The organ-dependent abundance of a Solanum lipid transfer protein is up-regulated upon osmotic constraints and associated with cold acclimation ability

Journal of Experimental Botany

Volumn 59, Issue 8, 2008, Pages 2191-2203

  Kiełbowicz Matuk, Agnieszka ^a   Rey, Pascal ^b   Rorat, Tadeusz ^a  

^a INSTITUTE OF PLANT GENETICS   (Poland)

^b IRFM   (France)

Author keywords

Cold acclimation; Gene expression; Lipid transfer protein; Solanum sogarandinum; Solanum tuberosum

Indexed keywords

CARRIER PROTEIN; LIPID TRANSFER PROTEIN; SODIUM CHLORIDE; VEGETABLE PROTEIN;

ACCLIMATIZATION; AMINO ACID SEQUENCE; ARTICLE; CHEMISTRY; COLD; COMPARATIVE STUDY; DISASTER; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; OSMOSIS; PHYSIOLOGY; PLANT; SEQUENCE ALIGNMENT; SOLANUM; SPECIES DIFFERENCE; UPREGULATION;

ACCLIMATIZATION; AMINO ACID SEQUENCE; CARRIER PROTEINS; COLD; GENE EXPRESSION REGULATION, PLANT; MOLECULAR SEQUENCE DATA; NATURAL DISASTERS; OSMOSIS; PLANT PROTEINS; PLANTS; SEQUENCE ALIGNMENT; SODIUM CHLORIDE; SOLANUM; SPECIES SPECIFICITY; UP-REGULATION;

SOLANUM; SOLANUM SOGARANDINUM; SOLANUM TUBEROSUM; URSUS;

EID: 44949225085     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ern088     Document Type: Article

References (86)

1. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389-3402.
2. Arondel V, Vergnolle C, Cantrel C, Kader JC. 2000. Lipid transfer proteins are encoded by a small multigene family in Arabidopsis thaliana. Plant Science 157, 1-12.
3. Blein JP, Coutos-Thevenot P, Marion D, Ponchet M. 2002. From elicitins to lipid-transfer proteins: a new insight in cell signaling involved in plant defense mechanisms. Trends in Plant Sciences 7, 293-296.
4. Boutrot F, Guirao A, Alary R, Joudrier P, Gautier MF. 2005. Wheat non-specific lipid transfer protein genes display a complex pattern of expression in developing seeds. Biochimica et Biophysica Acta 1730, 114-125.
5. Bray EA, Bailey-Serres J, Weretilnyk E. 2000. Responses to abiotic stresses. In: Buchannan BB, Gruissem W, Jones RL, eds. Biochemistry and molecular biology of plants. Rockville, MD: American Society of Plant Physiologists, 167-176.
6. Buhot N, Douliez JP, Jacquemard A, et al. 2001. A lipid transfer protein binds to a receptor involved in the control of plant defense responses. FEBS Letters 509, 27-30.
7. Canevascini S, Caderas D, Mandel T, Fleming AJ, Dupuis I, Kuhlemeier C. 1996. Tissue-specific expression and promoter analysis of the tobacco Itp1 gene. Plant Physiology 112, 513-524.
8. Carvalho AO, Tavares OLM, Santos IS, Cunha M, Gomes VM. 2001. Antimicrobal peptides and immunolocalization of a LTP in Vigna unguiculata seeds. Plant Physiology and Biochemistry 39, 137-146.
9. Castro MS, Gerhardt IR, Orru S, Pucci P, Błoch CJR. 2003. Purification and characterization of a small (7.3 kDa) putative lipid transfer protein from maize seeds. Journal of Chromatography. B: Analytical Technologies in the Biomedical and Life Sciences 794, 109-114.
10. Charvolin D, Douliez JP, Marion D, Cohen-Addad C, Pebay-Peyroula E. 1999. The crystal structure of a wheat nonspecific lipid transfer protein (ns-LTP1) complexed with two molecules of phospholipid at 2.1 Å resolution. European Journal of Biochemistry 264, 562-568.
11. Cheng HCh, Cheng PT, Peng P, Lyu PCh, Sun YJ. 2004. Lipid binding in rice nonspecific lipid transfer protein-1 complexes from Oryza sativa. Protein Science 13, 2304-2315.
12. Chinnusamy V, Zhu J, Zhu JK. 2006. Gene regulation during cold acclimation in plants. Physiologia Plantarum 126, 1-4.
13. Colmenero-Flores JM, Campos F, Garciarrubio A, Alejandra A. 1997. Characterization of Phaseolus vulgaris cDNA clones responsive to water deficit: identification of a novel late embryogenesis abundant-like protein. Plant Molecular Biology 35, 393-405.
14. Conti A, Fortunato D, Ortolani C, Giuffrida MG, Pravettoni V, Napolitano L, Farioli L, Perono Garoffo L, Trambaioli C, Pastorello EA. 2001. Determination of the primary structure of two lipid transfer proteins from apricot (Prunus armeniaca). Journal of Chromatography. B: Biomedical Applications 756, 123-129.
15. Cushman JC, Bohnert HJ. 2000. Genomic approaches to plant stress tolerance. Current Opinion in Plant Biology 3, 117-124.
16. Da Silva VA, Landon C, Industri B, Marais A, Marion D, Ponchet M, Vovelle F. 2005. Solution structure of a tobacco lipid transfer protein exhibiting new biophysical and biological features. Proteins 59, 356-367.
17. Douliez JP, Jegou S, Pato C, Molle D, Tran V, Marion D. 2001. Binding of two mono-acylated lipid monomers by the barley lipid transfer protein, LTP1, as viewed by fluorescence, isothermal titration calorimetry and molecular modeling. European Journal of Biochemistry 268, 384-388.
18. Douliez JP, Michon T, Elmorjani K, Marion D. 2000. Steady-state tyrosine fluorescence to study the lipid-binding properties of a wheat non-specific lipid-transfer protein (nsLTP1). Biochimica et Biophysica Acta 1467, 65-72.
19. Dunn MA, Hughes MA, Zhang L, Pearce RS, Quigley AS, Jack PL. 1991. Nucleotide sequence and molecular analysis of the low temperature induced cereal gene, BLT4. Molecular and General Genetics 229, 389-394.
20. Edqvist J, Farbos I. 2002. Characterization of germination-specific lipid transfer proteins from Euphorbia lagascae. Planta 215, 41-50.
21. Eklund DM, Edqvist J. 2003. Localization of nonspecific lipid transfer proteins correlates with programmed cell death responses during endosperm degradation in Euphorbia lagascae seedlings. Plant Physiology 132, 1249-1259.
