Differential proteomic analysis of grapevine leaves by iTRAQ reveals responses to heat stress and subsequent recovery

BMC Plant Biology

Volumn 14, Issue 1, 2014, Pages

  Liu, Guo Tian ^a,b   Ma, Ling ^a,b   Duan, Wei ^a   Wang, Bai Chen ^a   Li, Ji Hu ^a,b   Xu, Hong Guo ^a   Yan, Xue Qing ^c   Yan, Bo Fang ^a,b   Li, Shao Hua ^a,d   Wang, Li Jun ^a  

^a INSTITUTE OF BOTANY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c Beijing Computing Center   (China)

^d Wuhan Institute of Botany Chinese Academy of Sciences   (China)

Author keywords

Cabernet sauvignon; Heat stress; iTRAQ; Photosynthesis; Proteomics; Recovery

Indexed keywords

PHOTOSYSTEM II; THIOBARBITURIC ACID REACTIVE SUBSTANCE; VEGETABLE PROTEIN;

CELL FRACTIONATION; CELL MEMBRANE; CLASSIFICATION; ELECTRON TRANSPORT; GENE ONTOLOGY; HEAT SHOCK RESPONSE; ISOTOPE LABELING; METABOLISM; PHOTOSYNTHESIS; PHOTOSYSTEM II; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT LEAF; PROCEDURES; PROTEIN TRANSPORT; PROTEOMICS; SEQUENCE HOMOLOGY; TEMPERATURE; VITIS;

CELL MEMBRANE; ELECTRON TRANSPORT; GENE ONTOLOGY; HEAT-SHOCK RESPONSE; ISOTOPE LABELING; PHOTOSYNTHESIS; PHOTOSYSTEM II PROTEIN COMPLEX; PLANT LEAVES; PLANT PROTEINS; PROTEIN TRANSPORT; PROTEOMICS; SEQUENCE HOMOLOGY, AMINO ACID; STRESS, PHYSIOLOGICAL; SUBCELLULAR FRACTIONS; TEMPERATURE; THIOBARBITURIC ACID REACTIVE SUBSTANCES; VITIS;

EID: 84900476790     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-14-110     Document Type: Article

References (85)

