Skip to main content
Comparative and Functional Genomics logoLink to Comparative and Functional Genomics
. 2002 Jun;3(3):226–243. doi: 10.1002/cfg.169

Studying the Functional Genomics of Stress Responses in Loblolly Pine With the Expresso Microarray Experiment Management System

Lenwood S Heath 1, Naren Ramakrishnan 1,, Ronald R Sederoff 2, Ross W Whetten 2, Boris I Chevone 3, Craig A Struble 4, Vincent Y Jouenne 1, Dawei Chen 1, Leonel van Zyl 2, Ruth Grene 3
PMCID: PMC2447276  PMID: 18628855

Abstract

Conception, design, and implementation of cDNA microarray experiments present a variety of bioinformatics challenges for biologists and computational scientists. The multiple stages of data acquisition and analysis have motivated the design of Expresso, a system for microarray experiment management. Salient aspects of Expresso include support for clone replication and randomized placement; automatic gridding, extraction of expression data from each spot, and quality monitoring; flexible methods of combining data from individual spots into information about clones and functional categories; and the use of inductive logic programming for higher-level data analysis and mining. The development of Expresso is occurring in parallel with several generations of microarray experiments aimed at elucidating genomic responses to drought stress in loblolly pine seedlings. The current experimental design incorporates 384 pine cDNAs replicated and randomly placed in two specific microarray layouts. We describe the design of Expresso as well as results of analysis with Expresso that suggest the importance of molecular chaperones and membrane transport proteins in mechanisms conferring successful adaptation to long-term drought stress.

