Identification of leaf proteins differentially accumulated during cold acclimation between Festuca pratensis plants with distinct levels of frost tolerance

Journal of Experimental Botany

Volumn 60, Issue 12, 2009, Pages 3595-3609

  Kosmala, Arkadiusz ^a   Bocian, Aleksandra ^a   Rapacz, Marcin ^b   Jurczyk, Barbara ^b   Zwierzykowski, Zbigniew ^a  

^a INSTITUTE OF PLANT GENETICS   (Poland)

^b UNIVERSITY OF AGRICULTURE IN KRAKOW   (Poland)

Author keywords

2 D electrophoresis; Cold acclimation; Expression profiles; Festuca pratensis; Frost tolerance; Grasses; Low temperature stress; Mass spectrometry; Protein abundance; Proteome

Indexed keywords

VEGETABLE PROTEIN;

ARTICLE; CHEMISTRY; COLD; COMPARATIVE STUDY; FESCUE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PLANT LEAF; TWO DIMENSIONAL GEL ELECTROPHORESIS;

COLD TEMPERATURE; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FESTUCA; GENE EXPRESSION REGULATION, PLANT; PLANT LEAVES; PLANT PROTEINS;

FESTUCA; FESTUCA PRATENSIS; LOLIUM; POACEAE;

EID: 68949149921     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erp205     Document Type: Article

References (78)