1. Wahid A, Gelani S, Ashraf M, Foolad M. Heat tolerance in plants: An overview. Environ Exp Bot 2007, 61(3):199-223.
2. Lobell DB, Burke MB, Tebaldi C, Mastrandrea MD, Falcon WP, Naylor RL. Prioritizing climate change adaptation needs for food security in 2030. Science 2008, 319(5863):607-610. 10.1126/science.1152339, 18239122.
3. Howarth C. Genetic improvements of tolerance to high temperature. Abiotic Stresses: Plant Resistance through Breeding and Molecular Approaches 2005, New York: Howarth Press Inc.
4. Bokszczanin KL, Fragkostefanakis S, . Solanaceae Pollen Thermotolerance Initial Training Network C Perspectives on deciphering mechanisms underlying plant heat stress response and thermotolerance. Front Plant Sci 2013, 4:315. 3750488, 23986766, Solanaceae Pollen Thermotolerance Initial Training Network C.
5. Govindjee. Sixty-three years since Kautsky: chlorophyll a fluorescence. Aust J Plant Physiol 1995, 22(2):131-160.
6. Stirbet A. On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and photosystem II: basics and applications of the OJIP fluorescence transient. J Photochem Photobiol 2011, 104(1):236-257.
7. Smertenko A, Draber P, Viklicky V, Opatrny Z. Heat stress affects the organization of microtubules and cell. Plant Cell Environ 1997, 20:1534-1542.
8. Schöffl F, Prandl R, Reindl A. Molecular responses to heat stress. Molecular Responses to Cold, Drought, Heat and Salt Stress in Higher Plants 1999, 83-93. Austin, Texas: RG Landes Co.
9. Lee DG, Ahsan N, Lee SH, Kang KY, Bahk JD, Lee IJ, Lee BH. A proteomic approach in analyzing heat-responsive proteins in rice leaves. Proteomics 2007, 7(18):3369-3383. 10.1002/pmic.200700266, 17722143.
10. Lin SK, Chang MC, Tsai YG, Lur HS. Proteomic analysis of the expression of proteins related to rice quality during caryopsis development and the effect of high temperature on expression. Proteomics 2005, 5(8):2140-2156. 10.1002/pmic.200401105, 15852341.
11. Skylas DJ, Cordwell SJ, Hains PG, Larsen MR, Basseal DJ, Walsh BJ, Blumenthal C, Rathmell W, Copeland L, Wrigley CW. Heat shock of wheat during grain filling: proteins associated with heat-tolerance. J Cereal Sci 2002, 35(2):175-188.
12. Majoul T, Bancel E, Triboi E, Ben Hamida J, Branlard G. Proteomic analysis of the effect of heat stress on hexaploid wheat grain: characterization of heat-responsive proteins from total endosperm. Proteomics 2003, 3(2):175-183. 10.1002/pmic.200390026, 12601810.
13. Sule A, Vanrobaeys F, Hajos G, Van Beeumen J, Devreese B. Proteomic analysis of small heat shock protein isoforms in barley shoots. Phytochemistry 2004, 65(12):1853-1863. 10.1016/j.phytochem.2004.03.030, 15276443.
14. Ferreira S, Hjerno K, Larsen M, Wingsle G, Larsen P, Fey S, Roepstorff P, Pais MS. Proteome profiling of Populus euphratica Oliv. Upon heat stress. Ann Bot 2006, 98(2):361-377. 10.1093/aob/mcl106, 2803470, 16740589.
15. Valcu C-M, Lalanne C, Plomion C, Schlink K. Heat induced changes in protein expression profiles of Norway spruce (Picea abies) ecotypes from different elevations. Proteomics 2008, 8(20):4287-4302. 10.1002/pmic.200700992, 18814337.
16. Ng ZX, Chua KH, Kuppusamy UR. Proteomic analysis of heat treated bitter gourd (Momordica charantia L. var. Hong Kong Green) using 2D-DIGE. Food Chem 2014, 148:155-161.
17. Zieske LR. A perspective on the use of iTRAQ reagent technology for protein complex and profiling studies. J Exp Bot 2006, 57(7):1501-1508. 10.1093/jxb/erj168, 16574745.
18. Wu WW, Baek GWSJ, Shen R-F. Comparative study of three proteomic quantitative metheods, DIGE, clCAT, and iTRAQ, using 2D Gel- or LC- MALDI TOF/TOF. J Proteome Res 2005, 5:651-658.
