Nature.

[9]  Dennis A. Benson,et al.  GenBank , 2014, Nucleic acids research.

[10]  Lili Tu,et al.  Small RNA and degradome profiling reveals a role for miRNAs and their targets in the developing fibers of Gossypium barbadense. , 2014, The Plant journal : for cell and molecular biology.

[11]  Philip C J Donoghue,et al.  Evolutionary history of plant microRNAs. , 2014, Trends in plant science.

[12]  Hongbing Shen,et al.  Genetic Variations in the Flanking Regions of miR-101-2 Are Associated with Increased Risk of Breast Cancer , 2014, PloS one.

[13]  YANGXiao-hui,et al.  Variation in growth, leaf, and wood property traits of Chinese white poplar (Populus tomentosa), a major industrial tree species in Northern China , 2014 .

[14]  A. Lusis,et al.  Systems genetics approaches to understand complex traits , 2013, Nature Reviews Genetics.

[15]  Q. Du,et al.  Allelic Variation in a Cellulose Synthase Gene (PtoCesA4) Associated with Growth and Wood Properties in Populus tomentosa , 2013, G3: Genes, Genomes, Genetics.

[16]  M. Laakso,et al.  Genetic regulation of human adipose microRNA expression and its consequences for metabolic traits. , 2013, Human molecular genetics.

[17]  Xuemei Chen,et al.  Biogenesis, Turnover, and Mode of Action of Plant MicroRNAs[OPEN] , 2013, Plant Cell.

[18]  Hong Luo,et al.  MicroRNA-mediated gene regulation: potential applications for plant genetic engineering , 2013, Plant Molecular Biology.

[19]  R. Sederoff,et al.  Ptr-miR397a is a negative regulator of laccase genes affecting lignin content in Populus trichocarpa , 2013, Proceedings of the National Academy of Sciences.

[20]  Deqiang Zhang,et al.  Sexual Dimorphism Floral MicroRNA Profiling and Target Gene Expression in Andromonoecious Poplar (Populus tomentosa) , 2013, PloS one.

[21]  Daniel J. Gaffney,et al.  Global Properties and Functional Complexity of Human Gene Regulatory Variation , 2013, PLoS genetics.

[22]  Jingyuan Fu,et al.  Human Disease-Associated Genetic Variation Impacts Large Intergenic Non-Coding RNA Expression , 2013, PLoS genetics.

[23]  Shane J. Neph,et al.  Systematic Localization of Common Disease-Associated Variation in Regulatory DNA , 2012, Science.

[24]  Attila Gyenesei,et al.  BiForce Toolbox: powerful high-throughput computational analysis of gene–gene interactions in genome-wide association studies , 2012, Nucleic Acids Res..

[25]  Andrea Polle,et al.  Salt stress induces the formation of a novel type of 'pressure wood' in two Populus species. , 2012, The New phytologist.

[26]  M. Axtell,et al.  Deep Annotation of Populus trichocarpa microRNAs from Diverse Tissue Sets , 2012, PloS one.

[27]  Detlef Weigel,et al.  Plant secondary siRNA production determined by microRNA-duplex structure , 2012, Proceedings of the National Academy of Sciences.

[28]  M. Todesco,et al.  Natural Variation in Biogenesis Efficiency of Individual Arabidopsis thaliana MicroRNAs , 2012, Current Biology.

[29]  Hong-Mei Zhang,et al.  Genome‐wide identification of SNPs in microRNA genes and the SNP effects on microRNA target binding and biogenesis , 2012, Human mutation.

[30]  Javier F. Palatnik,et al.  Functional Specialization of the Plant miR396 Regulatory Network through Distinct MicroRNA–Target Interactions , 2012, PLoS genetics.

[31]  Peter F. Stadler,et al.  ViennaRNA Package 2.0 , 2011, Algorithms for Molecular Biology.

