Abstract
Aspen (Populus tremuloides) is a temperate North American tree species with a geographical distribution more extensive than any other tree species on the continent. Because it is economically important for pulp and paper industries and ecologically important for its role as a foundation species in forest ecosystems, the decline of aspen in large portions of its range is of serious concern. The availability and annotation of the black cottonwood (Populus trichocarpa) genome enables a range of high throughput sequencing approaches that can be used to understand rangewide patterns of genetic variation, adaptation, and responses to environmental challenges in other Populus species, including aspen. Gene expression studies are particularly useful for understanding the molecular basis of ecological responses, but are limited by the availability of transcriptome data. We explored the aspen transcriptome through the use of high-throughput sequencing with two main goals: (1) characterization of the expressed portion of the P. tremuloides genome in leaves and (2) assessment of variation in gene expression among genets collected from distinct latitudes but reared in a common garden. We also report a large single nucleotide polymorphism dataset that provides the groundwork for future studies of aspen evolution and ecology, and we identify a set of differentially expressed genes across individuals and population boundaries for the leaf transcriptome of P. tremuloides.
Similar content being viewed by others
References
Bajgain P, Richardson BA, Price JC, Cronn RC, Udall JA (2011) Transcriptome characterization and polymorphism detection between subspecies of big sagebrush (Artemisia tridentata). BMC Genomics 12:370
Bashir A, Bansal V, Bafna V (2010) Designing deep sequencing experiments: detecting structural variation and estimating transcript abundance. BMC Genomics 11:385
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc Series B (Methodological) 57:289–300
Beritognolo I, Harfouche A, Brilli F, Prosperini G, Gaudet M, Brosché M, Salani F, Kuzminsky E, Auvinen P, Paulin L (2011) Comparative study of transcriptional and physiological responses to salinity stress in two contrasting Populus alba L. genotypes. Tree Physiol 31(12):1335–1355
Bräutigam A, Mullick T, Schliesky S, Weber APM (2011) Critical assessment of assembly strategies for non-model species mRNA-Seq data and application of next-generation sequencing to the comparison of C(3) and C(4) species. J Exp Bot 62:3093–3102
Cervera MT, Storme V, Soto A, Ivens B, Van Montagu M, Rajora OP, Boerjan W (2005) Intraspecific and interspecific genetic and phylogenetic relationships in the genus Populus based on AFLP markers. TAG Theoretical Appl Genet 111(7):1440–1456
Chen JH, Sun H, Wen J, Yang YP (2010) Molecular phylogeny of Salix L. (Salicaceae) inferred from three chloroplast datasets and its systematic implications. Taxon 59(1):29–37
Chen K, Peng Y, Wang Y, Korpelainen H, Li C (2007) Genetic relationships among poplar species in section Tacamahaca (Populus L.) from western Sichuan, China. Plant Sci 172(2):196–203
Chong DKX, Yang RC, Yeh FC (1994) Nucleotide divergence between populations of trembling aspen (Populus tremuloides) estimated with RAPDS. Curr Genet 26(4):374–376
Cohen D, Bogeat-Triboulot MB, Tisserant E, Balzergue S, Martin-Magniette ML, Lelandais G, Ningre N, Renou JP, Tamby JP, Le Thiec D (2010) Comparative transcriptomics of drought responses in Populus: a meta-analysis of genome-wide expression profiling in mature leaves and root apices across two genotypes. BMC Genomics 11(1):630
Cole CT (2005) Allelic and population variation of microsatellite loci in aspen (Populus tremuloides). New Phytol 167:155–164
Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18):3674–3676
Coppe A, Pujolar JM, Maes GE, Larsen PF, Hansen MM, Bernatchez L, Zane L, Bortoluzzi S (2010) Sequencing, de novo annotation and analysis of the first Anguilla anguilla transcriptome: EeelBase opens new perspectives for the study of the critically endangered European eel. BMC Genomics 11:635
Cronn R, Liston A, Parks M, Gernandt DS, Shen R, Mockler T (2008) Multiplex sequencing of plant chloroplast genomes using Solexa sequencing-by-synthesis technology. Nucl Acids Res 36:e122
