Plant Molecular Biology Reporter

, Volume 28, Issue 2, pp 222–230 | Cite as

A Cross-species Transcriptional Profile Analysis of Heartwood Formation in Black Walnut

  • Zhonglian Huang
  • Chung-Jui Tsai
  • Scott A. Harding
  • Richard Meilan
  • Keith Woeste
Article

Abstract

The value of black walnut (Juglans nigra L.) is determined by the quality and quantity of darkly colored heartwood in its stem. We are exploring the regulation of heartwood production by identifying genes associated with the transition from sapwood to heartwood. We analyzed microarray data from a cross-species hybridization where black walnut cDNA was probed using a 7K gene aspen array. Results showed that only about 17% (1,253 vs 7K) of the probes in the microarray hybridized with genes from black walnut. Genes showing differential abundance in response to time change and developmental stage in the stem were identified and investigated. Eleven genes were identified as upregulated only in the transition zone (TZ) or interior sapwood of a tree harvested in fall; 55 genes were upregulated only in the TZs of trees harvested in summer; 74 genes were upregulated in the TZ of trees harvested in summer and in fall. Most of these genes were classified as “no hits”, but some, such as the orthologs of Arabidopsis genes At2g14900 and At3g04710, were putatively related to cell rescue and defense. Genes related to other functional classifications such as signal transduction, metabolism, and protein fate and synthesis were also identified in this experiment. Overall, these analyses provide insight into the mechanism regulating heartwood formation in black walnut.

