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Expression and nucleotide diversity of the poplar COBL gene

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Abstract

The COBRA gene encodes a putative glycosyl-phosphatidylinositol-anchored protein that regulates cellulose deposition and oriented cell expansion in the plant cell wall. This study reports the identification of PtCOBL4, a first COBRA gene from the tree Populus tomentosa. The full-length cDNA of PtCOBL4 was isolated from a xylem cDNA library. The deduced protein sequence shares 72.7% identity with Arabidopsis AtCOBL4 protein involved in secondary cell wall deposition. Analysis of differential tissue expression by real-time polymerase chain reaction (PCR) indicated that PtCOBL4 is expressed predominantly in the mature xylem zone. By using the sequenced whole genome and DNA microarray data of Populus, we demonstrated that COBRA is a multigene family of 11 members, each of which exhibit different tissue-specific expression patterns. To evaluate the functional consequences of nucleotide polymorphisms in the PtCOBL4 locus, the patterns of variation in a 2,002-bp region of the gene were surveyed in 40 unrelated individuals representative of almost the entire natural range of P. tomentosa. Sixty-one single-nucleotide polymorphisms (SNPs) were identified at a frequency of one SNP per 32.8 bp of sequence, giving an estimated nucleotide diversity of π T = 0.00800 and θ w = 0.00716. Within coding regions, nonsynonymous diversity (π nonsyn = 0.00285) was markedly lower than synonymous diversity (π syn = 0.02128); the π nonsyn/π syn ratio was 0.13, significantly less than 1, indicating that the synonymous sites were subject to strong purifying selection. These results provide the necessary foundation for improving the quantity and quality of cellulose via genetic engineering or by candidate-gene-based association genetics in P. tomentosa.

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References

  • Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  Google Scholar 

  • Baucher M, Halpin C, Petit-Conil M, Boerjan W (2003) Lignin: genetic engineering and impact on pulping. Crit Rev Biochem Mol Biol 38:305–350

    Article  PubMed  Google Scholar 

  • Brady SM, Song S, Dhugga KS, Rafalski JA, Benfey PN (2007) Combining expression and comparative evolutionary analysis. The COBRA gene family. Plant Physiol 1430:172–187

    Google Scholar 

  • Brown GR, Gill GP, Kuntz RJ, Langley CH, Neale DB (2004) Nucleotide diversity and linkage disequilibrium in loblolly pine. Proc Natl Acad Sci U S A 101(42):15255–15260

    Article  PubMed  Google Scholar 

  • Brown DM, Zeef LA, Ellis J, Goodacre R, Turner SR (2005) Identification of novel genes in Arabidopsis involved in secondary cell wall formation using expression profiling and reverse genetics. Plant Cell 17:2281–2295

    Article  PubMed  Google Scholar 

  • Ching A, Dhugga KS, Appenzeller L, Meeley B, Bourret TM, Howard RJ, Rafalski A (2006) Brittle stalk 2 encodes a putative glycosylphosphatidylinositol-anchored protein that affects mechanical strength of maize tissues by altering the composition and structure of secondary cell walls. Planta 224:1174–1184

    Article  PubMed  Google Scholar 

  • Corpet F, Servant F, Gouzy J, Kahn D (2000) ProDom and ProDom-CG: tools for protein domain analysis and whole genome comparisons. Nucleic Acids Res 28:267–269

    Article  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

    Article  Google Scholar 

  • Djerbi S, Lindskog M, Arvestad L, Sterky F, Teeri TT (2005) The genome sequence of black cottonwood (Populus trichocarpa) reveals 18 conserved cellulose synthase (CesA) genes. Planta 221:739–746

    Article  PubMed  Google Scholar 

  • Eisenhaber B, Bork P, Yuan Y, Loeffler G, Eisenhaber F (2000) Automated annotation of GPI anchor sites: case study C. elegans. Trends Biol Sci 25:340–341

    Article  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution Int J Org Evolution 39:783–791

