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Transcriptome sequencing and comparative analysis of diploid and autotetraploid Paulownia australis

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Abstract

Paulownia is a fast-growing tree native to China. It can provide high-quality timber and a green environment for humans and has been planted in many countries. Compared with diploid Paulownia australis, autotetraploid P. australis exhibits predominance in terms of yields, qualities, growth, and resistance to stress. However, the molecular and biological mechanisms of its predominant characteristics are still unclear. We performed paired-end sequencing of the transcriptomes of diploid and autotetraploid P. australis plants using the Illumina/Solexa Genome Analyzer platform and compared changes in the expression of genes after chromosome doubling. We obtained a total of 48,445,468 and 46,437,758 high-quality reads from diploid P. australis (PA2) and autotetraploid P. australis (PA4), respectively. After assembly, 90,881 (PA2) and 88,566 (PA4) unigenes were obtained. The unigenes from both transcriptomes were then assembled into 93,300 all-unigenes, which included 50,892 clusters and 42,408 singletons. The all-unigene sequences were searched against public protein databases (Nr, Nt, Swiss-Prot, KOG, and KEGG) using BLASTX with a cutoff E-value of 10−5. Gene expression levels in the two libraries were compared, and a total of 8851 differentially expressed unigenes were identified. A large number of unigenes were found to be related to carbohydrate and energy metabolism, biosynthesis of cell wall, and stress tolerance. Many of the differentially expressed P. australis genes were attributable to chromosome doubling between the PA2 and PA4 plants. Functional analysis revealed variations in the mechanism of growth and stress resistance between PA2 and PA4.

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Abbreviations

GAIIx :

Genome Analyzer IIx

ABA:

Abscisic acid

Nr:

NCBI nonredundant protein sequence database

Nt:

NCBI nucleotide databases

COG:

Clusters of orthologous

GO:

Gene Ontology

KEGG:

Kyoto Encyclopedia of Genes and Genomes

DEU:

Differentially expressed unigenes

qRT-PCR:

Quantitative real-time PCR

CDS:

Coding sequences

FPKM:

Fragments per kilobyte per million fragments

FDR:

false discovery rate

CAT:

Catalase

SOD:

Superoxide dismutases

MDAR:

Monodehydroascorbate reductase

DHAR:

Dehydroascorbate reductase

GPX:

Glutathione peroxidase

APX:

Ascorbate peroxidase

GR:

Glutathione transferase

PSI:

Photosystem I

Pn:

Net photosynthetic rate

References

  • Abe H, Urao T, Ito T, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell Online 15(1):63–78

    Article  CAS  Google Scholar 

  • Agarwal M, Hao Y, Kapoor A, Dong CH, Fujii H, Zheng X, Zhu JK (2006) A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem 281(49):37636–37645

    Article  CAS  PubMed  Google Scholar 

  • Albersheim P (1976) The primary cell wall. In: Bonner J, Varner JE (eds) Plant biochemistry, 3rd edition. Academic Press, New York, pp 225–274

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Lorian Schaeffer and Barbara Wold Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628

    Article  CAS  PubMed  Google Scholar 

  • Audic S, Claverie JM (1997) The significance of digital gene expression profiles. Genome Res 7(10):986–995

    CAS  PubMed  Google Scholar 

  • 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. doi:10.1186/1471-2164-12-370

