Plant Structure and Specificity – Challenges and Sample Preparation Considerations for Proteomics

  • Sophie Alvarez
  • Michael J. Naldrett
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 919)


Plants are considered as a simple structured organism when compared to humans and other vertebrates. The number of organs and tissue types is very limited. Instead the origin of the complexity comes from the high number and variety of plant species that exist, with >300,000 compared to 5000 in mammals. Proteomics, defined as the large-scale study of the proteins present in a tissue, cell or cellular compartment at a defined time point, was introduced in 1994. However, the first publications reported in the plant proteomics field only appeared at the beginning of the twenty-first century. Since these early years, the increase of proteomic studies in plants has only followed a linear trend. The main reason for this stems from the challenges specific to studying plants, those of protein extraction from cells with variously strengthened cellulosic cell walls, and a high abundance of interfering compounds, such as phenolic compounds and pigments located in plastids throughout the plant. Indeed, the heterogeneity between different organs and tissue types, between species and different developmental stages, requires the use of optimized plant protein extraction methods as described in this section. The second bottleneck of plant proteomics, which will not be discussed or reviewed here, is the lack of genomic information. Without sequence databases of the >300,000 species, proteomic studies of plants, especially of those that are not considered economically relevant, are impossible to accomplish.


Plant proteomics Plant cell lysis Plant secretome Plant organs Plant meristem and suspension culture cells Green algae and plastids Plant protein extraction  


  1. 1.
    The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815CrossRefGoogle Scholar
  2. 2.
    Acosta-Muniz CH, Escobar-Tovar L, Valdes-Rodriguez S, Fernandez-Pavia S, Arias-Saucedo LJ, de la Cruz Espindola Barquera M, Gomez Lim MA (2012) Identification of avocado (Persea americana) root proteins induced by infection with the oomycete Phytophthora cinnamomi using a proteomic approach. Physiol Plant 144:59–72PubMedCrossRefGoogle Scholar
  3. 3.
    Ahsan N, Lee SH, Lee DG, Lee H, Lee SW, Bahk JD, Lee BH (2007) Physiological and protein profiles alternation of germinating rice seedlings exposed to acute cadmium toxicity. C R Biol 330:735–746PubMedCrossRefGoogle Scholar
  4. 4.
    Alvarez S, Berla BM, Sheffield J, Cahoon RE, Jez JM, Hicks LM (2009) Comprehensive analysis of the Brassica juncea root proteome in response to cadmium exposure by complementary proteomic approaches. Proteomics 9:2419–2431PubMedCrossRefGoogle Scholar
  5. 5.
    Alvarez S, Goodger JQ, Marsh EL, Chen S, Asirvatham VS, Schachtman DP (2006) Characterization of the maize xylem sap proteome. J Proteome Res 5:963–972PubMedCrossRefGoogle Scholar
  6. 6.
    Alvarez S, Hicks LM, Pandey S (2011) ABA-dependent and -independent G-protein signaling in Arabidopsis roots revealed through an iTRAQ proteomics approach. J Proteome Res 10:3107–3122PubMedCrossRefGoogle Scholar
  7. 7.
    Alvarez S, Roy Choudhury S, Hicks LM, Pandey S (2013) Quantitative proteomics-based analysis supports a significant role of GTG proteins in regulation of ABA response in Arabidopsis roots. J Proteome Res 12:1487–1501PubMedCrossRefGoogle Scholar
  8. 8.
    Alvarez S, Roy Choudhury S, Pandey S (2014) Comparative quantitative proteomics analysis of the ABA response of roots of drought-sensitive and drought-tolerant wheat varieties identifies proteomic signatures of drought adaptability. J Proteome Res 13:1688–1701PubMedCrossRefGoogle Scholar
  9. 9.
    Alvarez S, Zhu M, Chen S (2009) Proteomics of Arabidopsis redox proteins in response to methyl jasmonate. J Proteome 73:30–40CrossRefGoogle Scholar
  10. 10.
    Amiour N, Imbaud S, Clement G, Agier N, Zivy M, Valot B, Balliau T, Armengaud P, Quillere I, Canas R, Tercet-Laforgue T, Hirel B (2012) The use of metabolomics integrated with transcriptomic and proteomic studies for identifying key steps involved in the control of nitrogen metabolism in crops such as maize. J Exp Bot 63:5017–5033PubMedCrossRefGoogle Scholar
  11. 11.