Di Y, Schafer DW, Cumbie JS, Chang JH (2011) The NBP negative binomial model for assessing differential gene expression from RNA-Seq. Stat Appl Genet Mol Biol 10:art24
Eckenwalder J (1977) North American cottonwoods (Populus, Salicaceae) of sections Abaso and Aigeros. J Arnold Arboret 58:193–208
Eckert AJ, Bower AD, Wegrzyn JL, Pande B, Jermstad KD, Krutovsky KV, Clair JBS, Neale DB (2009) Asssociation genetics of coastal Douglas Fir (Pseudotsuga menziesu var. menziesii, Pinaceae). I. cold-hardiness related traits. Genetics 182(4):1289–1302
Ellison CE, Hall C, Kowbel D, Welch J, Brem RB, Glass NL, Taylor JW (2011) Population genomics and local adaptation in wild isolates of a model microbial eukaryote. Proc Nat Acad Sci (USA) 108:2831–2836
Fang Z, Cui X (2011) Design and validation issues in RNA-seq experiments. Brief Bioinform 12:280–287
Fisher RA (1922) On the interpretation of χ2 from contingency tables, and the calculation of P. J Roy Stat Soc 85(1):87–94
Fladung M, Buschbom J (2009) Identification of single nucleotide polymorphisms in different Populus species. Trees-Struct Funct 23(6):1199–1212
Frey BR, Lieffers VJ, Landhausser SM (2004) Predicting landscape patterns of aspen dieback: mechanisms and knowledge gaps. Canad J Forest Res 34(7):1379–1390
Geraldes A, Pang J, Thiessen N, Cezard T, Moore R, Zhao Y, Tam A, Wang S, Friedmann M, Birol I, Jones SJM, Cronk QCB, Douglas CJ (2011) SNP discovery in black cottonwood (Populus trichocarpa) by population transcriptome resequencing. Mol Ecol Resour 11:81–92
Grisel N, Zoller S, Künzli-Gontarczyk M, Lampart T, Münsterkötter M, Brunner I, Bovet L, Métraux J-P, Sperisen C (2010) Transcriptome responses to aluminum stress in roots of aspen (Populus tremula). BMC Plant Biol 10:15
Hamanishi ET, Raj S, Wilkins O, Thomas BR, Mansfield SD, Plant AL, Campbell MM (2010) Intraspecific variation in the Populus balsamifera drought transcriptome. Plant Cell Env 33:1742–1755
Hamzeh M, Dayanandan S (2004) Phylogeny of Populus (Salicaceae) based on nucleotide sequences of chloroplast trnT-trnF region and nuclear rDNA. Amer J Bot 91(9):1398–1408
Hamzeh M, Périnet P, Dayanandan S (2006) Genetic relationships among species of Populus (Salicaceae) based on nuclear genomic data. J Torrey Bot Soc 133(4):519–527
Hogg EH, Brandt JP, Michaelian M (2008) Impacts of a regional drought on the productivity, dieback, and biomass of western Canadian aspen forests. Canad J Forest Res 38:1373–1384
Hogg EH, Hurdle PA (1995) The aspen parkland in western Canada: a dry-climate analogue for the future boreal forest? Water Air Soil Pollut 82(1):391–400
Isebrands JG, McDonal EP, Kruger E, Hendrey G, Percy K, Pregitzer K, Sober J, Karnosky DF (2001) Growth responses of Populus tremuloides clones to interacting elevated carbon dioxide and tropospheric ozone. Environ Pollut 115:359–371
Iverson LR, Prasad AM (2002) Potential redistribution of tree species habitat under five climate change scenarios in the eastern US. For Ecol Manag 155:205–222
Jiang H, Peng S, Zhang S, Li X, Korpelainen H, Li C (2012) Transcriptional profiling analysis in Populus yunnanensis provides insights into molecular mechanisms of sexual differences in salinity tolerance. J Exp Bot 63:3709–3726
Jones JR (1985) Distribution. In: DeByle NV, Winokur RP (eds) Aspen: ecology and management in the western United States. General Technical Report RM-1 19. US Department of Agriculture, Forest Service, Fort Collins, pp 9–10
Kawahara-Miki R, Wada K, Azuma N, Chiba S (2011) Expression profiling without genome sequence information in a non-model species, pandalid shrimp (Pandalus latirostris), by next-generation sequencing. PLoS One 6(10):e26043
Kelleher CT, Wilkin J, Zhuang J, Cortés AJ, Quintero ÁLP, Gallagher TF, Bohlmann J, Douglas CJ, Ellis BE, Ritland K (2012) SNP discovery, gene diversity, and linkage disequilibrium in wild populations of Populus tremuloides. Tree Genet Genomes 8:821–829
Kurz WA, Apps MJ (1999) A 70-year retrospective analysis of carbon fluxes in the Canadian forest sector. Ecol Appl 9(2):526–547
Langmead B, Trapnell C, Pop M, Salzberg S (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10(3):R25
Larsen PE, Sreedasyam A, Trivedi G, Podila GK, Cseke LJ, Collart FR (2011) Using next generation transcriptome sequencing to predict an ectomycorrhizal metabolome. BMC Systems Biol 5:14