    Google Scholar 

  • González-Martínez SC, Ersoz E, Brown GR, Wheeler NC, Neale DB (2006) DNA sequence variation and selection of tag single-nucleotide at candidate genes for drought-stress response in Pinus taeda L. Genetics 172:1915–1926

    Article  PubMed  Google Scholar 

  • Heuertz M, Paoli ED, Källman T, Larsson H, Jurman I, Morgante M, Lascoux M, Gyllenstrand N (2006) Multilocus patterns of nucleotide diversity, linkage disequilibrium and demographic history of Norway spruce [Picea abies (L.) Karst]. Genetics 174:2095–2105

    Article  PubMed  Google Scholar 

  • Hu WJ, Harding SA, Lung J, Popko JL, Ralph J, Stokke DD, Tsai CJ, Chiang VL (1999) Repression of lignin biosynthesis promotes cellulose accumulation and growth in transgenic trees. Nat Biotechnol 17:808–812

    Article  PubMed  Google Scholar 

  • Huang ZH (1992) The study on the climatic regionalization of the distributional region of Populus tomentosa. Journal of Beijing Forestry University 14:26–32

    Google Scholar 

  • Ingvarsson PK (2008) Multilocus patterns of nucleotide polymorphism and the demographic history of Populus tremula. Genetics 180:329–340

    Article  PubMed  Google Scholar 

  • Joshi CP, Bhandari S, Ranjan P, Kalluri UC, Liang X, Fujino T, Samuga A (2004) Genomics of cellulose biosynthesis in poplars. New Phytol 164:53–61

    Article  Google Scholar 

  • Krutovsky KV, Neale DB (2005) Nucleotide diversity and linkage disequilibrium in cold-hardiness-and wood quality-related candidate genes in Douglas Fir. Genetics 171:2029–2041

    Article  PubMed  Google Scholar 

  • Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132

    Article  PubMed  Google Scholar 

  • Li L, Zhou Y, Cheng X, Sun J, Marita JM, Ralph J, Chiang VL (2003a) Combinatorial modification of multiple lignin traits in trees through multigene cotransformation. Proc Natl Acad Sci U S A 100:4939–4944

    Article  PubMed  Google Scholar 

  • Li Y, Qian Q, Zhou Y, Yan M, Sun L, Zhang M, Fu Z, Wang Y, Han B, Pang X, Chen M, Li J (2003b) BRITTLE CULM1, which encodes a COBRA-like protein, affects the mechanical properties of rice plants. Plant Cell 15:2020–2031

    Article  PubMed  Google Scholar 

  • Lukashin AV, Borodovsky M (1998) GeneMark.hmm: new solutions for gene finding. Nucleic Acids Res 26:1107–1115

    Article  PubMed  Google Scholar 

  • Mellerowicz EJ, Sundberg B (2008) Wood cell walls: biosynthesis, developmental dynamics and their implications for wood properties. Curr Opin Plant Biol 11:293–300

    Article  PubMed  Google Scholar 

  • Mutwil M, Debolt S, Persson S (2008) Cellulose synthesis: a complex complex. Curr Opin Plant Biol 11:252–257

    Article  PubMed  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Google Scholar 

  • Nielsen H, Engelbrecht J, Brunak S, von Heijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10:1–6

    Article  PubMed  Google Scholar 

  • Oakley RV, Wang YS, Ramakrishna W, Harding SA, Tsai CJ (2007) Differential expression and expression of α- and β-tubulin gene families in Populus. Plant Physiol 145:961–973

    Article  PubMed  Google Scholar 

  • Plomion C, Leprovost G, Stokes A (2001) Wood formation in trees. Plant Physiol 127:1513–1523

    Article  PubMed  Google Scholar 

  • Quang ND, Ikeda S, Harada K (2008) Nucleotide variation in Quercus crispula Blume. Heredity 101:166–174