    Ban Y, Kobayashi Y, Hara T, Hamada T, Hashimoto T, Takeda S, Hattori T (2013) Alpha-tubulin is rapidly phosphorylated in response to hyperosmotic stress in rice and Arabidopsis. Plant Cell Physiol 54:848–858PubMedCrossRefGoogle Scholar
  12. 12.
    Bayer EM, Bottrill AR, Walshaw J, Vigouroux M, Naldrett MJ, Thomas CL, Maule AJ (2006) Arabidopsis cell wall proteome defined using multidimensional protein identification technology. Proteomics 6:301–311PubMedCrossRefGoogle Scholar
  13. 13.
    Bhardwaj J, Yadav SK (2013) A common protein extraction protocol for proteomic analysis: horse gram a case study. Am J Agric Biol Sci 8:293–301CrossRefGoogle Scholar
  14. 14.
    Borderies G, Jamet E, Lafitte C, Rossignol M, Jauneau A, Boudart G, Monsarrat B, Esquerre-Tugaye MT, Boudet A, Pont-Lezica R (2003) Proteomics of loosely bound cell wall proteins of Arabidopsis thaliana cell suspension cultures: a critical analysis. Electrophoresis 24:3421–3432PubMedCrossRefGoogle Scholar
  15. 15.
    Boudart G, Jamet E, Rossignol M, Lafitte C, Borderies G, Jauneau A, Esquerre-Tugaye MT, Pont-Lezica R (2005) Cell wall proteins in apoplastic fluids of Arabidopsis thaliana rosettes: identification by mass spectrometry and bioinformatics. Proteomics 5:212–221PubMedCrossRefGoogle Scholar
  16. 16.
    Brautigam A, Hoffmann-Benning S, Weber AP (2008) Comparative proteomics of chloroplast envelopes from C3 and C4 plants reveals specific adaptations of the plastid envelope to C4 photosynthesis and candidate proteins required for maintaining C4 metabolite fluxes. Plant Physiol 148:568–579PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Calderan-Rodrigues MJ, Jamet E, Bonassi MB, Guidetti-Gonzalez S, Begossi AC, Setem LV, Franceschini LM, Fonseca JG, Labate CA (2014) Cell wall proteomics of sugarcane cell suspension cultures. Proteomics 14:738–749PubMedCrossRefGoogle Scholar
  18. 18.
    Carpentier SC, Witters E, Laukens K, Deckers P, Swennen R, Panis B (2005) Preparation of protein extracts from recalcitrant plant tissues: an evaluation of different methods for two-dimensional gel electrophoresis analysis. Proteomics 5:2497–2507PubMedCrossRefGoogle Scholar
  19. 19.
    Casasoli M, Spadoni S, Lilley KS, Cervone F, De Lorenzo G, Mattei B (2008) Identification by 2-D DIGE of apoplastic proteins regulated by oligogalacturonides in Arabidopsis thaliana. Proteomics 8:1042–1054PubMedCrossRefGoogle Scholar
  20. 20.
    Charmont S, Jamet E, Pont-Lezica R, Canut H (2005) Proteomic analysis of secreted proteins from Arabidopsis thaliana seedlings: improved recovery following removal of phenolic compounds. Phytochemistry 66:453–461PubMedCrossRefGoogle Scholar
  21. 21.
    Chen Q, Yang L, Ahmad P, Wan X, Hu X (2011) Proteomic profiling and redox status alteration of recalcitrant tea (Camellia sinensis) seed in response to desiccation. Planta 233:583–592PubMedCrossRefGoogle Scholar
  22. 22.
    Chen ZY, Brown RL, Rajasekaran K, Damann KE, Cleveland TE (2006) Identification of a maize kernel pathogenesis-related protein and evidence for its involvement in resistance to Aspergillus flavus infection and Aflatoxin production. Phytopathology 96:87–95PubMedCrossRefGoogle Scholar
  23. 23.
    Cheng L, Gao X, Li S, Shi M, Javeed H, Jing X, Yang G, He G (2010) Proteomic analysis of soybean [Glycine max (L.) Meer.] seeds during imbibition at chilling temperature. Mol Breed 26:1–17CrossRefGoogle Scholar
  24. 24.
