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Characterization of genes with tissue-specific differential expression patterns in Populus

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Abstract

Like many plants, Populus has an evolutionary history in which several, both recent and more ancient, genome duplication events have occurred and, therefore, constitutes an excellent model system for studying the functional evolution of genes. In the present study, we have focused on the properties of genes with tissue-specific differential expression patterns in poplar. We identified the genes by analyzing digital expression profiles derived by mapping 90,000+ expressed sequence tags (ESTs) from 18 sources to the predicted genes of Populus. Our sequence analysis suggests that tissue-specific differentially expressed genes have less diverged paralogs than average, indicating that gene duplication events is an important event in the pathway leading to this type of expression pattern. The functional analysis showed that genes coding for proteins involved in processes of functional importance for the specific tissue(s) in which they are expressed and genes coding for regulatory or responsive proteins are most common among the differentially expressed genes, demonstrating that the expression differentiation process is under strong selective pressure. Thus, our data supports a model where gene duplication followed by gene specialization or expansion of the regulatory and responsive networks leads to tissue-specific differential expression patterns. We have also searched for clustering of genes with similar expression pattern into gene-expression neighborhoods within the Populus genome. However, we could not detect any major clustering among the analyzed genes with highly specific expression patterns.

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References

  • Adams KL, Wendel JF (2005) Polyploidy and genome evolution in plants. Curr Opin Plant Biol 8:135–141

    Article  PubMed  CAS  Google Scholar 

  • Andersson-Gunneras S, Mellerowicz EJ, Love J, Segerman B, Ohmiya Y, Coutinho PM, Nilsson P, Henrissat B, Moritz T, Sundberg B (2006) Making cellulose enriched gelatinous fibers in poplar: global analysis of transcripts and metabolites identifies biochemical and developmental regulators in secondary wall biosynthesis. Plant J 45:144–165

    Article  PubMed  Google Scholar 

  • Audic S, Claverie JM (1997) The significance of digital gene expression profiles. Genome Res 7:986–995

    PubMed  CAS  Google Scholar 

  • Bhalerao R, Keskitalo J, Sterky F, Erlandsson R, Bjorkbacka H, Birve SJ, Karlsson J, Gardestrom P, Gustafsson P, Lundeberg J et al (2003) Gene expression in autumn leaves. Plant Physiol 131:430–442

    Article  PubMed  Google Scholar 

  • Blanc G, Hokamp K, Wolfe KH (2003) A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. Genome Res 13:137–144

    Article  PubMed  CAS  Google Scholar 

  • Blanc G, Wolfe KH (2004) Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16:1679–1691

    Article  PubMed  CAS  Google Scholar 

  • Cohen BA, Mitra RD, Hughes JD, Church GM (2000) A computational analysis of whole-genome expression data reveals chromosomal domains of gene expression. Nat Genet 26:183–186

    Article  PubMed  CAS  Google Scholar 

  • Evertsz EM, Au-Young J, Ruvolo MV, Lim AC, Reynolds MA (2001) Hybridization cross-reactivity within homologous gene families on glass cDNA microarrays. Biotechniques 31:1182, 1184, 1186 passim

    PubMed  CAS  Google Scholar 

  • Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545

    PubMed  CAS  Google Scholar 

  • Gu Z, Steinmetz LM, Gu X, Scharfe C, Davis RW, Li WH (2003) Role of duplicate genes in genetic robustness against null mutations. Nature 421:63–66

    Article  PubMed  CAS  Google Scholar 

  • He X, Zhang J (2005) Rapid subfunctionalization accompanied by prolonged and substantial neofunctionalization in duplicate gene evolution. Genetics 169:1157–1164

    Article  PubMed  Google Scholar 

  • Hutchison L (1994) Some wood-inhabiting yeasts of trembling aspen (Populus tremuloides) from Alberta and northeastern British Columbia. Mycologia 86:386–391

    Article  Google Scholar 

  • Hutchison L (1999) Wood-inhabiting microfungi isolated from Populus tremuloides from Alberta and northeastern British Columbia. Can J Bot 77:898–905

    Article  Google Scholar 

  • Lercher MJ, Urrutia AO, Hurst LD (2002) Clustering of housekeeping genes provides a unified model of gene order in the human genome. Nat Genet 31:180–183

    Article  PubMed  CAS  Google Scholar 

  • Lercher MJ, Blumenthal T, Hurst LD (2003) Coexpression of neighboring genes in Caenorhabditis elegans is mostly due to operons and duplicate genes. Genome Res 13:238–243

    Article  PubMed  CAS  Google Scholar 

  • Lynch M, Force A (2000) The probability of duplicate gene preservation by subfunctionalization. Genetics 154:459–473

    PubMed  CAS  Google Scholar 

  • Maere S, De Bodt S, Raes J, Casneuf T, Van Montagu M, Kuiper M, Van de Peer Y (2005) Modeling gene and genome duplications in eukaryotes. Proc Natl Acad Sci USA 102:5454–5459

    Article  PubMed  CAS  Google Scholar 

  • Mathe C, Sagot MF, Schiex T, Rouze P (2002) Current methods of gene prediction, their strengths and weaknesses. Nucleic Acids Res 30:4103–4117

