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Genome-wide identification of novel long non-coding RNAs in Populus tomentosa tension wood, opposite wood and normal wood xylem by RNA-seq

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Abstract

Increasing evidence shows that long non-coding RNAs (lncRNAs) function as important regulatory factors during plant development, but few reports have examined lncRNAs in trees. Here, we report our genome-scale identification and characterization of lncRNAs differentially expressed in the xylem of tension wood, opposite wood and normal wood in Populus tomentosa, by high-throughput RNA sequencing. We identified 1,377 putative lncRNAs by computational analysis, and expression and structure analyses showed that the lncRNAs had lower expression levels and shorter lengths than protein-coding transcripts in Populus. Of the 776 differently expressed (log2FC ≥1 or ≤-1, FDR ≤0.01) lncRNAs, 389 could potentially target 1,151 genes via trans-regulatory effects. Functional annotation of these target genes demonstrated that they are involved in fundamental processes, and in specific mechanisms such as response to stimuli. We also identified 16 target genes involved in wood formation, including cellulose and lignin biosynthesis, suggesting a potential role for lncRNAs in wood formation. In addition, three lncRNAs harbor precursors of four miRNAs, and 25 were potentially targeted by 44 miRNAs where a negative expression relationship between them was detected by qRT-PCR. Thus, a network of interactions among the lncRNAs, miRNAs and mRNAs was constructed, indicating widespread regulatory interactions between non-coding RNAs and mRNAs. Lastly, qRT-PCR validation confirmed the differential expression of these lncRNAs, and revealed that they have tissue-specific expression in P. tomentosa. This study presents the first global identification of lncRNAs and their potential functions in wood formation, providing a starting point for detailed dissection of the functions of lncRNAs in Populus.

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Abbreviations

lncRNAs:

Long non-coding RNAs

4CL:

4-Coumarate-CoA ligase

CCOMT:

Caffeoyl-CoA 3-O-methyltransferase

CESA:

Cellulose synthase

CSLD4:

Cellulose synthase-like protein D4

CW:

Compression wood

GA2ox:

Gibberellin 2-oxidase

GO:

Gene ontology

NW:

Normal wood

OW:

Opposite wood

ppo:

Polyphenol oxidase

TF:

Transcription factor

TW:

Tension wood

References

  • Andersson-Gunnerås S, Mellerowicz EJ, Love J, Segerman B, Ohmiya Y, Coutinho PM, Nilsson P, Henrissat B, Moritz T, Sundberg B (2006) Biosynthesis of cellulose-enriched tension wood in Populus: global analysis of transcripts and metabolites identifies biochemical and developmental regulators in secondary wall biosynthesis. Plant J 45:144–165

    Article  PubMed  Google Scholar 

  • Bernal AJ, Yoo C-M, Mutwil M, Jensen JK, Hou G, Blaukopf C, Sørensen I, Blancaflor EB, Scheller HV, Willats WG (2008) Functional analysis of the cellulose synthase-like genes CSLD1, CSLD2, and CSLD4 in tip-growing Arabidopsis cells. Plant Physiol 148:1238–1253

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Boerner S, McGinnis KM (2012) Computational identification and functional predictions of long noncoding RNA in Zea mays. PLoS ONE 7:e43047

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bond AM, VanGompel MJ, Sametsky EA, Clark MF, Savage JC, Disterhoft JF, Kohtz JD (2009) Balanced gene regulation by an embryonic brain ncRNA is critical for adult hippocampal GABA circuitry. Nat Neurosci 12:1020–1027

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cai X, Cullen BR (2007) The imprinted H19 noncoding RNA is a primary microRNA precursor. RNA 13:313–316

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep 11:113–116

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dayan J, Voronin N, Gong F, Sun T-p, Hedden P, Fromm H, Aloni R (2012) Leaf-induced gibberellin signaling is essential for internode elongation, cambial activity, and fiber differentiation in tobacco stems. Plant Cell 24:66–79

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ding J, Lu Q, Ouyang Y, Mao H, Zhang P, Yao J, Xu C, Li X, Xiao J, Zhang Q (2012) A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. PNAS 109:2654–2659