    Article  PubMed  Google Scholar 

  • Rajangam AS, Kumar M, Aspeborg H, Guerriero G, Arvestad L, Pansri P, Brown CJ, Hober S, Blomqvist K, Divne C, Ezcurra I, Mellerowicz E, Sundberg B, Bulone V, Teeri TT (2008) MAP20, a microtubule-associated protein in the secondary cell walls of hybrid aspen, is a target of the cellulose synthesis inhibitor 2,6-dichlorobenzonitrile. Plant Physiol 148:1283–1294

    Article  PubMed  Google Scholar 

  • Roudier F, Schindelman G, DeSalle R, Benfey PN (2002) The COBRA family of putative GPI-anchored proteins in Arabidopsis. A new fellowship in expansion. Plant Physiol 130:538–548

    Article  PubMed  Google Scholar 

  • Rozas J, Sánchez-Delbarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    Article  PubMed  Google Scholar 

  • Schindelman G, Morikami A, Jung J, Baskin TI, Carpita NC, Derbyshire P, McCann MC, Benfey PN (2001) COBRA encodes a putative GPI anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis. Genes Dev 15:1115–1127

    Article  PubMed  Google Scholar 

  • Schneider JA, Pungliya MS, Choi JY, Jiang R, Sun XJ, Salisbury BA, Stephens JC (2003) DNA variability of human genes. Mech Ageing Dev 124:17–25

    Article  PubMed  Google Scholar 

  • Sindhu A, Langewisch T, Olek A, Multani DS, McCann MC, Vermerris W, Carpita NC, Johal G (2007) Maize brittle stalk2 encodes a COBRA-like protein expressed in early organ development but required for tissue flexibility at maturity. Plant Physiol 145:1444–1459

    Article  PubMed  Google Scholar 

  • Sjödin A, Bylesjö M, Skogström O, Eriksson D, Nilsson P, Rydén P, Jansson S, Karlsson J (2006) UPSC-BASE—Populus transcriptomics online. The Plant J 48:806–817

    Article  Google Scholar 

  • Suzuki S, Li L, SunYH CVL (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  PubMed  Google Scholar 

  • Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (and other methods). Version 4. Sinauer, Sunderland

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Udenfriend S, Kodukula K (1995a) How glycosylphosphatidylinositol-anchored membrane proteins are made. Annu Rev Biochem 64:563–591

    PubMed  Google Scholar 

  • Udenfriend S, Kodukula K (1995b) Prediction of omega site in nascent precursor of glycosylphosphatidylinositol protein. Methods Enzymol 250:571–581

    Article  PubMed  Google Scholar 

  • Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:188–193

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the National Changjiang Scholar Funds of China (Bailian Li), the project of National Natural Science Foundation of China (no. 30600479, 30872042), Major Science Foundation of Ministry of Education of China (no. 307006), A Foundation for the Author of National Excellent Doctoral Dissertation of PR China (no. 200770), A Program for New Century Excellent Talents in University (no. NCET-07-0084), and Introduction of Foreign Advanced Agricultural Science and Technology into China (no. 2009-4-22).

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Authors and Affiliations

  1. National Engineering Laboratory for Tree Breeding, Beijing, 100083, People’s Republic of China

    Deqiang Zhang, Xiaohui Yang, Zhiyi Zhang & Bailian Li

  2. Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, Beijing, 100083, People’s Republic of China

    Deqiang Zhang, Xiaohui Yang, Zhiyi Zhang & Bailian Li

  3. Department of Forestry, North Carolina State University, Raleigh, NC, 27695-8203, USA

    Bailian Li

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  1. Deqiang Zhang
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  2. Xiaohui Yang
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  3. Zhiyi Zhang
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  4. Bailian Li
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Corresponding authors

Correspondence to Deqiang Zhang or Bailian Li.

Additional information

Communicated by S. González-Martínez

Sequence data from this article have been deposited with the GenBank Data Library under the accession nos. GQ410777 (PtCOBL4 cDNA) and GU053528–GU053567.

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Zhang, D., Yang, X., Zhang, Z. et al. Expression and nucleotide diversity of the poplar COBL gene. Tree Genetics & Genomes 6, 331–344 (2010). https://doi.org/10.1007/s11295-009-0252-7

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