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Populus euphratica: the transcriptomic response to drought stress

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Abstract

Populus euphratica Olivier is widely established in arid and semiarid regions but lags in the availability of transcriptomic resources in response to water deficiency. To investigate the mechanisms that allow P. euphratica to maintain growth in arid regions, the responses of the plant to soil water deficit were analyzed at a systems level using physiological and pyrosequencing approaches. We generated 218,601 and 287,120 reads from non-stressed control and drought-stressed P. euphratica leaves respectively, totaling over 200 million base pairs. After assembly, 24,013 transcripts were yielded with an average length of 1,128 bp. We determined 2,279 simple sequence repeats, which may have possible information for understanding drought adaption of woody plants. Stomatal closure was inhibited under moderate drought to maintain a relatively high rate of CO2 assimilation and water transportation, which was supposed to be important for P. euphratica to maintain normal growth and develop vigorous root systems in an adverse environment. This was accompanied by strong transcriptional remodeling of stress-perception, signaling and transcription regulation, photoprotective system, oxidative stress detoxification, and other stress responsive genes. In addition, genes involved in stomatal closure inhibition, ascorbate–glutathione pathway and ubiquitin–proteasome system that may specially modulate the drought stress responses of P. euphratica are highlighted. Our analysis provides a comprehensive picture of how P. euphratica responds to drought stress at physiological and transcriptome levels which may help to understand molecular mechanisms associated with drought response and could be useful for genetic engineering of woody plants.

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References

  • Baerenfaller K, Massonnet C, Walsh S, Baginsky S, Bühlmann P, Hennig L, Hirsch-Hoffmann M, Howell KA, Kahlau S, Radziejwoski A (2012) Systems-based analysis of Arabidopsis leaf growth reveals adaptation to water deficit. Mol Syst Biol 8:606

    Article  CAS  PubMed  Google Scholar 

  • Barakat A, DiLoreto DS, Zhang Y, Smith C, Baier K, Powell WA, Wheeler N, Sederoff R, Carlson JE (2009) Comparison of the transcriptomes of American chestnut (Castanea dentata) and Chinese chestnut (Castanea mollissima) in response to the chestnut blight infection. BMC Plant Biol 9:51

    Article  PubMed  Google Scholar 

  • Baud S, Vaultier MN, Rochat C (2004) Structure and expression profile of the sucrose synthase multigene family in Arabidopsis. J Exp Bot 55:397–409

    Article  CAS  PubMed  Google Scholar 

  • Bieniawska Z, Paul Barratt D, Garlick AP, Thole V, Kruger NJ, Martin C, Zrenner R, Smith AM (2007) Analysis of the sucrose synthase gene family in Arabidopsis. Plant J 49:810–828

    Article  CAS  PubMed  Google Scholar 

  • Bogeat-Triboulot MB, Brosché M, Renaut J, Jouve L, Le Thiec D, Fayyaz P, Vinocur B, Witters E, Laukens K, Teichmann T (2007) Gradual soil water depletion results in reversible changes of gene expression, protein profiles, ecophysiology, and growth performance in Populus euphratica, a poplar growing in arid regions. Plant Physiol 143:876–892

    Article  CAS  PubMed  Google Scholar 

  • Bray EA (1997) Plant responses to water deficit. Trends Plant Sci 2:48–54

    Article  Google Scholar 

  • Breshears DD, Myers OB, Meyer CW, Barnes FJ, Zou CB, Allen CD, McDowell NG, Pockman WT (2008) Tree die-off in response to global change-type drought: mortality insights from a decade of plant water potential measurements. Front Ecol Environ 7:185–189

    Article  Google Scholar 

  • Brinker M, Brosche M, Vinocur B, Abo-Ogiala A, Fayyaz P, Janz D, Ottow EA, Cullmann AD, Saborowski J, Kangasjarvi J, Altman A, Polle A (2010) Linking the salt transcriptome with physiological responses of a salt-resistant Populus species as a strategy to identify genes important for stress acclimation. Plant Physiol 154:1697–1709

    Article  CAS  PubMed  Google Scholar 

  • Brosché M, Vinocur B, Alatalo ER, Lamminmaki A, Teichmann T, Ottow EA, Djilianov D, Afif D, Bogeat-Triboulot M, Altman A (2005) Gene expression and metabolite profiling of Populus euphratica growing in the Negev desert. Genome Biol 6:R101

    Article  PubMed  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought—from genes to the whole plant. Funct Plant Biol 30:239–264

