Skip to main content
Log in

Cloning and analysis of cellulose synthase genes (CesA) in Acacia mangium

  • Original Article
  • Published:
Tree Genetics & Genomes Aims and scope Submit manuscript

Abstract

Cellulose synthase (CesA) plays a major regulatory role in the cellulose synthesis pathway in plants and is an important factor in controlling wood fiber quality and yield. In this study, two cellulose synthase genes, AmCesA1 and AmCesA2, were cloned from Acacia mangium using transcriptome de novo sequencing analysis and RACE. In silico analysis revealed that AmCesA1 cDNA was 3793 bp in size, had a 3249 bp ORF, and encoded a 1082 amino acid protein; AmCesA2 cDNA was 3743 bp in size, had a 3228 bp ORF, and encoded a 1075 amino acid protein. AmCesA1 was determined to have six transmembrane regions, and AmCesA2 was determined to have eight transmembrane regions. Cluster analysis showed that AmCesA1 had high degrees of similarity with Glycine max GmCesA1 and Arachis duranensis AdCesA1. AmCesA2 had high degrees of similarity with Leucaena leucocephala LlCesA7 and LlCesA8. Southern blot analysis showed that multiple copies of AmCesA1 were present in the Acacia mangium genome, but only a single copy of AmCesA2 was present. Real-time RT-PCR showed that both genes were widely expressed in roots, stems, and leaves, but AmCesA2 was more highly expressed in stems. The two genes responded to GA3, 6-BA, and MeJA treatments, and the response to GA3 was relatively strong. Here, we presume that the two genes are involved in the formation of primary cell walls and that AmCesA2 is also involved in the formation of secondary cell walls. The expression of both genes was upregulated under different hormone treatments, which indicated that the two genes positively regulate the hormone response.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Albert H, Dale EC, Lee E, Ow DW (1995) Site-specific integration of DNA into wild-type and mutant lox sites placed in the plant genome. Plant J 7:649–659

    Article  CAS  PubMed  Google Scholar 

  • Arioli T, Peng L, Betzner AS, Burn J, Wittke W, Herth W, Camilleri C, Höfte H, Plazinski J, Birch R, Cork A, Glover J, Redmond J, Williamson RE (1998) Molecular analysis of cellulose biosynthesis in Arabidopsis. Science 279:717–720

    Article  CAS  PubMed  Google Scholar 

  • Burton RA, Shirley NJ, King BJ, Harvey AJ, Fincher GB (2004) The CesA gene family of barley. Quantitative analysis of transcripts reveals two groups of co-expressed genes. Plant Physiol 134:224–236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burton RA, Gidley MJ, Fincher GB (2010) Heterogeneity in the chemistry, structure and function of plant cell walls. Nat Chem Biol 6:724–732

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Shao Z, Wang H, Zhu Y, Zhu S, Huang MR (2015) Cloning and expression of PeAFB genes in Populus. Sci Silvae Sin 51:26–32

    Google Scholar 

  • Cosgrove DJ (2014) Re-constructing our models of cellulose and primary cell wall assembly. Curr Opin Plant Biol 22:122–131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Denness L, McKenna JF, Segonzac C, Wormit A, Madhou P, Bennett M, Mansfield J, Zipfel C, Hamann T (2011) Cell wall damage-induced lignin biosynthesis is regulated by a reactive oxygen species- and jasmonic acid-dependent process in Arabidopsis. Plant Physiol 156:1364–1374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doblin MS, Kurek I, Wilk JD, Delmer DP (2002) Cellulose biosynthesis in plants: from genes to rosettes. Plant Cell Physiol 43:1407–1420

    Article  CAS  PubMed  Google Scholar 

  • Ellis C, Turner JG (2001) The Arabidopsis mutant cev1 has constitutively active jasmonate and ethylene signal pathways and enhanced resistance to pathogens. Plant Cell Online 13:1025–1033