    Cheng WH, Taliercio EW, Chourey PS (1996) The miniature1 seed locus of maize encodes a cell wall invertase required for normal development of Endosperm and maternal cells in the Pedicel. Plant Cell 8:971–983PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Chitteti BR, Peng Z (2007) Proteome and phosphoproteome differential expression under salinity stress in rice (Oryza sativa) roots. J Proteome Res 6:1718–1727PubMedCrossRefGoogle Scholar
  26. 26.
    Chivasa S, Ndimba BK, Simon WJ, Robertson D, Yu XL, Knox JP, Bolwell P, Slabas AR (2002) Proteomic analysis of the Arabidopsis thaliana cell wall. Electrophoresis 23:1754–1765PubMedCrossRefGoogle Scholar
  27. 27.
    Cho K, Torres NL, Subramanyam S, Deepak SA, Sardesai N, Han O, Williams CE, Ishii H, Iwahashi H, Rakwal R (2006) Protein extraction/solubilization protocol for monocot and dicot plant gel-based proteomics. J Plant Biol 49:413–420CrossRefGoogle Scholar
  28. 28.
    Cordoba-Pedregosa M, Gonzalez-Reyes JA, Canadillas M, Navas P, Cordoba F (1996) Role of apoplastic and cell-wall peroxidases on the stimulation of root elongation by Ascorbate. Plant Physiol 112:1119–1125PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Damerval C, De Vienne D, Zivy M, Thiellement H (1986) Technical improvements in two-dimensional electrophoresis increase the level of genetic variation detected in wheat-seedling proteins. Electrophoresis 7:52–54CrossRefGoogle Scholar
  30. 30.
    Dani V, Simon WJ, Duranti M, Croy RR (2005) Changes in the tobacco leaf apoplast proteome in response to salt stress. Proteomics 5:737–745PubMedCrossRefGoogle Scholar
  31. 31.
    de Souza IR, MacAdam JW (2001) Gibberellic acid and dwarfism effects on the growth dynamics of B73 maize (Zea mays L.) leaf blades: a transient increase in apoplastic peroxidase activity precedes cessation of cell elongation. J Exp Bot 52:1673–1682PubMedCrossRefGoogle Scholar
  32. 32.
    Domozych DS, Ciancia M, Fangel JU, Mikkelsen MD, Ulvskov P, Willats WG (2012) The cell walls of green algae: a journey through evolution and diversity. Front Plant Sci 3:82PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Du CX, Fan HF, Guo SR, Tezuka T, Li J (2010) Proteomic analysis of cucumber seedling roots subjected to salt stress. Phytochemistry 71:1450–1459PubMedCrossRefGoogle Scholar
  34. 34.
    Feiz L, Irshad M, Pont-Lezica R, Canut H, Jamet E (2006) Evaluation of cell wall preparations for proteomics: a new procedure for purifying cell walls from Arabidopsis hypocotyls. Plant Methods 2:10PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Gallardo K, Job C, Groot SP, Puype M, Demol H, Vandekerckhove J, Job D (2001) Proteomic analysis of arabidopsis seed germination and priming. Plant Physiol 126:835–848PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Gallardo K, Job C, Groot SP, Puype M, Demol H, Vandekerckhove J, Job D (2002) Proteomics of Arabidopsis seed germination. A comparative study of wild-type and gibberellin-deficient seeds. Plant Physiol 129:823–837PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Gao BB, Stuart L, Feener EP (2008) Label-free quantitative analysis of one-dimensional PAGE LC/MS/MS proteome: application on angiotensin II-stimulated smooth muscle cells secretome. Mol Cell Proteomics MCP 7:2399–2409PubMedCrossRefGoogle Scholar
  38. 38.
    Hajduch M, Ganapathy A, Stein JW, Thelen JJ (2005) A systematic proteomic study of seed filling in soybean. Establishment of high-resolution two-dimensional reference maps, expression profiles, and an interactive proteome database. Plant Physiol 137:1397–1419PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Hajheidari M, Abdollahian-Noghabi M, Askari H, Heidari M, Sadeghian SY, Ober ES, Salekdeh GH (2005) Proteome analysis of sugar beet leaves under drought stress. Proteomics 5:950–960PubMedCrossRefGoogle Scholar
  40. 40.
    Harder A, Wildgruber R, Nawrocki A, Fey SJ, Larsen PM, Gorg A (1999) Comparison of yeast cell protein solubilization procedures for two-dimensional electrophoresis. Electrophoresis 20:826–829PubMedCrossRefGoogle Scholar
  41. 41.