    Article  CAS  Google Scholar 

  • Chaves M, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Chen Y, Li W, Xu C (2006) Characterization of photosynthesis of Populus euphratica grown in the arid region. Photosynthetica 44:622–626

    Article  Google Scholar 

  • Cheng MC, Hsieh EJ, Chen JH, Chen HY, Lin TP (2012) Arabidopsis RGLG2, functioning as a RING E3 ligase, interacts with AtERF53 and negatively regulates the plant drought stress response. Plant Physiol 158:363–375

    Article  CAS  PubMed  Google Scholar 

  • Cheong YH, Pandey GK, Grant JJ, Batistic O, Li L, Kim BG, Lee SC, Kudla J, Luan S (2007) Two calcineurin B-like calcium sensors, interacting with protein kinase CIPK23, regulate leaf transpiration and root potassium uptake in Arabidopsis. Plant J 52:223–239

    Article  CAS  PubMed  Google Scholar 

  • 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 21:3674–3676

    Article  CAS  PubMed  Google Scholar 

  • Cruz de Carvalho MH (2008) Drought stress and reactive oxygen species: production, scavenging and signaling. Plant Signal Behav 3:156–165

    Article  PubMed  Google Scholar 

  • Dubey A, Farmer A, Schlueter J, Cannon SB, Abernathy B, Tuteja R, Woodward J, Shah T, Mulasmanovic B, Kudapa H (2011) Defining the transcriptome assembly and its use for genome dynamics and transcriptome profiling studies in pigeonpea (Cajanus cajan L.). DNA Res 18:153–164

    Article  CAS  PubMed  Google Scholar 

  • Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agronom Sustain Dev 29:185–212

    Google Scholar 

  • Fernandez O, Béthencourt L, Quero A, Sangwan RS, Clément C (2010) Trehalose and plant stress responses: friend or foe? Trends Plant Sci 15:409–417

    Article  CAS  PubMed  Google Scholar 

  • Foley JA, DeFries R, Asner GP, Barford C, Bonan G, Carpenter SR, Chapin FS, Coe MT, Daily GC, Gibbs HK, Helkowski JH, Holloway T, Howard EA, Kucharik CJ, Monfreda C, Patz JA, Prentice IC, Ramankutty N, Snyder PK (2005) Global consequences of land use. Science 309:570–574

    Article  CAS  PubMed  Google Scholar 

  • Gao SQ, Chen M, Xu ZS, Zhao CP, Li L, Xu H, Tang Y, Zhao X, Ma YZ (2011) The soybean GmbZIP1 transcription factor enhances multiple abiotic stress tolerances in transgenic plants. Plant Mol Biol 75:537–553

    Article  CAS  PubMed  Google Scholar 

  • Gosti F, Beaudoin N, Serizet C, Webb AAR, Vartanian N, Giraudat J (1999) ABI1 protein phosphatase 2C is a negative regulator of abscisic acid signaling. Plant Cell Online 11:1897–1909

    CAS  Google Scholar 

  • Gries D, Zeng F, Foetzki A, Arndt SK, Bruelheide H, Thomas FM, Zhang X, Runge M (2003) Growth and water relations of Tamarix ramosissima and Populus euphratica on Taklamakan desert dunes in relation to depth to a permanent water table. Plant Cell Environ 26:725–736

    Article  Google Scholar 

  • Griffiths J, Murase K, Rieu I, Zentella R, Zhang ZL, Powers SJ, Gong F, Phillips AL, Hedden P, Sun T (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell Online 18:3399–3414

    Article  CAS  Google Scholar 

  • Guo Y, Huang C, Xie Y, Song F, Zhou X (2010) A tomato glutaredoxin gene SlGRX1 regulates plant responses to oxidative, drought and salt stresses. Planta 232:1499–1509

    Article  CAS  PubMed  Google Scholar 

  • Hajheidari M, Eivazi A, Buchanan BB, Wong JH, Majidi I, Salekdeh GH (2007) Proteomics uncovers a role for redox in drought tolerance in wheat. J Proteome Res 6:1451–1460

    Article  CAS  PubMed  Google Scholar 

  • Hamanishi ET, Campbell MM (2011) Genome-wide responses to drought in forest trees. Forestry 84:273–283

    Article  Google Scholar 

  • Harb A, Krishnan A, Ambavaram MMR, Pereira A (2010) Molecular and physiological analysis of drought stress in Arabidopsis reveals early responses leading to acclimation in plant growth. Plant Physiol 154:1254–1271