Full Text

The Full Text of this article is available as a PDF (369.0 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aharoni A., Keizer L. C., Bouwmeester H. J., Sun Z., Alvarez-Huerta M., Verhoeven H. A., Blaas J., van Houwelingen A. M., De Vos R. C., van der Voet H. Identification of the SAAT gene involved in strawberry flavor biogenesis by use of DNA microarrays. Plant Cell. 2000 May;12(5):647–662. doi: 10.1105/tpc.12.5.647. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alexandre H., Ansanay-Galeote V., Dequin S., Blondin B. Global gene expression during short-term ethanol stress in Saccharomyces cerevisiae. FEBS Lett. 2001 Jun 1;498(1):98–103. doi: 10.1016/s0014-5793(01)02503-0. [DOI] [PubMed] [Google Scholar]
  3. Bard J. B. A bioinformatics approach to investigating developmental pathways in the kidney and other tissues. Int J Dev Biol. 1999;43(5):397–403. [PubMed] [Google Scholar]
  4. Brachat A., Pierrat B., Brüngger A., Heim J. Comparative microarray analysis of gene expression during apoptosis-induction by growth factor deprivation or protein kinase C inhibition. Oncogene. 2000 Oct 19;19(44):5073–5082. doi: 10.1038/sj.onc.1203882. [DOI] [PubMed] [Google Scholar]
  5. Brown M. P., Grundy W. N., Lin D., Cristianini N., Sugnet C. W., Furey T. S., Ares M., Jr, Haussler D. Knowledge-based analysis of microarray gene expression data by using support vector machines. Proc Natl Acad Sci U S A. 2000 Jan 4;97(1):262–267. doi: 10.1073/pnas.97.1.262. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Callis J., Vierstra R. D. Protein degradation in signaling. Curr Opin Plant Biol. 2000 Oct;3(5):381–386. doi: 10.1016/s1369-5266(00)00100-x. [DOI] [PubMed] [Google Scholar]
  7. Cho R. J., Campbell M. J., Winzeler E. A., Steinmetz L., Conway A., Wodicka L., Wolfsberg T. G., Gabrielian A. E., Landsman D., Lockhart D. J. A genome-wide transcriptional analysis of the mitotic cell cycle. Mol Cell. 1998 Jul;2(1):65–73. doi: 10.1016/s1097-2765(00)80114-8. [DOI] [PubMed] [Google Scholar]
  8. Chu S., DeRisi J., Eisen M., Mulholland J., Botstein D., Brown P. O., Herskowitz I. The transcriptional program of sporulation in budding yeast. Science. 1998 Oct 23;282(5389):699–705. doi: 10.1126/science.282.5389.699. [DOI] [PubMed] [Google Scholar]
  9. Claverie J. M. Computational methods for the identification of differential and coordinated gene expression. Hum Mol Genet. 1999;8(10):1821–1832. doi: 10.1093/hmg/8.10.1821. [DOI] [PubMed] [Google Scholar]
  10. Costa P., Bahrman N., Frigerio J. M., Kremer A., Plomion C. Water-deficit-responsive proteins in maritime pine. Plant Mol Biol. 1998 Nov 1;38(4):587–596. doi: 10.1023/a:1006006132120. [DOI] [PubMed] [Google Scholar]
  11. Cushman J. C., Bohnert H. J. Genomic approaches to plant stress tolerance. Curr Opin Plant Biol. 2000 Apr;3(2):117–124. doi: 10.1016/s1369-5266(99)00052-7. [DOI] [PubMed] [Google Scholar]
  12. Degenhardt B., Gimmler H. Cell wall adaptations to multiple environmental stresses in maize roots. J Exp Bot. 2000 Mar;51(344):595–603. doi: 10.1093/jexbot/51.344.595. [DOI] [PubMed] [Google Scholar]
  13. Dong J. Z., Dunstan D. I. Characterization of three heat-shock-protein genes and their developmental regulation during somatic embryogenesis in white spruce [Picea glauca (Moench) Voss]. Planta. 1996;200(1):85–91. doi: 10.1007/BF00196653. [DOI] [PubMed] [Google Scholar]
  14. Eisen M. B., Spellman P. T., Brown P. O., Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A. 1998 Dec 8;95(25):14863–14868. doi: 10.1073/pnas.95.25.14863. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Epstein C. B., Butow R. A. Microarray technology - enhanced versatility, persistent challenge. Curr Opin Biotechnol. 2000 Feb;11(1):36–41. doi: 10.1016/s0958-1669(99)00065-8. [DOI] [PubMed] [Google Scholar]
  16. Gang D. R., Kasahara H., Xia Z. Q., Vander Mijnsbrugge K., Bauw G., Boerjan W., Van Montagu M., Davin L. B., Lewis N. G. Evolution of plant defense mechanisms. Relationships of phenylcoumaran benzylic ether reductases to pinoresinol-lariciresinol and isoflavone reductases. J Biol Chem. 1999 Mar 12;274(11):7516–7527. doi: 10.1074/jbc.274.11.7516. [DOI] [PubMed] [Google Scholar]
