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Genome-Wide Analysis of Gene Expression in Response to Drought Stress in Populus simonii

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Abstract

Drought tolerance varies considerably in different species of Populus, and is a complex trait, involving the interplay of a vast array of genes. Although Populus simonii is one of the most important commercial plantation tree species in China, genes controlling drought-stress tolerance in this organism have not yet been identified. Here, transcriptomic changes during drought stress in P. simonii were detected using an Affymetrix GeneChip. In total, 1,028 transcripts were identified as differentially expressed under drought stress, of which 496 transcripts increased and 532 decreased in abundance (two-way ANOVA, fold change >4 and P < 0.01). Expression changes of 20 candidate genes were validated by real-time PCR, indicating significant differences between the controls and water-deficit treatments. Gene annotation demonstrated that the majority of these P. simonii genes encode products involved in phytohormone metabolism, osmoregulation, and oxidative stress. Based on gene ontology (GO) classification, the increased genes were classified into six significantly enriched GO terms involved in 64 pathways, and the decreased genes were classified into 39 significantly enriched GO terms representing 42 pathways. Bioinformatics analysis showed that the differential expression of plant hormone-related, transcription factor, cytochrome P450 gene superfamily, carbohydrate metabolism, and amino acid transporter genes may contribute to drought-stress tolerance in P. simonii. Our study provides global gene expression patterns during drought stress and will be valuable for further study of the molecular mechanisms of drought tolerance in P. simonii.

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Abbreviations

ABA:

Abscisic acid

IAA:

Indole-3-acetic acid

JGI:

Joint Genome Institute

TAIR:

The Arabidopsis information resource

qRT-PCR:

Real-time quantitative reverse transcription PCR

GO:

Gene Ontology

HSP:

Heat shock protein

TF:

Transcription factor

EL:

Electrolyte leakage

POD:

Peroxidase

MDA:

Malondialdehyde

PAL:

Phenylalanine ammonia lyase

FC:

Fold change

D:

Water-deficit treatment

CK:

Control

DEGs:

Differentially expressed genes

References

  • Baloglu M, Oz M, Oktem H, Yucel M (2012) Expression analysis of TaNAC69-1 and TtNAMB-2, wheat NAC family transcription factor genes under abiotic stress conditions in durum wheat (Triticum turgidum). Plant Mol Biol Report 30:1246–1252

    Article  CAS  Google Scholar 

  • Bari R, Jones JDG (2009) Role of plant hormones in plant defense responses. Plant Mol Biol 69:473–488

    Article  PubMed  CAS  Google Scholar 

  • Baud S, Guyon V, Kronenberger J, Wuilleme S, Miquel M, Caboche M, Lepiniec L, Rochat C (2003) Multifunctional acetyl-CoA carboxylase 1 is essential for very long chain fatty acid elongation and embryo development in Arabidopsis. Plant J 33:75–86

    Article  PubMed  CAS  Google Scholar 

  • Blatt MR (2000) Cellular signaling and volume control in stomatal movements in plants. Annu Rev Cell Dev Biol 16:221–241

    Article  PubMed  CAS  Google Scholar 

  • Brown DE, Rashotte AM, Murphy AS, Normanly J, Tague BW, Peer WA, Taiz L, Muday GK (2001) Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol 126:524–535

    Article  PubMed  CAS  Google Scholar 

  • Brunner AM, Busov VB, Strauss SH (2004) Poplar genome sequence: functional genomics in an ecologically dominant plant species. Trends Plant Sci 9:49–56

    Article  PubMed  CAS  Google Scholar 

  • Caruso A, Chefdor F, Carpin S, Depierreux C, Delmotte FM, Kahlem G, Morabito D (2008) Physiological characterization and identification of genes differentially expressed in response to drought induced by PEG 6000 in Populus canadensis leaves. J Plant Physiol 165:932–941

    Article  PubMed  CAS  Google Scholar 

  • Cohen D, Bogeat-Triboulot MB, Tisserant E, Balzergue S, Martin-Magniette ML, Lelandais G, Ningre N, Renou JP, Tamby JP, Le Thiec D, Hummel I (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 11:630

    Article  PubMed  Google Scholar 

  • Ditt RF, Nester EW, Comai L (2001) Plant gene expression response to Agrobacterium tumefaciens. Proc Natl Acad Sci USA 98:10954–10959

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Dudley SA (1996) Differing selection on plant physiological traits in response to environmental water availability: a test of adaptive hypotheses. Evolution 50:92–102

    Article  Google Scholar 

  • Hadiarto T, Tran LSP (2011) Progress studies of drought-responsive genes in rice. Plant Cell Rep 30:297–310

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • 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 Environ 33:1742–1755

    Article  PubMed  CAS  Google Scholar 

  • Hansen JD, Pyee J, Xia Y, Wen TJ, Robertson DS, Kolattukudy PE, Nikolau BJ, Schnable PS (1997) The glossy1 locus of maize and an epidermis-specific cDNA from Kleinia odora define a class of receptor-like proteins required for the normal accumulation of cuticular waxes. Plant Physiol 113:1091–1100