    Article  CAS  PubMed  Google Scholar 

  • Hiremath PJ, Farmer A, Cannon SB, Woodward J, Kudapa H, Tuteja R, Kumar A, BhanuPrakash A, Mulaosmanovic B, Gujaria N (2011) Large-scale transcriptome analysis in chickpea (Cicer arietinum L.), an orphan legume crop of the semi-arid tropics of Asia and Africa. Plant Biotechnol J 9:922–931

    Article  CAS  PubMed  Google Scholar 

  • Hu H, Boisson-Dernier A, Israelsson-Nordström M, Böhmer M, Xue S, Ries A, Godoski J, Kuhn JM, Schroeder JI (2009) Carbonic anhydrases are upstream regulators of CO2-controlled stomatal movements in guard cells. Nat Cell Biol 12:87–93

    Article  PubMed  Google Scholar 

  • Huang D, Wu W, Abrams SR, Cutler AJ (2008) The relationship of drought-related gene expression in Arabidopsis thaliana to hormonal and environmental factors. J Exp Bot 59:2991–3007

    Article  CAS  PubMed  Google Scholar 

  • Hukin D, Cochard H, Dreyer E, Thiec DL, Bogeat-Triboulot MB (2005) Cavitation vulnerability in roots and shoots: does Populus euphratica Oliv., a poplar from arid areas of Central Asia, differ from other poplar species? J Exp Bot 56:2003–2010

    Article  CAS  PubMed  Google Scholar 

  • Hundertmark M, Hincha DK (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 9:118

    Article  PubMed  Google Scholar 

  • Isokpehi RD, Simmons SS, Cohly HHP, Ekunwe SIN, Begonia GB, Ayensu WK (2011) Identification of drought-responsive universal stress proteins in viridiplantae. Bioinform Biol Insights 5:41

    Article  CAS  PubMed  Google Scholar 

  • Kent WJ (2002) BLAT—the BLAST-like alignment tool. Genome Res 12:656–664

    CAS  PubMed  Google Scholar 

  • Kerepesi I, Galiba G (2000) Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Sci 40:482–487

    Article  CAS  Google Scholar 

  • Kiran Kumar Ghanti S, Sujata K, Vijay Kumar B, Nataraja Karba N, Janardhan Reddy K, Srinath Rao M, Kavi Kishor P (2011) Heterologous expression of P5CS gene in chickpea enhances salt tolerance without affecting yield. Biol Plant 55:634–640

    Article  Google Scholar 

  • Ko JH, Yang SH, Han KH (2006) Upregulation of an Arabidopsis RING-H2 gene, XERICO, confers drought tolerance through increased abscisic acid biosynthesis. Plant J 47:343–355

    Article  CAS  PubMed  Google Scholar 

  • Kondrák M, Marincs F, Kalapos B, Juhász Z, Bánfalvi Z (2011) Transcriptome analysis of potato leaves expressing the trehalose-6-phosphate synthase 1 gene of yeast. PLoS One 6:e23466

    Article  PubMed  Google Scholar 

  • Lee BR, Jin YL, Jung WJ, Avice JC, Morvan-Bertrand A, Ourry A, Park CW, Kim TH (2008) Water-deficit accumulates sugars by starch degradation—not by de novo synthesis—in white clover leaves (Trifolium repens). Physiol Plant 134:403–411

    Article  CAS  PubMed  Google Scholar 

  • Li BS, Qin YR, Duan H, Yin WL, Xia XL (2011) Genome-wide characterization of new and drought stress responsive microRNAs in Populus euphratica. J Exp Bot 62:3765–3779

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT Method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lu T, Lu G, Fan D, Zhu C, Li W, Zhao Q, Feng Q, Zhao Y, Guo Y, Huang X, Han B (2010) Function annotation of the rice transcriptome at single-nucleotide resolution by RNA-seq. Genome Res 20:1238–1249

    Article  CAS  PubMed  Google Scholar 

  • Marshall A, Aalen RB, Audenaert D, Beeckman T, Broadley MR, Butenko MA, Caño-Delgado AI, de Vries S, Dresselhaus T, Felix G (2012) Tackling drought stress: RECEPTOR-LIKE KINASES present new approaches. Plant Cell Online 24:2262–2278

    Article  CAS  Google Scholar 

  • Merewitz EB, Gianfagna T, Huang BR (2011) Protein accumulation in leaves and roots associated with improved drought tolerance in creeping bentgrass expressing an ipt gene for cytokinin synthesis. J Exp Bot 62:5311–5333

