The genetics and genomics of the drought response in Populus

Plant Journal

Volumn 48, Issue 3, 2006, Pages 321-341

  Street, Nathaniel Robert ^a   Skogström, Oskar ^b   Sjödin, Andreas ^b   Tucker, James ^a   Rodríguez Acosta, Maricela ^a   Nilsson, Peter ^c   Jansson, Stefan ^b   Taylor, Gail ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b UMEÅ UNIVERSITY   (Sweden)

^c ALBANOVA UNIVERSITY CENTER   (Sweden)

Author keywords

Drought; Microarray; Poplar; QTL; Transcriptome

Indexed keywords

GENE EXPRESSION; MICROARRAYS; QUANTITATIVE TRAIT LOCI (QTL); TRANSCRIPTOME;

BIODIVERSITY; DROUGHT; GENES; GENETIC ENGINEERING;

FORESTRY;

MESSENGER RNA;

ARTICLE; ASPEN; DISASTER; EXPRESSED SEQUENCE TAG; GENETICS; GENOME; PLANT GENOME; QUANTITATIVE TRAIT LOCUS; SPECIES DIFFERENCE;

DISASTERS; EXPRESSED SEQUENCE TAGS; GENOME, PLANT; NATURAL DISASTERS; POPULUS; QUANTITATIVE TRAIT LOCI; RNA, MESSENGER; SPECIES SPECIFICITY;

ABSCISSION; BIODIVERSITY; DROUGHT; GENES; GENETIC ENGINEERING; POPULUS; POPULUS TRICHOCARPA;

POPULUS; POPULUS DELTOIDES; POPULUS TRICHOCARPA;

EID: 33750022915     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2006.02864.x     Document Type: Article

References (76)

