Biologia plantarum 2012, 56:64-70 | DOI: 10.1007/s10535-012-0017-2

Differential gene expression in response to cold stress in Lepidium apetalum during seedling emergence

H. X. Zhao1,2, Q. Li1, G. Li1,*, Y. Du2
1 College of Life Science and Technology, Xinjiang University, Urumqi, P.R. China
2 College of Life Science, Xinjiang Normal University, Urumqi, P.R. China

Germination of Lepidium apetalum Wild. seeds is invariably arrested by cold stress. cDNA-amplified fragment length polymorphism (AFLP) technique was used to isolate genes relevant to chilling stress (4 °C) during seedling emergence. 43 transcript-derived fragments (TDFs) were found to be up-regulated and 17 down-regulated during chilling stress. Eighteen TDF of up-regulated genes were cloned and sequenced. Some of these genes are involved in the stress response, some play important roles in energy and substrate metabolism, and some encode unknown proteins such as TDF119. Two sequences, designated TDF217 and TDF223, may correspond to novel genes. The expression profiles of 6 from 18 TDFs were analyzed by quantitative real-time PCR under chilling and abscisic acid (ABA) stress. It was demonstrated that all 6 genes were significantly induced by chilling and their expression was decreased when the temperature was shifted from 4 to 25 °C. The transcriptional levels of 5 TDFs were strongly enhanced also in response to exogenous ABA. Based on the characteristics of genes isolated from seedlings exposed to cold stress, we conclude that Lepidium adapts to cold stress by regulating many signal transduction pathways, including both ABA-dependent and ABA-independent signaling pathways.

Keywords: AFLP; chilling; quantitative real-time PCR
Subjects: AFLP; chilling; quantitative real-time PCR; gene expression; temperature - low; PCR; transcript-derived fragments
Species: Lepidium apetalum; Arabidopsis thaliana

Received: April 22, 2010; Accepted: January 6, 2011; Published: March 1, 2012Show citation

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Zhao, H.X., Li, Q., Li, G., & Du, Y. (2012). Differential gene expression in response to cold stress in Lepidium apetalum during seedling emergence. Biologia plantarum56(1), 64-70. doi: 10.1007/s10535-012-0017-2.
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References

