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Isolation of developing secondary xylem specific cellulose synthase genes and their expression profiles during hormone signalling in Eucalyptus tereticornis

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Abstract

Cellulose synthases (CesA) represent a group of β-1, 4 glycosyl transferases involved in cellulose biosynthesis. Recent reports in higher plants have revealed that two groups of CesA gene families exist, which are associated with either primary or secondary cell wall deposition. The present study aimed at identifying developing secondary xylem specific cellulose synthase genes from Eucalyptus tereticornis,a species predominantly used in paper and pulp industries in the tropics. The differential expression analysis of the three EtCesAgenes using qRT-PCR revealed 49 to 87 fold relative expression in developing secondary xylem tissues. Three full length gene sequences of EtCesA1, EtCesA2and EtCesA3 were isolated with the size of 2940, 3114 and 3123 bp, respectively. Phytohormone regulation of all three EtCesAgenes were studied by exogenous application of gibberellic acid, naphthalene acetic acid, indole acetic acid and 2, 4-epibrassinolide in internode tissues derived from three-month-old rooted cuttings. All threeEtCesA transcripts were upregulated by indole acetic acid and gibberellic acid. This study demonstrates that the increased cellulose deposition in the secondary wood induced by hormones can be attributed to the upregulation of xylem specific CesAs.

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References

  • Aloni R., Feigenbaum P., Kalev N., and Rozovsky S. 2000 Hormonal control of vascular differentiation in plants: the physiological basis of cambium ontogeny and xylem evolution. In Cell and molecular biology of wood formation (ed. R. A. Savidge, J. R. Barnett and R. Napier), pp. 223-236. BIOS Scientific Publishers, Oxford.

  • Aloni R. 2001 Foliar and axial aspects of vascular differentiation- hypothesis and evidence. J. Plant Growth Regul. 20, 22–34.

    Article  CAS  Google Scholar 

  • Appenzeller L., Doblin M., Barreiro R., Wang H. Y., Niu X. M., Kollipara K., et al. 2004 Cellulose synthesis in maize: isolation and expression analysis of the cellulose synthase (CesA) gene family. Cellulose 11, 287–299.

    Article  CAS  Google Scholar 

  • Beyer Jr E. M. and Morgan P. W. 1970 Effect of ethylene on the uptake, distribution, and metabolism of indoleacetic acid-1–14C and -2–14C and naphthaleneacetic acid-1–14C. Plant Physiol. 46, 157–162.

  • Bjorklund S., Antti H., Uddestrand I., Moritz T., and Sundberg B. 2007 Cross-talk between gibberellin and auxin in development of Populus wood: gibberellin stimulates polar auxin transport and has a common transcriptome with auxin. Plant J. 52, 499–511.

    Article  PubMed  Google Scholar 

  • Boer E. 1997 Eucalyptus tereticornis J.E. Smith. In Proseabase PROSEA (plant resources of south-east Asia) foundation (ed. I. Faridah Hanum and G. Van der Maesen), Bogor, Indonesia.

  • Burton R. A., Shirley N. J., King B. J., Harvey A. J. and Fincher G. B. 2004 The CesA gene family of barley (Hordeum vulgare): quantitative analysis of transcripts reveals two groups of co-expressed genes. Plant Physiol. 134, 224–236.

  • Bustin S. A., Benes V., Garson J. A., Hellemans J., Huggett J., Kubista M., et al. 2009 The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55, 611–622.

    Article  CAS  PubMed  Google Scholar 

  • Cano-Delgado A., Yin Y.H., Yu C., Vafeados D., Mora-Garcia S., Cheng J. C. et al. 2004 BRL1 and BRL3 are novel brassinosteroid receptors that function in vascular differentiation in Arabidopsis. Development 131, 5341–5351.

  • Chen C. Y., Hsieh M. H., Yang C. C., Lin C. S. and Wang A. 2010 Analysis of the cellulose synthase genes associated with primary cell wall synthesis in Bambusa oldhamii. Phytochemistry 71, 1270–1279.

  • Crowell E. F., Gonneau M., Stierhof Y. D., Hofte H., and Vernhettes S. 2010 Regulated trafficking of cellulose synthases. Curr. Opin. Plant Biol. 13, 700–705.

