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Association Studies in Populus tomentosa Reveal the Genetic Interactions of Pto-MIR156c and Its Targets in Wood Formation.

ABSTRACT: MicroRNAs (miRNAs) regulate gene expression in many biological processes, but the significance of the interaction between a miRNA and its targets in perennial trees remains largely unknown. Here, we employed transcript profiling and association studies in Populus tomentosa (Pto) to decipher the effect of genetic variation and interactions between Pto-miR156c and its potential targets (Pto-SPL15, Pto-SPL20, and Pto-SPL25) in 435 unrelated individuals from a natural population of P. tomentosa. Single-SNP (single-nucleotide polymorphism) based association studies with analysis of the underlying additive and dominant effects identified 69 significant associations (P < 0.01), representing 51 common SNPs (minor allele frequency > 0.05) from Pto-MIR156c and its three potential targets, with six wood and growth traits, revealing their common roles in wood formation. Epistasis analysis uncovered 129 significant SNP-SNP associations with ten traits, indicating the potential genetic interactions of Pto-MIR156c and its three putative targets. Interestingly, expression analysis in stem (phloem, cambium, and xylem) revealed that Pto-miR156c expression showed strong negative correlations with Pto-SPL20 (r = -0.90, P < 0.01) and Pto-SPL25 (r = -0.65, P < 0.01), and a positive correlation with Pto-SPL15 (r = 0.40, P < 0.01), which also indicated the putative interactions of Pto-miR156c and its potential targets and their common roles in wood formation. Thus, our study provided an alternative approach to decipher the interaction between miRNAs and their targets and to dissect the genetic architecture of complex traits in trees.

SUBMITTER: Quan M

PROVIDER: S-EPMC4971429 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Association Studies in Populus tomentosa Reveal the Genetic Interactions of Pto-MIR156c and Its Targets in Wood Formation.

Quan Mingyang M Wang Qingshi Q Phangthavong Souksamone S Yang Xiaohui X Song Yuepeng Y Du Qingzhang Q Zhang Deqiang D

Frontiers in plant science 20160803

MicroRNAs (miRNAs) regulate gene expression in many biological processes, but the significance of the interaction between a miRNA and its targets in perennial trees remains largely unknown. Here, we employed transcript profiling and association studies in Populus tomentosa (Pto) to decipher the effect of genetic variation and interactions between Pto-miR156c and its potential targets (Pto-SPL15, Pto-SPL20, and Pto-SPL25) in 435 unrelated individuals from a natural population of P. tomentosa. Sin ...[more]

PMID: 27536313

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Project description:MicroRNAs (miRNAs) play crucial regulatory roles in plant growth and development by interacting with RNA molecules, including messenger RNAs (mRNAs) and long non-coding RNAs (lncRNAs); however, the genetic networks of miRNAs and their targets influencing the phenotypes of perennial trees remain to be investigated. Here, we integrated expression profiling and association analysis of underlying physiology and expression traits to dissect the allelic variations and genetic interactions of Pto-MIR167a and its targets, sponge lncRNA ARFRL, and Pto-ARF8, in 435 unrelated individuals of Populus tomentosa. Tissue-specific expression analysis in eight tissues, including stem, leaf, root, and shoot apex, revealed negative correlations between Pto-MIR167a and lncRNA ARFRL and Pto-ARF8 (r = -0.60 and -0.61, respectively, P < 0.01), and a positive correlation between sponge lncRNA ARFRL and Pto-ARF8 (r = 0.90, P < 0.01), indicating their potential regulatory roles in tree growth and wood formation. Single nucleotide polymorphism (SNP)-based association studies detected 53 significant associations (P < 0.01, Q < 0.1) representing 41 unique SNPs from the three genes and six traits, suggesting their potential roles in wood formation. Epistasis uncovered 88 pairwise interactions for 10 traits, which provided substantial evidence for genetic interactions among Pto-MIR167a, lncRNA ARFRL, and Pto-ARF8. Using gene expression-based association mapping, we also examined SNPs within the three genes that influence phenotypes by regulating the expression of Pto-ARF8. Interestingly, SNPs in the precursor region of Pto-MIR167a altered its secondary structure stability and transcription, thereby affecting the expression of its targets. In summary, we elucidated the genetic interactions between Pto-MIR167a and its targets, sponge lncRNA ARFRL, and Pto-ARF8, in tree growth and wood formation, and provide a feasible method for further investigation of multi-factor genetic networks influencing phenotypic variation in the population genetics of trees.

Project description:BackgroundWood formation affects the chemical and physical properties of wood, and thus affects its utility as a building material or a feedstock for biofuels, pulp and paper. To obtain genome-wide insights on the transcriptome changes and regulatory networks in wood formation, we used high-throughput RNA sequencing to characterize cDNA libraries of mature xylem from tension wood (TW), opposite wood (OW), and normal wood (NW), in the industrial tree species Populus tomentosa.ResultsOur sequencing generated 140,978,316 (TW), 128,972,228 (OW), and 117,672,362 (NW) reads, corresponding to 10,127 (TW), 10,129 (OW), and 10,129 (NW) unique genes. Of these, 361 genes were differentially transcribed between TW and OW (log2FC ≥ 1 or ≤ -1, FDR < 0.05), 2,658 differed between OW and NW, and 2,417 differed between TW and NW. This indicates that NW differs significantly from the wood in branches; GO term analysis also indicated that OW experienced more transcriptome remodeling. The differentially expressed genes included 97 encoding transcription factors (TFs), 40 involved in hormone signal transduction, 33 in lignin biosynthesis, 21 in flavonoid biosynthesis, and 43 in cell wall metabolism, including cellulose synthase, sucrose synthase, and COBRA. More than half of the differentially expressed TF showed more than 4-fold lower transcript levels in NW compared with TW or OW, indicating that TF abundances differed dramatically in different wood types and may have important roles in the formation of reaction wood. In addition, transcripts of most of the genes involved in lignin biosynthesis were more abundant in OW compared with TW, consistent with the higher lignin content of OW. We constructed two transcriptomic networks for the regulation of lignin and cellulose biosynthesis, including TFs, based on the co-expression patterns of different genes. Lastly, we used reverse transcription quantitative PCR to validate the differentially expressed genes identified.ConclusionsHere, we identified the global patterns and differences in gene expression among TW, OW, and NW, and constructed two transcriptomic regulatory networks involved in TW formation in P. tomentosa. We also identified candidate genes for molecular breeding of wood quality, and provided a starting point to decipher the molecular mechanisms of wood formation in Populus.

Dataset Information

Association Studies in Populus tomentosa Reveal the Genetic Interactions of Pto-MIR156c and Its Targets in Wood Formation.

Publications

Association Studies in Populus tomentosa Reveal the Genetic Interactions of Pto-MIR156c and Its Targets in Wood Formation.

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