  1. Agarwal, P.K., Jha, B.: Transcription factors in plants and ABA dependent and independent abiotic stress signaling. - Biol. Plant. 54: 201-212, 2010. Go to original source...
  2. Allen, D.J., Ort, D.R.: Impacts of chilling temperatures on photosynthesis in warm-climate plants. - Trends Plant Sci. 6: 36-42, 2001. Go to original source...
  3. Bachem, C.W., Van der Hoeven, R.S., De Bruijn, S.M., Vreugdenhil, D., Zabeau, M., Visser, R.G.: Visualization of differential gene expression using a novel method of RNA fingerprinting based on AFLP: analysis of gene expression during potato tuber development. - Plant J. 9: 745-753, 1996. Go to original source...
  4. Baird, S.D., Lewis, S.M., Turcotte, M., Holcik, M.: A search for structurally similar cellular internal ribosome entry sites. - Nucl. Acids Res. 35: 4664-4677, 2007. Go to original source...
  5. Bellefroid, E.J., Sahin, M., Poncelet, D.A., Riviere, M., Bourguignon, C., Martial, J.A., Morris, P.L., Pieler, T., Szpirer, C., Ward, D.C.: Kzf1 - a novel KRAB zinc finger protein encoding gene expressed during rat spermatogenesis. - Biochim biophys Acta. 1398: 321-329, 1998. Go to original source...
  6. Cheng, L.B., Huan, S.T., Sheng, Y.D., Hua, X.J., Shu, Q.Y., Song, S.Q., Jing, X.M.: GMCHI, cloned from soybean [Glycine max (L.) Meer.], enhances survival in transgenic Arabidopsis under abiotic stress. - Plant Cell Rep. 28: 145-153, 2009a. Go to original source...
  7. Cheng, L.B., Li, S.Y., He, G.Y.: Isolation and expression profile analysis of genes relevant to chilling stress curing seed imbibition in soybean [Glycine max (L.)Meer.]. - Agr. Sci. China 8: 521-528, 2009b. Go to original source...
  8. Chern, M.S., Eiben, H.G., Bustos M.M.: The developmentally regulated bZIP factor ROM1 modulates transcription from lectin and storage protein genes in bean embryos. - Plant J. 10: 135-148, 1996. Go to original source...
  9. Choo, H.J., Kim, B.W., Kwon, O.B., Lee, C.S., Choi, J.S., Ko, Y.G.: Secretion of adenylate kinase 1 is required for extracellular ATP synthesis in C2C12 myotubes. - Exp. mol. Med. 40: 220-228, 2008. Go to original source...
  10. Donson, J., Fang, Y., Espiritu-Santo, G., Xing, W., Salazar, A., Miyamoto, S., Armendarez, V., Volkmuth, W.: Comprehensive gene expression analysis by transcript profiling. - Plant mol. Biol. 48: 75-97, 2002. Go to original source...
  11. Dzeja, P.P., Terzic, A.: Phosphotransfer networks and cellular energetics. - J. exp. Biol. 206: 2039-2047, 2003. Go to original source...
  12. Fowler, S., Thomashow, M.F.: 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, 2002. Go to original source...
  13. Guo, J.R., Schnieder, F., Verreet, J.A.: Differences between the fingerprints generated from total RNA and poly-A RNA using a modified procedure of cDNA-AFLP and silver staining. - Biotechnol Lett. 28: 267-270, 2006. Go to original source...
  14. Guy, C.: Cold acclimation and freezing stress tolerance: role of protein metabolism. - Annu. Rev. Plant. Physiol Plant mol. Biol. 41: 187-223, 1990. Go to original source...
  15. Holmes, D.I., Wahab, N.A., Mason, R.M.: Cloning and characterization of ZNF236, a glucose-regulated Kruppellike zinc-finger gene mapping to human chromosome 18q22-q23. - Genomics 60: 105-109, 1999. Go to original source...
  16. Holmgren, A.: Hydrogen donor system for Escherichia coli ribonucleoside-diphosphate reductase dependent upon glutathione. - Proc. nat. Acad. Sci. USA 73: 2275-2279, 1976. Go to original source...
  17. Hughes, M.A., Dunn, M.A.: The molecular biology of plant acclimation to low temperature. - J. exp. Biol. 47: 291-305, 1996. Go to original source...
  18. Hurst, H.C.: Protein Profile. - Academic Press, London 1995.
  19. Hu, X.J., Zhang, Z.B., Xu, P., Fu, Z.Y., Hu, S.B. Song, W.Y.: Multifunctional genes: the ross-talk among the regulation networks of abiotic stress responses. - Biol. Plant. 54: 213-223, 2010. Go to original source...