1. Achard, P., Cheng, H., De Grauwe, L., Decat, J., Schoutteten, H., Moritz, T., Van Der Staeten, D., Peng, J. and Harberd, N.P. (2006) Integration of plant responses to environmentally activated phytohormones signals. Science, 311, 91-94.
2. Aharoni A., Dixit S., Jetter R., Thoenes E., van Arkel G. and Pereira A. (2004) The SHINE Clade of AP2 Domain Transcription Factors Activates Wax Biosynthesis, Alters Cuticle Properties, and Confers Drought Tolerance when Overexpressed in Arabidopsis. Plant Cell 16, 2463-2480.
3. Amlin, N.M. and Rood, S.B. (2003) Drought stress and recovery of riparian cottonwoods due to water table alteration along Willow Creek, Alberta. Trees Struct. Funct. 17, 351-358.
4. Andersson, A., Keskitalo, J., Sjödin, A. et al. (2004) A transcriptional timetable of autumn senescence. Genome Biol. 5, R24.
5. Baxter, C.J., Sabar, M., Quick, W.P. and Sweetlove, L.J. (2005) Comparison of changes in fruit gene expression in tomato introgression lines provides evidence of genome-wide transcriptional changes and reveals links to mapped QTLs and described traits. J. Exp. Bot. 56, 1591-1604.
6. Bhalerao, R., Keskitalo, J., Sterky, F. et al. (2003) Gene expression in autumn leaves. Plant Physiol. 131, 430-442.
7. Borevitz J.O., Liang D., Plouffe D., Chang H-S., Zhu T., Weigel D., Berry C.C., Winzeler E. and Chory J. (2003) Large-Scale Identification of Single-Feature Polymorphisms in Complex Genomes. Genome Res. 13, 513-523.
8. Borevitz J.O., Maloof J.N., Lutes J., Dabi T., Redfern J.L., Trainer G.T., Werner J.D., Asami T., Berry C.C., Weigel D. and Chory J. (2002) Quantitative Trait Loci Controlling Light and Hormone Response in Two Accessions of Arabidopsis thaliana. Genetics 160, 683-696.
9. Boyer, J.S. (1982) Plant productivity and environment. Science, 218, 443-448.
10. Bradshaw, H.D. and Stettler, R.F. (1993) Molecular-genetics of growth and development in Populus. 1. Triploidy in hybrid poplars. Theor. Appl. Genet. 86, 301-307.
11. Bradshaw, H.D., Ceulemans, R., Davis, J. and Stettler, R. (2000) Emerging model systems in plant biology: poplar (Populus) as a model forest tree. J. Plant Growth Regul. 19, 306-313.
12. Bray, E.A. (2004) Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. J. Exp. Bot. 55, 2331-2341.
13. Bray, E.A., Bailey-Serres, J. and Weretilnyk, E. (2000) Responses to abiotic stress. In Responses to Abiotic Stress (Gruissen, W., Buchanan, B. and Jones, R., eds). Rockville, MD: American Society of Plant Physiologists, pp. 1158-1249.
14. Brunner, A.M., Busov, V.B. and Strauss, S.H. (2004) Poplar genome sequence: functional genomics in an ecologically dominant plant species. Trends Plant Sci. 9, 49-56.
15. Buchanan-Wollaston V., Earl S., Harrison E., Mathas E., Navabpour S., Page T. and Pink D. (2003) The molecular analysis of leaf senescence - a genomics approach. Plant Biotechnology Journal 1, 3-22.
16. Buchanan-Wollaston, V., Page, T., Harrison, E. et al. (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J. 42, 567-585.
17. Chang, S., Puryear, J. and Cairney, J. (1993) A simple and efficient method for isolating RNA from pine trees. Plant Mol. Biol. Rep. 11, 113-116.
18. Churchill G.A. and Doerge R.W. (1994) Empirical Threshold Values for Quantitative Triat Mapping. Genetics 138, 963-971.
19. Cochard H., Ridolfi M. and Dreyer E. (1996) Responses to Water Stress in an ABA-Unresponsive Hybrid Poplar (Populus koreana x trichocarpa cv. Peace). II. Hydraulic Properties and Xylem Embolism. New Phytologist 134, 455-461.
20. Cui X. and Churchill G. (2003) Statistical tests for differential expression in cDNA microarray experiments. Genome Biology 4, 210.
21. Doyle, J.J. and Doyle, J.L. (1987) DNA isolation from leaves. Phytochem. Bull. 19, 11-15.
22. Dudley A.M., Aach J., Steffen M.A. and Church G.M. (2002) Measuring absolute expression with microarrays with a calibrated reference sample and an extended signal intensity range. Proc Natl Acad Sci U S A 99, 7554-7559.
23. Erickson, R.O. and Michelini, F.J. (1957) The plastochron index. Am. J. Bot. 44, 297-305.
24. Ewing, R.M., Kahla, A.B., Poirot, O., Lopez, F., Audic, S. and Claverie, J.M. (1999) Large-scale statistical analyses of rice ESTs reveal correlated patterns of gene expression. Genome Res. 9, 950-959.
25. Fleming, A.J. (2005) The control of leaf development. New Phytol. 166, 9-20.
