Abstract
Thlaspi arvense, a wild species from the Brassicaceae family, was shown to have a higher level of freezing tolerance than either of its close relatives, the model plant Arabidopsis thaliana or the crop Brassica napus (canola). Over 600 clones were sequenced from a subtractive cDNA library generated from cold treated T. arvense tissue, establishing that T. arvense shared significant sequence identity with both A. thaliana and B. napus (90–92%). In light of the strong sequence similarity between T. arvense and A. thaliana and to exploit the available genomics resources for Arabidopsis, the efficacy of using long 70 mer oligonucleotide whole genome Arabidopsis microarrays was tested for T. arvense. Gene expression in T. arvense leaf tissue during the very early stages of cold acclimation (or cold stress) was assayed at three time points and compared to an untreated control. This analysis highlights some of the difficulties and benefits of using cross-species microarray analysis. The data suggested that T. arvense responds in a similar fashion to cold stress as the model plant A. thaliana. However, for a number of genes quantitative differences in the level and timing of expression were identified. One of the most notable differences suggested that sulphur assimilation leading to the increased production of the methyl donor S-adenosyl-methionine was playing a role in the response of T. arvense to cold stress.
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References
Bacher M, Talke IN, Krall L, Kramer U (2004) Cross species microarray transcript profiling reveals high constitutive expression of metal homeostasis genes in shoots of the zinc hyperaccumulator Arabidopsis halleri. Plant J 37:251–268
Best KF, McIntyre GI (1975) The biology of Canadian weeds, 9. Thlapsi arvense L. Can J Plant Sci 55:279–292
Boyer JS (1982) Plant productivity and environment. Science 281:443–448
Chen W, Provart NJ, Glazebrook J, Katagiri F, Chang HS, Eulgem T, Mauch F, Luan S, Zou G, Whitham SA, Budworth PR, Tao Y, Xie Z, Chen X, Lam S, Kreps JA, Harper JF, Si-Ammour A, Mauch-Mani B, Heinlein M, Kobayashi K, Hohn T, Dangl JL, Wang X, Zhu T (2002) Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. Plant Cell 14:559–574
Chinnusamy V, Schumaker K, Zhu JK (2004) Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. J Exp Bot 55:225–236
Chou C-C, Chen C-H, Lee T-T, Peck K (2004) Optimisation of probe length and the number of probes per gene for optimal microarray analysis of gene expression. Nucl Acids Res 32:e99
Fowler S, Thomashow MF (2002) Arabidopsis transcriptome profiling indicates that multiple regulatory pathways are activated during cold acclimation in addition to the CBF cold response pathway. Plant Cell 14:1675–1690
Galloway GL, Malmberg RL, Price RA (1998) Phylogenetic utility of the nuclear gene arginine decarboxylase: an example from Brassicaceae. Mol Biol Evol 15:1312–1320
Gilmour SJ, Hajela RK, Thomashow MF (1998) Cold acclimation of Arabidopsis thaliana. Plant Physiol 879:745–750
Gong Q, Li P, Ma S, Indu Rupassara S, Bohnert HJ (2005) Salinity stress adaptation competence in the extremophile Thellungiella halophila in comparison with its relative Arabidopsis thaliana. Plant J 44:826–839
Griffith M, McIntyre HCH (1993) The interrelationship between growth and frost tolerance in winter rye. Physiol Plant 87:335–344
Guy CL (1990) Cold acclimation and freezing tolerance: role of protein metabolism. Ann Rev Plant Physiol Mol Biol 41:187–223
Havaux M, Eymery F, Porfirova S, Rey P, Dormann P (2005) Vitamin E protects against photoinhibition and photooxidative stress in Arabidopsis thaliana. Plant Cell 17:3451–3469
Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106
Jang JY, Kim DG, Kim YO, Kim JS, Kang H (2004) An expression analysis of a gene family encoding plasma membrane aquaporins in response to abiotic stresses in Arabidopsis thaliana. Plant Mol Biol 54:713–725
Kane MD, Jatkoe TA, Stumpf CR, Lu J, Thomas JD, Madore SJ (2000) Assessment of the sensitivity and specificity of oligonucleotide (50mer) microarrays. Nucl Acids Res 28:4552–4557
Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291
Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (2004) Overexpression of spermidine synthase enhances tolerance to multiple environmental stresses and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol 45:712–722
Kocsy G, Szalai G, Vágújfalvi A, Stéhli L, Orosz G, Galiba G (2000) Genetic study of glutathione accumulation during cold hardening in wheat. Planta 210:295–301
Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 230:2129–2141