19. Aggarwal K, Choe LH, Lee KH. Shotgun proteomics using the iTRAQ isobaric tags. Brief Funct Genomic Proteomic 2006, 5(2):112-120. 10.1093/bfgp/ell018, 16772272.
20. Ross PL, Huang YN, Marchese JN, Williamson B, Parker K, Hattan S, Khainovski N, Pillai S, Dey S, Daniels S, Purkayastha S, Juhasz P, Martin S, Bartlet-Jones M, He F, Jacobson A, Pappin DJ. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol Cell Proteomics 2004, 3(12):1154-1169. 10.1074/mcp.M400129-MCP200, 15385600.
21. Vivier MA, Pretorius IS. Genetically tailored grapevines for the wine industry. Trends Biotechnol 2002, 20(11):472-478. 10.1016/S0167-7799(02)02058-9, 12413822.
22. Sepulveda G, Kliewer WM. Stomatal response of three grapevine cultivars (Vitis vinifera L.) to high temperature. Am J Enol Vitic 1986, 37:44-52.
23. Howell GS. Sustainable grape productivity and the growth-yield relationship: A review. Am J Enol Vitic 2001, 52(3):165-174.
24. Caprio JM, Quamme HA. Weather conditions associated with grape production in the Okanagan Valley of British Columbia and potential impact of climate change. Can J Plant Sci 2002, 82(4):755-763.
25. Wang LJ, Li SH. Salicylic acid-induced heat or cold tolerance in relation to Ca (2+) homeostasis and antioxidant systems in young grape plants. Plant Sci 2006, 170(4):685-694.
26. Mori K, Goto-Yamamoto N, Kitayama M, Hashizume K. Loss of anthocyanins in red-wine grape under high temperature. J Exp Bot 2007, 58(8):1935-1945. 10.1093/jxb/erm055, 17452755.
27. Wang LJ, Loescher W, Duan W, Li W-D, Yang S-H, Li S-H. Heat acclimation induced acquired heat tolerance and cross adaptation in different grape cultivars: relationships to photosynthetic energy partitioning. Funct Plant Biol 2009, 36(6):516-526.
28. Luo HB, Ma L, Xi HF, Duan W, Li SH, Loescher W, Wang JF, Wang LJ. Photosynthetic responses to heat treatments at different temperatures and following recovery in grapevine (Vitis amurensis L) leaves. PLoS One 2011, 6(8):e23033. 10.1371/journal.pone.0023033, 3162573, 21887227.
29. Liu GT, Wang JF, Grant C, Dai ZW, Duan W, Xu HG, Wu BH, Fan PG, Wang LJ, Li SH. Transcriptomic analysis of grape (Vitis vinifera L.) leaves during and after recovery from heat stress. BMC Plant Biol 2012, 12:174. 10.1186/1471-2229-12-174, 3497578, 23016701.
30. Agrawal GK, Rakwal R. Rice proteomics: A cornerstone for cereal food crop proteomes. Mass Spectrom Rev 2006, 25(1):1-53. 10.1002/mas.20056, 15957154.
31. Martinez-Esteso MJ, Selles-Marchart S, Lijavetzky D, Pedreno MA, Bru-Martinez R. A DIGE-based quantitative proteomic analysis of grape berry flesh development and ripening reveals key events in sugar and organic acid metabolism. J Exp Bot 2011, 62(8):2521-2569. 10.1093/jxb/erq434, 21576399.
32. Basha SM, Mazhar H, Vasanthaiah HKN. Proteomics approach to identify unique xylem sap proteins in pierce's disease-tolerant Vitis species. Appl Biochem Biotechnol 2010, 160(3):932-944. 10.1007/s12010-009-8620-1, 19412582.
33. Martinez-Esteso MJ, Casado-Vela J, Selles-Marchart S, Elortza F, Pedreno MA, Bru-Martinez R. iTRAQ-based profiling of grape berry exocarp proteins during ripening using a parallel mass spectrometric method. Mol Biosyst 2011, 7(3):749-765. 10.1039/c0mb00194e, 21113525.
34. Sharathchandra RG, Stander C, Jacobson D, Ndimba B, Vivier MA. Proteomic analysis of grape berry cell cultures reveals that developmentally regulated ripening related processes can be studied using cultured cells. PLoS One 2011, 6(2):e14708. 10.1371/journal.pone.0014708, 3040747, 21379583.