    Article  CAS  Google Scholar 

  • Ellis C, Karafyllidis I, Wasternack C, Turner JR (2002) The Arabidopsis mutant cevl links cell wall signaling to jasmonate and ethylene responses. Plant Cell 14:1557–1566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fagard M, Desnos T, Desprez T, Goubet F, Refregier G, Mouille G, McCann M, Rayon C, Vernhettes S, Höfte H (2000) PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. Plant Cell 12:2409–2423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fernandes AN, Thomas LH, Altaner CM, Callow P, Forsyth VT, Apperley DC, Kennedy CJ, Jarvis MC (2011) Nanostructure of cellulose microfibrils in spruce wood. Proc Natl Acad Sci U S A 108:1195–1203

    Article  Google Scholar 

  • Gening ML, Tsvetkov YE, Pier GB, Nifantiev NE (2007) Synthesis of beta-(1-->6)-linked glucosamine oligosaccharides corresponding to fragments of the bacterial surface polysaccharide poly-N-acetylglucosamine. Carbohydr Res 342:567–575

    Article  CAS  PubMed  Google Scholar 

  • Genovesi V, Fornalé S, Fry SC, Ruel K, Ferrer PO, Encina AO, Sonbol FM, Bosch J, Puigdomènech P, Rigau J, CaparrósRuiz D (2008) ZmXTH1, a new xyloglucan endotransglucosylase/hydrolase in maize, affects cell wall structure and composition in Arabidopsis thaliana. J Exp Bot 59:875–889

    Article  CAS  PubMed  Google Scholar 

  • Gonneau M, Desprez T, Guillot A, Vernhettes S, Höfte H (2014) Catalytic subunit stoichiometry within the cellulose synthase complex. Plant Physiol 166:1709–1712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grant SR (1999) Dissecting the mechanisms of post transcriptional gene silencing: divide and conquer. Cell 96:303–306

    Article  CAS  PubMed  Google Scholar 

  • Hill JL Jr, Hammudi MB, Tien M (2014) The Arabidopsis cellulose synthase complex: a proposed hexamer of cesa trimers in an equimolar stoichiometry. Plant Cell 26:4834–4842

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holland N, Holland D, Helentjaris T, Dhugga KS, Xoconostle-Cazares B, Delmer DP (2000) A comparative analysis of the plant cellulose synthase (CesA) gene family. Plant Physiol 123:1313–1324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang D, Wang SG, Zhang BC, Shang-Guan K, Shi YY, Zhang DM, Liu XL, Wu K, Xu ZP, Fu XD, Zhou YH (2015) A gibberellin-mediated DELLA-NAC signaling cascade regulates cellulose synthesis in rice. Plant Cell 27:1681–1696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iannacoe R, Grieco PD, Cellini F (1997) Specific sequence modification of a cry3 bendotoxin gene result in high levels of expression and insect resistance. Plant Mol Biol 34:485–496

    Article  Google Scholar 

  • Jung KW, Oh SI, Kim YY, Yoo KS, Cui MH, Shin JS (2008) Arabidopsis Histidine-containing Phosphotransfer factor 4 (AHP4) negatively regulates secondary wall thickening of the anther endothecium during flowering. Mol Cell 25:294–300

    CAS  Google Scholar 

  • Lerouxel O, Cavalier DM, Liepman AH, Keegstra K (2007) Biosynthesis of plant cell wall polysaccharides—a complex process. Curr Opin Plant Biol 9:621–630

    Article  CAS  Google Scholar 

  • Li X, Mo XR, Shou HX, Wu P (2006) Cytokinin-mediated cell cycling arrest of pericycle founder cells in lateral root initiation of Arabidopsis. Plant Cell Physiol 47:1112–1123

    Article  CAS  PubMed  Google Scholar 

  • Liu YB, Lu SM, Zhang JF, Liu S, Lu YT (2007) A xyloglucan endotransglucosylase/hydrolase involves in growth of primary root and alters the deposition of cellulose in Arabidopsis. Planta 226:1547–1560