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Banks JA, Nishiyama T, Hasebe M, Bowman JL, Gribskov M, dePamphilis C, Albert VA, Aono N, Aoyama T, Ambrose BA, Ashton NW, Axtell MJ, Barker E, Barker MS, Bennetzen JL, Bonawitz ND, Chapple C, Cheng C, Correa LG, Dacre M, DeBarry J, Dreyer I, Elias M, Engstrom EM, Estelle M, Feng L, Finet C, Floyd SK, Frommer WB, Fujita T, Gramzow L, Gutensohn M, Harholt J, Hattori M, Heyl A, Hirai T, Hiwatashi Y, Ishikawa M, Iwata M, Karol KG, Koehler B, Kolukisaoglu U, Kubo M, Kurata T, Lalonde S, Li K, Li Y, Litt A, Lyons E, Manning G, Maruyama T, Michael TP, Mikami K, Miyazaki S, Morinaga S, Murata T, Mueller-Roeber B, Nelson DR, Obara M, Oguri Y, Olmstead RG, Onodera N, Petersen BL, Pils B, Prigge M, Rensing SA, Riano-Pachon DM, Roberts AW, Sato Y, Scheller HV, Schulz B, Schulz C, Shakirov EV, Shibagaki N, Shinohara N, Shippen DE, Sorensen I, Sotooka R, Sugimoto N, Sugita M, Sumikawa N, Tanurdzic M, Theissen G, Ulvskov P, Wakazuki S, Weng JK, Willats WW, Wipf D, Wolf PG, Yang L, Zimmer AD, Zhu Q, Mitros T, Hellsten U, Loque D, Otillar R, Salamov A, Schmutz J, Shapiro H, Lindquist E, Lucas S, Rokhsar D, Grigoriev IV (2011) The Selaginella genome identifies genetic changes associated with the evolution of vascular plants. Science 332(6032):960–963. doi:10.1126/science.1203810

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Baskin TI (2001) On the alignment of cellulose microfibrils by cortical microtubules: a review and a model. Protoplasma 215(1–4):150–171

    Article  CAS  PubMed  Google Scholar 

  • Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188

    Article  Google Scholar 

  • Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21(18):3674–3676. doi:10.1093/bioinformatics/bti610

    Article  CAS  PubMed  Google Scholar 

  • Dai XY, Xu YY, Ma QB, Xu WY, Wang T, Xue YB, Chong K (2007) Overexpression of an R1R2R3 MYB gene, OsMYB3R-2, increases tolerance to freezing, drought, and salt stress in transgenic Arabidopsis. Plant Physiol 143(4):1739–1751. doi:10.1104/pp. 106.094532

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Davies WJ, Zhang J (1991) Root signals and the regulation of growth and development of plants in drying soil. Annu Rev Plant Biol 42(1):55–76

    Article  CAS  Google Scholar 

  • Ding ZH, Li SM, An XL, Liu X, Qin HJ, Wang DW (2009) Transgenic expression of MYB15 confers enhanced sensitivity to abscisic acid and improved drought tolerance in Arabidopsis thaliana. J Gen Genomics Yi Chuan Xue Bao 36(1):17–29. doi:10.1016/S1673-8527(09)60003-5

    Article  CAS  Google Scholar 

  • Du L, Li YC, Mu HZ, Zhang TY, Liu FF, Huang HJ, Liu GF (2011) Photosynthetic characteristics of tetraploid and diploid Betula platyphylla. J Northeast For Univ 2:002

    Google Scholar 

  • Einspahr DW (1984) Duction and utilization of triploid hybrid Aspen. Iowa State J Res 58(4):401–409

    Google Scholar 

  • Eifler I (1960) The individual results of crosses between B. verrucosa and B. pubescens. Silvae Genet 9(6):159–165

    Google Scholar 

  • Einspahr DW, Van Buijtenen JP, Peckham JR (1963) Natural variation and heritability in triploid aspen. Silvae Genet 12(2):51–58

    Google Scholar 

  • Fan GQ, Wei Z, Yang ZQ (2009) Induction of autotetraploid of Paulownia australis and its in vitro plantlet regeneration. J Northwest A & F Univ-Nat Sci Ed 37(10):83–90

    Google Scholar 

  • Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S (2004) Architecture of the photosynthetic oxygen-evolving center. Science 303(5665):1831–1838. doi:10.1126/science.1093087

    Article  CAS  PubMed  Google Scholar 

  • Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29(7):644–652. doi:10.1038/nbt.1883

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hall T (2008) Paulownia: an agroforestry gem. Trees Life J 3:3