    Haslam RP, Downie AL, Raventon M, Gallardo K, Job D, Pallett KE, John P, Parry MAJ, Coleman JOD (2003) The assessment of enriched apoplastic extracts using proteomic approaches. Ann Appl Biol 143:81–91CrossRefGoogle Scholar
  42. 42.
    Hebeler R, Oeljeklaus S, Reidegeld KA, Eisenacher M, Stephan C, Sitek B, Stuhler K, Meyer HE, Sturre MJ, Dijkwel PP, Warscheid B (2008) Study of early leaf senescence in Arabidopsis thaliana by quantitative proteomics using reciprocal 14 N/15N labeling and difference gel electrophoresis. Mol Cell Proteomics MCP 7:108–120PubMedCrossRefGoogle Scholar
  43. 43.
    Hiilovaara-Teijo M, Hannukkala A, Griffith M, Yu XM, Pihakaski-Maunsbach K (1999) Snow-mold-induced apoplastic proteins in winter rye leaves lack antifreeze activity. Plant Physiol 121:665–674PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Holmes P, Farquharson R, Hall PJ, Rolfe BG (2006) Proteomic analysis of root meristems and the effects of acetohydroxyacid synthase-inhibiting herbicides in the root of Medicago truncatula. J Proteome Res 5:2309–2316PubMedCrossRefGoogle Scholar
  45. 45.
    Hopkins JF, Spencer DF, Laboissiere S, Neilson JA, Eveleigh RJ, Durnford DG, Gray MW, Archibald JM (2012) Proteomics reveals plastid- and periplastid-targeted proteins in the chlorarachniophyte alga Bigelowiella natans. Genome Biol Evol 4:1391–1406PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Hu G, Koh J, Yoo M-J, Grupp K, Chen S, Wendel JF (2013) Proteomic profiling of developing cotton fibers from wild and domesticate Gossypium barbadense. New Phytol 200:570–582PubMedCrossRefGoogle Scholar
  47. 47.
    Hu G, Koh J, Yoo MJ, Pathak D, Chen S, Wendel JF (2014) Proteomics profiling of fiber development and domestication in upland cotton (Gossypium hirsutum L.). Planta 240:1237PubMedCrossRefGoogle Scholar
  48. 48.
    Hurkman WJ, Tanaka CK (1986) Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. Plant Physiol 81:802–806PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Irshad M, Canut H, Borderies G, Pont-Lezica R, Jamet E (2008) A new picture of cell wall protein dynamics in elongating cells of Arabidopsis thaliana: confirmed actors and newcomers. BMC Plant Biol 8:94PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Jiang Y, Yang B, Harris NS, Deyholos MK (2007) Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots. J Exp Bot 58:3591–3607PubMedCrossRefGoogle Scholar
  51. 51.
    Kamal AH, Cho K, Kim DE, Uozumi N, Chung KY, Lee SY, Choi JS, Cho SW, Shin CS, Woo SH (2012) Changes in physiology and protein abundance in salt-stressed wheat chloroplasts. Mol Biol Rep 39:9059–9074PubMedCrossRefGoogle Scholar
  52. 52.
    Kamal AH, Cho K, Komatsu S, Uozumi N, Choi JS, Woo SH (2012) Towards an understanding of wheat chloroplasts: a methodical investigation of thylakoid proteome. Mol Biol Rep 39:5069–5083PubMedCrossRefGoogle Scholar
  53. 53.
    Komatsu S, Kajiwara H, Hirano H (1993) A rice protein library: a data-file of rice proteins separated by two-dimensional electrophoresis. TAG Theor Appl Genet Theoretische und angewandte Genetik 86:935–942PubMedGoogle Scholar
  54. 54.
    Komatsu S, Muhammad A, Rakwal R (1999) Separation and characterization of proteins from green and etiolated shoots of rice (Oryza sativa L.): towards a rice proteome. Electrophoresis 20:630–636PubMedCrossRefGoogle Scholar
  55. 55.
    Komatsu S, Rakwal R, Li Z (1999) Separation and characterization of proteins in rice (Oryza sativa) suspension cultured cells. Plant Cell Tissue Organ Cult 55:183–192CrossRefGoogle Scholar
  56. 56.
    Krishnan HB, Natarajan SS (2009) A rapid method for depletion of Rubisco from soybean (Glycine max) leaf for proteomic analysis of lower abundance proteins. Phytochemistry 70:1958–1964PubMedCrossRefGoogle Scholar
  57. 57.