    Article  PubMed  CAS  Google Scholar 

  • Heilman PE, Hinckley TM, Roberts DA, Ceulemans R (1996) Production physiology. In: Stettler RF, Bradshaw HDJ, Heilman PE, Hinckley TM (eds) Biology of Populus and its implications for management and conservation. NRC, Ottawa, pp 459–490

    Google Scholar 

  • Hirner A, Ladwig F, Stransky H, Okumoto S, Keinath M, Harms A, Frommer WB, Koch W (2006) Arabidopsis LHT1 is a high-affinity transporter for cellular amino acid uptake in both root epidermis and leaf mesophyll. Plant Cell 18:1931–1946

    Article  PubMed  CAS  Google Scholar 

  • Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611

    Article  CAS  Google Scholar 

  • Hu WH, Hu GC, Han B (2009) Genome-wide survey and expression profiling of heat shock proteins and heat shock factors revealed overlapped and stress specific response under abiotic stresses in rice. Plant Sci 176:583–590

    Article  CAS  Google Scholar 

  • Jiang YY, Dong JL, Chen RJ, Gao XL, Xu ZJ (2011) Isolation of a novel PP2C gene from rice and its response to abiotic stresses. Afr J Biotechnol 10:7143–7154

    Article  CAS  Google Scholar 

  • Jin H, Huang F, Cheng H, Song H, Yu D (2012) Overexpression of the GmNAC2 gene, an NAC transcription factor, reduces abiotic stress tolerance in Tobacco. Plant Mol Biol Report :1–8

  • Kandlbinder A, Finkemeier I, Wormuth D, Hanitzsch M, Dietz KJ (2004) The antioxidant status of photosynthesizing leaves under nutrient deficiency: redox regulation, gene expression and antioxidant activity in Arabidopsis thaliana. Physiol Plant 120:63–73

    Article  PubMed  CAS  Google Scholar 

  • Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M (2012) KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res 40:D109–D114

    Article  PubMed  CAS  Google Scholar 

  • Krishnan A, Pereira A (2008) Integrative approaches for mining transcriptional regulatory programs in Arabidopsis. Brief Funct Genomic Proteomic 7:264–274

    Article  PubMed  CAS  Google Scholar 

  • Lamesch P, Berardini TZ, Li D, Swarbreck D, Wilks C, Sasidharan R, Muller R, Dreher K, Alexander DL, Garcia-Hernandez M, Karthikeyan AS, Lee CH, Nelson WD, Ploetz L, Singh S, Wensel A, Huala E (2012) The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res 40:D1202–D1210

    Article  PubMed  CAS  Google Scholar 

  • Lee BH, Lee H, Xiong L, Zhu JK (2002) A mitochondrial complex I defect impairs cold-regulated nuclear gene expression. Plant Cell 14:1235–1251

    Article  PubMed  CAS  Google Scholar 

  • Lubkowitz M (2011) The oligopeptide transporters: a small gene family with a diverse group of substrates and functions? Mol Plant 4:407–415

    Article  PubMed  CAS  Google Scholar 

  • Lutts S, Kinet JM, Bouharmont J (1996) NaCl-induced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance. Ann Bot 78:389–398

    Article  CAS  Google Scholar 

  • Mariutto M, Duby F, Adam A, Bureau C, Fauconnier ML, Ongena M, Thonart P, Dommes J (2011) The elicitation of a systemic resistance by Pseudomonas putida BTP1 in tomato involves the stimulation of two lipoxygenase isoforms. BMC Plant Biol 11:29

    Article  PubMed  CAS  Google Scholar 

  • Marron N, Delay D, Petit JM, Dreyer E, Kahlem G, Delmotte FM, Brignolas F (2002) Physiological traits of two Populus × euramericana clones, Luisa Avanzo and Dorskamp, during a water stress and re-watering cycle. Tree Physiol 22:849–858

    Article  PubMed  CAS  Google Scholar 

  • Monclus R, Dreyer E, Villar M, Delmotte FM, Delay D, Petit JM, Barbaroux C, Thiec D, Brechet C, Brignolas F (2006) Impact of drought on productivity and water use efficiency in 29 genotypes of Populus deltoides × Populus nigra. New Phytol 169:765–777

    Article  PubMed  Google Scholar 

  • Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) NAC transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:97–103

    Article  PubMed  CAS  Google Scholar 

  • Narusaka Y, Narusaka M, Seki M, Umezawa T, Ishida J, Nakajima M, Enju A, Shinozaki K (2004) Crosstalk in the responses to abiotic and biotic stresses in Arabidopsis: analysis of gene expression in cytochrome P450 gene superfamily by cDNA microarray. Plant Mol Biol 55:327–342