    Google Scholar 

  • Iseli C, Jongeneel CV, Bucher P (1999) ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. Proceedings/International Conference on Intelligent Systems for Molecular Biology; ISMB International Conference on Intelligent Systems for Molecular Biology :138–148

  • Johnsson H (1953) Development of triploid and diploid Populus tremula during the juvenile period. Z Forstgenet 2(4):73–77

    Google Scholar 

  • Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36(Database issue):D480–D484. doi:10.1093/nar/gkm882

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kavar T, Maras M, Kidrič M, Šuštar-Vozlič J, Meglič V (2008) Identification of genes involved in the response of leaves of Phaseolus vulgaris to drought stress. Mol Breed 21(2):159–172

    Article  CAS  Google Scholar 

  • Keegstra K, Talmadge KW, Bauer WD, Albersheim P (1973) The structure of plant cell walls: III. A model of the walls of suspension-cultured sycamore cells based on the interconnections of the macromolecular components. Plant Physiol 51(1):188–197

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li WL, Berlyn GP, Ashton PMS (1996) Polyploids and their structural and physiological characteristics relative to water deficit in Betula papyrifera (Betulaceae). Am J Bot 83:15–20

    Article  Google Scholar 

  • Li W, Zhang CY, Lu QT, Wen XG, Lu CM (2011a) The combined effect of salt stress and heat shock on proteome profiling in Suaeda salsa. J Plant Physiol 168(15):1743–1752. doi:10.1016/j.jplph.2011.03.018

    Article  CAS  PubMed  Google Scholar 

  • Li XG, Wu HX, Southerton SG (2011b) Transcriptome profiling of wood maturation in Pinus radiata identifies differentially expressed genes with implications in juvenile and mature wood variation. Gene 487(1):62–71. doi:10.1016/j.gene.2011.07.028

    Article  CAS  PubMed  Google Scholar 

  • Liao Y, Zou HF, Wang HW, Zhang WK, Ma B, Zhang JS, Chen SY (2008) Soybean GmMYB76, GmMYB92, and GmMYB177 genes confer stress tolerance in transgenic Arabidopsis plants. Cell Res 18(10):1047–1060. doi:10.1038/cr.2008.280

    Article  CAS  PubMed  Google Scholar 

  • Liu QZ, Liu P, Zhao HJ, Sun YG (2002) Biological and photosynthetic physiological characteristics of autotetraploid ‘Royal Gala’ apple. Sci Agric Sin 35:1573–1578

    CAS  Google Scholar 

  • Masterson J (1994) Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms. Science 264(5157):421–424. doi:10.1126/science.264.5157.421

    Article  CAS  PubMed  Google Scholar 

  • Mu HZ, Liu ZJ, Lin L, Li HY, Jiang J, Liu GF (2012) Transcriptomic analysis of phenotypic changes in birch (Betula platyphylla) autotetraploids. Int J Mol Sci 13(10):13012–13029. doi:10.3390/ijms131013012

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nongpiur R, Soni P, Karan R, Singla-Pareek SL, Pareek A (2012) Histidine kinases in plants: cross talk between hormone and stress responses. Plant Signal Behav 7(10):1230–1237

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Paredez AR, Somerville CR, Ehrhardt DW (2006) Visualization of cellulose synthase demonstrates functional association with microtubules. Science 312(5779):1491–1495. doi:10.1126/science.1126551

    Article  CAS  PubMed  Google Scholar 

  • Park HC, Kim ML, Kim HS, Park JH, Jung MS, Shen M, Kang CH, Kim MC, Lee SY, Cho MJ, Chung WS, Yun DJ (2010) Specificity of DNA sequences recognized by the zinc-finger homeodomain protein, GmZF-HD1 in soybean. Phytochemistry 71(16):1832–1838. doi:10.1016/j.phytochem.2010.07.010

