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The genome sequence of black cottonwood (Populus trichocarpa) reveals 18 conserved cellulose synthase (CesA) genes

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Abstract

The genome sequence of Populus trichocarpa was screened for genes encoding cellulose synthases by using full-length cDNA sequences and ESTs previously identified in the tissue specific cDNA libraries of other poplars. The data obtained revealed 18 distinct CesA gene sequences in P. trichocarpa. The identified genes were grouped in seven gene pairs, one group of three sequences and one single gene. Evidence from gene expression studies of hybrid aspen suggests that both copies of at least one pair, CesA3-1 and CesA3-2, are actively transcribed. No sequences corresponding to the gene pair, CesA6-1 and CesA6-2, were found in Arabidopsis or hybrid aspen, while one homologous gene has been identified in the rice genome and an active transcript in Populus tremuloides. A phylogenetic analysis suggests that the CesA genes previously associated with secondary cell wall synthesis originate from a single ancestor gene and group in three distinct subgroups. The newly identified copies of CesA genes in P. trichocarpa give rise to a number of new questions concerning the mechanism of cellulose synthesis in trees.

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Notes

  1. The only exception to the clustering of apparently secondary cell wall associated CesA genes is OsCesA9 from rice. However, as described in Materials and methods, this gene is represented by a partial cDNA, which was not stable in the phylogenetic analysis, and it may thus end up in a different position once the full length gene is available.

Abbreviations

CesA:

Cellulose synthase

CDS:

Coding sequence

EST:

Expressed sequence tag

UTR:

Untranslated region

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Arioli T, Peng L, Betzner AS, Burn J, Wittke W, Herth W, Camilleri C, Hofte 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

    CAS  PubMed  Google Scholar 

  • Bowers JE, Chapman BA, Rong J, Paterson AH (2003) Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422:433–438

    CAS  PubMed  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

    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

    CAS  PubMed  Google Scholar 

  • Dayhoff MO, Schwartz RM, Orcutt BC (1978) A model of evolutionary change in proteins. in Atlas of protein sequence and structure, vol. 5, Suppl 3. National Biomedical Research Foundation, Washington, pp 345–352

  • Desprez T, Vernhettes S, Fagard M, Refregier G, Desnos T, Aletti E, Py N, Pelletier S, Hofte H (2002) Resistance against herbicide isoxaben and cellulose deficiency caused by distinct mutations in same cellulose synthase isoform CESA6. Plant Physiol 128: 482–490

    CAS  PubMed  Google Scholar 

  • Djerbi S, Aspeborg H, Nilsson P, Sundberg B, Mellerowicz E, Blomqvist K, Teeri TT (2004) Identification and expression analysis of genes encoding putative cellulose synthases (CesA) in the hybrid aspen, Populus tremula (L.) × P. tremuloides (Michx.). Cellulose 11:301–312

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792–1797

    CAS  PubMed  Google Scholar 

  • Fagard M, Desnos T, Desprez T, Goubet F, Refregier G, Mouille G, McCann M, Rayon C, Vernhettes S, Hofte H (2000) PROCUSTE1 encodes a cellulose synthase required for normal cell elongation specifically in roots and dark-grown hypocotyls of Arabidopsis. Plant Cell 12:2409–2424

    CAS  PubMed  Google Scholar 

  • Felsenstein J (1989) PHYLIP—phylogeny inference package, version 3.2. Cladistics 5:164–166

    Google Scholar 

  • Hamzeh M, Dayanandan S (2004) Phylogeny of Populus (Salicaceae) based on nucleotide sequences of chloroplast TRNT-TRNF region and nuclear rDNA. Am J Bot 91:1398–1408

    CAS  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

    CAS  PubMed  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Imanishi T, Itoh T, Suzuki Y, O’Donovan C, Fukuchi S, Koyanagi KO, Barrero RA, Tamura T, Yamaguchi-Kabata Y, Tanino M, Yura K, Miyazaki S, Ikeo K, Homma K, Kasprzyk A, Nishikawa T, Hirakawa M, Thierry-Mieg J, Thierry-Mieg D, Ashurst J, Jia L, Nakao M, Thomas MA, Mulder N, Karavidopoulou Y, Jin L, Kim S, Yasuda T, Lenhard B, Eveno E, Yamasaki C, Takeda J, Gough C, Hilton P, Fujii Y, Sakai H, Tanaka S, Amid C, Bellgard M, Bonaldo Mde F, Bono H, Bromberg SK, Brookes AJ, Bruford E, Carninci P, Chelala C, Couillault C, de Souza SJ, Debily MA, Devignes MD, Dubchak I, Endo T, Estreicher A, Eyras E, Fukami-Kobayashi K, Gopinath GR, Graudens E, Hahn Y, Han M, Han ZG, Hanada K, Hanaoka H, Harada E, Hashimoto K, Hinz U, Hirai M, Hishiki T, Hopkinson I, Imbeaud S, Inoko H, Kanapin A, Kaneko Y, Kasukawa T, Kelso J, Kersey P, Kikuno R, Kimura K, Korn B, Kuryshev V, Makalowska I, Makino T, Mano S, Mariage-Samson R, Mashima J, Matsuda H, Mewes HW, Minoshima S, Nagai K, Nagasaki H, Nagata N, Nigam R, Ogasawara O, Ohara O, Ohtsubo M, Okada N, Okido T, Oota S, Ota M, Ota T, Otsuki T, Piatier-Tonneau D, Poustka A, Ren SX, Saitou N, Sakai K, Sakamoto S, Sakate R, Schupp I, Servant F, Sherry S, Shiba R, Shimizu N, Shimoyama M, Simpson AJ, Soares B, Steward C, Suwa M, Suzuki M, Takahashi A, Tamiya G, Tanaka H, Taylor T, Terwilliger JD, Unneberg P, Veeramachaneni V, Watanabe S, Wilming L, Yasuda N, Yoo HS, Stodolsky M, Makalowski W, Go M, Nakai K, Takagi T, Kanehisa M, Sakaki Y, Quackenbush J, Okazaki Y, Hayashizaki Y, Hide W, Chakraborty R, Nishikawa K, Sugawara H, Tateno Y, Chen Z, Oishi M, Tonellato P, Apweiler R, Okubo K, Wagner L, Wiemann S, Strausberg RL, Isogai T, Auffray C, Nomura N, Gojobori T, Sugano S (2004) Integrative annotation of 21,037 human genes validated by full-length cDNA clones. PLoS Biol 2:856–875