    Article  PubMed  CAS  Google Scholar 

  • Niewiadomski P, Knappe S, Geimer S, Fischer K, Schulz B, Unte US, Rosso MG, Ache P, Flugge UI, Schneider A (2005) The Arabidopsis plastidic glucose 6-phosphate/phosphate translocator GPT1 is essential for pollen maturation and embryo sac development. Plant Cell 17:760–775

    Article  PubMed  CAS  Google Scholar 

  • Nishizawa A, Yabuta Y, Shigeoka S (2008) Galactinol and raffinose constitute a novel function to protect plants from oxidative damage. Plant Physiol 147:1251–1263

    Article  PubMed  CAS  Google Scholar 

  • Rao MV, Paliyath G, Ormrod DP (1996) Ultraviolet-B- and ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. Plant Physiol 110:125–136

    Article  PubMed  CAS  Google Scholar 

  • Rosegrant MW, Cline SA (2003) Global food security: challenges and policies. Science 302:1917–1919

    Article  PubMed  CAS  Google Scholar 

  • Seo PJ, Park CM (2009) Auxin homeostasis during lateral root development under drought condition. Plant Signal Behav 4:1002–1004

    Article  PubMed  CAS  Google Scholar 

  • Shafroth PB, Stromberg JC, Patten DT (2000) Woody riparian vegetation response to different alluvial water table regimes. West N Am Nat 60(1):66–76

    Google Scholar 

  • Sjodin 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 

  • Song YP, Wang ZL, Bo WH, Ren YY, Zhang ZY, Zhang DQ (2012) Transcriptional profiling by cDNA-AFLP analysis showed differential transcript abundance in response to water stress in Populus hopeiensis. BMC Genomics 13:286

    Article  PubMed  CAS  Google Scholar 

  • Su X, Chu Y, Li H, Hou Y, Zhang B, Huang Q, Hu Z, Huang R, Tian Y (2011) Expression of multiple resistance genes enhances tolerance to environmental stressors in transgenic poplar (Populus × euramericana ‘Guariento’). PLoS One 6:e24614

    Article  PubMed  CAS  Google Scholar 

  • Tardieu F, Tuberosa R (2010) Dissection and modelling of abiotic stress tolerance in plants. Curr Opin Plant Biol 13:206–212

    Article  PubMed  Google Scholar 

  • Tuskan GA, Difazio S, Jansson S et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604

    Article  PubMed  CAS  Google Scholar 

  • Valliyodan B, Nguyen HT (2006) Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Curr Opin Plant Biol 9:189–195

    Article  PubMed  CAS  Google Scholar 

  • Wasson AP, Pellerone FI, Mathesius U (2006) Silencing the flavonoid pathway in Medicago truncatula inhibits root nodule formation and prevents auxin transport regulation by rhizobia. Plant Cell 18:71617–71629

    Google Scholar 

  • Wei Z, Du Q, Zhang J, Li B, Zhang D (2012) Genetic diversity and population structure in Chinese indigenous poplar (Populus simonii) populations using microsatellite markers. Plant Mol Biol Report. doi:10.1007/s11105-012-0527-2 (Online first)

  • Wilkins O, Waldron L, Nahal H, Provart NJ, Campbell MM (2009) Genotype and time of day shape the Populus drought response. Plant J 60:703–715

    Article  PubMed  CAS  Google Scholar 

  • Yang L, Ji W, Gao P, Li Y, Cai H, Bai X, Chen Q, Zhu Y (2012) GsAPK, an ABA-activated and Calcium-independent SnRK2-type kinase from G. soja, mediates the regulation of plant tolerance to salinity and ABA stress. PLoS One 7:e33838

    Article  PubMed  CAS  Google Scholar 

  • Yin CY, Duan BL, Wang X, Li CY (2004) Morphological and physiological responses of two contrasting poplar species to drought stress and exogenous abscisic acid application. Plant Sci 167:1091–1097

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Zhang DQ, Xu BH, Yang XH, Zhang ZY, Li BL (2011) The sucrose synthase gene family in Populus: structure, expression, and evolution. Tree Genet Genomes 7:443–456

    Article  Google Scholar 

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Acknowledgments

This work was supported by grants from the following sources: the Forestry Public Benefic Research Program (No. 201204306), Project of the National Natural Science Foundation of China (No. 30600479, 30872042), Program for New Century Excellent Talents in University (No. NCET-07-0084).

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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, Yuepeng Song, He Zhang & Deqiang Zhang

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

    Jinhui Chen, Yuepeng Song, He Zhang & Deqiang Zhang

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  1. Jinhui Chen
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  2. Yuepeng Song
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  3. He Zhang
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  4. Deqiang Zhang
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Correspondence to Deqiang Zhang.

Additional information

All samples were uploaded to Gene Expression Omnibus (http://www.ncbi.nlm.nih.ov/geo/) accession number GSE37608.

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Chen, J., Song, Y., Zhang, H. et al. Genome-Wide Analysis of Gene Expression in Response to Drought Stress in Populus simonii . Plant Mol Biol Rep 31, 946–962 (2013). https://doi.org/10.1007/s11105-013-0563-6

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