    Article  CAS  PubMed  Google Scholar 

  • Mittler R, Zilinskas BA (2004) Regulation of pea cytosolic ascorbate peroxidase and other antioxidant enzymes during the progression of drought stress and following recovery from drought. Plant J 5:397–405

    Article  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  CAS  PubMed  Google Scholar 

  • Molina C, Rotter B, Horres R, Udupa SM, Besser B, Bellarmino L, Baum M, Matsumura H, Terauchi R, Kahl G (2008) SuperSAGE: the drought stress-responsive transcriptome of chickpea roots. BMC Genomics 9:553

    Article  PubMed  Google Scholar 

  • Mori IC, Murata Y, Yang Y, Munemasa S, Wang YF, Andreoli S, Tiriac H, Alonso JM, Harper JF, Ecker JR (2006) CDPKs CPK6 and CPK3 function in ABA regulation of guard cell S-type anion-and Ca2+-permeable channels and stomatal closure. PLoS Biol 4:e327

    Article  PubMed  Google Scholar 

  • Murgia I, Tarantino D, Vannini C, Bracale M, Carravieri S, Soave C (2004) Arabidopsis thaliana plants overexpressing thylakoidal ascorbate peroxidase show increased resistance to Paraquat-induced photooxidative stress and to nitric oxide-induced cell death. Plant J 38:940–953

    Article  CAS  PubMed  Google Scholar 

  • Nezames CD, Deng XW (2012) The COP9 signalosome: its regulation of cullin-based E3 ubiquitin ligases and role in photomorphogenesis. Plant Physiol 160:38–46

    Article  CAS  PubMed  Google Scholar 

  • Noctor G, Veljovic-Jovanovic S, Driscoll S, Novitskaya L, Foyer CH (2002) Drought and oxidative load in the leaves of C3 plants: a predominant role for photorespiration? Ann Bot 89:841–850

    Article  CAS  PubMed  Google Scholar 

  • Ogata H, Goto S, Sato K, Fujibuchi W, Bono H, Kanehisa M (1999) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 27:29–34

    Article  CAS  PubMed  Google Scholar 

  • Okamoto M, Kuwahara A, Seo M, Kushiro T, Asami T, Hirai N, Kamiya Y, Koshiba T, Nambara E (2006) CYP707A1 and CYP707A2, which encode abscisic acid 8′-hydroxylases, are indispensable for proper control of seed dormancy and germination in Arabidopsis. Plant Physiol 141:97–107

    Article  CAS  PubMed  Google Scholar 

  • Ottow EA, Brinker M, Teichmann T, Fritz E, Kaiser W, Brosche M, Kangasjarvi J, Jiang XN, Polle A (2005) Populus euphratica displays apoplastic sodium accumulation, osmotic adjustment by decreases in calcium and soluble carbohydrates, and develops leaf succulence under salt stress. Plant Physiol 139:1762–1772

    Article  CAS  PubMed  Google Scholar 

  • Padmalatha KV, Dhandapani G, Kanakachari M, Kumar S, Dass A, Patil DP, Rajamani V, Kumar K, Pathak R, Rawat B, Leelavathi S, Reddy PS, Jain N, Powar KN, Hiremath V, Katageri IS, Reddy MK, Solanke AU, Reddy VS, Kumar PA (2012) Genome-wide transcriptomic analysis of cotton under drought stress reveal significant down-regulation of genes and pathways involved in fibre elongation and up-regulation of defense responsive genes. Plant Mol Biol 78:223–246

    Article  CAS  PubMed  Google Scholar 

  • Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Curr Opin Plant Biol 14:290–295

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Rodríguez P, Riaño-Pachón DM, Corrêa LGG, Rensing SA, Kersten B, Mueller-Roeber B (2010) PlnTFDB: updated content and new features of the plant transcription factor database. Nucleic Acids Res 38:D822–D827

    Article  PubMed  Google Scholar 

  • Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig W, Peplies J, Glöckner FO (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35:7188–7196

    Article  CAS  PubMed  Google Scholar 

  • 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 31:452–461

    Article  PubMed  Google Scholar 

  • Raghavendra AS, Gonugunta VK, Christmann A, Grill E (2010) ABA perception and signalling. Trends Plant Sci 15:395–401