    CAS  Google Scholar 

  • Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8:275–282

    CAS  PubMed  Google Scholar 

  • Krogh A, Larsson B, von Heijne G, Sonnhammer EL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580

    CAS  PubMed  Google Scholar 

  • Kurek I, Kawagoe Y, Jacob-Wilk D, Doblin M, Delmer D (2002) Dimerization of cotton fiber cellulose synthase catalytic subunits occurs via oxidation of the zinc-binding domains. Proc Natl Acad Sci USA 99: 11109–11114

    CAS  PubMed  Google Scholar 

  • Makalowski W, Boguski MS (1998) Evolutionary parameters of the transcribed mammalian genome: an analysis of 2,820 orthologous rodent and human sequences. Proc Natl Acad Sci USA 95:9407–9412

    CAS  PubMed  Google Scholar 

  • Needleman SB, Wunsch CD (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol 48:443–453

    CAS  PubMed  Google Scholar 

  • Prince VE, Pickett FB (2002) Splitting pairs: the diverging fates of duplicated genes. Nat Rev Genet 3:827–837

    CAS  PubMed  Google Scholar 

  • Raes J, Vandepoele K, Simillion C, Saeys Y, Van de Peer Y (2003) Investigating ancient duplication events in the Arabidopsis genome. J Struct Funct Genomics 3:117–129

    CAS  PubMed  Google Scholar 

  • Richmond TA, Somerville CR (2000) The cellulose synthase superfamily. Plant Physiol 124:495–498

    CAS  PubMed  Google Scholar 

  • Samuga A, Joshi CP (2004) Differential expression patterns of two new primary cell wall-related cellulose synthase cDNAs, PtrCesA6 and PtrCesA7 from aspen trees. Gene 334:73–82

    CAS  PubMed  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 USA 98:10079–10084

    CAS  PubMed  Google Scholar 

  • Simillion C, Vandepoele K, Van Montagu MC, Zabeau M, Van de Peer Y (2002) The hidden duplication past of Arabidopsis thaliana. Proc Natl Acad Sci USA 99:13627–13632

    CAS  PubMed  Google Scholar 

  • Sterky F, Bhalerao RR, Unneberg P, Segerman B, Nilsson P, Brunner AM, Charbonnel-Campaa L, Lindvall JJ, Tandre K, Strauss SH, Sundberg B, Gustafsson P, Uhlen M, Bhalerao RP, Nilsson O, Sandberg G, Karlsson J, Lundeberg J, Jansson S (2004) A Populus EST resource for plant functional genomics. Proc Natl Acad Sci USA 101: 13951–13956

    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

    CAS  PubMed  Google Scholar 

  • Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    CAS  PubMed  Google Scholar 

  • Thornton JW, DeSalle R (2000) Gene family evolution and homology: genomics meets phylogenetics. Annu Rev Genomics Hum Genet 1:41–73

    CAS  PubMed  Google Scholar 

  • Vandepoele K, Simillion C, Van de Peer Y (2003) Evidence that rice and other cereals are ancient aneuploids. Plant Cell 15:2192–2202

    CAS  PubMed  Google Scholar 

  • Williamson RE, Burn JE, Hocart CH (2002) Towards the mechanism of cellulose synthesis. Trends Plant Sci 7:461–467

    CAS  PubMed  Google Scholar 

  • Wullschleger SD, Jansson S, Taylor G (2002) Genomics and forest biology: Populus emerges as the perennial favorite. Plant Cell 14:2651–2655

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Per Unneberg, Peter Savolainen and Peter Nilsson for fruitful discussions and critical reading of the manuscript. The EU project QLK5-CT2001-00443 and the Knut and Alice Wallenberg foundation are gratefully acknowledged for financial support.

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Correspondence to Tuula T. Teeri.

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Djerbi, S., Lindskog, M., Arvestad, L. et al. The genome sequence of black cottonwood (Populus trichocarpa) reveals 18 conserved cellulose synthase (CesA) genes. Planta 221, 739–746 (2005). https://doi.org/10.1007/s00425-005-1498-4

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  • DOI: https://doi.org/10.1007/s00425-005-1498-4

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