26. Flexas J. and Medrano H. (2002) Drought-inhibition of photosynthesis in C-3 plants: Stomatal and non-stomatal limitations revisited. Annals of Botany 89, 183-189.
27. Gebre, G.M. and Kuhns, M.R. (1993) Effects of water-stress preconditioning on gas-exchange and water relations of Populus deltoides clones. Can. J. Forest Res. 23, 1291-1297.
28. Gebre, G.M., Tschaplinski, T.J., Tuskan, G.A. and Todd, D.E. (1998) Clonal and seasonal differences in leaf osmotic potential and organic solutes of five hybrid poplar clones grown under field conditions. Tree Physiol. 18, 645-652.
29. Gentleman, R., Carey, V., Bates, D. et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80.
30. Graham, L.E., Graham, J.M. and Wilcox, L.W. (2002) Plant Biology. New Jersey, USA: Prentice Hall.
31. Harvey, H.P. and Van Den Driessche, R. (1997) Nutrition, xylem cavitation and drought resistance in hybrid poplar. Tree Physiol. 17, 647-654.
32. Hazen, S.P., Hawley, R.M., Davis, G.L., Henrissat, B. and Walton, J.D. (2003) Quantitative trait loci and comparative genomics of cereal cell wall composition. Plant Physiol. 132, 263-271.
33. Hazen S.P. and Kay S.A. (2003) Gene arrays are not just for measuring gene expression. Trends in Plant Science 8, 413-416.
34. Hazen, S., Pathan, M., Sanchez, A., Baxter, I., Dunn, M., Estes, B., Chang, H., Zhu, T., Kreps, J. and Nguyen, H. (2004) Expression profiling of rice segregating for drought tolerance QTLs using a rice genome array. Funct. Integr. Genomics, 5, 104-116.
35. Hukin D., Cochard H., Dreyer E., Thiec D.L. and Bogeat-Triboulot M.B. (2005) Cavitation vulnerability in roots and shoots: does Populus euphratica Oliv., a poplar from arid areas of Central Asia, differ from other poplar species? Journal of Experimental Botany 418, 2003-2010.
36. IPCC (2001) Climate Change 2001: the Scientific Basis. Summary for Policymakers and Technical Summary. Cambridge, UK: Cambridge University Press.
37. Jansen, R.C. and Nap, J.P. (2001) Genetical genomics: the added value from segregation. Trends Genet. 17, 388-391.
38. Karp, C.L., Grupe, A., Schadt, E. et al. (2000) Identification of complement factor 5 as a susceptibility locus for experimental allergic asthma. Nat. Immunol. 1, 221-226.
39. Kendziorski, C.M., Zhang, Y., Lan, H. and Attie, A.D. (2003) The efficiency of pooling mRNA in microarray experiments. Biostatistics, 4, 465-477.
40. Kendziorski, C., Irizarry, R.A., Chen, K.S., Haag, J.D. and Gould, M.N. (2005) On the utility of pooling biological samples in microarray experiments. Proc. Natl Acad. Sci. USA, 102, 4252-4257.
41. Kirst M., Basten C.J., Myburg A.A., Zeng Z-B. and Sederoff R.R. (2005) Genetic Architecture of Transcript-Level Variation in Differentiating Xylem of a Eucalyptus Hybrid. Genetics 169, 2295-2303.
42. Kirst, M., Myburg, A.A., De Leon, J.P.G., Kirst, M.E., Scott, J. and Sederoff, R. (2004) Coordinated genetic regulation of growth and lignin revealed by quantitative trait locus analysis of cDNA microarray data in an interspecific backcross of eucalyptus. Plant Physiol. 135, 2368-2378.
43. Kreps, J.A., Wu, Y., Chang, H.-S., Zhu, T., Wang, X. and Harper, J.F. (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol. 130, 2129-2141.
44. Larson, P.R. and Isebrands, J.G. (1971) The plastochron index as applied to developmental studies of cottonwood. Can. J. Forest Res. 1, 1-11.
45. Lim, P.O., Woo, H.R. and Nam, H.G. (2003) Molecular genetics of leaf senescence in Arabidopsis. Trends Plant Sci. 8, 272-278.
46. Lindroth, A. and Båth, A. (1999) Assessment of regional willow coppice yield in Sweden on basis of water availability. For. Ecol. Manage. 121, 57-65.
47. Marron, N., Delay, D., Petit, J.M., Dreyer, E., Kahlem, G., Delmotte, F.M. and Brignolas, F. (2002) Physiological traits of two Populus x euramericana clones, Luisa Avanzo and Dorskamp, during a water stress and re-watering cycle. Tree Physiol. 22, 849-858.
48. McShane, L.M., Shih, J.H. and Michalowska, A.M. (2003) Statistical issues in the design and analysis of gene expression microarray studies of animal models. J. Mammary Gland Biol. Neoplasia, 8, 359-374.
49. Mittler R., Vanderauwera S., Gollery M. and Van Breusegem F. (2004) Reactive oxygen gene network of plants. Trends in Plant Science 9, 490-498.
50. Moreau C., Aksenov N., Lorenzo M., Segerman B., Funk C., Nilsson P., Jansson S. and Tuominen H. (2005) A genomic approach to investigate developmental cell death in woody tissues of Populus trees. Genome Biology 6, R34.