Laroche A, Geng X-M, Singh J (1992) Differentiation of freezing tolerance and vernalization responses in Cruciferae exposed to low temperatures. Plant Cell Environ 15:439–445
Larsson O, Wahlestedt C, Timmons JA (2005) Considerations when using the significance analysis of microarrays (SAM) algorithm. BMC Bioinformatics 6:129
Lee H-S, Wang J, Tian L, Jiang H, Black MA, Madlung A, Watson B, Lukens L, Pires JC, Wang JJ, Comai L, Osborn TC, Doerge RW, Chen ZJ (2004) Sensitivity of oligonucleotides and cDNAs for microarray analysis of gene expression in Arabidopsis and its related species. Plant Biotech J 2:55–57
Lee BH, Henderson DA, Zhu JK (2005) The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 17:3155–3175
Levitt J (1980) Response of plants to environmental stresses, 2nd edn. Academic Press, New York
Mo H, Pua EC (2002) Up-regulation of arginine decarboxylase gene expression and accumulation of polyamines in mustard (Brassica juncea) in response to stress. Physiol Plant 114:439–449
Nadeau P, Delaney S, Chouinard L (1987) Effects of cold hardening on the regulation of polyamine levels in wheat (Triticum aestivum L.) and Alfalfa (Medicago sativa L.). Plant Physiol 84:73–77
Parkin IAP, Gulden SM, Sharpe AG, Lukens L, Trick M, Osborn TC, Lydiate DJ (2005) Segmental structure of the Brassica napus genome based on comparative analysis with Arabidopsis thaliana. Genetics 171:765–781
Ravanel S, Gakiere B, Job D, Douce R (1998) The specific features of methionine biosynthesis and metabolism in plants. Proc Natl Acad Sci USA 95:7805–7812
Sánchez-Aguayo I, Rodríguez-Galán JM, García R, Torreblanca J, Pardo JM (2004) Salt stress enhances xylem development and expression of S-adenosyl-L-methionine synthase in lignifying tissues of tomato plants. Planta 220:278–285
Taji T, Seki M, Satou M, Sakurai T, Kobayashi M, Ishiyama K, Narusaka Y, Narusaka M, Zhu JK, Shinozaki K (2004) Comparative genomics in salt tolerance between Arabidopsis and Arabidopsis-related halophyte salt cress using Arabidopsis microarray. Plant Physiol 135:1697–1709
Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Ann Rev Plant Physiol Plant Mol Biol 50:571–599
Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98:5116–5121
Van Buskirk HA, Thomashow MF (2006) Arabidopsis transcription factors regulating cold acclimation. Physiol Plant 126:72–80
Vogel JT, Zarka DG, Van Buskirk HA, Fowler SG, Thomashow MF (2005) Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. Plant J 41:195–211
Wang HY, Malek RL, Kwitek AE, Greene AS, Luu TV, Behbahani B, Frank B, Quackenbush J, Lee NH (2003) Assessing unmodified 70-mer oligonucleotide performance on glass-slide microarrays. Genome Biol 4(1):R5
Webb MS, Uemura M, Steponkus PL (1994) A comparison of freezing injury in oat and rye: two cereals at the extremes of freezing tolerance. Plant Physiol 104:467–478
Wong CE, Li Y, Whitty BR, Diaz-Camino C, Akhter SR, Brandle JE, Golding GB, Weretilnyk EA, Moffatt BA, Griffith M (2005) Expressed sequence tags from the Yukon ecotype of Thellungiella reveal that gene expression in response to cold, drought and salinity shows little overlap. Plant Mol Biol 58:561–574
Woo HR, Goh CH, Park JH, Teyssendier de la Serve B, Kim JH, Park YI, Nam HG (2002) Extended leaf longevity in the ore4-1 mutant of Arabidopsis with a reduced expression of a plastid ribosomal protein gene. Plant J 31:331–340
Xin Z, Browse J (2000) Cold comfort farm: the acclimation of plants to freezing temperatures. Plant Cell Environ 23:893–902
Yamada K, Lim J, Dale JM, Chen H, Shinn P, Palm CJ, Southwick AM, Wu HC, Kim C, Nguyen M et al (2003) Empirical analysis of transcriptional activity in the Arabidopsis genome. Science 302:842–846
Zhou XJ, Gibson G (2004) Cross-species comparison of genome-wide expression patterns. Genome Biol 5:232
Acknowledgements
The authors would like to thank Drs Steve Robinson and Dwayne Hegedus for critical reading of this manuscript and Drs Branimir Gjetvaj and Andrew Sharpe for assistance with EST development. This work was funded in part by the Saskatchewan Agricultural Development Fund and in part by the Genome Prairie project ‘Functional Genomics of Abiotic Stress’.
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Sharma, N., Cram, D., Huebert, T. et al. Exploiting the wild crucifer Thlaspi arvense to identify conserved and novel genes expressed during a plant’s response to cold stress. Plant Mol Biol 63, 171–184 (2007). https://doi.org/10.1007/s11103-006-9080-4
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DOI: https://doi.org/10.1007/s11103-006-9080-4