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Du S, Uno H, Yamamoto F (2004) Roles of auxin and gibberellin in gravity-induced tension wood formation in Aesculus turbinata seedlings. IAWA J 25:337–348

    Article  Google Scholar 

  • Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64–W70

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gibb EA, Brown CJ, Lam WL (2011) The functional role of long non-coding RNA in human carcinomas. Mol Cancer 10:1–17

    Article  Google Scholar 

  • Goodrich JA, Kugel JF (2006) Non-coding-RNA regulators of RNA polymerase II transcription. Nat Rev Mol Cell Biol 7:612–616

    Article  CAS  PubMed  Google Scholar 

  • Guo D, Chen F, Inoue K, Blount JW, Dixon RA (2001) Downregulation of caffeic acid 3-O-methyltransferase and caffeoyl CoA 3-O-methyltransferase in transgenic alfalfa: impacts on lignin structure and implications for the biosynthesis of G and S lignin. Plant Cell 13:73–88

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Han L, Zhang K, Shi Z, Zhang J, Zhu J, Zhu S, Zhang A, Jia Z, Wang G, Yu S (2012) LncRNA profile of glioblastoma reveals the potential role of lncRNAs in contributing to glioblastoma pathogenesis. Int J Oncol 40:2004–2012

    CAS  PubMed  Google Scholar 

  • Hu Y, Gai Y, Yin L, Wang X, Feng C, Feng L, Li D, Jiang X-N, Wang D-C (2010) Crystal structures of a Populus tomentosa 4-coumarate: CoA ligase shed light on its enzymatic mechanisms. Plant Cell 22:3093–3104

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Israelsson M, Sundberg B, Moritz T (2005) Tissue-specific localization of gibberellins and expression of gibberellin-biosynthetic and signaling genes in wood-forming tissues in aspen. Plant J 44:494–504

    Article  CAS  PubMed  Google Scholar 

  • Jalali S, Jayaraj GG, Scaria V (2012) Integrative transcriptome analysis suggest processing of a subset of long non-coding RNAs to small RNAs. Biol Direct 7:25

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jalali S, Bhartiya D, Lalwani MK, Sivasubbu S, Scaria V (2013) Systematic transcriptome wide analysis of lncRNA–miRNA interactions. PLoS ONE 8:e53823

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Jin J, Zhang H, Kong L, Gao G, Luo J (2013) PlantTFDB 3.0: a portal for the functional and evolutionary study of plant transcription factors. Nucleic Acids Res 42:D1182–D1187

    Article  PubMed Central  PubMed  Google Scholar 

  • Joseleau J-P, Imai T, Kuroda K, Ruel K (2004) Detection in situ and characterization of lignin in the G-layer of tension wood fibres of Populus deltoides. Planta 219:338–345

    Article  CAS  PubMed  Google Scholar 

  • Kapranov P, Cheng J, Dike S, Nix DA, Duttagupta R, Willingham AT, Stadler PF, Hertel J, Hackermuller J, Hofacker IL, Bell I, Cheung E, Drenkow J, Dumais E, Patel S, Helt G, Ganesh M, Ghosh S, Piccolboni A, Sementchenko V, Tammana H, Gingeras TR (2007) RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 316:1484–1488

    Article  CAS  PubMed  Google Scholar 

  • Kwon M (2007) Review: Tension wood as a model system to explore the carbon partitioning between lignin and cellulose biosynthesis in woody plants. J App Biol Chem 50:83–87

    Google Scholar 

  • Lu S, Sun Y-H, 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  CAS  PubMed Central  PubMed  Google Scholar 

  • Lu S, Sun YH, Chiang VL (2008) Stress-responsive microRNAs in Populus. Plant J 55:131–151

    Article  CAS  PubMed  Google Scholar 

  • Lu T, Zhu C, Lu G, Guo Y, Zhou Y, Zhang Z, Zhao Y, Li W, Lu Y, Tang W (2012) Strand-specific RNA-seq reveals widespread occurrence of novel cis-natural antisense transcripts in rice. BMC Genom 13:721