  20. Ichimura, K., Mizoguchi, T., Yoshida, R.: Various abiotic stresses rapidly activate Arabidopsis MAP kinases ATM PK and ATM PK 6. - Plant J. 24: 655-665, 2000. Go to original source...
  21. Ismail, A.M., Hall, A.E.: Variation in traits associated with chilling tolerance during emergence in cowpea germplasm. - Field Crops Res. 77: 99-113, 2002. Go to original source...
  22. Jaglo-Ottosen, K.R., Gilmour, S.J., Zarka, D.G., Schabenberger, O., Thomashow, M.F.: Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. - Science 280: 104-106, 1998. Go to original source...
  23. Kasuga, M., Liu, Q., Miura, S., Yamaguchi-Shinozaki, K., Shinozaki, K.: Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. - Nat. Biotechnol. 17: 287-291, 1999. Go to original source...
  24. Kong, J., Cao, W.H., Zhang, J.S.: Transgenic analysis of a salt - inhibited OsZFP1 gene fromrice. - Acta bot. sin. 46: 573-577, 2004.
  25. Liu, P., Zhao, S., Meng, Q.W., Wei, Y.Y., Zou, Q.: Effects of cold hardening on photosynthetic performance and chilling induced photo inhibition in sweet pepper leaves. - Plant Physiol. mol. Biol. 28: 51-58, 2002.
  26. Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. - Methods 25: 402-408, 2001. Go to original source...
  27. Mallappa, C., Yadav, V., Negi, P., Chattopadhyay, S.: A basic leucine zipper transcription factor, G-box-binding factor 1, regulates blue light-mediated photomorphogenic growth in Arabidopsis. - J. biol. Chem. 281: 22190-22199, 2006. Go to original source...
  28. Maruyama, K., Sakuma, Y., Kasuga, M., Ito, Y., Seki, M., Goda, H., Shimada, Y., Yoshida, S., Shinozaki, K., Yamaguchi-Shinozaki, K.: Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. - Plant J. 38: 982-993, 2004. Go to original source...
  29. Nag, R., Maity, M.K., Dasgupta, M.: Dual DNA binding property of ABA insensitive 3 like factors targeted to promoters responsive to ABA and auxin. - Plant mol. Biol. 59: 821-838, 2005. Go to original source...
  30. Nuhse, T.S., Peck, S.C., Hirt, H., Boller, T.: Microbial elicitors induce activation and dual phosphorylation of the Arabidopsis thaliana MAPK 6. - J. biol. Chem. 275: 7521-7526, 2000. Go to original source...
  31. Petersen, M., Brodersen, P., Naested, H., Andreasson, E., Lindhart, U., Johansen, B., Nielsen, H.B., Lacy, M., Austin, M.J., Parker, J.E., Sharma, S.B., Klessig, D.F., Martienssen, R., Mattsson, O., Jensen, A.B., Mundy, J.: Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. - Cell 103: 1111-1120, 2000. Go to original source...
  32. Randak, C.O., Welsh, M.J.: Adenylate kinase activity in ABC transporters. - J. biol. Chem. 280: 34385-34388, 2005. Go to original source...
  33. 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 13: 61-72, 2001. Go to original source...
  34. Seki, M., Narusaka, M., Ishida, J., Nanjo, T., Fujita, M., Oono, Y., Kamiya, A., Nakajima, M., Enju, A., Sakurai, T., Satou, M., Akiyama, K., Taji, T., Yamaguchi-Shinozaki, K., Carninci, P., Kawai, J., Hayashizaki, Y., Shinozaki, K.: 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, 2002. Go to original source...
  35. Siridechadilok, B., Fraser, C.S., Hall, R.J., Doudna, J.A., Nogales, E.: Structural roles for human translation factor eIF3 in initiation of protein synthesis. - Science 310: 1513-1515, 2005. Go to original source...
  36. Stanojevic, V., Habener, J.F., Holz, G.G., Leech, C.A.: Cytosolic adenylate kinases regulate K-ATP channel activity in human beta-cells. - Biochem. biophys. Res. Commun. 368: 614-619, 2008. Go to original source...
  37. Strauss, A.J., Kruger, G.H.J., Strasser, R.J., Van Heerden, P.D.R.: Ranking of dark chilling tolerance in soybean genotypes probed by the chlorophyll a fluorescence transient O-J-I-P. - Environ. exp. Bot. 56: 147-157, 2006. Go to original source...