  17. Gasch A. P., Spellman P. T., Kao C. M., Carmel-Harel O., Eisen M. B., Storz G., Botstein D., Brown P. O. Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell. 2000 Dec;11(12):4241–4257. doi: 10.1091/mbc.11.12.4241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Geisler M., Frangne N., Gomès E., Martinoia E., Palmgren M. G. The ACA4 gene of Arabidopsis encodes a vacuolar membrane calcium pump that improves salt tolerance in yeast. Plant Physiol. 2000 Dec;124(4):1814–1827. doi: 10.1104/pp.124.4.1814. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Gilchrest B. A., Bohr V. A. Aging processes, DNA damage, and repair. FASEB J. 1997 Apr;11(5):322–330. doi: 10.1096/fasebj.11.5.9141498. [DOI] [PubMed] [Google Scholar]
  20. Golub T. R., Slonim D. K., Tamayo P., Huard C., Gaasenbeek M., Mesirov J. P., Coller H., Loh M. L., Downing J. R., Caligiuri M. A. Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science. 1999 Oct 15;286(5439):531–537. doi: 10.1126/science.286.5439.531. [DOI] [PubMed] [Google Scholar]
  21. Gracey A. Y., Troll J. V., Somero G. N. Hypoxia-induced gene expression profiling in the euryoxic fish Gillichthys mirabilis. Proc Natl Acad Sci U S A. 2001 Feb 13;98(4):1993–1998. doi: 10.1073/pnas.98.4.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Greller L. D., Tobin F. L. Detecting selective expression of genes and proteins. Genome Res. 1999 Mar;9(3):282–296. [PMC free article] [PubMed] [Google Scholar]
  23. Hilsenbeck S. G., Friedrichs W. E., Schiff R., O'Connell P., Hansen R. K., Osborne C. K., Fuqua S. A. Statistical analysis of array expression data as applied to the problem of tamoxifen resistance. J Natl Cancer Inst. 1999 Mar 3;91(5):453–459. doi: 10.1093/jnci/91.5.453. [DOI] [PubMed] [Google Scholar]
  24. Hong S. W., Vierling E. Mutants of Arabidopsis thaliana defective in the acquisition of tolerance to high temperature stress. Proc Natl Acad Sci U S A. 2000 Apr 11;97(8):4392–4397. doi: 10.1073/pnas.97.8.4392. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Jelinsky S. A., Estep P., Church G. M., Samson L. D. Regulatory networks revealed by transcriptional profiling of damaged Saccharomyces cerevisiae cells: Rpn4 links base excision repair with proteasomes. Mol Cell Biol. 2000 Nov;20(21):8157–8167. doi: 10.1128/mcb.20.21.8157-8167.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Kannan K., Amariglio N., Rechavi G., Jakob-Hirsch J., Kela I., Kaminski N., Getz G., Domany E., Givol D. DNA microarrays identification of primary and secondary target genes regulated by p53. Oncogene. 2001 Apr 26;20(18):2225–2234. doi: 10.1038/sj.onc.1204319. [DOI] [PubMed] [Google Scholar]
  27. Kawasaki S., Borchert C., Deyholos M., Wang H., Brazille S., Kawai K., Galbraith D., Bohnert H. J. Gene expression profiles during the initial phase of salt stress in rice. Plant Cell. 2001 Apr;13(4):889–905. doi: 10.1105/tpc.13.4.889. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Khan J., Bittner M. L., Saal L. H., Teichmann U., Azorsa D. O., Gooden G. C., Pavan W. J., Trent J. M., Meltzer P. S. cDNA microarrays detect activation of a myogenic transcription program by the PAX3-FKHR fusion oncogene. Proc Natl Acad Sci U S A. 1999 Nov 9;96(23):13264–13269. doi: 10.1073/pnas.96.23.13264. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Monni O., Barlund M., Mousses S., Kononen J., Sauter G., Heiskanen M., Paavola P., Avela K., Chen Y., Bittner M. L. Comprehensive copy number and gene expression profiling of the 17q23 amplicon in human breast cancer. Proc Natl Acad Sci U S A. 2001 May 1;98(10):5711–5716. doi: 10.1073/pnas.091582298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Mullineaux P., Ball L., Escobar C., Karpinska B., Creissen G., Karpinski S. Are diverse signalling pathways integrated in the regulation of arabidopsis antioxidant defence gene expression in response to excess excitation energy? Philos Trans R Soc Lond B Biol Sci. 2000 Oct 29;355(1402):1531–1540. doi: 10.1098/rstb.2000.0713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Perou C. M., Jeffrey S. S., van de Rijn M., Rees C. A., Eisen M. B., Ross D. T., Pergamenschikov A., Williams C. F., Zhu S. X., Lee J. C. Distinctive gene expression patterns in human mammary epithelial cells and breast cancers. Proc Natl Acad Sci U S A. 1999 Aug 3;96(16):9212–9217. doi: 10.1073/pnas.96.16.9212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Reymond P., Weber H., Damond M., Farmer E. E. Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell. 2000 May;12(5):707–720. doi: 10.1105/tpc.12.5.707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Rial D. V., Arakaki A. K., Ceccarelli E. A. Interaction of the targeting sequence of chloroplast precursors with Hsp70 molecular chaperones. Eur J Biochem. 2000 Oct;267(20):6239–6248. doi: 10.1046/j.1432-1327.2000.01707.x. [DOI] [PubMed] [Google Scholar]