35. Zamboni A, Di Carli M, Guzzo F, Stocchero M, Zenoni S, Ferrarini A, Tononi P, Toffali K, Desiderio A, Lilley KS, Pe ME, Benvenuto E, Delledonne M, Pezzotti M. Identification of putative stage-specific grapevine berry biomarkers and omics data integration into networks. Plant Physiol 2010, 154(3):1439-1459. 10.1104/pp.110.160275, 2971619, 20826702.
36. Zhao FX, Chen LH, Perl A, Chen SW, Ma HQ. Proteomic changes in grape embryogenic callus in response to Agrobacterium tumefaciens-mediated transformation. Plant Sci 2011, 181(4):485-495. 10.1016/j.plantsci.2011.07.016, 21889056.
37. Margaria P, Palmano. Response of the Vitis vinifera L. cv. 'Nebbiolo' proteome to flavescence doree phytoplasma infection. Proteomics 2011, 11(2):212-224. 10.1002/pmic.201000409, 21204249.
38. Giribaldi M, Purrotti M, Pacifico D, Santini D, Mannini F, Caciagli P, Rolle L, Cavallarin L, Giuffrida MG, Marzachi C. A multidisciplinary study on the effects of phloem-limited viruses on the agronomical performance and berry quality of Vitis vinifera cv. Nebbiolo. J Proteomics 2011, 75(1):306-315. 10.1016/j.jprot.2011.08.006, 21856458.
39. Marsh E, Alvarez S, Hicks LM, Barbazuk WB, Qiu W, Kovacs L, Schachtman D. Changes in protein abundance during powdery mildew infection of leaf tissues of Cabernet Sauvignon grapevine (Vitis vinifera L). Proteomics 2010, 10(10):2057-2064. 10.1002/pmic.200900712, 20232356.
40. Cobos R, Barreiro C, Maria Mateos R, Coque J-JR. Cytoplasmic- and extracellular-proteome analysis of Diplodia seriata: a phytopathogenic fungus involved in grapevine decline. Proteome Sci 2010, 8:46. 10.1186/1477-5956-8-46, 2944164, 20828386.
41. Grimplet J, Wheatley MD, Jouira HB, Deluc LG, Cramer GR, Cushman JC. Proteomic and selected metabolite analysis of grape berry tissues under well-watered. Proteomics 2009, 9(9):2503-2528. 10.1002/pmic.200800158, 19343710.
42. Vincent D, Ergul A, Bohlman MC, Tattersall EAR, Tillett RL, Wheatley MD, Woolsey R, Quilici DR, Joets J, Schlauch K, Schooley DA, Cushman JC, Cramer GR. Proteomic analysis reveals differences between Vitis vinifera L. cv. Chardonnay and cv. Cabernet Sauvignon and their responses to water deficit and salinity. J Exp Bot 2007, 58(7):1873-1892. 10.1093/jxb/erm012, 17443017.
43. Jellouli N, Ben Jouira H, Skouri H, Ghorbel A, Gourgouri A, Mliki A. Proteomic analysis of Tunisian grapevine cultivar Razegui under salt stress. J Plant Physiol 2008, 165(5):471-481. 10.1016/j.jplph.2007.02.009, 17942184.
44. Galmes J, Medrano H, Flexas J. Photosynthetic limitations in response to water stress and recovery in Mediterranean plants with different growth forms. New Phytol 2007, 175(1):81-93. 10.1111/j.1469-8137.2007.02087.x, 17547669.
45. Sengupta D, Kannan M, Reddy AR. A root proteomics-based insight reveals dynamic regulation of root proteins under progressive drought stress and recovery in Vigna radiata (L.) Wilczek. Planta 2011, 233(6):1111-1127. 10.1007/s00425-011-1365-4, 21298284.
46. Mirzaei M, Pascovici D, Atwell BJ, Haynes PA. Differential regulation of aquaporins, small GTPases and V-ATPases proteins in rice leaves subjected to drought stress and recovery. Proteomics 2012, 12(6):864-877. 10.1002/pmic.201100389, 22539437.
47. Salavati A, Khatoon A, Nanjo Y, Komatsu S. Analysis of proteomic changes in roots of soybean seedlings during recovery after flooding. J Proteomics 2012, 75(3):878-893. 10.1016/j.jprot.2011.10.002, 22037232.
48. Vinocur B, Altman A. Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr Opin Biotechnol 2005, 16(2):123-132. 10.1016/j.copbio.2005.02.001, 15831376.
49. Strasser BJ. Donor side capacity of photosystem II probed by chlorophyll a fluorescence transients. Photosynth Res 1997, 52:147-155.
