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Novel gene expression profiles define the metabolic and physiological processes characteristic of wood and its extractive formation in a hardwood tree species, Robinia pseudoacacia

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Abstract

Wood is of critical importance to humans as a primary feedstock for biofuel, fiber, solid wood products, and various natural compounds including pharmaceuticals. The trunk wood of most tree species has two distinctly different regions: sapwood and heartwood. In addition to the major constituents, wood contains extraneous chemicals that can be removed by extraction with various solvents. The composition and the content of the extractives vary depending on such factors as, species, growth conditions, and time of year when the tree is cut. Despite the great commercial and keen scientific interest, little is known about the tree-specific biology of the formation of heartwood and its extractives. In order to gain insight on the molecular regulations of heartwood and its extractive formation, we carried out global examination of gene expression profiles across the trunk wood of black locust (Robinia pseudoacacia L.) trees. Of the 2,915 expressed sequenced tags (ESTs) that were generated and analyzed in the current study, 55.3% showed no match to known sequences. Cluster analysis of the ESTs identified a total of 2278 unigene sets, which were used to construct cDNA microarrays. Microarray hybridization analyses were then performed to survey the changes in gene expression profiles of trunk wood. The gene expression profiles of wood formation differ according to the region of trunk wood sampled, with highly expressed genes defining the metabolic and physiological processes characteristic of each region. For example, the gene encoding sugar transport had the highest expression in the sapwood, while the structural genes for flavonoid biosynthesis were up-regulated in the sapwood-heartwood transition zone. This analysis also established the expression patterns of 341 previously unknown genes.

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References

  • Adams, M., Kerlavage, A., Fields, C., and Venter, J. 1993. 3,400 new expressed sequence tags identify diversity of transcripts in human brain. Nat Genet 4: 256–267.

    Google Scholar 

  • Allona, I., Quinn, M., Shoop, E., Swope, K., Cyr, S., Carlis, J., Riedl, J., Retzel, E., Campbell, M., Sederoff, R., and Whetten, R. 1998. Analysis of xylem formation in pine by cDNA sequencing. Proc Natl Acad Sci USA 95: 9693–9698.

    Google Scholar 

  • Audic, S. and Claverie, J-M. 1997. The significance of digital gene expression profiles. Genome Research 7: 986–995.

    Google Scholar 

  • Bairoch, A. and Apweiler, R. 2000. The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000. Nucleic Acids Res. 28: 45–48.

    Google Scholar 

  • Barker, W., Garavelli, J., Huang, H., McGarvey, P., Orcutt, B., Srinivasarao, G., Xiao, C., Yeh, L.-S.L., Ledley, R., Janda, J., Pfeiffer, F., Mewes, H.-W., Tsugita, A. and Wu, C. 2000. The Protein Information Resource (PIR). Nucleic Acids Res. 28: 41–44.

    Google Scholar 

  • Baugh, L., Hill, A., Brown, E., and Hunter, C. 2001. Quantitative analysis of mRNA amplification by in vitro transcription. Nuccleic Acid Res. 29: e29.

    Google Scholar 

  • Benson, D., Karsch-Mizrachi, I., Lipman, D., Ostell, J., Rapp, B., and Wheeler, D. 2000. GenBank. Nucleic Acids Res. 28: 15–18.

    Google Scholar 

  • Beritognolo, I., Magel, E., Abdel-Latif, A., Charpentier, J., Jay-Allemand, C., and Breton, C. 2002. Expression of genes encoding chalcone synthase, flavanone 3-hydroxylase, and dihydroflavonol 4-reductase correlates with flavanol accumulation during heartwood formation in Juglans nigra L. Tree Physiol. 22: 291–300.

    Google Scholar 

  • Bevan, M., Bancroft, I., Bent, E., Love, K., Goodman, H., Dean, C., Bergkamp, R., Dirkse, W., Van Staveren, M., Stiekema, W., Drost, L., Ridley, P., Hudson, S.A., Patel, K., Murphy, G., Piffanelli, P., Wedler, H., Wedler, E., Wambutt, R., Weitzenegger, T., Pohl, T.M., Terryn, N., Gielen, J., Villarroel, R., and Chalwatzis, N. 1998. Analysis of 1.9 Mb contiguous sequence from chromosome 4 of Arabidopsis thaliana. Nature 391: 485–488.