    Article  CAS  PubMed  Google Scholar 

  • Liu YX, Chen JR, Peng Y, Huang S, Zhao Y, Huang LH, Guo QQ, Zhang XW (2014) The cDNA cloning and expression analysis on cellulose synthase BnCesA4 in Boehmeria nivea. Crop Res 28:472–478

    Google Scholar 

  • Maleki SS, Mohammadi K, Ji KS (2016) Characterization of cellulose synthesis in plant cells. Sci World J 2016:1–8

    Article  CAS  Google Scholar 

  • Morgan JL, Strumillo J, Zimmer J (2013) Crystallographic snapshot of cellulose synthesis and membrane translocation. Nature 493:181–U192

    Article  CAS  PubMed  Google Scholar 

  • Napoli C, Lemieux C, Jorgensen R (1990) Introduction of a chimeric chalcone synthase gene into Petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2:279–289

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ong SS, Wickneswari R (2012) Characterization of microRNAs expressed during secondary wall biosynthesis in Acacia mangium. PLoS One 7:e49662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pear JR, Kawagoe Y, Schreckengost WE, Delmer DP, Stalker DM (1996) Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase. Proc Natl Acad Sci U S A 93:12637–12642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perlak FJ, Fuchs RL, Dean DA, Mcpherson SL, Fischhoff DA (1991) Modification of the coding sequence enhances plant expressing of insect control protein genes. Proc Natl Acad Sci U S A 88:3324–3328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruan WC, Pan T, Ji KS (2015) Cloning and analysis on PmCesA1 gene encoding Pinus massoniana cellulose synthase. Mol Plant Breed 13:861–870

    Google Scholar 

  • Sauretgüeto S, Calder G, Harberd NP (2012) Transient gibberellin application promotes Arabidopsis thaliana hypocotyl cell elongation without maintaining transverse orientation of microtubules on the outer tangential wall of epidermal cells. Plant J 69:628–639

    Article  CAS  Google Scholar 

  • Scheible WR, Eshed R, Richmond T, Delmer D, Somerville C (2001) Modifications of cellulose synthase confer resistance to isoxaben and thiazolidinone herbicides in Arabidopsis ixr1 mutants. Proc Natl Acad Sci U S A 98:10079–10084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sethaphong L, Davis JK, Slabaugh E, Singh A, Haigler CH, Yingling YG (2016) Prediction of the structures of the plant-specific regions of vascular plant cellulose synthase and correlated functional analysis. Cellulose 23:145–161

    Article  CAS  Google Scholar 

  • Singer SD, Cox KD, Liu Z (2011) Enhancer-promoter interference and its prevention in transgenic plants. Plant Cell Rep 30:723–731

    Article  CAS  PubMed  Google Scholar 

  • Singh B, Cheek HD, Haigler CH (2009) A synthetic auxin (NAA) suppresses secondary wall cellulose synthesis and enhances elongation in cultured cotton fiber. Plant Cell Rep 28:1023–1032

    Article  CAS  PubMed  Google Scholar 

  • Slabaugh E, Sethaphong L, Xiao CW, Amick J, Anderson CT, Haigler CH, Yingling YG (2014) Computational and genetic evidence that different structural conformations of a non-catalytic region affect the function of plant cellulose synthase. J Exp Bot 65:6645–6653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Somerville C (2006) Cellulose synthesis in higher plants. Annu Rev Cell Dev Biol 22:53–78

    Article  CAS  PubMed  Google Scholar 

  • Song DL, Shen JH, Li LG (2010) Characterization of cellulose synthase complexes in Populus xylem differentiation. New Phytol 187:777–790

    Article  CAS  PubMed  Google Scholar 

  • Tanaka K, Murata K, Yamazaki M, Onosato K, Miyao A, Hirochika H (2003) Three distinct rice cellulose synthase catalytic subunit genes required for cellulose synthesis in the secondary wall. Plant Physiol 133:73–83