    Krishnan HB, Oehrle NW, Natarajan SS (2009) A rapid and simple procedure for the depletion of abundant storage proteins from legume seeds to advance proteome analysis: a case study using Glycine max. Proteomics 9:3174–3188PubMedCrossRefGoogle Scholar
  58. 58.
    Kwon HK, Yokoyama R, Nishitani K (2005) A proteomic approach to apoplastic proteins involved in cell wall regeneration in protoplasts of Arabidopsis suspension-cultured cells. Plant Cell Physiol 46:843–857PubMedCrossRefGoogle Scholar
  59. 59.
    Lan P, Li W, Wen TN, Shiau JY, Wu YC, Lin W, Schmidt W (2011) iTRAQ protein profile analysis of Arabidopsis roots reveals new aspects critical for iron homeostasis. Plant Physiol 155:821–834PubMedCrossRefGoogle Scholar
  60. 60.
    Li ZC, McClure JW, Hagerman AE (1989) Soluble and bound apoplastic activity for peroxidase, beta-d-glucosidase, malate dehydrogenase, and nonspecific Arylesterase, in barley (Hordeum vulgare L.) and oat (Avena sativa L.) primary leaves. Plant Physiol 90:185–190PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Liu D, Ford KL, Roessner U, Natera S, Cassin AM, Patterson JH, Bacic A (2013) Rice suspension cultured cells are evaluated as a model system to study salt responsive networks in plants using a combined proteomic and metabolomic profiling approach. Proteomics 13:2046–2062PubMedCrossRefGoogle Scholar
  62. 62.
    Luche S, Santoni V, Rabilloud T (2003) Evaluation of nonionic and zwitterionic detergents as membrane protein solubilizers in two-dimensional electrophoresis. Proteomics 3:249–253PubMedCrossRefGoogle Scholar
  63. 63.
    Lv DW, Subburaj S, Cao M, Yan X, Li X, Appels R, Sun DF, Ma W, Yan YM (2014) Proteome and phosphoproteome characterization reveals new response and defense mechanisms of Brachypodium distachyon leaves under salt stress. Mol Cell Proteomics MCP 13:632–652PubMedCrossRefGoogle Scholar
  64. 64.
    Macadam JW, Sharp RE, Nelson CJ (1992) Peroxidase activity in the leaf elongation zone of tall fescue: II. Spatial distribution of apoplastic peroxidase activity in genotypes differing in length of the elongation zone. Plant Physiol 99:879–885PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Marsh E, Alvarez S, Hicks LM, Barbazuk WB, Qiu W, Kovacs L, Schachtman D (2010) Changes in protein abundance during powdery mildew infection of leaf tissues of Cabernet Sauvignon grapevine (Vitis vinifera L.). Proteomics 10:2057–2064PubMedCrossRefGoogle Scholar
  66. 66.
    Marsoni M, Vanini C, Campa M, Cucchi U, Espen L, Bracale M (2005) Protein extraction from grape tissues by two-dimensional electrophoresis. Vitis 44:181–186Google Scholar
  67. 67.
    Maytalman D, Mert Z, Baykal AT, Inan C, Gunel A, Hasancebi S (2013) Proteomic analysis of early responsive resistance proteins of wheat (Triticum aestivum) to yellow rust (Puccinia striformis f. sp. tritici) using ProteomeLab PF2D. Plant OMICS J 6:24–35Google Scholar
  68. 68.
    Mechin V, Consoli L, Le Guilloux M, Damerval C (2003) An efficient solubilization buffer for plant proteins focused in immobilized pH gradients. Proteomics 3:1299–1302PubMedCrossRefGoogle Scholar
  69. 69.
    Mechin V, Thevenot C, Le Guilloux M, Prioul JL, Damerval C (2007) Developmental analysis of maize endosperm proteome suggests a pivotal role for pyruvate orthophosphate dikinase. Plant Physiol 143:1203–1219PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Morrow DL, Jones RL (1986) Localization and partial characterization of the extracellular proteins centrifuged from pea internodes. Physiol Plant 67:397–407CrossRefGoogle Scholar
  71. 71.