    Google Scholar 

  • Burtin, P., Jay-Allemand, C., Charpentier, J., and Janin, G. 1998 Natural wood colouring process in Juglans sp. (J. nigra, J. regia and hybrid J. nigra 23 × J. regia) depends on native phenolic compounds accumulated in the transition zone between sapwood and heartwood. Trees 12: 258–264.

    Google Scholar 

  • Carrodus, B., and Triffett, A. 1975. Analysis of respiratory gases in woody stems by mass spectrometry. New Phytol. 74: 243–246.

    Google Scholar 

  • Cercos, M., Santamaria, S., and Carbonell, J. 1999. Cloning and characterization of TPE4A, a thiol-protease gene induced during ovary senescence and seed germination in pea. Plant Physiol. 119: 1341–1348.

    Google Scholar 

  • Covitz, P., Smith, L., and Long, S. 1998. Expressed Sequence Tags from a Root-Hair-Enriched Medicago truncatula cDNA library. Plant. Physiol. 117: 1325–1332.

    Google Scholar 

  • Dazzo, F., and Hubbell, H. 1975. Cross-reactive antigens and lectins as determinants of symbiotic specificity in the Rhizobium–clover association. Appl. Microbiol. 30: 1017–1033.

    Google Scholar 

  • de Vetten, N., ter Horst, J., van Schaik, H.-P., de Boer, A., Mol, J., and Koes, R. 1999. A cytochrome b5 is required for full activity of flavonoid 3?,5?-hydroxylase, a cytochrome P450 involved in the formation of blue flowers. Proc Natl Acad Sci USA 96: 778–783.

    Google Scholar 

  • Dent, G., O'Dell, D, and Eberwine, H. 2001. Gene expression profiling in the amygdala: An approach to examine the moleculat substrates of mammalian behavior. Physiol. Behavior 73: 841–847.

    Google Scholar 

  • Eisen, M., Spellman, P., Brown, P., and Botstein, D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA 95: 14863–14868.

    Google Scholar 

  • Eulgem, T., Rushton, P., Schmelzer, E., Hahlbrock, K., and Somssich, I. 1999 Early nuclear events in plant defence signalling: rapid gene activation by WRKY transcription factors. EMBO J. 18: 4689–4699.

    Google Scholar 

  • Ewing, B., Hillier, L., Wendl M., and Green, P. 1998. Basecalling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res. 8: 175–185.

    Google Scholar 

  • Fukuda, H. (1996). Xylogenesis: initiation, prpgression, and cell death. Ann Rev Plant Physiol Plant Mol Biol 47, 299–325.

    Google Scholar 

  • García-Hernández, M., Murphy, A., and Taiz, L. 1998. Matallothioneins 1 and 2 have distinct but overlapping expreeion patterns in Arabidopsis. Plant Physiol. 118: 387–397.

    Google Scholar 

  • Hauch, S. and Magel, E. 1998. Extractable activities and protein content of sucrose-phosphate synthase, sucrose synthase and neutral invertase in trunk tissues of Robinia pseudoacacia L. are related to cambial wood production and heartwood formation. Planta 207: 266–274.

    Google Scholar 

  • Hertzberg, M., Aspeborg, H., Schrader, J., Andersson, A., Erlandsson, R., Blomqvist, K., Bhalerao, R., Uhlén, M., Teeri, T., Lundberg, J., Sundberg, B., Nisson, P., and Sandberg, G. 2001. A transcriptional roadmap to wood formation. Proc. Natl. Acad. Sci. USA 98: 14732–14737.

    Google Scholar 

  • Hihara, Y., Kamei, A., Kanehisa, M., Kaplan, A., and Ikeuchi, M. 2001. DNA Microarray Analysis of Cyanobacterial Gene Expression during Acclimation to High Light, Plant Cell 13: 793–806.

    Google Scholar 

  • Hillinger, C., Holl, W., and Ziegler, H. 1996a. Lipids and lipolytic enzymes in the trunkwood of Robinia pseudoacacia L. during heartwood formation. I. Radial distribution of lipid classes. Trees 10: 366–375.

    Google Scholar 

  • Hillinger, C., Holl, W., and Ziegler, H. 1996b. Lipids and lipolytic enzymes in the trunkwood of Robinia pseudoacacia L. during heartwood formation. II. Radial distribution of lipases and phospholipases. Trees 10: 376–381.

    Google Scholar 

  • Hillis W. 1987. Heartwood and the exudates, Spinger, Berlin, Heidelberg, New York.

    Google Scholar 

  • Ingemarsson, B. 1995. Ethylene effects on peroxidases and cell growth patterns in Picea abies hypocotyl cuttings. Physiol. Plant. 94: 211–218.