50. Nguyen THN, Brechenmacher L, Aldrich JT, Clauss TR, Gritsenko MA, Hixson KK, Libault M, Tanaka K, Yang F, Yao Q, Paš a-Tolic L, Xu D, Nguyen HT, Stacey G. Quantitative phosphoproteomic analysis of soybean root hairs inoculated with bradyrhizobium japonicum. Mol Cell Proteomics 2012, 11:1140-1155. 10.1074/mcp.M112.018028, 3494206, 22843990.
51. Tolin S, Arrigoni G, Trentin AR, Veljovic-Jovanovic S, Pivato M, Zechman B, Masi A. Biochemical and quantitative proteomics investigations in Arabidopsis ggt1 mutant leaves reveal a role for the gamma-glutamyl cycle in plant's adaptation to environment. Proteomics 2013, 13(12-13):2031-2045.
52. Tolin S, Arrigoni G, Moscatiello R, Masi A, Navazio L, Sablok G, Squartini A. Quantitative analysis of the naringenin-inducible proteome in Rhizobium leguminosarum by isobaric tagging and mass spectrometry. Proteomics 2013, 13(12-13):1961-1972.
53. Wang L, Liang W, Xing J, Tan F, Chen Y, Huang L, Cheng CL, Chen W. Dynamics of chloroplast proteome in salt-stressed mangrove Kandelia candel (L) Druce. J Proteome Res 2013, 12(11):5124-5136. 10.1021/pr4006469, 24070322.
54. Srivastava A, Guisse B, Greppin H, Strasser RJ. Regulation of antenna structure and electron transport in photosystem II of Pisum sativum under elevated temperature probed by the fast polyphasic chlorophyll a fluorescence transient: OKJIP. Biochim Biophys Acta 1997, 1320:95-106.
55. Camejo D, Rodriguez P, Morales A, Dell'Amico JM, Torrecillas A, Alarcon JJ. High temperature effects on photosynthetic activity of two tomato cultivars with different heat susceptibility. J Plant Physiol 2005, 162(3):281-289. 10.1016/j.jplph.2004.07.014, 15832680.
56. Efeoglu B, Terzioglu S. Photosynthetic responses of two wheat varieties to high temperature. EurAsia J BioSci 2009, 3:97-106.
57. Roose JL, Wegener KM, Pakrasi HB. The extrinsic proteins of photosystem II. Photosynth Res 2007, 92(3):369-387. 10.1007/s11120-006-9117-1, 17200881.
58. Suorsa M, Sirpio S, Allahverdiyeva Y, Paakkarinen V, Mamedov F, Styring S, Aro EM. PsbR, a missing link in the assembly of the oxygen-evolving complex of plant photosystem II. J Biol Chem 2006, 281(1):145-150. 10.1074/jbc.M510600200, 16282331.
59. Ashraf M, Harris PJC. Photosynthesis under stressful environments: An overview. Photosynthetica 2013, 51(2):163-190.
60. Amunts A, Drory O, Nelson N. The structure of a plant photosystem I supercomplex at 3.4 angstrom resolution. Nature 2007, 447(7140):58-63. 10.1038/nature05687, 17476261.
61. Vierling E. The roles of heat shock proteins in plants. Annu Rev Plant Biol 1991, 42(1):579-620.
62. Frydman J. Folding of newly translated proteins in vivo: The role of molecular chaperones. Annu Rev Biochem 2001, 70:603-647. 10.1146/annurev.biochem.70.1.603, 11395418.
63. Buchner J. Hsp90 & Co. - a holding for folding. Trends Biochem Sci 1999, 24(4):136-141. 10.1016/S0968-0004(99)01373-0, 10322418.
64. Young JC, Moarefi I, Hartl FU. Hsp90: a specialized but essential protein-folding tool. J Cell Biol 2001, 154(2):267-274. 10.1083/jcb.200104079, 2150759, 11470816.
65. Richter K, Buchner J. Hsp90: Chaperoning signal transduction. J Cell Physiol 2001, 188(3):281-290. 10.1002/jcp.1131, 11473354.
66. Pratt WB, Krishna P, Olsen LJ. Hsp90-binding immunophilins in plants: the protein movers. Trends Plant Sci 2001, 6(2):54-58. 10.1016/S1360-1385(00)01843-4, 11173288.
67. Boston RS, Viitanen PV, Vierling E. Molecular chaperones and protein folding in plants. Plant Mol Biol 1996, 32(1-2):191-222.