    Article  CAS  PubMed  Google Scholar 

  • Peltier JB, Emanuelsson O, Kalume DE, Ytterberg J, Friso G, Rudella A, Liberles DA, Soderberg L, Roepstorff P, von Heijne G, van Wijk KJ (2002) Central functions of the lumenal and peripheral thylakoid proteome of Arabidopsis determined by experimentation and genome-wide prediction. Plant Cell 14(1):211–236

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pertea G, Huang X, Liang F, Antonescu V, Sultana R, Karamycheva S, Lee Y, White J, Cheung F, Parvizi B, Tsai J, Quackenbush J (2003) TIGR gene indices clustering tools (TGICL): a software system for fast clustering of large EST datasets. Bioinformatics 19(5):651–652

    Article  CAS  PubMed  Google Scholar 

  • Pustovoitova TN, Eremin GV, Rassvetaeva EG, Zhdanova NE, Zholkevich VN (1996) Drought resistance, recovery capacity, and phytohormone content in polyploid plum leaves. Russ J Plant Physiol 43:232–235

    CAS  Google Scholar 

  • Romeis T, Ludwig AA, Martin R, Jones JD (2001) Calcium-dependent protein kinases play an essential role in a plant defence response. EMBO J 20(20):5556–5567. doi:10.1093/emboj/20.20.5556

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Romero-Aranda R, Bondada B, Syvertsen J, Grosser J (1997) Leaf characteristics and net gas exchange of diploid and autotetraploid citrus. Ann Bot 79(2):153–160

    Article  Google Scholar 

  • Saleh B, Allario T, Dambier D, Ollitrault P, Morillon R (2008) Tetraploid citrus rootstocks are more tolerant to salt stress than diploid. C R Biol 331(9):703–710

    Article  PubMed  Google Scholar 

  • Selvendran RR, O’Neill MA (1987) Isolation and analysis of cell walls from plant material. Methods Biochem Anal 32:25–153

    Article  CAS  PubMed  Google Scholar 

  • Singhal GS, Renger G, Sopory SK, Irrgang KD, Govindjee (1999) Concepts in photobiology: photosynthesis and photomorphogenesis. Springer PP:23–24

  • Soltis PS (2005) Ancient and recent polyploidy in angiosperms. New Phytol 166(1):5–8

    Article  PubMed  Google Scholar 

  • Spokevicius AV, Southerton SG, MacMillan CP, Qiu D, Gan S, Tibbits JF, Moran GF, Bossinger G (2007) Beta-tubulin affects cellulose microfibril orientation in plant secondary fibre cell walls. Plant J Cell Mol Biol 51(4):717–726. doi:10.1111/j.1365-313X.2007.03176.x

    Article  CAS  Google Scholar 

  • Torres TT, Metta M, Ottenwalder B, Schlotterer C (2008) Gene expression profiling by massively parallel sequencing. Genome Res 18(1):172–177. doi:10.1101/gr.6984908

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tran LSP, Nakashima K, Sakuma Y, Osakabe Y, Qin F, Simpson SD, Maruyama K, Fujita Y, Shinozaki K, Yamaguchi-Shinozaki K (2007) Co-expression of the stress-inducible zinc finger homeodomain ZFHD1 and NAC transcription factors enhances expression of the ERD1 gene in Arabidopsis. Plant J 49(1):46–63

    Article  CAS  PubMed  Google Scholar 

  • Wang ZY, Fang BP, Chen JY, Zhang XJ, Luo ZX, Huang LF, Chen XL, Li YJ (2010) De novo assembly and characterization of root transcriptome using Illumina paired-end sequencing and development of cSSR markers in sweetpotato (Ipomoea batatas). BMC Genomics 11(1):726

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang Z, Gerstein M, Snyder M (2009) RNA-Seq: a revolution-ary tool for transcriptomics. Nat Rev Genet 10(1):57–63

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Warner DA, Ku MS, Edwards GE (1987) Photosynthesis, leaf anatomy, and cellular constituents in the polyploid C(4) grass Panicum virgatum. Plant Physiol 84(2):461–466