Keywords

Microarray Gene expression Heartwood formation Black walnut 

References

  1. Abeles FB, Morgan PW, Saltveit ME Jr (1992) Ethylene in plant biology, 2nd edn. Academic, San Diego, p 296Google Scholar
  2. Andersson A, Keskitalo J, Sjödin A, Bhalerao R, Sterky F, Wissel K, Tandre K, Aspeborg H, Moyle R, Ohmiya Y, Bhalerao R, Brunner A, Gustafsson P, Karlsson J, Lundeberg J, Nilsson O, Sandberg G, Strauss S, Sundberg B, Uhlen M, Jansson S, Nilsson P (2004) A transcriptional timetable of autumn senescence. Genome Biol 5(4):R24CrossRefPubMedGoogle Scholar
  3. Bar-Or C, Czosnek H, Koltai H (2007) Cross-species microarray hybridizations: a developing tool for studying species diversity. Trends Genet 23(4):200–207CrossRefPubMedGoogle Scholar
  4. Beritognolo I, Magel E, Abdel-Latif A, Charpentier JP, Jay-Allemand G, 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 22:291–300PubMedGoogle Scholar
  5. Carrodus BB (1971) Carbon dioxide and the formation of heartwood. New Phytol 70:939–943CrossRefGoogle Scholar
  6. Chen JC, Jiang CZ, Gookin TE, Hunter DA, Clark DG, Reid MS (2004) Chalcone synthase as a reporter in virus-induced gene silencing studies of flower senescence. Plant Mol Biol 55:521–530CrossRefPubMedGoogle Scholar
  7. Churchill GA (2002) Fundamentals of experimental design for cDNA microarrays. Nat Genet 32(Suppl):490–495CrossRefPubMedGoogle Scholar
  8. Debeaujon I, Peeters AJM, Leon-Kloosterziel KM, Koornneef M (2001) The TRANSPARENT TESTA12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium. Plant Cell 13:853–871CrossRefPubMedGoogle Scholar
  9. DeBell J, Morrell JJ, Gartner BL (1999) Within-stem variation in tropolone content and decay resistance of second-growth western redcedar. For Sci 45(2):101–107Google Scholar
  10. Dhaubhadel S, McGarvey BD, Williams R, Gijzen M (2003) Isoflavonoid biosynthesis and accumulation in developing soybean seeds. Plant Mol Biol 53:733–743CrossRefPubMedGoogle Scholar
  11. Dhawale S, Souciet G, Kuhn DN (1989) Increase of chalcone synthase mRNA in pathogen-inoculated soybeans with race-specific resistance is different in leaves and roots. Plant Physiol 91:911–916CrossRefPubMedGoogle Scholar
  12. Dong XN (2004) The role of membrane-bound ankyrin-repeat protein ACD6 in programmed cell death and plant defense. Sci STKE 24(221):pe6Google Scholar
  13. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95:14863–14868CrossRefPubMedGoogle Scholar
  14. Feinbaum RL, Ausubel FM (1988) Transcriptional regulation of the Arabidopsis thaliana chalcone synthase gene. Mol Cell Biol 8:1985–1992PubMedGoogle Scholar
  15. Frey-Wyssling A, Bosshard HH (1959) Cytology of the ray cells in sapwood and heartwood. Holzforschung 13:129–137CrossRefGoogle Scholar
  16. Goodman CD, Casati P, Walbot V (2004) A multidrug resistance-associated protein involved in anthocyanin transport in Zea mays. Plant Cell 16:1812–1826CrossRefPubMedGoogle Scholar
  17. Harding S, Jiang HY, Jeong ML, Casado FL, Ling HW, Tsai CJ (2005) Functional genomics analysis of foliar condensed tannin and phenolic glycoside regulation in natural cottonwood hybrids. Tree Physiol 25:1475–1486PubMedGoogle Scholar
  18. Hauch S, 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 207:266–274CrossRefGoogle Scholar
  19. Heller W, Forkmann G (1988) Biosynthesis. In: Harborne JB (ed) The flavonoids. Chapman and Hall, London, pp 399–524Google Scholar
  20. Helm RF (2000) Heartwood formation in woody plants. Biotech Times 7:1–3Google Scholar
  21. Hertzberg M, Aspeborg H, Schrader J, Andersson A, Erlandsson R, Blomqvist K, Bhalerao R, Uhlen M, Teeri TT, Lundeberg J (2001) A transcriptional roadmap to wood formation. Proc Natl Acad Sci U S A 98:14732–14737CrossRefPubMedGoogle Scholar
  22. Higuchi T (1997) Biochemistry and molecular biology. Springer-Verlag, Berlin, p 362Google Scholar
  23. Hillis WE (1987) Heartwood and tree exudates. In: Timell TE (ed) Springer Series in Wood Science. Springer-Verlag, Heidelberg, p 268Google Scholar
  24. Kolosova N, Miller B, Ralph S, Ellis BE, Douglas C, Ritland K, Bohlmann J (2004) Isolation of high-quality RNA from gymnosperm and angiosperm trees. Biotech 36:821–824Google Scholar
  25. Magel E (2000) Biochemistry and physiology of heartwood formation. In: Savidge R, Barnett J, Napier R (eds) Molecular and cell biology of wood formation. BIOS Scientific Publishers, Oxford, pp 363–376Google Scholar
  26. Magel E, Hillinger C, Wagner T, Holl W (2001) Oxidative pentose phosphate pathway and pyridine nucleotides in relation to heartwood formation in Robinia pseudoacacia L. Phytochemistry 57(7):1061–1068CrossRefPubMedGoogle Scholar
  27. Mayer I, Koch G, Puls J (2006) Topochemical investigations on wood extractives and their influence on color changes in American black cherry (Prunus serotina Borkh.). Holzforschung 60:589–594CrossRefGoogle Scholar
  28. Miller AR, Crawford DL, Roberts LW (1985) Lignification and xylogenesis in Lactuca pith explants cultured in vitro in the presence of auxin and cytokinin: a role of endogenous ethylene. J Exp Bot 36:110–118CrossRefGoogle Scholar
  29. Nelson ND (1978) Xylem ethylene, phenol-oxidizing enzymes and nitrogen and heartwood formation in walnut and cherry. Can J Bot 56:626–634CrossRefGoogle Scholar
  30. Nobuchi T, Takai K, Harada H (1987a) Distribution of heartwood phenols in the trunk of Sugi (Cryptomeria japonica D. Don) and partial characterization of heartwood formation. Mokuzai Gakkaishi 33:88–96Google Scholar
  31. Nobuchi T, Tokuchi N, Harada H (1987b) Variability of heartwood formation and cytological features in broadleaved trees. Mokuzai Gakkaishi 33:596–604Google Scholar
  32. Pourcel L, Routaboul JM, Kerhoas L, Caboche M, Lepiniec L, Debeaujon I (2005) TRANSPARENT TESTA10 encodes a laccase-like enzyme involved in oxidative polymerization of flavonoids in Arabidopsis seed coat. Plant Cell 17:2966–2980CrossRefPubMedGoogle Scholar
  33. Ranjan P, Kao YY, Jiang H, Joshi CP, Harding SA, Tsai CJ (2004) Suppression subtractive hybridization-mediated transcriptome analysis from multiple tissues of aspen (Populus tremuloides) trees altered in phenylpropanoid metabolism. Planta 219:694–704CrossRefPubMedGoogle Scholar
  34. Rhee SY, Beavis W, Berardini TZ, Chen G, Dixon D, Doyle A, Garcia-Hernandez M, Huala E, Lander G, Montoya M, Miller N, Mueller LA, Mundodi S, Reiser L, Tacklind J, Weems DC, Wu Y, Xu I, Yoo D, Yoon J, Zhang P (2003) The Arabidopsis Information Resource (TAIR): a model organism database providing a centralized, curated gateway to Arabidopsis biology, research materials and community. Nucleic Acids Res 31(1):224–228CrossRefPubMedGoogle Scholar
  35. Shain L, Mackay JFG (1973) Seasonal fluctuation in respiration of aging xylem in relation to heartwood formation in Pinus radiata. Can J Bot 51:737–741CrossRefGoogle Scholar
  36. Shirley BW, Kubasek WL, Storz G, Bruggemann E, Koorneef M, Ausubel FM, Goodman HM (1995) Analysis of Arabidopsis mutants deficient in flavonoid biosynthesis. Plant J 8:659–671Google Scholar
  37. Taylor G, Street NR, Tricker PJ, Sjödin A, Graham LE, Skogström O, Calfapietra C, Scarascia-Mugnozza G, Jansson S (2005) The transcriptome of Populus in elevated CO2. New Phytol 167:43–154CrossRefGoogle Scholar
  38. Yang J, Kamadem DP, Keathley DE, Han KH (2004) Seasonal changes in gene expression at the sapwood-heartwood transition zone of black locust (Robinia pseudoacacia) revealed by cDNA microarray analysis. Tree Physiol 24(4):461–474PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Zhonglian Huang
    • 1
  • Chung-Jui Tsai
    • 2
  • Scott A. Harding
    • 2
  • Richard Meilan
    • 1
  • Keith Woeste
    • 3
  1. 1.Department of Forestry and Natural Resources, Hardwood Tree Improvement and Regeneration Center (HTIRC)Purdue UniversityWest LafayetteUSA
  2. 2.Warnell School of Forestry and Natural Resources and Department of GeneticsUniversity of GeorgiaAthensUSA
  3. 3.USDA Forest Service Northern Research Station Hardwood Tree Improvement and Regeneration CenterPurdue UniversityWest LafayetteUSA

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