Association Genetics in Populus Reveal the Allelic Interactions of Pto-MIR167a and Its Targets in Wood Formation

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 b...

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Main Authors: Mingyang Quan, Liang Xiao, Wenjie Lu, Xin Liu, Fangyuan Song, Jingna Si, Qingzhang Du, Deqiang Zhang
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-06-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2018.00744/full
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record_format Article
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language English
format Article
sources DOAJ
author Mingyang Quan
Mingyang Quan
Mingyang Quan
Liang Xiao
Liang Xiao
Liang Xiao
Wenjie Lu
Wenjie Lu
Wenjie Lu
Xin Liu
Xin Liu
Xin Liu
Fangyuan Song
Fangyuan Song
Fangyuan Song
Jingna Si
Jingna Si
Jingna Si
Qingzhang Du
Qingzhang Du
Qingzhang Du
Deqiang Zhang
Deqiang Zhang
Deqiang Zhang
spellingShingle Mingyang Quan
Mingyang Quan
Mingyang Quan
Liang Xiao
Liang Xiao
Liang Xiao
Wenjie Lu
Wenjie Lu
Wenjie Lu
Xin Liu
Xin Liu
Xin Liu
Fangyuan Song
Fangyuan Song
Fangyuan Song
Jingna Si
Jingna Si
Jingna Si
Qingzhang Du
Qingzhang Du
Qingzhang Du
Deqiang Zhang
Deqiang Zhang
Deqiang Zhang
Association Genetics in Populus Reveal the Allelic Interactions of Pto-MIR167a and Its Targets in Wood Formation
Frontiers in Plant Science
association genetics
Pto-miR167a
auxin response factor
long non-coding RNA
epistasis
wood formation
author_facet Mingyang Quan
Mingyang Quan
Mingyang Quan
Liang Xiao
Liang Xiao
Liang Xiao
Wenjie Lu
Wenjie Lu
Wenjie Lu
Xin Liu
Xin Liu
Xin Liu
Fangyuan Song
Fangyuan Song
Fangyuan Song
Jingna Si
Jingna Si
Jingna Si
Qingzhang Du
Qingzhang Du
Qingzhang Du
Deqiang Zhang
Deqiang Zhang
Deqiang Zhang
author_sort Mingyang Quan
title Association Genetics in Populus Reveal the Allelic Interactions of Pto-MIR167a and Its Targets in Wood Formation
title_short Association Genetics in Populus Reveal the Allelic Interactions of Pto-MIR167a and Its Targets in Wood Formation
title_full Association Genetics in Populus Reveal the Allelic Interactions of Pto-MIR167a and Its Targets in Wood Formation
title_fullStr Association Genetics in Populus Reveal the Allelic Interactions of Pto-MIR167a and Its Targets in Wood Formation
title_full_unstemmed Association Genetics in Populus Reveal the Allelic Interactions of Pto-MIR167a and Its Targets in Wood Formation
title_sort association genetics in populus reveal the allelic interactions of pto-mir167a and its targets in wood formation
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2018-06-01
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.
topic association genetics
Pto-miR167a
auxin response factor
long non-coding RNA
epistasis
wood formation
url https://www.frontiersin.org/article/10.3389/fpls.2018.00744/full
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spelling doaj-21e50d479292467b84cc618ebdc6d61f2020-11-24T21:20:12ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2018-06-01910.3389/fpls.2018.00744361498Association Genetics in Populus Reveal the Allelic Interactions of Pto-MIR167a and Its Targets in Wood FormationMingyang Quan0Mingyang Quan1Mingyang Quan2Liang Xiao3Liang Xiao4Liang Xiao5Wenjie Lu6Wenjie Lu7Wenjie Lu8Xin Liu9Xin Liu10Xin Liu11Fangyuan Song12Fangyuan Song13Fangyuan Song14Jingna Si15Jingna Si16Jingna Si17Qingzhang Du18Qingzhang Du19Qingzhang Du20Deqiang Zhang21Deqiang Zhang22Deqiang Zhang23Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaNational Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaKey Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaBeijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaNational Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaKey Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaBeijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaNational Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaKey Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaBeijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaNational Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaKey Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaBeijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaNational Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaKey Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaBeijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaNational Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaKey Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaBeijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaNational Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaKey Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaBeijing Advanced Innovation Center for Tree Breeding by Molecular Design, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaNational Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaKey Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, Beijing, ChinaMicroRNAs (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.https://www.frontiersin.org/article/10.3389/fpls.2018.00744/fullassociation geneticsPto-miR167aauxin response factorlong non-coding RNAepistasiswood formation