    Article  CAS  PubMed  Google Scholar 

  • Delbarre A., Muller P. and Imhoff V. 1996 Comparison of mechanisms controlling uptake and accumulation of 2, 4-dichlorophenoxy acetic acid, naphthalene-1-acetic acid and indole-3-acetic acid in suspension-cultured tobacco cells. Planta 198, 532–541.

  • Delmer D. P. and Amor Y. 1995 Cellulose biosynthesis. Plant Cell 7, 987–1000.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Delmer D. P. 1999 Cellulose biosynthesis: exciting times for a difficult field of study. Annu Rev. Plant Physiol. Plant Mol. Biol. 50, 245–276.

    Article  CAS  PubMed  Google Scholar 

  • Delmer D. P. and Haigler C. H. 2002 The regulation of metabolic flux to cellulose, a major sink for carbon in plants. Metab. Eng. 4, 22–28.

    Article  CAS  PubMed  Google Scholar 

  • Demura T. and Fukuda H. 2007 Transcriptional regulation in wood formation. Trends Plant Sci. 12, 64–70.

    Article  CAS  PubMed  Google Scholar 

  • Digby J. and Wareing P. F. 1966 Effect of Applied growth hormone on cambial division and differentiation of cambial derivatives. Ann. Bot. 30, 539–546.

    CAS  Google Scholar 

  • Doblin M. S., Kurek I., Wilk J. D., and Delmer D. P. 2002 Cellulose biosynthesis in plants: from genes to rosettes. Plant Cell Physiol. 43, 1407–1420.

  • Endler A. and Persson S. 2010. Cellulose synthases and synthesis in Arabidopsis. Mol. Plant 4, 199–211.

  • Eriksson M. E., Israelsson B. M., Olsson O., and Moritz T. 2000 Increased gibberellin biosynthesis in transgenic trees promotes growth, biomass production and xylem fiber length. Nat. Biotechnol. 18, 784–788.

    Article  CAS  PubMed  Google Scholar 

  • Fagard M., Desons T., Goubet D. F., Refregier G., Mouille G., McCann M. et al. 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.

  • Funada R., Miura T., Shimizu Y., Kinase T., Nakaba S., Kubo T., and Sano Y. 2008 Gibberellin-induced formation of tension wood in angiosperm trees. Planta 227, 1409–1414.

    Article  CAS  PubMed  Google Scholar 

  • Goda H., Sawa S., Asami T., Fujioka S., Shimada Y., and Yoshida S. 2004 Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis. Plant Physiol. 134, 1555–1573.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Groover A. and Robischon M. 2006 Developmental mechanisms regulating secondary growth in woody plants. Curr. Opin. Plant Biol. 9, 55–58.

    Article  CAS  PubMed  Google Scholar 

  • Holland N., Holland D., Helentjaris T., Dhugga K. S., Xoconostle-Cazares B., and Delmer D. P. 2000 A comparative analysis of the plant cellulose synthase gene (CesA) gene family. Plant Physiol. 123, 1313–1323.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Iglesias Trabado G. and Wilstermann D. 2008 Global cultivated eucalypt forests map 2008 version 1.0.1. GIT Forestry Consulting’s Eucalyptologics. Eucalyptus universalis. Available at http://www.git-forestry.com/ (accessed 20 December 2012)

  • Ito Y., Nakanomyo I., Motose H., Iwamoto K., Sawa S., Dohmae N., and Fukuda H. 2006 Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 313, 842–845.

    Article  CAS  PubMed  Google Scholar 

  • Kalluri U. C. and Joshi C. P. 2004 Differential expression patterns of two cellulose synthase genes are associated with primary and secondary cell wall development in aspen trees. Planta 220, 47–55.

    Article  CAS  PubMed  Google Scholar 

  • Joshi C. P, Bhandari S., Ranjan P., Kalluri U. C., Liang X., Fujino T., and Samuga A. 2004 Genomics of cellulose biosynthesis in Poplars. New Phytol. 164, 53–61.

