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Allelic Interactions among Pto-MIR475b and Its Four Target Genes Potentially Affect Growth and Wood Properties in Populus.

ABSTRACT: MicroRNAs (miRNAs) play crucial roles in plant growth and development, but few studies have illuminated the allelic interactions among miRNAs and their targets in perennial plants. Here, we combined analysis of expression patterns and single-nucleotide polymorphism (SNP)-based association studies to explore the interactions between Pto-MIR475b and its four target genes (Pto-PPR1, Pto-PPR2, Pto-PPR3, and Pto-PPR4) in 435 unrelated individuals of Populus tomentosa. Expression patterns showed a significant negative correlation (r = -0.447 to -0.411, P < 0.01) between Pto-MIR475b and its four targets in eight tissues of P. tomentosa, suggesting that Pto-miR475b may negatively regulate the four targets. Single SNP-based association studies identified 93 significant associations (P < 0.01, Q < 0.1) representing associations of 80 unique SNPs in Pto-MIR475b and its four targets with nine traits, revealing their potential roles in tree growth and wood formation. Moreover, one common SNP in the precursor region significantly altered the secondary structure of the pre-Pto-miR475b and changed the expression level of Pto-MIR475b. Analysis of epistatic interactions identified 115 significant SNP-SNP associations (P < 0.01) representing 45 unique SNPs from Pto-MIR475b and its four targets for 10 traits, revealing that genetic interactions between Pto-MIR475b and its targets influence quantitative traits of perennial plants. Our study provided a feasible strategy to study population genetics in forest trees and enhanced our understanding of miRNAs by dissecting the allelic interactions between this miRNA and its targets in P. tomentosa.

SUBMITTER: Xiao L

PROVIDER: S-EPMC5478899 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Allelic Interactions among Pto-MIR475b and Its Four Target Genes Potentially Affect Growth and Wood Properties in Populus.

Xiao Liang L Quan Mingyang M Du Qingzhang Q Chen Jinhui J Xie Jianbo J Zhang Deqiang D

Frontiers in plant science 20170621

MicroRNAs (miRNAs) play crucial roles in plant growth and development, but few studies have illuminated the allelic interactions among miRNAs and their targets in perennial plants. Here, we combined analysis of expression patterns and single-nucleotide polymorphism (SNP)-based association studies to explore the interactions between Pto-MIR475b and its four target genes (Pto-PPR1, Pto-PPR2, Pto-PPR3, and Pto-PPR4) in 435 unrelated individuals of Populus tomentosa. Expr ...[more]

PMID: 28680433

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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:BACKGROUND: S-adenosyl-l-homocysteine hydrolase (SAHH) is the only eukaryotic enzyme capable of S-adenosyl-l-homocysteine (SAH) catabolism for the maintenance of cellular transmethylation potential. Recently, biochemical and genetic studies in herbaceous species have obtained important discoveries in the function of SAHH, and an extensive characterization of SAHH family in even one tree species is essential, but currently lacking. RESULTS: Here, we first identified the SAHH family from Populus tomentosa using molecular cloning method. Phylogenetic analyses of 28 SAHH proteins from dicotyledons, monocotyledons, and lower plants revealed that the sequences formed two monophyletic groups: the PtrSAHHA with PtoSAHHA and PtrSAHHB with PtoSAHHB. Examination of tissue-specific expression profiles of the PtoSAHH family revealed similar expression patterns; high levels of expression in xylem were found. Nucleotide diversity and linkage disequilibrium (LD) in the PtoSAHH family, sampled from P. tomentosa natural distribution, revealed that PtoSAHH harbors high single-nucleotide polymorphism (SNP) diversity (? = 0.01059 ± 0.00122 and 0.00930 ± 0.00079,respectively) and low LD (r2 > 0.1, within 800 bp and 2,200 bp, respectively). Using an LD-linkage analysis approach, two noncoding SNPs (PtoSAHHB_1065 and PtoSAHHA_2203) and the corresponding haplotypes were found to significantly associate with ?-cellulose content, and a nonsynonymous SNP (PtoSAHHB_410) within the SAHH signature motifs showed significant association with fiber length, with an average of 3.14% of the phenotypic variance explained. CONCLUSIONS: The present study demonstrates that PtoSAHHs were split off prior to the divergence of interspecies in Populus, and SAHHs may play a key role promoting transmethylation reactions in the secondary cell walls biosynthesis in trees. Hence, our findings provide insights into SAHH function and evolution in woody species and also offer a theoretical basis for marker-aided selection breeding to improve the wood quality of Populus.

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Allelic Interactions among Pto-MIR475b and Its Four Target Genes Potentially Affect Growth and Wood Properties in Populus.

Publications

Allelic Interactions among <i>Pto-MIR475b</i> and Its Four Target Genes Potentially Affect Growth and Wood Properties in <i>Populus</i>.

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