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wei WL, Qi XQ, Wang LH, Zhang YX, Hua W, Li DH, Lv HX, Zhang XR (2011) Characterization of the sesame (Sesamum indicum L.) global transcriptome using Illumina paired-end sequencing and development of EST-SSR markers. BMC Genomics 12:451. doi:10.1186/1471-2164-12-451

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yamada K, Lim J, Dale JM, Chen H, Shinn P, Palm CJ, Southwick AM, Wu HC, Kim C, Nguyen M, Pham P, Cheuk R, Karlin-Newmann G, Liu SX, Lam B, Sakano H, Wu T, Yu G, Miranda M, Quach HL, Tripp M, Chang CH, Lee JM, Toriumi M, Chan MM, Tang CC, Onodera CS, Deng JM, Akiyama K, Ansari Y, Arakawa T, Banh J, Banno F, Bowser L, Brooks S, Carninci P, Chao Q, Choy N, Enju A, Goldsmith AD, Gurjal M, Hansen NF, Hayashizaki Y, Johnson-Hopson C, Hsuan VW, Iida K, Karnes M, Khan S, Koesema E, Ishida J, Jiang PX, Jones T, Kawai J, Kamiya A, Meyers C, Nakajima M, Narusaka M, Seki M, Sakurai T, Satou M, Tamse R, Vaysberg M, Wallender EK, Wong C, Yamamura Y, Yuan S, Shinozaki K, Davis RW, Theologis A, Ecker JR (2003) Empirical analysis of transcriptional activity in the Arabidopsis genome. Science 302(5646):842–846. doi:10.1126/science.1088305

    Article  CAS  PubMed  Google Scholar 

  • Ye J, Fang L, Zheng HK, Zhang Y, Chen J, Zhang ZJ, Wang J, Li ST, Li RQ, Bolund L, Wang J (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34(Web Server issue):W293–W297. doi:10.1093/nar/gkl031

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhai XQ, Zhang XS, Zhao ZL, Deng MJ, Fan GQ (2012) Study on wood physical properties of tetraploid. Paulownia Fortunei J Henan Agric Univ 46(6):651–654

    Google Scholar 

  • Zhang XS, Zhai XQ, Fan GQ, Deng MJ, Zhao ZL (2013a) Observation on microstructure of leaves and stress tolerance analysis of different tetraploid Paulownia. J Henan Agric Univ 46:646–650

    Google Scholar 

  • Zhang XS, Zhai XQ, Zhao ZL, Deng MJ, Fan GQ (2013b) Study on the photosynthetic characteristics of different species of tetraploid Paulownia plants. J Henan Agric Univ 47(4):400–404

    Google Scholar 

  • Zhu J, Shi H, Lee BH, Damsz B, Cheng S, Stirm V, Zhu JK, Hasegawa PM, Bressan RA (2004) An Arabidopsis homeodomain transcription factor gene, HOS9, mediates cold tolerance through a CBF-independent pathway. Proc Natl Acad Sci U S A 101(26):9873–9878. doi:10.1073/pnas.0403166101

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhu ZH, Chao CJ, Lu XY, Xiong YG (1986) Paulownia in China: cultivation and utilization. International Development Research Centre, Beijing, pp 1–2

    Google Scholar 

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Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (Grant No. 30271082, 30571496, U1204309), by the Outstanding Talents Project of Henan Province (Grant No. 122101110700), and by the Science and Technology Innovation Team Project of Zhengzhou City (Grant No. 121PCXTD515).

Conflict of interest

The authors declare no conflict of interest.

Data archiving statement

The raw sequence data are available at the NIH Short Read Archive database (http://www.ncbi.nlm.nih.gov/sra) under the accession number SRP032321 (Alias: PRJNA224949).

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Correspondence to Guoqiang Fan.

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Communicated by D. B. Neale

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Xu, E., Fan, G., Niu, S. et al. Transcriptome sequencing and comparative analysis of diploid and autotetraploid Paulownia australis . Tree Genetics & Genomes 11, 5 (2015). https://doi.org/10.1007/s11295-014-0828-8

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