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Genome-wide identification of BXL genes in Populus trichocarpa and their expression under different nitrogen treatments

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Abstract

β-d-xylosidase (BXL) hydrolyzes xylobiose and xylo-oligosaccharides into xylose monomers, and is a rate-limiting enzyme in the degradation of hemicellulose in the cell wall. In this study, ten genes encoding putative BXL proteins were identified in the Populus trichocarpa genome by bioinformatics methods. In the phylogenetic analysis, the PtBXLs formed two subfamilies. PtBXL8 and PtBXL9 were closely related to AtBXL1, an important enzyme in the normal development of the Arabidopsis cell wall structure. Chromosomal distribution and genome synteny analyses revealed two tandem-duplicated gene pairs PtBXL3/4 and PtBXL6/7 on chromosomes II and V, respectively, and six segmental-duplicated gene pairs on chromosomes II, V, VIII, X, and XIV among the PtBXL gene family. Tissue-specific expression data from PlantGenIE indicated that PtBXL2, 4, 5, and 10 were highly expressed in stems. Quantitative real-time RT-PCR analyses revealed that PtBXL4, 5, and 9 were up-regulated in the upper stem in response to the low and high ammonium and nitrate treatments. The influence of nitrogen on the expression of PtBXL4, 5, and 9 genes may affect the formation of the plant secondary cell wall. This comprehensive analysis of the BXL family in poplar provides new insights into their regulation by nitrogen and increases our understanding of the roles of BXLs in hemicellulose metabolism in the secondary cell wall and during plant development.

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References

  • Bailey TL et al (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37:W202–W208

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bewley JD, Burton RA, Morohashi Y, Fincher GB (1997) Molecular cloning of a cDNA encoding a (1 → 4)-β-mannan endohydrolase from the seeds of germinated tomato (Lycopersicon esculentum). Planta 203:454–459

    CAS  PubMed  Google Scholar 

  • Bolser D, Staines DM, Pritchard E, Kersey P (2016) Ensembl plants: integrating tools for visualizing, mining, and analyzing plant genomics data. In: Plant bioinformatics. Springer, pp 115–140

  • Bustamante CA, Rosli HG, Añón MC, Civello PM, Martínez GA (2006) β-Xylosidase in strawberry fruit: isolation of a full-length gene and analysis of its expression and enzymatic activity in cultivars with contrasting firmness. Plant Sci 171:497–504

    CAS  PubMed  Google Scholar 

  • Bustamante CA, Civello PM, Martínez GA (2009) Cloning of the promoter region of β-xylosidase (FaXyl1) gene and effect of plant growth regulators on the expression of FaXyl1 in strawberry fruit. Plant Sci 177:49–56

    CAS  Google Scholar 

  • Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10

    PubMed  PubMed Central  Google Scholar 

  • Cavagnaro T, Smith FA, Lorimer M, Haskard K, Ayling SM, Smith SE (2001) Quantitative development of Paris-type arbuscular mycorrhizas formed between Asphodelus fistulosus and Glomus coronatum. New Phytol 149:105–113

    PubMed  Google Scholar 

  • Chen C, Xia R, Chen H, He Y (2018) TBtools, a toolkit for biologists integrating various biological data handling tools with a user-friendly interface BioRxiv:289660

  • Collins T, Gerday C, Feller G (2005) Xylanases, xylanase families and extremophilic xylanases. FEMS Microbiol Rev 29:3–23

    CAS  PubMed  Google Scholar 

  • Decou R et al (2009) Cloning and expression analysis of a wood-associated xylosidase gene (PtaBXL1) in poplar tension wood. Phytochemistry 70:163–172

    CAS  PubMed  Google Scholar 

  • Di Santo MC, Pagano EA, Sozzi GO (2009) Differential expression of α-l-arabinofuranosidase and α-l-arabinofuranosidase/β-d-xylosidase genes during peach growth and ripening. Plant Physiol Biochem 47:562–569