1. Aebersold R, Mann M. 2003. Mass spectrometry-based proteomics. Nature 422, 198-207.
2. Amme S, Matros A, Schlesier B, Mock HP. 2006. Proteome analysis of cold stress response in Arabidopsis thaliana using DIGE-technology. Journal of Experimental Botany 57, 1537-1546.
3. Bae MS, Cho EJ, Choi EY, Park OK. 2003. Analysis of the Arabidopsis nuclear proteome and its response to cold stress. The Plant Journal 36, 652-663.
4. Baldi P, Valé G, Mazzucotelli E, Govoni C, Faccioli P, Stanca M, Cattivelli L. 2001. The transcripts of several components of the protein synthesis machinery are cold-regulated in a chloroplast-dependent manner in barley and wheat. Journal of Plant Physiology 158, 1541-1546.
5. Canovas FM, Dumas-Gaudot E, Recorbet G, Jorrin J, Mock HP, Rossignol M. 2004. Plant proteome analysis. Proteomics 4, 285-298.
6. Cui S, Huang F, Wang J, Xiao M, Cheng Y, Liu J. 2005. A proteomic analysis of cold stress responses in rice seedlings. Proteomics 5, 3162-3172.
7. Dal Bosco C, Busconi M, Govoni C, Baldi P, Stanca AM, Crosatti C, Bassi R, Cattivelli L. 2003. Cor gene expression in barley mutants affected in chloroplast development and photosyn-thetic electron transport. Journal of Plant Physiology 131, 793-802.
8. Ellis RJ. 1981. Chloroplast proteins: synthesis, transport, and assembly. Annual Review of Plant Physiology 32, 111-137.
9. Ensminger I, Busch F, Huner NPA. 2006. Photostasis and cold acclimation: sensing low temperature through photosynthesis. Physiologia Plantarum 126, 28-44.
10. 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. The Plant Cell 14, 1675-1690.
11. Gelhaye E, Rouhier N, Navrot N, Jacquot JP. 2005. The plant thioredoxin system. Cellular and Molecular Life Sciences 62, 24-35.
12. Gilmour SJ, Sebolt AM, Salazar MP, Everard JD, Thomashow MF. 2000. Overexpression of the Arabidopsis CBF3 transcriptional activator mimics multiple biochemical changes associated with cold acclimation. Plant Physiology 124, 1854-1865.
13. Goulas E, Schubert M, Kieselbach T, Kleczkowski LA, Gardeström P, Schröder W, Hurry V. 2006. The chloroplast lumen and stromal proteomes of Arabidopsis thaliana show differential sensitivity to short- and long-term exposure to low temperature. The Plant Journal 47, 720-734.
14. Gray GR, Chauvin LP, Sarhan F, Huner NPA. 1997. Cold acclimation and freezing tolerance. A complex interaction of light and temperature. Plant Physiology 114, 467-474.
15. Green BR, Durnford DG. 1996. The chlorophyll-carotenoid proteins of oxygenic photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 47, 685-714.
16. Griffith M, Lumb C, Wiseman SB, Wisniewski M, Johnson RW, Marangoni AG. 2005. Antifreeze proteins modify the freezing process in planta. Plant Physiology 138, 330-340.
17. Hannah MA, Heyer AG, Hincha DK. 2005. A global survey of gene regulation during cold acclimation in Arabidopsis thaliana. PLoS Genetics 1, e26.
18. Hashimoto M, Komatsu S. 2007. Proteomics analysis of rice seedlings during cold stress. Proteomics 7, 1293-1302.
19. Hisano H, Kanazawa A, Yoshida M, Humphreys MO, lizuka M, Kitamura K, Yamada T. 2008. Coordinated expression of functionally diverse fructosyltransferase genes is associated with fructan accumulation in response to low temperature in perennial ryegrass. New Phytologist 178, 766-780.
20. Hochstrasser DF, Harrrington MG, Hochstrasser AC, Miller MJ, Meril CR. 1988. Methods for increasing the resolution of two-dimensional protein electrophoresis. Analytical Biochemistry 73, 424-435.
21. Humphreys MO. 1989. Assessment of perennial ryegrass (Lolium perenne L.) for breeding. II. Components of winter hardiness. Euphytica 41, 99-106.
22. Humphreys MW, Gasior D, Leśniewska-Bocianowska A, Zwierzykowski Z, Rapacz M. 2007. Androgenesis as a means of dissecting complex genetic and physiological controls: selecting useful gene combinations for breeding freezing tolerant grasses. Euphytica 158, 337-345.
23. Huner NPA, öquist G, Hurry VM, Krol M, Falk S, Griffith M. 1993. Photosynthesis, photoinhibition and low temperature acclimation in cold tolerant plants. Photosynthetic Research 37, 19-39.
24. Hurkman WJ, Tanaka CK. 1986. Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. Plant Physiology 81, 802-806.
25. Imin N, Kerim T, Rolfe BG, Weinman JJ. 2004. Efect of early cold stress on the maturation of rice anthers. Proteomics 4, 1873-1882.
26. Issakidis-Bourguet E, Mouaheb N, Meyer Y, Miginiac-Maslow M. 2001. Heterologous complementation of yeast reveals a new putative function for chloroplast m-type thioredoxin. The Plant Journal 25, 127-135.
27. Kawamura Y, Uemura M. 2003. Mass spectrometric approach for identifying putative plasma membrane proteins of Arabidopsis leaves associated with cold acclimation. The Plant Journal 36, 141-154.
28. Kosmala A, Zwierzykowski Z, Gasior D, Rapacz M, Zwierzykowska E, Humphreys MW. 2006. GISH/FISH mapping of genes for freezing tolerance transferred from Festuca pratensis to Lolium multiflorum. Heredity 96, 243-251.