  34. Ruan Y., Gilmore J., Conner T. Towards Arabidopsis genome analysis: monitoring expression profiles of 1400 genes using cDNA microarrays. Plant J. 1998 Sep;15(6):821–833. doi: 10.1046/j.1365-313x.1998.00254.x. [DOI] [PubMed] [Google Scholar]
  35. Schaffer R., Landgraf J., Pérez-Amador M., Wisman E. Monitoring genome-wide expression in plants. Curr Opin Biotechnol. 2000 Apr;11(2):162–167. doi: 10.1016/s0958-1669(00)00084-7. [DOI] [PubMed] [Google Scholar]
  36. Schnaider T., Oikarinen J., Ishiwatari-Hayasaka H., Yahara I., Csermely P. Interactions of Hsp90 with histones and related peptides. Life Sci. 1999;65(22):2417–2426. doi: 10.1016/s0024-3205(99)00508-1. [DOI] [PubMed] [Google Scholar]
  37. Seki M., Narusaka M., Abe H., Kasuga M., Yamaguchi-Shinozaki K., Carninci P., Hayashizaki Y., Shinozaki K. Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. Plant Cell. 2001 Jan;13(1):61–72. doi: 10.1105/tpc.13.1.61. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sherlock G. Analysis of large-scale gene expression data. Curr Opin Immunol. 2000 Apr;12(2):201–205. doi: 10.1016/s0952-7915(99)00074-6. [DOI] [PubMed] [Google Scholar]
  39. Shinozaki K., Yamaguchi-Shinozaki K. Gene Expression and Signal Transduction in Water-Stress Response. Plant Physiol. 1997 Oct;115(2):327–334. doi: 10.1104/pp.115.2.327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Shinozaki K., Yamaguchi-Shinozaki K. Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Curr Opin Plant Biol. 2000 Jun;3(3):217–223. [PubMed] [Google Scholar]
  41. Somerville C., Somerville S. Plant functional genomics. Science. 1999 Jul 16;285(5426):380–383. doi: 10.1126/science.285.5426.380. [DOI] [PubMed] [Google Scholar]
  42. Uno Y., Furihata T., Abe H., Yoshida R., Shinozaki K., Yamaguchi-Shinozaki K. Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci U S A. 2000 Oct 10;97(21):11632–11637. doi: 10.1073/pnas.190309197. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Wang A., Pierce A., Judson-Kremer K., Gaddis S., Aldaz C. M., Johnson D. G., MacLeod M. C. Rapid analysis of gene expression (RAGE) facilitates universal expression profiling. Nucleic Acids Res. 1999 Dec 1;27(23):4609–4618. doi: 10.1093/nar/27.23.4609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Wang R., Guegler K., LaBrie S. T., Crawford N. M. Genomic analysis of a nutrient response in Arabidopsis reveals diverse expression patterns and novel metabolic and potential regulatory genes induced by nitrate. Plant Cell. 2000 Aug;12(8):1491–1509. doi: 10.1105/tpc.12.8.1491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. White J. A., Todd J., Newman T., Focks N., Girke T., de Ilárduya O. M., Jaworski J. G., Ohlrogge J. B., Benning C. A new set of Arabidopsis expressed sequence tags from developing seeds. The metabolic pathway from carbohydrates to seed oil. Plant Physiol. 2000 Dec;124(4):1582–1594. doi: 10.1104/pp.124.4.1582. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Wu Y., Cosgrove D. J. Adaptation of roots to low water potentials by changes in cell wall extensibility and cell wall proteins. J Exp Bot. 2000 Sep;51(350):1543–1553. doi: 10.1093/jexbot/51.350.1543. [DOI] [PubMed] [Google Scholar]
  47. Yang G. P., Ross D. T., Kuang W. W., Brown P. O., Weigel R. J. Combining SSH and cDNA microarrays for rapid identification of differentially expressed genes. Nucleic Acids Res. 1999 Mar 15;27(6):1517–1523. doi: 10.1093/nar/27.6.1517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Zhu B., Choi D. W., Fenton R., Close T. J. Expression of the barley dehydrin multigene family and the development of freezing tolerance. Mol Gen Genet. 2000 Sep;264(1-2):145–153. doi: 10.1007/s004380000299. [DOI] [PubMed] [Google Scholar]

Articles from Comparative and Functional Genomics are provided here courtesy of Wiley

RESOURCES