    Article  CAS  Google Scholar 

  • Joshi C. P. and Mansfield S. D. 2007 The cellulose paradox: simple molecule, complex biosynthesis. Curr. Opin. Plant Sci. 10, 220–226.

    Article  CAS  Google Scholar 

  • Karpaga Raja Sundari B. and Ghosh Dasgupta M. 2012 Selection and validation of reference genes for real-time qRT-PCR normalization in different tissues of Eucalyptus tereticornis. Silvae Genet. 61, 221–300.

    Google Scholar 

  • Kawagoe Y. and Delmer D. P. 1997 Pathways and genes involved in cellulose biosynthesis. Genet. Eng. 19, 63–87.

    Article  CAS  Google Scholar 

  • Kim S. K., Abe H., Little C. H. A. and Pharis R. P. 1990 Identification of two brassinosteroids from the cambial region of Scots pine (Pinus silverstris) by gas chromatography mass spectrometry, after detection using a dwarf rice lamina inclination bioassay. Plant Physiol. 94, 1709–1713.

  • Kim H. J., Murai N., Fanga D. D. and Barbara A. 2011 Functional analysis of Gossypium hirsutum cellulose synthase catalytic subunit 4 promoter in transgenic Arabidopsis and cotton tissues. Plant Sci 180, 323–332.

  • Kim H. J., Tripletta B. A., Zhang H. B., Lee M. K., Hinchliffe D. J., Li P., and Fang D. D. 2012 Cloning and characterization of homeologous cellulose synthase catalytic subunit 2 genes from allo-tetraploid cotton (Gossypium hirsutum L.) Gene 494, 181–189.

    Article  CAS  PubMed  Google Scholar 

  • Koizumi K., Sugiyama M., and Fukuda H. 2000 A series of novel mutants of Arabidopsis thaliana that are defective in the formation of continuous vascular network: calling the auxin signal flow canalization hypothesis into question. Development 127, 3197–3204.

    CAS  PubMed  Google Scholar 

  • Lau E. T., HoW. S. and Julaihi A. 2009 Molecular cloning of cellulose synthase genes SpCesA1 from developing xylem of Shorea parvifolia sp. parvifolia. Biotechnology 8, 416–424.

  • Lee K. J., Marcus S. E., and Knox J. P. 2011 Cell wall biology: perspectives from cell wall imaging. Mol. Plant 4, 212–219.

    Article  CAS  PubMed  Google Scholar 

  • Lei L., Li S. and Gu Y. 2012 Cellulose synthase complexes: composition and regulation. Front. Plant Sci. 3, 75.

  • Liang X. and Joshi C. P. 2004 Molecular cloning of ten distinct hyper variable regions from cellulose synthase gene superfamily in Aspen trees. Tree Physiol. 24, 543–550.

    Article  CAS  PubMed  Google Scholar 

  • Liu X., Wang Q., Chen P., Song F., Guan M., Jin L., et al. 2012 Four novel cellulose synthase (CESA) genes from Birch (Betula platyphylla Suk.) involved in primary and secondary cell wall biosynthesis. Int. J. Mol. Sci. 13, 12195–12212.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lu S., Li L., Yi X., Joshi C. P., and Chiang V. L. 2008 Differential expression of three eucalyptus secondary cell wall-related cellulose synthase genes in response to tension stress. J Exp. Bot. 59, 681–695.

    Article  CAS  PubMed  Google Scholar 

  • Mahonen A. P., Bishopp A., Higuchi M., Nieminen K. M., Kinoshita K., Tormakangas K., et al. 2006 Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science 311, 94–98.

    Article  PubMed  Google Scholar 

  • Mauriat M. and Moritz T. 2009 Analyses of GA20ox- and GID1-over-expressing aspen suggest that gibberellins play two distinct roles in wood formation. Plant J. 58, 989–1003.

    Article  CAS  PubMed  Google Scholar 

  • Muday G. K. and DeLong A. 2001 Polar auxin transport: controlling where and how much. Trends Plant Sci. 65, 535–542.

    Article  Google Scholar 

  • Nairn C. J. and Haselkorn T. 2005 Three loblolly Pine CesA genes expressed in developing xylem are orthologous to secondary wall CesA genes of angiosperms. New Phytol. 166, 907– 915.