    Article  CAS  Google Scholar 

  • Lu S, Li Q, Wei H, Chang M-J, Tunlaya-Anukit S, Kim H, Liu J, Song J, Sun Y-H, Yuan L (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  CAS  PubMed Central  PubMed  Google Scholar 

  • Lukiw WJ, Handley P, Wong L, Crapper McLachlan DR (1992) BC200 RNA in normal human neocortex, non-Alzheimer dementia (NAD), and senile dementia of the Alzheimer type (AD). Neurochem Res 17:591–597

    Article  CAS  PubMed  Google Scholar 

  • Maury S, Geoffroy P, Legrand M (1999) Tobacco O-methyltransferases involved in phenylpropanoid metabolism. The different caffeoyl-coenzyme a/5-hydroxyferuloyl-coenzyme a 3/5-o-methyltransferase and caffeic acid/5-hydroxyferulic acid 3/5-o-methyltransferase classes have distinct substrate specificities and expression patterns. Plant Physiol 121:215–224

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mellerowicz EJ, Sundberg B (2008) Wood cell walls: biosynthesis, developmental dynamics and their implications for wood properties. Curr Opin Plant Biol 11:293–300

    Article  CAS  PubMed  Google Scholar 

  • Mercer TR, Dinger ME, Mattick JS (2009) Long non-coding RNAs: insights into functions. Nat Rev Genet 10:155–159

    Article  CAS  PubMed  Google Scholar 

  • Meyers BC, Axtell MJ, Bartel B, Bartel DP, Baulcombe D, Bowman JL, Cao X, Carrington JC, Chen X, Green PJ (2008) Criteria for annotation of plant MicroRNAs. Plant Cell 20:3186–3190

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nugroho WD, Yamagishi Y, Nakaba S, Fukuhara S, Begum S, Marsoem SN, Ko J-H, Jin H-O, Funada R (2012) Gibberellin is required for the formation of tension wood and stem gravitropism in Acacia mangium seedlings. Ann Bot Lond 110:887–895

    Article  CAS  Google Scholar 

  • Pauli A, Valen E, Lin MF, Garber M, Vastenhouw NL, Levin JZ, Fan L, Sandelin A, Rinn JL, Regev A (2012) Systematic identification of long noncoding RNAs expressed during Zebrafish embryogenesis. Genome Res 22:577–591

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ponting CP, Oliver PL, Reik W (2009) Evolution and functions of long noncoding RNAs. Cell 136:629–641

    Article  CAS  PubMed  Google Scholar 

  • Puzey JR, Karger A, Axtell M, Kramer EM (2012) Deep annotation of Populus trichocarpa microRNAs from diverse tissue sets. PLoS ONE 7:e33034

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Roberts A, Pimentel H, Trapnell C, Pachter L (2011) Identification of novel transcripts in annotated genomes using RNA-Seq. Bioinformatics 27:2325–2329

    Article  CAS  PubMed  Google Scholar 

  • Saito R, Smoot ME, Ono K, Ruscheinski J, Wang PL, Lotia S, Pico AR, Bader GD, Ideker T (2012) A travel guide to Cytoscape plugins. Nat Methods 9:1069–1076

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schmittgen TD, Lee EJ, Jiang J, Sarkar A, Yang L, Elton TS, Chen C (2008) Real-time PCR quantification of precursor and mature microRNA. Methods 44:31–38

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sigova AA, Mullen AC, Molinie B, Gupta S, Orlando DA, Guenther MG, Almada AE, Lin C, Sharp PA, Giallourakis CC (2013) Divergent transcription of long noncoding RNA/mRNA gene pairs in embryonic stem cells. PNAS 110:2876–2881

  • Sjödin A, Street NR, Sandberg G, Gustafsson P, Jansson S (2009) The Populus genome integrative explorer (PopGenIE): a new resource for exploring the Populus genome. New Phytol 182:1013–1025

    Article  PubMed  Google Scholar 

  • Sun L, Zhang Z, Bailey TL, Perkins AC, Tallack MR, Xu Z, Liu H (2012) Prediction of novel long non-coding RNAs based on RNA-Seq data of mouse Klf1 knockout study. BMC Bioinform 13:331