    Google Scholar 

  • Kirst, M., Johnson, A., Retzel, E., van Zyl, L., Craig, D., Li, Z.J., Whetten, R., Baucom, C., Ulrich, E., Hubbard, Kristy, and Sederoff, R. (2002). Quantitative inference in functional genomics of loblolly pine (Pinus taeda L.) using ESTs and microarrays. In Proc. the 10th IAPTC&B Congress. (Ed) I. Vasil. Kluwer Academic Publishers, Dordrecht, Netherlands. Kozlowski, T. and Pallardy, S. (1997). Physiology of woody plants. San Diego, Academic Press.

    Google Scholar 

  • Lalonde, S., Boles, E., Hellmann, H., Barker, L., Patrick, J., Frommer, W., and Ward, J. 1999. The dual function of sugar carriers: transport and sugar sensing. Plant Cell 11: 707–726.

    Google Scholar 

  • Lee, M., Kuo, F., Whitmore, G., and Sklar, J. 2000. Importance of replication in microarray gene expression studies: Statistical methods and evidence from repetitive cDNA hybridizations. Proc. Natl. Acad. Sci. USA 97: 9834–9839.

    Google Scholar 

  • Livesey, F., Furukawa, T., Steffen, M., Church, G., and Cepko, C. 2000 Microarray analysis of the transcriptional network controlled by the photoreceptor homeobox gene Crx. Current Biology 10: 301–310.

    Google Scholar 

  • Lorenz, W. and Dean, J. 2002. SAGE profiling and demonstration of differential gene expression along the axial developmental gradient of lignifying xylem in loblolly pine (Pinus taeda). Tree Physiology 22: 301–310.

    Google Scholar 

  • Magel, E. 2000. Biochemistry and physiology of heartwood formation. In Molecular and Cell Biology of Wood Formation. Eds. R. Savidge, J. Barnett and R. Napier. BIOS Scientific Publishers, Oxford, pp. 363–376.

    Google Scholar 

  • Magel, E., Jay-Allemand, C., and Ziegler, H. 1994. Formation of heartwood substances in the stemwood of Robinia pseudoacacia L.: II. Distribution of nonstructural carbohydrates and wood extractives across the trunk. Trees 165–171.

  • Magel, E. and Hübner, B. 1997 Distribution of phenylalanine ammonia lyase and chalcone synthase within trunks of Robinia pseudoacacia L. Bot. Acta 110: 314–322.

    Google Scholar 

  • Matamoros, M., Baird, L., Escuredo, P., Dalton, D., Minchin, F., Iturbe-Ormaetxe, I., Rubio, M., Moran, J., Gordon, A., and Becana, M. 1999. Stress-induced legume root nodule senescence. Physiological, biochemical, and structural alterations. Plant Physiol 121: 97–112.

    Google Scholar 

  • Mauseth, J. 1998.Botany: an introduction to plant biology. Jones and Bartlett Publishers. Sudbury, Massachusetts.

    Google Scholar 

  • Miller, J., Arteca, R., and Pell, E. 1999. Senescence-associated gene expression during ozone-induced leaf senescence in Arabidopsis. Plant Physiol. 20: 1015–1024.

    Google Scholar 

  • Nelson, N. 1978. Xylem ethylene, phenol oxidising enzymes and nitrogen and heartwood formation in walnut and cherry. Can. J. Bot. 56: 626–634.

    Google Scholar 

  • Nilsson, M., Wikman, S., and Eklund, L. 2002. Induction of discolored wood in Scots pine (Pinus sylvestris). Tree Physiology 22: 331–338.

    Google Scholar 

  • Perez-Amador, M., Lidder, P., Johnson, M., Landgraf, J., Wisman, E., and Green, P. 2001. New molecular phenotypes in the dst mutants of Arabidopsis revealed by DNA microarray analysis. Plant Cell 13: 2703–2717.

    Google Scholar 

  • Reddy, A., and Poovaiah, B. 1990. Molecular cloning and sequencing of a cDNA for an auxin-repressed mRNA: correlation between fruit growth and repression of the auxin-regulated gene. Plant Mol Biol. 14: 127–136.

    Google Scholar 

  • Roberts, L. and Miller, A. 1983 Is ethylene involved in xylem of differentiation? Plant Physiol. 6: 1–24.