Liu Z, Furnier GR (1993) Comparison of allozyme, RFLP, and RAPD markers for revealing genetic variation within and between trembling aspen and bigtooth aspen. Theoret Appl Genet 87(1):97–105
Lund ST, Furnier GR, Mohn CA (1992) Isozyme variation in quaking aspen in Minnesota. Canad J Forest Res 22(4):521–524
Marioni JC, Mason CE, Mane SM, Stephens M, Gilad Y (2008) RNA-seq: an assessment of technical reproducibility and comparison with gene expression arrays. Genome Res 18:1509–1517
Matzkin LM (2008) The molecular basis of host adaptation in cactophilic Drosophila: molecular evolution of a glutathione S-transferase gene (GstD1) in Drosophila mojavensis. Genetics 178(2):1073–1083
Matzkin LM (2012) Population transcriptomics of cactus host shifts in Drosophila mojavensis. Mol Ecol 21:2428–2439
Metzker ML (2009) Sequencing technologies: the next generation. Nature Rev Genet 11(1):31–46
Mitton J, Grant M (1996) Genetic variation and the natural history of quaking aspen. Bioscience 46:25–31
Nagalakshmi U, Wang Z, Waern K, Shou C, Raha D, Gerstein M, Snyder M (2008) The transcriptional landscape of the yeast genome defined by RNA sequencing. Science (New York, NY) 320:1344–1349
Novaes E, Drost D, Farmerie W, Pappas G, Grattapaglia D, Sederoff R, Kirst M (2008) High-throughput gene and SNP discovery in Eucalyptus grandis, an uncharacterized genome. BMC Genomics 9(1):312
Perkins TT, Kingsley RA, Fookes MC, Gardner PP, James KD, Yu L, Assefa SA, He M, Croucher NJ, Pickard DJ (2009) A strand-specific RNA-Seq analysis of the transcriptome of the typhoid bacillus Salmonella Typhi. PLoS Genetics 5(7):e1000569
Qiu Q, Ma T, Hu Q, Liu B, Wu Y, Zhou H, Wang Q, Wang J, Liu J (2011) Genome-scale transcriptome analysis of the desert poplar, Populus euphratica. Tree Physiol 31(4):452–461
Quesada T, Li Z, Dervinis C, Li Y, Bocock PN, Tuskan GA, Casella G, Davis JM, Kirst M (2008) Comparative analysis of the transcriptomes of Populus trichocarpa and Arabidopsis thaliana suggests extensive evolution of gene expression regulation in angiosperms. New Phytol 180:408–420
Rehfeldt GE, Ferguson DE, Crookston NL (2009) Aspen, climate, and sudden decline in western USA. For Ecol Manag 258:2353–2364
Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140
Schier GA (1978) Vegetative propagation of Rocky Mountain aspen. USDA Forest Service General Technical Report INT-44
Severin AJ, Woody JL, Bolon Y-T, Joseph B, Diers BW, Farmer AD, Muehlbauer GJ, Nelson RT, Grant D, Specht JE, Graham MA, Cannon SB, May GD, Vance CP, Shoemaker RC (2010) RNA-Seq Atlas of Glycine max: a guide to the soybean transcriptome. BMC Plant Biol 10:16
Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313(5793):1596
Unneberg P, Strömberg M, Lundeberg J, Jansson S, Sterky F (2005) Analysis of 70,000 EST sequences to study divergence between two closely related Populus species. Tree Genet Genomes 1(3):109–115
Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolutionary tool for transcriptomics. Nature Rev Genet 10:57–63
Worrall JJ, Egeland L, Eager T, Mask RA, Johnson EW, Kemp PA, Shepperd WD (2008) Rapid mortality of Populus tremuloides in southwestern Colorado, USA. For Ecol Manag 255(3):686–696
Zenoni S, Ferrarini A, Giacomelli E, Xumerle L, Fasoli M, Malerba G, Bellin D, Pezzotti M, Delledonne M (2010) Characterization of transcriptional complexity during berry development in Vitis vinifera using RNA-Seq. Plant Physiol 152(4):1787–1795
Zhou S, Campbell TG, Stone EA, Mackay TFC, Anholt RRH (2012) Phenotypic plasticity of the Drosophila transcriptome. PLoS Genetics 8(3):e1002593
Acknowledgments
Thanks to Tim Benedict, Mary Lou Fairweather, and E. Pfalzer for sample collections. Thanks to Tara Jennings for laboratory assistance and Chris Sullivan for biocomputing assistance. This research was funded by the USDA Forest Service Western Forest Transcriptome Survey and National Fire Plan (2012-NFP-GSD-1).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by P. Ingvarsson
Rights and permissions
About this article
Cite this article
Rai, H.S., Mock, K.E., Richardson, B.A. et al. Transcriptome characterization and detection of gene expression differences in aspen (Populus tremuloides). Tree Genetics & Genomes 9, 1031–1041 (2013). https://doi.org/10.1007/s11295-013-0615-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11295-013-0615-y