    Article  CAS  PubMed  Google Scholar 

  • Nairn J. C., Lennon D. M., Wood-Jones A., Nairn A. V., and Dean J. F. D. 2008 Carbohydrate-related genes and cell wall biosynthesis in vascular tissues of loblolly pine (Pinus taeda). Tree Physiol. 28, 1099–1110.

    Article  CAS  PubMed  Google Scholar 

  • Nieminen K., Immanen J., Laxell M., Kauppinen L., Tarkowski P., Dolezal K., et al. 2008 Cytokinin signaling regulates cambial development in poplar. Proc. Natl. Acad. Sci. USA 105, 20032–20037.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Obembe O., Jacobsen E., Vincken J. P. and Visser R. G. F. 2009 Differential expression of cellulose synthase (CesA) gene transcripts in potato as revealed by RT-QPCR. Plant Physiol. Biochem. 47, 1116–1118.

  • Oh M. H., Sun J., Oh D. H., Zielinski R. E., Clouse S. D., and Huber S. C. 2011 Enhancing Arabidopsis leaf growth by engineering the brassinosteroid insensitive Receptor Kinase. Plant Physiol. 157, 120–131.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Orwa C., Mutua A., Kindt R., Jamnadass R. and Anthony S. 2009 Agroforestree database: a tree reference and selection guide version 4.0 (http://www.worldagroforestry.org/sites/treedbs/treedatabases.asp) (accessed on 20 Nov. 2013).

  • Pauly M. and Keegstra K. 2010 Plant cell wall polymers as precursors for biofuels. Curr. Opin. Plant Biol. 13, 305–312.

    Article  CAS  PubMed  Google Scholar 

  • Pear J. R., Kawagoe Y., Schreckengost W. E., Delmer D. P., and Stalker D. M. 1996 Higher plants contain homologs of the bacterial celA genes encoding the catalytic subunit of cellulose synthase. Proc. Natl. Acad. Sci. USA 93, 12637–12642.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ranik M. and Myburg A. A. 2006 Six new cellulose synthase genes from Eucalyptus are associated with primary and secondary cell wall biosynthesis. Tree Physiol. 26, 545–556.

    Article  CAS  PubMed  Google Scholar 

  • Richmond T. A. and Somerville C. R. 2000 The cellulose synthase superfamily. Plant Physiol. 124, 495–498.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Saxena I. M., Brown R. M., Fevre M., Geremia R. A., and Henrissat B. 1995 Multidomain architecture of β-glycosyltransferases: implications for mechanism of action. J. Bacteriol. 177, 1419–1424.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Saxena M. I. and Brown R. M. 2005 Cellulose biosynthesis: current views and evolving concepts. Ann. Bot. 96, 9–21.

    Article  CAS  PubMed  Google Scholar 

  • Singh B., Cheek H. D., and Haigler C. H. 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 

  • Somerville C. 2006 Cellulose synthesis in higher plants. Annu. Rev. Cell Dev. Bio. 22, 53–78.

    Article  CAS  Google Scholar 

  • Sundberg B., Uggla C., and Tuominen H. 2000 Cambial growth and auxin gradients. In Cell and molecular biology of wood formation (ed. R. Savidge, J. Barnett and R. Napier), pp. 169–188. BIOS Scientific Publishers, Oxford, UK.

  • Suzuki S., Li L. G., Sun Y. H., and Chiang V. L. 2006 The cellulose synthase gene superfamily and biochemical functions of xylem-specific cellulose synthase-like genes in Populus trichocarpa. Plant Physiol. 142, 1233–1245.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Taiz L. and Zeiger E. 2006 Plant physiology, 4th edition. Sinauer Associates, Sunderland, USA.

    Google Scholar 

  • Tamura K., Peterson D., Peterson N., Nei G. S. M., and Kumar S. 2011 MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28, 2731–2739.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tan X., Calderon-Villabolos L. I. A., Sharon M., Zheng C., Robinson C. V., Estelle M., and Zheng N. 2007 Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446, 640– 645.