29. Kosmala A, Zwierzykowski Z, Zwierzykowska E, Luczak M, Rapacz M, Gasior D, Humphreys M. 2007. Introgression mapping of genes for winter hardiness and frost tolerance transferred from Festuca arundinacea into Lolium multiflorum. Journal of Heredity 98, 311-316.
30. Kreps JA, Wu Y, Chang HS, Zhu T, Wang X, Harper JF. 2002. Transcriptome changes tor Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiology 130, 2129-2141.
31. Larsen A. 1978. Freezing tolerance in grasses. Methods for testing in controlled environments. Scientific Reports of the Agricultural University of Norway, Department of Farm Crops Report 57, 2-54.
32. Lee BH, Henderson DA, Zhu JK. 2005. The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. The Plant Cell 17, 3155-3175.
33. Lee DG, Ahsan N, Lee SH, Kang KY, Lee JJ, Lee BH. 2007. An approach to identify cold-induced low-abundant proteins in rice leaf. Comptes Rendus Biologies 330, 215-225.
34. Lee DG, Ahsan N, Lee SH, Lee JJ, Bahk JD, Kang KY, Lee BH. 2008. Chilling stress-induced proteomic changes in rice roots. Journal of Plant Physiology 166, 1-11.
35. Lee MH, Min MK, Lee YJ, Jin JB, Shin DH, Kim DH, Lee KH, Hwang I. 2002. ADP-ribosylation factor 1 of Arabidopsis plays a critical role in intracellular trafficking and maintenance of endoplasmic reticulum morphology in Arabidopsis. Plant Physiology 129 1507-1520.
36. Lemaitre T, Urbanczyk-Wochniak E, Flesch V, Bismuth E, Fernie AR, Hodges M. 2007. NAD-dependent isocitrate dehydroge-nase mutants of Arabidopsis suggest the enzyme is not limiting for nitrogen assimilation. Plant Physiology 144, 1546-1558.
37. Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K. 1998. Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. The Plant Cell 10, 1391-1406.
38. Machado CR, Praekelt UM, de Oliveira RC, Barbosa ACC, Byrne KL, Meacock PA, Menck CFM. 1997. Dual role for the yeast THI4 gene in thiamine biosynthesis and DNA damage tolerance. Journal of Molecular Biology 273, 114-121.
39. Manning VA, Hardison LK, Ciuffetti LM. 2007. Ptr ToxA interacts with a chloroplast-localized protein. Molecular Plant-Microbe Interactions 20, 168-177.
40. Maqbool A, Zahur M, Husnain T, Riazuddin S. 2009. GUSP1 and GUSP2, two drought responsive genes in Gossypium arboreum have homology to Universal Stress Proteins. Plant Molecular Biology Reporter DOI: 10.1007/s11105-008-0049-0.
41. Mohanty S, Grimm B, Tripathy BC. 2006. Light and dark modulation of chlorophyll biosynthetic genes in response to temperature. Planta 224, 692-699.
42. 6/f complex in chloroplasts: missing link in the evolution of protein transport pathways in chloroplasts? Journal of Biological Chemistry 276, 42761-42766.
43. Monroy AF, Dryanova A, Malette B, et al. 2007. Regulatory gene candidates and gene expression analysis of cold acclimation in winter and spring wheat. Plant Molecular Biology 64, 409-423.
44. Mooney BP, Miernyk JA, Greenlief CM, Thelen JJ. 2006. Using quantitative proteomics ofd Arabidopsis roots and leaves to predict metabolic activity. Physlologla Plantarum 128, 237-250.
45. NDong C, Danyluk J, Huner NP, Sarhan F. 2001. Survey of gene expression in winter rye during changes in growth temperature, irradiance or excitation pressure. Plant Molecular Biology 45, 691-703.
46. Neuhoff V, Arold N, Taube D, Ehrhardt W. 1988. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie Brilliant Blue G-250 and R-250. Electrophoresis 9, 255-262.
47. O'Farrell PH. 1975. High resolution two-dimensional electrophoresis of proteins. Journal of Biological Chemistry 250, 4007-4021.
48. Pulli S, Hjortsholm K, Larsen A, Gudleifsson B, Larsson S, Kristiansson B, Hömmö L, Tronsmo AM, Ruuth P, Kristensson C. 1996. Development and evaluation of laboratory testing methods for winter-hardiness breeding. Publications-Nordic Gene Bank 32, 1-68.
49. Rabbani MA, Maruyama K, Abe H, Khan MA, Katsura K, Ito Y, Yoshiwara K, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. 2003. Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA micro-array and RNA gel-blot analyses. Plant Physiology 133, 1755-1767.
50. Rapacz M. 1999. Frost resistance and cold acclimation abilities of spring-type oilseed rape. Plant Science 147, 55-64.
51. Rapacz M. 2002. Regulation of frost resistance during cold de-acclimation and reacclimation in oilseed rape. A possible role of PSII redox state. Physiologia Plantarum 115, 236-243.
52. Rapacz M, Ga̧sior D, Kosmala A, Zwierzykowski Z, Humphreys MW. 2007. The role of photosynthetic apparatus in cold acclimation of Lolium multiflorum. Characteristics of novel genotypes low-sensitive to PSII over-reduction. Acta Physiologiae Plantarum 29, 309-316.