22. Federico M, Kaeppler HF, Skadsen RW. 2005. The complex developmental expression of a novel stress-responsive barley Ltp gene is determined by a shortened promoter sequence. Plant Molecular Biology 57, 35-51.
23. Garcia-Garrido JM, Menossi M, Puigdomenech P, Martinez-Izquierdo JA, Delseny M. 1998. Characterization of a gene encoding an abscisic acid-inducible type-2 lipid transfer protein from rice. FEBS Letters 428, 193-199.
24. García-Olmedo F, Molina A, Segura A, Moreno M. 1995. The defensive role of nonspecific lipid-transfer proteins in plants. Trends in Microbiology 3, 72-74.
25. Gaudet DA, Laroche A, Frick M, Huel R, Puchalski B. 2003. Cold induced expression of plant defensin and lipid transfer protein transcripts in winter wheat. Physiologia Plantarum 117, 195-205.
26. Gillet B, Beyly A, Peltier G, Rey P. 1998. Molecular characterization of CDSP 34, a chloroplastic protein induced by water deficit in Solanum tuberosum L. plants, and regulation of CDSP 34 expression by ABA and high illumination. The Plant Journal 16, 257-262.
27. Gorjanović S, Spillner E, Beljanski MV, Gorjanović R, Pavlović M, Gojgić-Cvijanović G. 2005. Malting barley grain non-specific lipid-transfer protein (ns-LTP): importance for grain protection. Journal of the Institute of Brewing 111, 99-104.
28. Gorjanović S, Sužnjević D, Beljanski M, Hranisavljević J. 2004. Barley lipid-transfer protein as heavy metal scavenger. Environmental Chemistry Letters 2, 113-116.
29. Haas BJ, Volfovsky N, Town CD, Troukhan M, Alexandrov N, Feldmann KA, Flavell RB, White O, Salzberg SL. 2002. Full-length messenger RNA sequences greatly improve genome annotation. Genome Biology 3, 0029.1-0029.12.
30. Haley J, Bogorad L. 1989. A 4-kDa maize chloroplast polypeptide associated with the cytochrome b6-f complex: subunit 5, encoded by the chloroplast petE gene (chloroplast genes/electron transport). Proceedings of the National Academy of Sciences, USA 86, 1534-1538.
31. Han GW, Lee JY, Song HK, Chang C, Min K, Moon J. 2001. Structural basis of non-specific lipid binding in maize lipid-transfer protein complexes revealed by high-resolution X-ray crystallography. Journal of Molecular Biology 308, 263-278.
32. Heino P, Palva ET. 2003. Signal transduction in plant cold acclimation. In: Hirt H, Shinozaki K, eds. Topics in current genetics, Vol. 4. Plant responses to abiotic stress. Berlin: Springer-Verlag, 151-186.
33. Hincha DK, Neukamm B, Sror HAM, Sieg F, Weckwarth W, Rückels M, Lullien-Pellerin V, Schröder W, Schmitt JM. 2001. Cabbage cryoprotectin is a member of the nonspecific plant lipid transfer protein gene family. Plant Physiology 125, 835-846.
34. Hon WC, Griffith M, Chong P, Yang DSC. 1994. Extraction and isolation of antifreeze proteins from winter rye (Secale cereale L.) leaves. Plant Physiology 104, 971-980.
35. Horvath B, Bachem C, Trindade L, Visser R. 2002. Expression analysis of a family of nsLTP genes tissue specifically expressed throughout the plant and during tuber life cycle. Plant Physiology 129, 1494-1506.
36. Hughes MA, Dunn MA, Pearce RS, White AJ, Zhang L. 1992. An abscisic-acid-responsive, low temperature barley gene has homology with a maize phospholipid transfer protein. Plant, Cell and Environment 15, 861-865.
37. Isacsson U, Wettermark G. 1974. Chemiluminescence in analytical chemistry. Analytica Chimica Acta 68, 339-362.
38. Jung HW, Kim W, Hwang BK. 2003. Three pathogen-inducible genes encoding lipid transfer protein from pepper are differentially activated by pathogens, abiotic, and environmental stresses. Plant, Cell and Environment 26, 915-928.
39. Jung HW, Kim KD, Hwang BK. 2005. Identification of pathogen-responsive regions in the promoter of pepper lipid transfer protein gene (CALTP1) and the enhanced resistance of the CALTP1 transgenic Arabidopsis against pathogen and environmental stresses. Planta 221, 361-373.
40. Kader JC. 1996. Lipid-transfer proteins in plants. Annual Review of Plant Physiology and Plant Molecular Biology 47, 627-654.
41. Kader JC. 1997. Lipid-transfer proteins: a puzzling family of plant protein. Trends in Plant Science 2, 66-70.
42. Kawaguchi R, Williams AJ, Bray EA, Bailey-Serres J. 2003. Water-deficit-induced translation control in Nicotiana tabacum. Plant, Cell and Environment 26, 221-229.