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor NG, Scheible WR, Cutler S, Somerville CR, Turner SR (1999) The irregular xylem3 locus of Arabidopsis encodes a cellulose synthase required for secondary cell wall synthesis. Plant Cell 11:769–779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taylor NG, Laurie S, Turner SR (2000) Multiple cellulose synthase catalytic subunits are required for cellulose synthesis in Arabidopsis. Plant Cell 12:2529–2540

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turner SR, Somerville CR (1997) Collapsed xylem phenotype of Arabidopsis identifies mutants deficient in cellulose deposition in the secondary cell wall. Plant Cell 9:689–701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vishwakarma RK, Srivastava S, Singh S, Khan BM (2012) Molecular cloning and characterization of two differentially expressed cellulose synthase gene isoforms in Leucaena leucocephala: a pulp yielding tree species. Adv Biosci Biotechnol 3:92–100

    Article  CAS  Google Scholar 

  • Wang B, Tang Q, Hong N, Song L, Wang L, Shi Y, Hu Y (2011) Effect of cellulose acetate butyrate microencapsulated ammonium polyphosphate on the flame retardancy, mechanical, electrical, and thermal properties of intumescent flame-retardant ethylene-vinyl acetate copolymer/microencapsulated ammonium polyphosphate/p. ACS Appl Mater Interfaces 3:3754–3761

    Article  CAS  PubMed  Google Scholar 

  • Wang YL, Zhang XF, Yang SL, Wang CH, Lu GL, Wang R, Yang YJ, Li DL (2017) Heterogenous expression of Pyrus pyrifolia PpCAD2 and PpEXP2 in tobacco impacts lignin accumulation in transgenic plants. Gene 637:181–189

    Article  CAS  PubMed  Google Scholar 

  • Wei ZH, Qu ZS, Zhang LJ, Zhao SJ, Bi ZH, Ji XH, Wang XW, Wei HR (2015) Overexpression of poplar xylem sucrose synthase in tobacco leads to a thickened cell wall and increased height. PLoS One 10:e0120669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei KL, Zhou HJ, Jiang C, Zhao YQ, Song XQ, Lu MZ (2017) Interaction and expression of secondary wall CESAs in Populus. For Res 30:245–253

    Google Scholar 

  • Wu L, Joshi CP, Chiang VL (2000) A xylem-specific cellulose synthase gene from aspen (Populous tremuloides) is responsive to mechanical stress. Plant J 22:495–502

    Article  CAS  PubMed  Google Scholar 

  • Xu L, Liu YX, Fang LY (2012) Cloning and sequence character analysis of full-length cDNA of cellulose synthase PuCesA6 from Populus ussuriensis. J Southwest For Univ 32:26–32

    CAS  Google Scholar 

  • Yong SYC, Wickneswari R (2012) Molecular characterization of a cellulose synthase gene (AaxmCesA1) isolated from an Acacia auriculiformis x Acacia mangium hybrid. Plant Mol Biol Rep 31:303–313

    Article  CAS  PubMed Central  Google Scholar 

Download references

Data archiving statement

The mRNA sequence data are available for download at https://www.ncbi.nlm.nih.gov/nuccore/AY643519 and https://www.ncbi.nlm.nih.gov/nuccore/AY643520

The DNA sequence data have been submitted to NCBI.

Funding

This work was supported by the Heilongjiang Province vegetable industry technology collaborative innovation system (HNWSCTX201701).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yong Wang.

Additional information

Communicated by W. Ratnam

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ren, J., Yin, Y., Chen, D. et al. Cloning and analysis of cellulose synthase genes (CesA) in Acacia mangium. Tree Genetics & Genomes 14, 85 (2018). https://doi.org/10.1007/s11295-018-1299-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11295-018-1299-0

Keywords

Navigation