53. Rapacz M, Ga̧sior D, Zwierzykowski Z, Leśniewska- Bocianowska A, Humphreys MW, Gay AP. 2004. Changes in cold tolerance and the mechanisms of acclimation of photosystem II to cold hardening generated by anther culture of Festuca pratensisxLolium multiflorum cultivars. New Phytologist 162, 105-114.
54. Rapacz M, Wolanin B, Hura K, Tyrka M. 2008. The effects of cold acclimation on photosynthetic apparatus and the expression of COR14b in four genotypes of barley (Hordeum vulgare) contrasting in their tolerance to freezing and high-light treatment in cold conditions. Annals of Botany 101, 689-699.
55. Rodriguez-López M, Baroja-FernáQndez E, Zandueta-Criado A, Pozueta-Romero J. 2000. Adenosine diphosphate glucose pyro-phosphatase: a plastidial phosphodiesterase that prevents starch biosynthesis. Proceedings of the National Academy of Sciences, USA 97, 8705-8710.
56. Sandve SR, Rudi H, Asp T, Rognli OA. 2008. Tracking the evolution of a cold stress associated gene family in cold tolerant grasses. BMC Evolutionary Biology 8, 245.
57. Sarvikas P, Hakala M, Pätsikkä E, Tyystjärvi T, Tyystjärvi E. 2006. Action spectrum of photoinhibition in leaves of wild type and npq1-2 and npq4-1 mutants of Arabidopsis thaliana. Plant and Cell Physiology 473, 391-400.
58. Seki M, Narusaka M, Abe H, Kasuga M, Yamaguchi-Shinozaki K, Carninci P, Hayashizaki Y, Shinozaki K. 2001. Monitoring the expression pattern of 1300 Arabidopsis genes under drought and cold stresses by using a full-length cDNA microarray. The Plant Cell 13, 61-72.
59. 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. The Plant Journal 31, 279-292.
60. Shevchenko A, Wilm M, Vorm O, Mann M. 1996. Mass spectro-metric sequencing of proteins from silver stained polyacrylamide gels. Analytical Chemistry 68, 850-858.
61. Shi LX, Lorković ZJ, Oelmuller R, Schroder WP. 2000. The low molecular mass PsbW protein is involved in the stabilization of the dimeric photosystem II complex in Arabidopsis thaliana. Journal of Biological Chemistry 275, 37945-37950.
62. Shinozaki K, Yamaguchi-Shinozaki K. 2007. Gene networks involved in drought stress response and tolerance. Journal of Experimental Botany 58, 221-227.
63. Stefanowska M, Kuraś M, Kacperska A. 2002. Low temperature-induced modifications in cell ultrastructure and localization of phenolics in winter oilseed rape (Brassica napus L. var. oleifera L.) leaves. Annals of Botany 90, 637-645.
64. Stitt M, Hurry V. 2002. A plant for all seasons: alterations in photosynthetic carbon metabolism during cold acclimation in Arabidopsis. Current Opinion in Plant Biology 5, 199-206.
65. Tamura K, Yamada T. 2007. A perennial ryegrass CBF gene cluster is located in a region predicted by conserved synteny between Poaceae species. Theoretical and Applied Genetics 114, 273-283.
66. Tang M, Lu S, Jing Y, Zhou X, Sun J, Shen S. 2005. Isolation and identification of a cold-inducible gene encoding a putative DRE-binding transcription factor from Festuca arundinacea. Plant Physiology and Biochemistry 43, 233-239.
67. Thimm M, Goede A, Hougardy S, Preissner R. 2004. Comparison of 2D similarity and 3D superposition: application to searching a conformational drug database. Journal of Chemical Information and Computer Sciences 44, 1816-1822.
68. Thomas H, Humphreys MO. 1991. Progress and potential of interspecific hybrids of Lolium and Festuca. Journal of Agricultural Science 117, 1-8.
69. Thomashow MF. 1999. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annual Review of Plant Physiology and Plant Molecular Biology 50, 571-599.
70. Vítámvás P, Saalbach G, Prásil IT, Capková V, Opatrná J, Ahmed J. 2007. WCS120 protein family and proteins soluble upon boiling in cold-acclimated winter wheat. Journal of Plant Physiology 164, 1197-1207.
71. 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. The Plant Journal 41, 195-211.
72. Wolucka BA, Van Montagu M. 2007. The VTC2 cycle and the de novo biosynthesis pathways for vitamin C in plants: an opinion. Phytochemistry 68, 2602-2613.
73. Yamada T, Jones ES, Cogan NOI, Vecchies AC, Nomura T, Hisano H, Shimamoto Y, Smith KF, Hayward MD, Forster JW. 2004. QTL analysis of morphological, developmental, and winter hardiness-associated traits in perennial ryegrass. Crop Science 44, 925-935.
74. Yan SP, Zhang QY, Tang ZC, Su WA, Sun WN. 2006. Comparative proteomic analysis provides new insight into chilling stress response in rice. Molecular and Cellular Proteomics 5, 484-496.
75. Yang P, Li X, Wang X, Chen H, Chen F, Shen S. 2007. Proteomic analysis of rice (Oryza sativa) seeds during germination. Proteomics 7, 3358-3368.
76. Xiong Y, Fei SZ. 2006. Functional and phylogenetic analysis of a DREB/CBF-like gene in perennial ryegrass (Lolium perenne L). Planta 224, 878-888.
77. Zerges W. 2000. Translation in chloroplasts. Biochimie 82, 583-601.
78. Zhao H, Bughrara SS. 2008. Isolation and characterization of cold-regulated transcriptional activator LpCBF3 gene from perennial ryegrass (Lolium perenne L). Molecular Genetics and Genomics 279, 585-594.