    Google Scholar 

  • Di Santo MC, Ilina N, Pagano EA, Sozzi GO (2015) A Japanese plum α-l-arabinofuranosidase/β-d-xylosidase gene is developmentally regulated by alternative splicing. Plant Sci 231:173–183

    PubMed  Google Scholar 

  • Dickson R (1989) Carbon and nitrogen allocation in trees. In: Annales des sciences forestières, vol Supplement. EDP Sciences, pp 631s–647s

  • El-Gebali S et al (2018) The Pfam protein families database. Nucleic Acids Res 47:D427–D432

    PubMed Central  Google Scholar 

  • Euring D, Bai H, Janz D, Polle A (2014) Nitrogen-driven stem elongation in poplar is linked with wood modification and gene clusters for stress, photosynthesis and cell wall formation. BMC Plant Biol 14:391

    PubMed  PubMed Central  Google Scholar 

  • Gambino G, Perrone I, Gribaudo I (2008) A rapid and effective method for RNA extraction from different tissues of grapevine and other woody plants. Phytochem Anal 19:520–525

    CAS  PubMed  Google Scholar 

  • Gasteiger E, Hoogland C, Gattiker A, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. In: The proteomics protocols handbook. Springer, pp 571–607

  • Geiger DR, Koch KE, Shieh W-J (1996) Effect of environmental factors on whole plant assimilate partitioning and associated gene expression. J Exp Bot 1229–1238

    CAS  PubMed  Google Scholar 

  • Goodstein DM et al (2011) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–D1186

    PubMed  PubMed Central  Google Scholar 

  • Goujon T et al (2003) AtBXL1, a novel higher plant (Arabidopsis thaliana) putative beta-xylosidase gene, is involved in secondary cell wall metabolism and plant development. Plant J 33:677–690

    CAS  PubMed  Google Scholar 

  • Handford MG, Baldwin TC, Goubet F, Prime TA, Miles J, Yu X, Dupree P (2003) Localisation and characterisation of cell wall mannan polysaccharides in Arabidopsis thaliana. Planta 218:27–36

    CAS  PubMed  Google Scholar 

  • Henrissat B (1991) A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 280:309–316

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heredia A, Jiménez A, Guillén R (1995) Composition of plant cell walls Zeitschrift für Lebensmittel-Untersuchung und. Forschung 200:24–31

    CAS  Google Scholar 

  • Horton P, Park K-J, Obayashi T, Fujita N, Harada H, Adams-Collier C, Nakai K (2007) WoLF PSORT: protein localization predictor. Nucleic Acids Res 35:W585–W587

    PubMed  PubMed Central  Google Scholar 

  • Hrmova M, Varghese JN, De Gori R, Smith BJ, Driguez H, Fincher GB (2001) Catalytic mechanisms and reaction intermediates along the hydrolytic pathway of a plant β-d-glucan glucohydrolase. Structure 9:1005–1016

    CAS  PubMed  Google Scholar 

  • Hrmova M, De Gori R, Smith BJ, Fairweather JK, Driguez H, Varghese JN, Fincher GB (2002) Structural basis for broad substrate specificity in higher plant β-d-glucan glucohydrolases. Plant Cell 14:1033–1052

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hu B, Jin J, Guo A-Y, Zhang H, Luo J, Gao G (2014) GSDS 20: an upgraded gene feature visualization server. Bioinformatics 31:1296–1297

    PubMed  PubMed Central  Google Scholar 

  • Itai A, Yoshida K, Tanabe K, Tamura F (1999) A β-d-xylosidase-like gene is expressed during fruit ripening in Japanese pear (Pyrus pyrifolia Nakai). J Exp Bot 50:877–878

    CAS  Google Scholar 

  • Jiao Y et al (2017) Phenylalanine as a nitrogen source induces root growth and nitrogen-use efficiency in Populus ×canescens. Tree Physiol 38:1–17

    Google Scholar 

  • Knob A, Terrasan CF, Carmona E (2010) β-Xylosidases from filamentous fungi: an overview. World J Microbiol Biotechnol 26:389–407