51. Peng, X., Wood, C., Blalock, E., Chen, K., Landfield, P. and Stromberg, A. (2003) Statistical implications of pooling RNA samples for microarray experiments. BMC Bioinformatics, 4, 26.
52. Pinon, J. and Valadon, A. (1997) Behaviour towards major parasites of poplar cultivars registered in European Union. Ann. Sci. Forest, 54, 19-38.
53. Rae, A.M., Robinson, K.M., Street, N.R. and Taylor, G. (2004) Morphological and physiological traits influencing biomass productivity in short-rotation coppice poplar. Can. J. Forest Res. 34, 1488-1498.
54. Rao, M.V. and Davis, K.R. (1999) Ozone-induced cell death occurs via two distinct mechanisms in Arabidopsis: the role of salicylic acid. Plant J. 17, 603-614.
55. Reymond M., Muller B. and Tardieu F. (2004) Dealing with the genotypexenvironment interaction via a modelling approach: a comparison of QTLs of maize leaf length or width with QTLs of model parameters. J. Exp. Bot. 55, 2461-2472.
56. Ridolfi, M., Fauveau, M.L., Label, P., Garrec, J.P. and Dreyer, E. (1996) Water stress in an ABA-unresponsive hybrid poplar (Populus koveana x trichocarpa cv Peace) - response. New Phytol. 134, 445-454.
57. Robison, D.J. and Raffa, K.F. (1998) Productivity, drought tolerance and pest status of hybrid Populus: tree improvement and silvicultural implications. Biomass Bioenerg. 14, 1-20.
58. Rood, S.B., Patino, S., Coombs, K. and Tyree, M.T. (2000) Branch sacrifice: cavitation-associated drought adaptation of riparian cottonwoods. Trees Struct. Funct. 14, 248-257.
59. Seaton G., Haley C.S., Knott S.A., Kearsey M. and Visscher P.M. (2002) QTL Express: mapping quantitative trait loci in of simple and complex pedigrees. Bioinformatics 18, 339-340.
60. Seki, M., Narusaka, M., Ishida, J. et al. (2002) Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J. 31, 279-292.
61. Shih, J.H., Michalowska, A.M., Dobbin, K., Ye, Y., Qiu, T.H. and Green, J.E. (2004) Effects of pooling mRNA in microarray class comparisons. Bioinformatics, 20, 3318-3325.
62. Silva, C., Garcia-Mas, J., Sanchez, A.M., Arus, P. and Oliveira, M.M. (2005) Looking into flowering time in almond (Prunus dulcis (Mill) D.A. Webb): the candidate gene approach. Theor. Appl. Genet. 110, 959-968.
63. Sjödin, A., Bylesjö, M., Skogström, O., Eriksson, D., Nilsson, P., Rydén, P., Jansson, S. and Karlsson, J. (2006) UPSC-BASE - Populus transcriptome online. Plant J. in press.
64. Smyth, G.K. (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article 3.
65. Sterky, F., Bhalerao, R.R., Unneberg, P. et al. (2004) A Populus EST resource for plant functional genomics. Proc. Natl Acad. Sci. USA, 101, 13951-13956.
66. Tanaka, Y., Sano, T., Tamaoki, M., Nakajima, N., Kondo, N. and Hasezawa, S. (2005) Ethylene inhibits abscisic acid-induced stomatal closure in Arabidopsis. Plant Physiol. 138, 2237-2243.
67. Taylor, G. (2002) Populus: Arabidopsis for forestry. Do we need a model tree? Annu. Bot. 90, 681-689.
68. 2 enrichment (POPFACE) on leaf growth, cell expansion, and cell productionina closedcanopyofpoplar. Plant Physiol. 131, 177-185.
69. Tschaplinski, T.J., Tuskan, G.A., Gebre, G.M. and Todd, D.E. (1998) Drought resistance of two hybrid Populus clones grown in a large-scale plantation. Tree Physiol. 18, 653-658.
70. Tuskan, G.A. and Walsh, M.E. (2001) Short-rotation woody crop systems, atmospheric carbon dioxide and carbon management: a US case study. Forest Chron. 77, 259-264.
71. Vinciotti, V., Khanin, R., D'Alimonte, D. et al. (2005) An experimental evaluation of a loop versus a reference design for two-channel microarrays. Bioinformatics, 21, 492-501.
72. Wayne, M.L. and McIntyre, L.M. (2002) Combining mapping and arraying: an approach to candidate gene identification. Proc. Natl Acad. Sci. USA, 99, 14903-14906.
73. Weigel D. and Nordborg M. (2005) Natural Variation in Arabidopsis. How Do We Find the Causal Genes? Plant Physiol. 138, 567-568.
74. Wellburn, A.R. (1994) The spectral determination of chlorophyll-a and chlorophyll-b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J. Plant Physiol. 144, 307-313.
75. Wullschleger, S.D., Jansson, S. and Taylor, G. (2002) Genomics and forest biology: Populus emerges as the perennial favorite. Plant Cell, 14, 2651-2655.
76. Zhang, S.-D. and Gant, T.W. (2005) Effect of pooling samples on the efficiency of comparative studies using microarrays. Bioinformatics, 21, 4378-4383.