    Article  PubMed  CAS  Google Scholar 

  • Moreau C, Aksenov N, Lorenzo MG, Segerman B, Funk C, Nilsson P, Jansson S, Tuominen H (2005) A genomic approach to investigate developmental cell death in woody tissues of Populus trees. Genome Biol 6:R34

    Article  PubMed  Google Scholar 

  • Ohno S (1970) Evolution by gene duplication. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Oliver B, Misteli T (2005) A non-random walk through the genome. Genome Biol 6:214

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Sterky F, Bhalerao RR, Unneberg P, Segerman B, Nilsson P, Brunner AM, Charbonnel-Campaa L, Lindvall JJ, Tandre K, Strauss SH et al (2004) A Populus EST resource for plant functional genomics. Proc Natl Acad Sci USA 101:13951-13956

    Article  PubMed  Google Scholar 

  • Sterck L, Rombauts S, Jansson S, Sterky F, Rouze P, Van de Peer Y (2005) EST data suggest that poplar is an ancient polyploid. New Phytol 167:165–170

    Article  PubMed  Google Scholar 

  • Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, Carlson J, Chalot M, Chapman J, Chen GL, Cooper D, Coutinho PM, Couturier J, Covert S, Cronk Q, Cunningham R, Davis J, Degroeve S, Dejardin A, Depamphilis C, Detter J, Dirks B, Dubchak I, Duplessis S, Ehlting J, Ellis B, Gendler K, Goodstein D, Gribskov M, Grimwood J, Groover A, Gunter L, Hamberger B, Heinze B, Helariutta Y, Henrissat B, Holligan D, Holt R, Huang W, Islam-Faridi N, Jones S, Jones-Rhoades M, Jorgensen R, Joshi C, Kangasjarvi J, Karlsson J, Kelleher C, Kirkpatrick R, Kirst M, Kohler A, Kalluri U, Larimer F, Leebens-Mack J, Leple JC, Locascio P, Lou Y, Lucas S, Martin F, Montanini B, Napoli C, Nelson DR, Nelson C, Nieminen K, Nilsson O, Pereda V, Peter G, Philippe R, Pilate G, Poliakov A, Razumovskaya J, Richardson P, Rinaldi C, Ritland K, Rouze P, Ryaboy D, Schmutz J, Schrader J, Segerman B, Shin H, Siddiqui A, Sterky F, Terry A, Tsai CJ, Uberbacher E, Unneberg P, Vahala J, Wall K, Wessler S, Yang G, Yin T, Douglas C, Marra M, Sandberg G, Van de Peer Y, Rokhsar D (2006) The genome of black cottonwood, Populus trichocarpa. Science 313(5793):1596–1604

    Article  PubMed  CAS  Google Scholar 

  • Williams EJ, Bowles DJ (2004) Coexpression of neighboring genes in the genome of Arabidopsis thaliana. Genome Res 14:1060–1067

    Article  PubMed  CAS  Google Scholar 

  • Wolfe KH (2001) Yesterday’s polyploids and the mystery of diploidization. Nat Rev Genet 2:333–341

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

This work was supported by the Knut and Alice Wallenberg Foundation and the Swedish Foundation for Strategic Research.

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Correspondence to Bo Segerman.

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Communicated by: S. Strauss

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Table 1

List of genes identified as having a specific differential expression pattern. The columns are named as follows: “ModelID”, the name of the gene. “Upregulated in Lib”, the one-letter code for the EST library it was overrepresented (in cambial zone [AB]; active cambium [UB]; dormant cambium [UA]; tension wood [G]; wood cell death [X]; young leaves [C]; senescing leaves [I]; cold-stressed leaves [L]; dormant buds [Q]; petioles [P]; flower buds [F]; female catkins [M]; male catkins [V]). Ratio, the ratio between the observed number of ESTs and the expected. “p-value,” The p value of the Fisher test. “significance category,” the significance category based on Bonferroni correction for multiple tests were labeled with ‘*’ (5%), ‘**’ (1%), and ‘***’ (0.1%). “Total clones,” number of EST clones associated with this gene. “Lib clones,” number of EST clones associated with the library in column 2. “Closest AT,” closest Arabidopsis gene. “score,” BLASTP score toward closest Arabidopsis gene. “p val,” BLASTP p value toward closest Arabidopsis gene. “annotation,” Annotation of closest Arabidopsis gene. “GO,” gene ontology of closest Arabidopsis gene. “Broad category,” functional category assigned to this gene. “2nd category,” second level of functional category (PDF 440 kb).

Fig. 1

Complement to Fig. 5. Functions of the up-regulated genes. The functions of the identified genes were divided into broad categories, and their distribution in each library was plotted. a Protein biosynthesis/folding, b degradation/hydrolysis, c intracellular structure/storage, d transport/maintainment, e metabolism, f development/aging, g transcription, h response(PDF 559 kb)

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Segerman, B., Jansson, S. & Karlsson, J. Characterization of genes with tissue-specific differential expression patterns in Populus . Tree Genetics & Genomes 3, 351–362 (2007). https://doi.org/10.1007/s11295-006-0077-6

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