    Article  CAS  Google Scholar 

  • Tafer H, Hofacker IL (2008) RNAplex: a fast tool for RNA–RNA interaction search. Bioinformatics 24:2657–2663

    Article  CAS  PubMed  Google Scholar 

  • Taft RJ, Pang KC, Mercer TR, Dinger M, Mattick JS (2010) Non-coding RNAs: regulators of disease. J Pathol 220:126–139

    Article  CAS  PubMed  Google Scholar 

  • Timell T (1969) The chemical composition of tension wood. Svensk Papp Tidn 72:173–181

    CAS  Google Scholar 

  • Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604

    Article  CAS  PubMed  Google Scholar 

  • Wagner A, Donaldson L, Kim H, Phillips L, Flint H, Steward D, Torr K, Koch G, Schmitt U, Ralph J (2009) Suppression of 4-coumarate-CoA ligase in the coniferous gymnosperm Pinus radiata. Plant Physiol 149:370–383

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang W, Wang L, Chen C, Xiong G, Tan X-Y, Yang K-Z, Wang Z-C, Zhou Y, Ye D, Chen L-Q (2011a) Arabidopsis CSLD1 and CSLD4 are required for cellulose deposition and normal growth of pollen tubes. J Exp Bot 62:5161–5177

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wang XT, Song XY, Glass CK, Rosenfeld MG (2011b) The long arm of long noncoding RNAs: roles as sensors regulating gene transcriptional programs. CSH Perspect Biol 3:a003756

    Google Scholar 

  • Yoon JH, Abdelmohsen K, Gorospe M (2013) Post-transcriptional gene regulation by long noncoding RNA. J Mol Biol 425:3723–3730

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yoshida M, Yamamoto H, Okuyama T, Nakamura T (1999) Negative gravitropism and growth stress in GA3-treated branches of Prunus spachiana Kitamura f. spachiana cv. Plenarosea. J Wood Sci 45:368–372

    Article  Google Scholar 

  • Zhang D, Du Q, Xu B, Zhang Z, Li B (2010) The actin multigene family in Populus: organization, expression and phylogenetic analysis. Mol Genet Genomics 284:105–119

    Article  CAS  PubMed  Google Scholar 

  • Zhang D, Xu B, Yang X, Zhang Z, Li B (2011) The sucrose synthase gene family in Populus: structure, expression, and evolution. Tree Genet Genomes 7:443–456

    Article  Google Scholar 

  • Zhang J, Mujahid H, Hou Y, Nallamilli BR, Peng Z (2013a) Plant long ncRNAs: a new frontier for gene regulatory control. Am J Plant Sci 4:1038–1045

    Article  Google Scholar 

  • Zhang Z, Zhu Z, Watabe K, Zhang X, Bai C, Xu M, Wu F, Mo Y (2013b) Negative regulation of lncRNA GAS5 by miR-21. Cell Death Differ 20:1558–1568

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhong R, Morrison WH, Himmelsbach DS, Poole FL, Ye Z-H (2000) Essential role of caffeoyl coenzyme A O-methyltransferase in lignin biosynthesis in woody poplar plants. Plant Physiol 124:563–578

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the State Key Basic Research Program of China (No. 2012CB114506), and the Projects of the National Natural Science Foundation of China (No. 31170622, 30872042), and Shandong Province Agriculture Improved Variety Project (No. 2012213).

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Authors and Affiliations

  1. National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing, 100083, People’s Republic of China

    Jinhui Chen, Mingyang Quan & Deqiang Zhang

  2. Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, College of Biological Sciences and Technology, Beijing Forestry University, No. 35, Qinghua East Road, Beijing, 100083, People’s Republic of China

    Jinhui Chen, Mingyang Quan & Deqiang Zhang

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  1. Jinhui Chen
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  2. Mingyang Quan
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Correspondence to Deqiang Zhang.

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Chen, J., Quan, M. & Zhang, D. Genome-wide identification of novel long non-coding RNAs in Populus tomentosa tension wood, opposite wood and normal wood xylem by RNA-seq. Planta 241, 125–143 (2015). https://doi.org/10.1007/s00425-014-2168-1

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