    CAS  Google Scholar 

  • Kraiser T, Gras DE, Gutiérrez AG, González B, Gutiérrez RA (2011) A holistic view of nitrogen acquisition in plants. J Exp Bot 62:1455–1466

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lan T, Gao J, Zeng Q-Y (2013) Genome-wide analysis of the LEA (late embryogenesis abundant) protein gene family in Populus trichocarpa. Tree Genet Genom 9:253–264

    Google Scholar 

  • Lee RC, Hrmova M, Burton RA, Lahnstein J, Fincher GB (2003) Bifunctional family 3 glycoside hydrolases from barley with α-l-arabinofuranosidase and β-d-xylosidase activity characterization, primary structures, and COOH-terminal processing. J Biol Chem 278:5377–5387

    CAS  PubMed  Google Scholar 

  • Lee EJ, Koizumi N, Sano H (2004) Identification of genes that are up-regulated in concert during sugar depletion in Arabidopsis. Plant Cell Environ 27:337–345

    CAS  Google Scholar 

  • Lee EJ, Matsumura Y, Soga K, Hoson T, Koizumi N (2007) Glycosyl hydrolases of cell wall are induced by sugar starvation in Arabidopsis. Plant Cell Physiol 48:405–413

    CAS  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    CAS  PubMed  Google Scholar 

  • Liu C-C et al (2012) Genome-wide identification and characterization of a dehydrin gene family in poplar (Populus trichocarpa). Plant Mol Biol Report 30:848–859

    CAS  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

    CAS  PubMed  Google Scholar 

  • Lu Y et al (2019) Competing endogenous RNA networks underlying anatomical and physiological characteristics of poplar wood in acclimation to low nitrogen availability. Plant Cell Physiol 60:2478–2495

    PubMed  Google Scholar 

  • Luo Z-B, Langenfeld-Heyser R, Calfapietra C, Polle A (2005) Influence of free air CO2 enrichment (EUROFACE) and nitrogen fertilisation on the anatomy of juvenile wood of three poplar species after coppicing. Trees 19:109–118

    Google Scholar 

  • Miller D, Hable W, Gottwald J, Ellard-Ivey M, Demura T, Lomax T, Carpita N (1997) Connections: the hard wiring of the plant cell for perception, signaling, and response. Plant Cell 9:2105

    CAS  PubMed  PubMed Central  Google Scholar 

  • Minic Z, Rihouey C, Do CT, Lerouge P, Jouanin L (2004) Purification and characterization of enzymes exhibiting β-d-xylosidase activities in stem tissues of Arabidopsis. Plant Physiol 135:867–878

    CAS  PubMed  PubMed Central  Google Scholar 

  • Navarro A, Barton NH (2003) Chromosomal speciation and molecular divergence—accelerated evolution in rearranged chromosomes. Science 300:321–324

    CAS  PubMed  Google Scholar 

  • Novaes E et al (2009) Quantitative genetic analysis of biomass and wood chemistry of Populus under different nitrogen levels. New Phytol 182:878–890

    CAS  PubMed  Google Scholar 

  • Obel N, Porchia AC, Scheller HV (2002) Dynamic changes in cell wall polysaccharides during wheat seedling development. Phytochemistry 60:603–610

    CAS  PubMed  Google Scholar 

  • Pettengill EA, Parmentier-Line C, Coleman GD (2012) Evaluation of qPCR reference genes in two genotypes of Populus for use in photoperiod and low-temperature studies. BMC Res Notes 5:366

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pitre FE, Cooke JE, Mackay JJ (2007) Short-term effects of nitrogen availability on wood formation and fibre properties in hybrid poplar. Trees 21:249–259

    Google Scholar 

  • Pitre FE et al (2010) High nitrogen fertilization and stem leaning have overlapping effects on wood formation in poplar but invoke largely distinct molecular pathways. Tree Physiol 30:1273–1289