43. Kiełbowicz-Matuk A, Rey P, Rorat T. 2007. The abundance of a single domain cyclophilin in Solanaceae is regulated as a function of organ type and high temperature and not by other environmental constraints. Physiologia Plantarum 131, 387-398.
44. Knight H. 2000. Calcium signaling during abiotic stress in plants. International Review of Cytology 195, 269-324.
45. Liu H, Xue L, Li C, Zhang R, Ling Q. 2001. Calmodulin-binding protein BP-10, a probable new member of plant nonspecific lipid transfer protein superfamily. Biochemical and Biophysical Research Communications 285, 633-638.
46. Liu YJ, Samuel D, Lin CH, Lyu PC. 2002. Purification and characterization of a novel 7-kDa non-specific lipid transfer protein-2 from rice (Oryza sativa). Biochemical and Biophysical Research Communication 294, 535-540.
47. Martz F, Wilczynska M, Kleczkowski LA. 2002. Oligomerization status, with the monomer as active species, defines catalytic efficiency of UDP-glucose pyrophosphorylase. Biochemical Journal 367, 295-300.
48. Maruyama K, Sakuma Y, Kasuga M, Ito Y, Seki M, Goda H, Shimada Y, Yoshida S, Shinozaki K, Yamaguchi-Shinozaki K. 2004. Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. The Plant Journal 38, 982-993.
49. Mittler R. 2006. Abiotic stress, the field environment and stress combination. Trends in Plant Science 11, 15-19.
50. Murelli C, Rizza F, Albini FM, Dulio A, Terzi V, Cattivelli L. 1995. Metabolic changes associated with cold-acclimation in contrasting cultivars of barley. Physiologia Plantarum 94, 87-93.
51. Nakane E, Kawakita K, Doke N, Yoshioka H. 2003. Elicitation of primary and secondary metabolism during defense in potato. Journal of General Plant Pathology 69, 378-384.
52. Nielsen H, Engelbrecht J, Brunak S, von Heijne G. 1997. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Engineering 10, 1-6.
53. Örvar BL, Sangwan V, Omann F, Dhindsa RS. 2000. Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. The Plant Journal 23, 785-794.
54. Pasquato N, Berni R, Folli C, Folloni S, Cianci M, Pantano S, Helliwell JR, Zanotti G. 2006. Crystal structure of peach Pru p 3, the prototypic member of the family of plant non-specific lipid transfer protein pan-allergens. Journal of Molecular Biology 356, 684-694.
55. Pearce RS, Dunn MA, Rixon JE, Harrison P, Hughes MA. 1996. Expression of cold-induced genes and frost hardiness in the crown meristem of young barley (Hordeum vulgare L. cv. Igri) plants grown in different environments. Plant, Cell and Environment 12, 275-290.
56. Pearce RS, Houlston CE, Atherton KM, Rixon JE, Harrison P, Hughes MA, Dunn MA. 1998. Localization of expression of three cold-induced genes, blt101, blt4.9 and blt14, in different tissues of the crown and developing leaves of cold-acclimated cultivated barley. Plant Physiology 117, 787-795.
57. Pignocchi C, Foyer CH. 2003. Apoplastic ascorbate metabolism and its role in the regulation of cell signaling. Current Opinion in Plant Biology 6, 379-389.
58. Pignocchi C, Kiddle G, Hernández I, Foster SJ, Asensi A, Taybi T, Barnes J, Foyer CH. 2006. Ascorbate oxidase-dependent changes in the redox state of the apoplast modulate gene transcript accumulation leading to modified hormone signaling and orchestration of defense processes in tobacco. Plant Physiology 141, 423-435.
59. Pruvot G, Cuiné S, Peltier G, Rey P. 1996. Characterization of a novel drought-induced 34-kDa protein located in the thylakoids of Solanum tuberosum L. plants. Planta 198, 471-479.
60. Pyee J, Yu HS, Kolattukudy PE. 1994. Identification of a lipid transfer protein as the major protein in the surface wax of broccoli (Brassica oleracea) leaves. Archives of Biochemistry and Biophysics 311, 460-468.
61. Rajashekar CB, Lafta A. 1996. Cell-wall changes and cell tension in response to cold acclimation and exogenous abscisic acid in leaves and cell cultures. Plant Physiology 111, 605-612.
62. Rorat T, Grygorowicz WJ, Berbezy P, Irzykowski W. 1998. Isolation and expression of cold specific gene in potato (Solanum sogarandinum). Plant Science 133, 57-67.
63. Rorat T, Grygorowicz WJ, Irzykowski W, Rey P. 2004. Expression of KS-type dehydrins is primarily regulated by factors related to organ type and leaf developmental stage during vegetative growth. Planta 218, 878-885.