  38. Thieringer, H.A., Jones, P.G., Inouye, M.: Cold shock and adaptation. - Bioessays 20: 49-57, 1998. Go to original source...
  39. Thomashow, M.F.: Role of cold-responsive genes in plant freezing tolerance. - Plant Physiol. 118: 1-8, 1998. Go to original source...
  40. Thomashow, M.F.: Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. - Annu. Rev. Plant Physiol. Plant mol. Biol. 50: 571-599, 1999. Go to original source...
  41. Thurow, C., Schiermeyer, A., Krawczyk, S., Butterbrodt, T., Nickolov, K., Gatz, C.: Tobacco bZIP transcription factor TGA2.2 and related factor TGA2.1 have distinct roles in plant defense responses and plant development. - Plant J. 44: 100-113, 2005. Go to original source...
  42. Trachsel, H., Staehelin, T.: Initiation of mammalian protein synthesis. The multiple functions of the initiation factor eIF-3. - Biochim. biophys. Acta 565: 305-314, 1979. Go to original source...
  43. Van Heerden, P.D., Tsimilli, M.M., Kruger, G.H., Strasser, R.J.: Dark chilling effects on soybean genotypes during vegetative development: parallel studies of CO2 assimilation, chlorophyll a fluorescence kinetics O-J-I-P and nitrogen fixation. - Physiol Plant. 117: 476-491, 2003. Go to original source...
  44. Viswanathan, C., Zhu, J.K.: Molecular genetic analysis of coldregulated gene transcription. - Phil. Trans. roy. Soc. London B Biol. Sci. 357: 877-886, 2002. Go to original source...
  45. Vogel, J.T., Zarka, D.G., Van Buskirk, H.A., Fowler, S.G., Thomashow, M.F.: Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. - Plant J. 41: 195-211, 2005. Go to original source...
  46. Vos, P., Hogers, R., Bleeker, M., Reijans, M., Van de Lee, T., Hornes, M., Frijters, A., Pot, J., Peleman, J., Kuiper, M..: AFLP: a new technique for DNA fingerprinting. - Nucl. Acids Res. 23: 4407-4414, 1995. Go to original source...
  47. Vuylsteke, M., Daele, H., Vercauteren, A., Zabeau, M., Kuiper, M.: Genetic dissection of transcriptional regulation by cDNA-AFLP. - Plant J. 45: 439-446, 2006. Go to original source...
  48. Walker, D.J., Romero, P., Correal, E.: Cold tolerance, water relations and accumulation of osmolytes in Bituminaria bituminosa. - Biol. Plant. 54: 293-298, 2010. Go to original source...
  49. Winicov, I.I., Bastola, D.R.: Transgenic overexpression of the transcription factor alfin1 enhances expression of the endogenous MsPRP2 gene in alfalfa and improves salinity tolerance of the plants. - Plant Physiol. 120: 473-480, 1999. Go to original source...
  50. Yamaguchi-Shinozaki, K., Shinozaki, K.: Organization of cisacting regulatory elements in osmotic- and cold-stressresponsive promoters. - Trends Plant Sci. 10: 88-94, 2005. Go to original source...
  51. Xiao, P.G.: Modern Chinese Materia Medica. Vol. 2. - Chemical Industry Press, Beijing 2002.
  52. Yu, S.W., Tang, K.X.: MAP kinase cascades responding to environmental stress in plants. - Acta bot. sin. 46: 127-136, 2004.
  53. Zhang, X.Y., Liang, C., Wang, G. P., Luo, Y., Wang, W.: The protection of wheat plasma membrane under cold stress by glycine betaine overproduction. - Biol. Plant. 54: 83-88, 2010. Go to original source...
  54. Zhao, H.X., Li, Q., Zhou, J., Li, G.: The characteristics of low temperature tolerance during seed germination of the ephemeral plant lepidium. - Acta bot. yunnanica 32: 448-454, 2010.
  55. Zhou, M., Sandercock, A.M., Fraser, C.S., Ridlova, G., Stephens, E., Schenauer, M.R., Yokoi-Fong, T., Barsky, D., Leary, J.A., Hershe, J.W.: Mass spectrometry special feature: mass spectrometry reveals modularity and a complete subunit interaction map of the eukaryotic translation factor eIF3. - PNAS 105: 18139-18144, 2008. Go to original source...
  56. Zhou, T.Y., Guo, R.L.: Flora of China. - Beijing Science and Technology Press, Beijing 1987.