    CAS  PubMed  Google Scholar 

  • Potter SC, Luciani A, Eddy SR, Park Y, Lopez R, Finn RD (2018) HMMER web server: 2018 update. Nucleic Acids Res 46:W200–W204

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rahman AS, Sugitani N, Hatsu M, Takamizawa K (2003) A role of xylanase, α-l-arabinofuranosidase, and xylosidase in xylan degradation. Can J Microbiol 49:58–64

    CAS  PubMed  Google Scholar 

  • Rajoka M (2007) Kinetic parameters and thermodynamic values of β-xylosidase production by Kluyveromyces marxianus. Biores Technol 98:2212–2219

    CAS  Google Scholar 

  • Showalter AM (1993) Structure and function of plant cell wall proteins. Plant Cell 5:9

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sinnott ML (1990) Catalytic mechanism of enzymic glycosyl transfer. Chem Rev 90:1171–1202

    CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Sunna A, Antranikian G (1997) Xylanolytic enzymes from fungi and bacteria. Crit Rev Biotechnol 17:39–67

    CAS  PubMed  Google Scholar 

  • Tang H, Bowers JE, Wang X, Ming R, Alam M, Paterson AH (2008) Synteny and collinearity in plant genomes. Science 320:486–488

    CAS  PubMed  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tuncer M, Ball AS (2003) Co-operative actions and degradation analysis of purified xylan-degrading enzymes from Thermomonospora fusca BD25 on oat-spelt xylan. J Appl Microbiol 94:1030–1035

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Xu Z et al (2017a) Identification and expression analyses of the alanine aminotransferase (AlaAT) gene family in poplar seedlings. Sci Rep 7:45933

    CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Z et al (2017b) Genome-wide identification and expression profile analysis of CCH gene family in Populus. PeerJ 5:e3962

    PubMed  PubMed Central  Google Scholar 

  • Zhang J et al (2015) Hsf and Hsp gene families in Populus: genome-wide identification, organization and correlated expression during development and in stress responses. BMC Genom 16:181

    Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (No. 31600534 and 31570648), Natural Science Foundation of Heilongjiang Province, China (C2018009), Special Fund for Basic Scientific research operation Fee of Central University (2572017EA05) and The 111 project (B16010).

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Author notes

  1. Jinyuan Chen and Chunpu Qu contributed to the work equally and should be regarded as co-first authors.

Authors and Affiliations

  1. Key Laboratory of Saline-Alkali Vegetation Ecology Restoration (Northeast Forestry University), Ministry of Education, Harbin, 150040, People’s Republic of China

    Jinyuan Chen, Ruhui Chang, Juanfang Suo & Zhiru Xu

  2. College of Life Science, Northeast Forestry University, Harbin, 150040, People’s Republic of China

    Jinyuan Chen, Ruhui Chang, Juanfang Suo & Zhiru Xu

  3. State Key Laboratory of Tree Genetics and Breeding (Northeast Forestry University), School of Forestry, Northeast Forestry University, Harbin, 150040, People’s Republic of China

    Chunpu Qu, Jiajie Yu, Xue Sun, Guanjun Liu & Zhiru Xu

  4. School of Forestry, Northeast Forestry University, Harbin, 150040, People’s Republic of China

    Chunpu Qu, Jiajie Yu, Xue Sun & Guanjun Liu

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  1. Jinyuan Chen
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  2. Chunpu Qu
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  3. Ruhui Chang
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  4. Juanfang Suo
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  8. Zhiru Xu
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Contributions

JC and CQ conceived and designed the study, JC and CQ performed most of the experiments, RC and JS conducted the sampling, JY and XS performed bioinformatics calculations, GL and ZX processed and analyzed the data, and JC, CQ, and ZX wrote the manuscript.

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Correspondence to Zhiru Xu.

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Chen, J., Qu, C., Chang, R. et al. Genome-wide identification of BXL genes in Populus trichocarpa and their expression under different nitrogen treatments. 3 Biotech 10, 57 (2020). https://doi.org/10.1007/s13205-020-2061-5

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