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez MCS, Edsgard D, Hussain SS, Alquezar D, Rasmussen M, Gilbert T, Nielsen BH, Bartels D, Mundy J (2010) Transcriptomes of the desiccation-tolerant resurrection plant Craterostigma plantagineum. Plant J 63:212–228

    Article  CAS  PubMed  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386

    CAS  PubMed  Google Scholar 

  • Samuel D, Ganesh G, Yang PW, Chang MM, Wang SL, Hwang KC, Yu C, Jayaraman G, Kumar TKS, Trivedi VD (2000) Proline inhibits aggregation during protein refolding. Protein Sci 9:344–352

    Article  CAS  PubMed  Google Scholar 

  • Santoro MG (2000) Heat shock factors and the control of the stress response. Biochem Pharmacol 59:55–63

    Article  CAS  PubMed  Google Scholar 

  • Sato S, Hirakawa H, Isobe S, Fukai E, Watanabe A, Kato M, Kawashima K, Minami C, Muraki A, Nakazaki N (2011) Sequence analysis of the genome of an oil-bearing tree, Jatropha curcas L. DNA Res 18:65–76

    Article  CAS  PubMed  Google Scholar 

  • Sharma A, Dwivedi B, Singh B, Kumar K (1999) Introduction of Populus euphratica in Indian semi-arid trans-Gangetic Plains. Ann For 7:1–8

    Google Scholar 

  • Söderman E, Mattsson J, Engström P (2002) The Arabidopsis homeobox gene ATHB-7 is induced by water deficit and by abscisic acid. Plant J 10:375–381

    Article  Google Scholar 

  • Suorsa M, Järvi S, Grieco M, Nurmi M, Pietrzykowska M, Rantala M, Kangasjärvi S, Paakkarinen V, Tikkanen M, Jansson S (2012) PROTON GRADIENT REGULATION5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions. Plant Cell Online 24:2934–2948

    Article  CAS  Google Scholar 

  • Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2002) Important roles of drought-and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29:417–426

    Article  CAS  PubMed  Google Scholar 

  • Taji T, Seki M, Satou M, Sakurai T, Kobayashi M, Ishiyama K, Narusaka Y, Narusaka M, Zhu JK, Shinozaki K (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol 135:1697–1709

    Article  CAS  PubMed  Google Scholar 

  • Tan W, Blake TJ, Boyle TJB (2006) Drought tolerance in faster-and slower-growing black spruce (Picea mariana) progenies: II. Osmotic adjustment and changes of soluble carbohydrates and amino acids under osmotic stress. Physiol Plant 85:645–651

    Article  Google Scholar 

  • Tang L, Kwon SY, Kim SH, Kim JS, Choi JS, Cho KY, Sung CK, Kwak SS, Lee HS (2006) Enhanced tolerance of transgenic potato plants expressing both superoxide dismutase and ascorbate peroxidase in chloroplasts against oxidative stress and high temperature. Plant Cell Rep 25:1380–1386

    Article  CAS  PubMed  Google Scholar 

  • Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939

    Article  CAS  PubMed  Google Scholar 

  • Todaka D, Matsushima H, Morohashi Y (2000) Water stress enhances β-amylase activity in cucumber cotyledons. J Exp Bot 51:739–745

    Article  CAS  PubMed  Google Scholar 

  • Tognetti VB, Van Aken O, Morreel K, Vandenbroucke K, Van De Cotte B, De Clercq I, Chiwocha S, Fenske R, Prinsen E, Boerjan W (2010) Perturbation of indole-3-butyric acid homeostasis by the UDP-glucosyltransferase UGT74E2 modulates Arabidopsis architecture and water stress tolerance. Plant Cell Online 22:2660–2679

    Article  CAS  Google Scholar 

  • 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 313:1596–1604

    Article  CAS  PubMed  Google Scholar 

  • Verdoy D, De la Pena TC, Redondo FJ, Lucas MM, Pueyo JJ (2006) Transgenic Medicago truncatula plants that accumulate proline display nitrogen-fixing activity with enhanced tolerance to osmotic stress. Plant Cell Environ 29:1913–1923

    Article  CAS  PubMed  Google Scholar 

  • Wang L, Feng Z, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26:136–138

    Article  PubMed  Google Scholar 

  • Wang ZY, Xiong L, Li W, Zhu JK, Zhu J (2011) The plant cuticle is required for osmotic stress regulation of abscisic acid biosynthesis and osmotic stress tolerance in Arabidopsis. Plant Cell Online 23:1971–1984