    Article  CAS  PubMed  Google Scholar 

  • Tanaka K., Murata K., Yamazaki M., Onosato K., Miyao A., and 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 Central  PubMed  Google Scholar 

  • Taylor N. G., Wolf-Rudiger A., Scheible B., Cutler S. B., Chris S. R. B. and Turnera R. R. S. 1999 The irregular xylem3 locus of Arabidopsis encodes a cellulose synthase required for secondary cell wall synthesis. Plant Cell 11, 769–779.

  • Taylor N. G., Laurie S. and Turner S. R. 2000 Multiple cellulose synthase catalytic subunits are required for cellulose synthesis in Arabidopsis. Plant Cell 12, 2529–2539.

  • Thompson J., Higgins D., and Gibson T. 1994 ClustalW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic. Acids Res. 22, 4673– 4690.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Turnbull J. W. 1999 Eucalypt plantations. New For. 17, 37–52.

    Article  Google Scholar 

  • Uggla C., Moritz T., Sandberg G., and Sundberg B. 1996 Auxin as a positional signal in pattern formation in plants. Proc. Nat. Acad. Sci. USA 93, 9282–9286.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Uggla C., Mellerowicz E. J., and Sundberg B. 1998 Indole-3-acetic acid controls cambial growth in Scots pine by positional signaling. Plant Physiol. 117, 113–121.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Vergara C. E. and Carpita N. C. 2001 β-D-glycan synthases and the CesA gene family. Plant Mol. Biol. 47, 145–160.

    Article  CAS  PubMed  Google Scholar 

  • Vishwakarma R. K., Srivastava S., Singh S. and Khan B. M. 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.

  • Wang L. Q., Guo K., Li Y., Tu Y., Hu H., Wang B., et al. 2010 Expression profiling and integrative analysis of the CESA/CSL superfamily in rice. BMC Plant Biol. 10, 282.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Williamson R. E., Burn J. E., and Hocart C. H. 2002 Towards the mechanism of cellulose synthesis. Trends Plant Sci. 7, 461–467.

    Article  CAS  PubMed  Google Scholar 

  • Wu L., Joshi C. P., and Chiang V. L. 2000 A xylem-specific cellulose synthase gene from aspen (Populus tremuloides) is responsive to mechanical stress. Plant J. 22, 495–502.

    Article  CAS  PubMed  Google Scholar 

  • Wu A., Hu J. S., and Liu J. 2009 Functional analysis of a cotton cellulose synthase A4 gene promoter in transgenic tobacco plants. Plant Cell Rep. 28, 1539–1548.

    Article  CAS  PubMed  Google Scholar 

  • Yuan J. S., Reed A., Chen F., and Stewart C. N. 2006 Statistical analysis of real-time PCR data. BMC Bioinformatics 7, 85.

    Article  PubMed Central  PubMed  Google Scholar 

  • Zhong R. and Ye Z. H. 2010 The poplar PtrWNDs are transcriptional activators of secondary cell wall biosynthesis. Plant Signal Behav. 5, 469–472.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Acknowledgements

The authors acknowledge the research grant from Indian Council of Forestry Research and Education, Government of India, and KRSB acknowledges the fellowship received from the National Forestry Research Project. The authors also thank Dr R. Viswanathan, Head, Division of Plant Pathology, Sugarcane Breeding Institute, Coimbatore, India, for providing RT-PCR facility.

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  1. Division of Plant Biotechnology, Institute of Forest Genetics and Tree Breeding, P.B. No. 1061, Forest Campus, R.S. Puram, Coimbatore, 641 002, India

    BALACHANDRAN KARPAGA RAJA SUNDARI & MODHUMITA GHOSH DASGUPTA

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[Sundari B. K. R. and Dasgupta M. G. 2014 Isolation of developing secondary xylem specific cellulose synthase genes and their expression profiles during hormone signalling in Eucalyptus tereticornis. J. Genet. 93, xx–xx]

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KARPAGA RAJA SUNDARI, B., GHOSH DASGUPTA, M. Isolation of developing secondary xylem specific cellulose synthase genes and their expression profiles during hormone signalling in Eucalyptus tereticornis . J Genet 93, 403–414 (2014). https://doi.org/10.1007/s12041-014-0391-y

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