    Google Scholar 

  • Saxe, H., Ellsworth, D. S., and Heath, J. 1998. Tree and forest functioning in an enriched CO2 atmosphere. New Phytol. 139: 395–436.

    Google Scholar 

  • Schaffer, R., Landgraf, J., Accerbi, M., Simon, V., Larson, M., and Wisman, E. 2001. Microarray Analysis of Diurnal and Circadian-Regulated Genes in Arabidopsis. Plant Cell 13: 113–123.

    Google Scholar 

  • Sederoff, R., Kirst, M., Johnson, A., Retzel, E., Whetten, R., Vasques-Kool, J. & O'Malley, D. 2002. Homology of expressed genes in loblolly pine (Pinus taeda L.) with Arabidopsis thaliana. The 10th IAPTC&B Congress, February 23–28, 2002, Orlando, FL.

  • Seki, M., Narusaka, M., Abe, H., Kasuga, M., Yamaguchi-Shinozaki, K., Carninci, P., Hayashizaki, Y., and Shinozaki, K. 2001. Monitoring the Expression Pattern of 1300 Arabidopsis Genes under Drought and Cold Stresses by Using a Full-Length cDNA Microarray. Plant Cell 13: 61–72.

    Google Scholar 

  • Stafstrom, J., Ripley, B., Devitt, M., and Drake, B. 1998. Dormancy-associated gene expression in pea axillary buds. Cloning and expression of PsDRM1 and PsDRM2. Planta 205: 547–552.

    Google Scholar 

  • Sterky, F., Regan, S., Karlsson, J., Hertzberg, M., Rohde, A., Holmberg, A., Amini, B., Bhalerao, R., Larsson, M., Villarroel, R., Van Montagu, M., Sandberg, G., Olsson, O., Teeri, T. T., Boerjan, W., Gustafsson, P., Uhlen, M., Sundberg, B., and Lundeberg, J. 1998. Gene discovery in the wood-forming tissues of poplar: analysis of 5, 692 expressed sequence tags. Proc Natl Acad Sci USA 95: 13330–13335.

    Google Scholar 

  • Steward, C. 1966. Excretion and heartwood formation in living trees. Science 153: 1068–1074.

    Google Scholar 

  • Uggla, C., Magel, E., Moritz, T., and Sundberg, B. 2001. Function and dynamics of auxin and carbohydrates during early wood/late wood transition in Scots pine. Plant Physiol. 125: 2029–2039.

    Google Scholar 

  • Wang, E., Miller, L., Ohnmacht, G., Liu, E., and Marincola, F 2000. High-fidelity mRNA amplification for gene profiling. Nat. Biotech 18: 457–459.

    Google Scholar 

  • Williams, L., Lemoine, R., and Sauer, N. 2000. Sugar transporters in higher plants – a diversity of roles and complex regulation. Trens in Plant Science 5: 283–290.

    Google Scholar 

  • Wingler, A., von Schaewen, A., Leegood, R., Lea, P., and Quick, W. 1998. Regulation of leaf senescence by cytokinin, sugars, and light. Plant Physiol. 116: 329–335.

    Google Scholar 

  • Yu, Q., He, M., Lee, N., and Liu, E. (2002). Identification of MYCmediated death response pathways by microarray analysis. J Biol Chem. 277: 13059–13066.

    Google Scholar 

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Authors and Affiliations

  1. Department of Forestry, 126 Natural Resources, Michigan State University, East Lansing, MI, 48824-1222, USA

    Jaemo Yang, Sunchung Park, D. Pascal Kamdem, Daniel E. Keathley & Kyung-Hwan Han

  2. Academic Computing and Bioinformatics, Academic Health Center, University of Minnesota, 650 Children's Rehabilitation Center, UMHC Box 43, 426 Church St. S.E., Minneapolis, MN, 55455-0312, USA

    Ernest Retzel & Charlie Paule

  3. Veterinary PathoBiology, Advanced Genetic Analysis Center, University of Minnesota, 1971 Commonwealth Avenue, St. Paul, MN, 55108, USA

    Vivek Kapur

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  1. Jaemo Yang
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  2. Sunchung Park
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  3. D. Pascal Kamdem
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  4. Daniel E. Keathley
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  8. Kyung-Hwan Han
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Yang, J., Park, S., Kamdem, D.P. et al. Novel gene expression profiles define the metabolic and physiological processes characteristic of wood and its extractive formation in a hardwood tree species, Robinia pseudoacacia . Plant Mol Biol 52, 935–956 (2003). https://doi.org/10.1023/A:1025445427284

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