68. Kosova K, Vitamvas P, Prasil IT, Renaut J. Plant proteome changes under abiotic stress - Contribution of proteomics studies to understanding plant stress response. J Proteomics 2011, 74(8):1301-1322. 10.1016/j.jprot.2011.02.006, 21329772.
69. Vierling E. The role of heat-shock proteins in plants. Annu Rev Plant Physiol Plant Mol Biol 1991, 42:579-620.
70. Waters ER, Lee GJ, Vierling E. Evolution, structure and function of the small heat shock proteins in plants. J Exp Bot 1996, 47(296):325-338.
71. Wang W, Vinocur B, Shoseyov O, Altman A. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 2004, 9(5):244-252. 10.1016/j.tplants.2004.03.006, 15130550.
72. Yamaguchi-Shinozaki K, Kasuga M, Liu Q, Nakashima K, Sakuma Y, Abe H, Shinwari ZK, Seki M, Shinozaki K. Biological mechanisms of drought stress response. JIRCAS Working Report 2002, 23:1-8.
73. Palmblad M, Mills DJ, Bindschedler LV. Heat-shock response in Arabidopsis thaliana explored by multiplexed quantitative proteomics using differential metabolic labeling. J Proteome Res 2008, 7(2):780-785. 10.1021/pr0705340, 18189342.
74. Neta-Sharir I, Isaacson T, Lurie S, Weiss D. Dual role for tomato heat shock protein 21: protecting photosystem II from oxidative stress and promoting color changes during fruit maturation. Plant Cell 2005, 17(6):1829-1838. 10.1105/tpc.105.031914, 1143080, 15879560.
75. Xu C, Huang B. Differential proteomic response to heat stress in thermal Agrostis scabra and heat-sensitive Agrostis stolonifera. Physiol Plantarum 2010, 139(2):192-204.
76. Serrato AJ, Perez-Ruiz JM, Cejudo FJ. Cloning of thioredoxin h reductase and characterization of the thioredoxin reductase-thioredoxin h system from wheat. Biochem J 2002, 367:491-497. 10.1042/BJ20020103, 1222897, 12106017.
77. Gelhaye E, Rouhier N, Navrot N, Jacquot JP. The plant thioredoxin system. Cell Mol Life Sci 2005, 62(1):24-35. 10.1007/s00018-004-4296-4, 15619004.
78. Fukamatsu Y, Yabe N, Hasunuma K. Arabidopsis NDK1 is a component of ROS signaling by interacting with three catalases. Plant Cell Physiol 2003, 44(10):982-989. 10.1093/pcp/pcg140, 14581623.
79. Yoshida Y, Hasunuma K. Light-dependent subcellular localization of nucleoside diphosphate kinase-1 in Neurospora crassa. FEMS Microbiol Lett 2006, 261(1):64-68. 10.1111/j.1574-6968.2006.00329.x, 16842360.
80. Heath RL, Packer L. Photoperoxidation in isolated chloroplasts I. kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 1968, 125:189-198. 10.1016/0003-9861(68)90654-1, 5655425.
81. Qiao J, Huang S, Te R, Wang J, Chen L, Zhang W. Integrated proteomic and transcriptomic analysis reveals novel genes and regulatory mechanisms involved in salt stress responses in Synechocystis sp. PCC 6803. Appl Microbiol Biotechnol 2013, 97(18):8253-8264. 10.1007/s00253-013-5139-8, 23925534.
82. Martinez-Esteso MJ, Vilella-Anton MT, Pedreno MA, Valero ML, Bru-Martinez R. iTRAQ-based protein profiling provides insights into the central metabolism changes driving grape berry development and ripening. BMC Plant Biol 2013, 13(1):167. 10.1186/1471-2229-13-167, 4016569, 24152288.
83. Usadel B, Poree F, Nagel A, Lohse M, Czedik-Eysenberg A, Stitt M. A guide to using MapMan to visualize and compare Omics data in plants: a case study in the crop species, Maize. Plant Cell Environ 2009, 32(9):1211-1229. 10.1111/j.1365-3040.2009.01978.x, 19389052.
84. Du Z, Zhou X, Ling Y, Zhang Z, Su Z. agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 2010, 38(Web Server issue):W64-W70. 2896167, 20435677.
85. Emanuelsson O, Nielsen H, Brunak S, Heijne G. Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 2000, 300:1005-1016. 10.1006/jmbi.2000.3903, 10891285.