    Article  CAS  Google Scholar 

  • Watanabe S, Kojima K, Ide Y, Sasaki S (2000) Effects of saline and osmotic stress on proline and sugar accumulation in Populus euphratica in vitro. Plant Cell Tissue Organ Cult 63:199–206

    Article  CAS  Google Scholar 

  • Yamada M, Morishita H, Urano K, Shiozaki N, Yamaguchi-Shinozaki K, Shinozaki K, Yoshiba Y (2005) Effects of free proline accumulation in petunias under drought stress. J Exp Bot 56:1975–1981

    Article  CAS  PubMed  Google Scholar 

  • Yan DH, Fenning T, Tang S, Xia XL, Yin WL (2012) Genome-wide transcriptional response of Populus euphratica to long-term drought stress. Plant Sci 195:24–35

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Nguyen HT, Blum A (1999) Genetic analysis of osmotic adjustment in crop plants. J Exp Bot 50:291–302

    CAS  Google Scholar 

  • Zhang H, Jin J, Tang L, Zhao Y, Gu X, Gao G, Luo J (2011) PlantTFDB 2.0: update and improvement of the comprehensive plant transcription factor database. Nucleic Acids Res 39:D1114–D1117

    Article  CAS  PubMed  Google Scholar 

  • Zhao Y, Thammannagowda S, Staton M, Tang S, Xia X, Yin W, Liang H (2013) An EST dataset for Metasequoia glyptostroboides buds: the first EST resource for molecular genomics studies in Metasequoia. Planta 237:755–770

    Google Scholar 

  • Zhou Y, Gao F, Liu R, Feng J, Li H (2012) De novo sequencing and analysis of root transcriptome using 454 pyrosequencing to discover putative genes associated with drought tolerance in Ammopiptanthus mongolicus. BMC Genomics 13:266

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This research was supported by grants from the Ministry of Science and Technology of China (2011BAD38B01, 2009CB119101), the National Natural Science Foundation of China (31070597, 31270656, 30972339), the Scientific Research and Graduate Training Joint Programs from BMEC (Regulation of Tree WUE, Stress Resistance Mechanism of Poplar), and the National Institute of Food and Agriculture, USDA (SC-1700324 with a Clemson University Experiment Station technical contribution number of 6109). We thank Prof. Dr. Jiandong Qi (School of Information Science and Technology, Beijing Forestry University, Beijing, China) for his technical assistance in computer programming. We are also grateful to Yinghua Zhang, Chuyu Ye, Lily Guo, Haitao Xing and Bosheng Li for their helpful comments on the manuscript and technical assistance.

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Correspondence to Xinli Xia or Weilun Yin.

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11103_2013_107_MOESM1_ESM.tif

Overview of BlastX search results. BlastX search results of all the 24,013 PUTs against NCBI’s non-redundant, ExPASy Swiss-Prot and Populus trichocarpa genome annotation v2.0 databases using different E-value cutoffs. Blast cut-off of E ≤ 1e-5(left). Blast cut-off of E ≤ 1e-20(right). (TIFF 223 kb)

11103_2013_107_MOESM2_ESM.tif

Similarity of P. euphratica PUTs compared with model plants. PUTs with a cutoff E-value ≤ 1e-5 were marked as significant matches. The sequences with a cutoff E-value > 1e-5 were considered to be poor matches. (TIFF 243 kb)

11103_2013_107_MOESM3_ESM.tif

Overview of differentially regulated genes involved in different metabolic processes. Five hundred and two differentially expressed PUTs showed consistent expression pattern during drought in both high-throughput sequencing and microarray profiling. These PUTs were grouped under different functional categories using MapMan software. Gene transcripts that are induced or repressed as a result of drought stress are shown in red and green colours respectively as shown in the colour bar ranging from -3.0 to +3.0 (log2FC), one block represents one gene. (TIFF 621 kb)

11103_2013_107_MOESM4_ESM.tif

Distribution of transcription factor families. a, Distribution of 1,829 PUTs that were identified as TFs. DETs means Differentially Expressed Transcripts. NS represents transcripts having no significant changes in gene expression. b, Distribution of the transcription factor families differentially expressed under drought stress. The number in each bars indicates the PUTs in each transcription factor family. (TIFF 1406 kb)

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SSRs detection (XLS 1613 kb)

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Tang, S., Liang, H., Yan, D. et al. Populus euphratica: the transcriptomic response to drought stress. Plant Mol Biol 83, 539–557 (2013). https://doi.org/10.1007/s11103-013-0107-3

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