[32]  Patrick Xuechun Zhao,et al.  psRNATarget: a plant small RNA target analysis server , 2011, Nucleic Acids Res..

[33]  P. Rigault,et al.  Association Genetics of Wood Physical Traits in the Conifer White Spruce and Relationships With Gene Expression , 2011, Genetics.

[34]  R. Zhong,et al.  Evolutionary conservation of the transcriptional network regulating secondary cell wall biosynthesis. , 2010, Trends in plant science.

[35]  C. Harris,et al.  Genetic variation in microRNA networks: the implications for cancer research , 2010, Nature Reviews Cancer.

[36]  Detlef Weigel,et al.  Structure Determinants for Accurate Processing of miR172a in Arabidopsis thaliana , 2010, Current Biology.

[37]  Mark D. Robinson,et al.  edgeR: a Bioconductor package for differential expression analysis of digital gene expression data , 2009, Bioinform..

[38]  John J Rossi,et al.  SNPs in human miRNA genes affect biogenesis and function. , 2009, RNA.

[39]  Huanming Yang,et al.  SNP detection for massively parallel whole-genome resequencing. , 2009, Genome research.

[40]  D. Bartel.  MicroRNAs: Target Recognition and Regulatory Functions , 2009, Cell.

[41]  V. Chiang,et al.  Stress-responsive microRNAs in Populus. , 2008, The Plant journal : for cell and molecular biology.

[42]  J. de Meaux,et al.  Structurally different alleles of the ath-MIR824 microRNA precursor are maintained at high frequency in Arabidopsis thaliana , 2008, Proceedings of the National Academy of Sciences.

[43]  Barbara Jarzab,et al.  Common SNP in pre-miR-146a decreases mature miR expression and predisposes to papillary thyroid carcinoma , 2008, Proceedings of the National Academy of Sciences.

[44]  D. Bartel,et al.  Endogenous siRNA and miRNA Targets Identified by Sequencing of the Arabidopsis Degradome , 2008, Current Biology.

[45]  Ruiqiang Li,et al.  SOAP: short oligonucleotide alignment program , 2008, Bioinform..

[46]  M. Purugganan,et al.  Sequence Variation of MicroRNAs and Their Binding Sites in Arabidopsis1[W] , 2008, Plant Physiology.

[47]  Stijn van Dongen,et al.  miRBase: tools for microRNA genomics , 2007, Nucleic Acids Res..

[48]  Edward S. Buckler,et al.  TASSEL: software for association mapping of complex traits in diverse samples , 2007, Bioinform..

[49]  K. Keegstra,et al.  Functional Genomic Analysis Supports Conservation of Function Among Cellulose Synthase-Like A Gene Family Members and Suggests Diverse Roles of Mannans in Plants1[W][OA] , 2007, Plant Physiology.

[50]  G. Martin,et al.  A novel link between tomato GRAS genes, plant disease resistance and mechanical stress response. , 2006, Molecular plant pathology.

[51]  M. Gribskov,et al.  The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray) , 2006, Science.

[52]  Vincent L. Chiang,et al.  Novel and Mechanical Stress–Responsive MicroRNAs in Populus trichocarpa That Are Absent from Arabidopsisw⃞ , 2005, The Plant Cell Online.

[53]  B. Sundberg,et al.  Patterns of Auxin Distribution during Gravitational Induction of Reaction Wood in Poplar and Pine1 , 2004, Plant Physiology.

[54]  A. Kinney,et al.  Guar Seed ß-Mannan Synthase Is a Member of the Cellulose Synthase Super Gene Family , 2004, Science.

[55]  J. Cairney,et al.  A simple and efficient method for isolating RNA from pine trees , 1993, Plant Molecular Biology Reporter.

[56]  Kyung-Hwan Han,et al.  Developmental and seasonal expression of PtaHB1, a Populus gene encoding a class III HD-Zip protein, is closely associated with secondary growth and inversely correlated with the level of microRNA (miR166). , 2006, The New phytologist.