64. Rorat T, Irzykowski W. 1996. Changes in mRNA population during cold acclimation in two potato lines of Solanum sogarandinum differing by their cold hardines. Acta Physiologia Plantarum 18, 25-32.
65. Rorat T, Irzykowski W, Grygorowicz WJ. 1997. Identification and expression of novel cold induced genes in potato (Solanum sogarandinum). Plant Science 124, 69-78.
66. Rorat T, Szabala BM, Grygorowicz WJ, Wojtowicz B, Yin Z, Rey P. 2006. Expression of SK3-type dehydrin in transporting organs is associated with cold acclimation in Solanum species. Planta 224, 205-221.
67. Samuel D, Liu YJ, Cheng CHS, Lyu PCH. 2002. Solution structure of plant nonspecific lipid transfer protein-2 from rice (Oryza sativa). Journal of Biological Chemistry 277, 35267-35273.
68. Sato S, Nakamura Y, Kaneko T, Katoh T, Asamizu E, Tabata S. 2000. Structural analysis of Arabidopsis thaliana chromosome 3. I. Sequence features of the regions of 4,504,864 bp covered by sixty P1 and TAC clones. DNA Research 7, 131-135.
69. Schultz J, Copley RR, Doerks T, Ponting CP, Bork P. 2000. SMART: a web-based tool for the study of genetically mobile domains. Nucleic Acids Research 28, 231-234.
70. Seki M, Kamei A, Yamaguchi-Shinozaki K, Shinozaki K. 2003. Molecular responses to drought, salinity and frost: common and different paths for plant protection. Current Opinion in Biotechnology 14, 194-199.
71. Shinozaki K, Yamaguchi-Shinozaki K. 2000. Molecular responses to dehydration and low temperature: differences and cross-talk between two stress signaling pathways. Current Opinion in Plant Biology 3, 217-223.
72. Smart LB, Cameron KD, Bennett AB. 2000. Isolation of genes predominantly expressed in guard cells and epidermal cells of Nicotiana glauca. Plant Molecular Biology 42, 857-869.
73. 1H-NMR and fluorescence studies of the complexation of DMPG by wheat non-specific lipid transfer protein: global fold of the complex. FEBS Letters 416, 130-134.
74. Thoma S, Hecht U, Kippers A, Botella J, De Vries S, Somerville C. 1994. Tissue-specific expression of a gene encoding a cell wall-localized lipid transfer protein from Arabidopsis. Plant Physiology 105, 35-45.
75. Thoma S, Kaneko Y, Somerville C. 1993. A non-specific lipid transfer protein from Arabidopsis is a cell wall protein. The Plant Journal 3, 427-436.
76. Thomashow MF. 2001. So what's new in the field of plant cold acclimation? Lots! Plant Physiology 125, 89-93.
77. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673-4680.
78. Torres-Schumann S, Godoy JA, Pintor-Toro JA. 1992. A probable lipid transfer protein gene is induced by NaCl in stems of tomato plants. Plant Molecular Biology 18, 749-757.
79. Treviño MB, O'Connell MA. 1998. Three drought-responsive members of the nonspecific lipid-transfer protein gene family in Lycopersicon pennellii show different developmental patterns of expression. Plant Physiology 116, 1461-1468.
80. Van Buskirk HA, Thomashow MF. 2006. Arabidopsis transcription factors regulating cold acclimation. Physiologia Plantarum 126, 72-80.
81. Vieira Dos Santos C, Cuiné S, Rouhier N, Rey P. 2005. The Arabidopsis plastidic methionine sulfoxide reductase B proteins: sequence and activity characteristics, comparison of the expression with plastidic methionine sulfoxide reductase A, and induction by photooxidative stress. Plant Physiology 138, 909-922.
82. Wang Z, Xie W, Chi F, Li C. 2005. Identification of non-specific lipid transfer protein-1 as a calmodulin-binding protein in Arabidopsis. FEBS Letters 579, 1683-1687.
83. Wu G, Robertson AJ, Liu X, Zheng P, Wilen RW, Nesbitt NT, Gusta LV. 2004. A lipid transfer protein gene BG-14 is differentially regulated by abiotic stresses, ABA, anisomycin, and sphingosine in bromegrass (Bromus inermis). Journal of Plant Physiology 161, 449-458.
84. Yamaguchi-Shinozaki K, Shinozaki K. 2006. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annual Review of Plant Biology 57, 781-803.
85. Yubero-Serrano EM, Moyano E, Medina-Escobar N, Munoz-Blanco J, Caballero JL. 2003. Identification of a strawberry gene encoding a non-specific lipid transfer protein that responds to ABA, wounding and cold stress. Journal of Experimental Botany 54, 1865-1877.
86. Zhu JK. 2004. Cell signalling under salt, water and cold stresses. Current Opinion in Plant Biology 4, 401-406.