    Nam MH, Huh SM, Kim KM, Park WJ, Seo JB, Cho K, Kim DY, Kim BG, Yoon IS (2012) Comparative proteomic analysis of early salt stress-responsive proteins in roots of SnRK2 transgenic rice. Proteome Sci 10:25PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Noah AM, Niemenak N, Sunderhaus S, Haase C, Omokolo DN, Winkelmann T, Braun HP (2013) Comparative proteomic analysis of early somatic and zygotic embryogenesis in Theobroma cacao L. J Proteome 78:123–133CrossRefGoogle Scholar
  73. 73.
    O’Farrell PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250:4007–4021PubMedPubMedCentralGoogle Scholar
  74. 74.
    Olivieri F, Godoy AV, Escande A, Casalongue CA (1998) Analysis of intercellular washing fluids of potato tubers and detection of increased proteolytic activity upon fungal infection. Physiol Plant 10:232–238CrossRefGoogle Scholar
  75. 75.
    Pavokovic D, Kriznik B, Krsnik-Rasol M (2012) Evaluation of protein extraction methods for proteomic analysis of non-model recalcitrant plant tissues. Croat Chem Acta 85:177–183CrossRefGoogle Scholar
  76. 76.
    Pawlowski TA (2007) Proteomics of European beech (Fagus sylvatica L.) seed dormancy breaking: influence of abscisic and gibberellic acids. Proteomics 7:2246–2257PubMedCrossRefGoogle Scholar
  77. 77.
    Pawlowski TA (2009) Proteome analysis of Norway maple (Acer platanoides L.) seeds dormancy breaking and germination: influence of abscisic and gibberellic acids. BMC Plant Biol 9:48PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Peltier JB, Cai Y, Sun Q, Zabrouskov V, Giacomelli L, Rudella A, Ytterberg AJ, Rutschow H, van Wijk KJ (2006) The oligomeric stromal proteome of Arabidopsis thaliana chloroplasts. Mol Cell Proteomics MCP 5:114–133PubMedCrossRefGoogle Scholar
  79. 79.
    Peltier JB, Friso G, Kalume DE, Roepstorff P, Nilsson F, Adamska I, van Wijk KJ (2000) Proteomics of the chloroplast: systematic identification and targeting analysis of lumenal and peripheral thylakoid proteins. Plant Cell 12:319–341PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Peng Z, Wang M, Li F, Lv H, Li C, Xia G (2009) A proteomic study of the response to salinity and drought stress in an introgression strain of bread wheat. Mol Cell Proteomics MCP 8:2676–2686PubMedCrossRefGoogle Scholar
  81. 81.
    Pirovani CP, Carvalho HA, Machado RC, Gomes DS, Alvim FC, Pomella AW, Gramacho KP, Cascardo JC, Pereira GA, Micheli F (2008) Protein extraction for proteome analysis from cacao leaves and meristems, organs infected by Moniliophthora perniciosa, the causal agent of the witches’ broom disease. Electrophoresis 29:2391–2401PubMedCrossRefGoogle Scholar
  82. 82.
    Qiu X, Wong G, Audet J, Bello A, Fernando L, Alimonti JB, Fausther-Bovendo H, Wei H, Aviles J, Hiatt E, Johnson A, Morton J, Swope K, Bohorov O, Bohorova N, Goodman C, Kim D, Pauly MH, Velasco J, Pettitt J, Olinger GG, Whaley K, Xu B, Strong JE, Zeitlin L, Kobinger GP (2014) Reversion of advanced Ebola virus disease in nonhuman primates with ZMapp. Nature 514:47PubMedPubMedCentralGoogle Scholar
  83. 83.
    Raharjo TJ, Widjaja I, Roytrakul S, Verpoorte R (2004) Comparative proteomics of Cannabis sativa plant tissues. J Biomol Tech JBT 15:97–106PubMedGoogle Scholar
  84. 84.
    Rodrigues EP, Torres AR, da Silva Batista JS, Huergo L, Hungria M (2012) A simple, economical and reproducible protein extraction protocol for proteomics studies of soybean roots. Genet Mol Biol 35:348–352PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Roger D, David A, David H (1996) Immobilization of flax protoplasts in agarose and alginate beads. Correlation between ionically bound cell-wall proteins and morphogenetic response. Plant Physiol 112:1191–1199PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Samyn B, Sergeant K, Carpentier S, Debyser G, Panis B, Swennen R, Van Beeumen J (2007) Functional proteome analysis of the banana plant (Musa spp.) using de novo sequence analysis of derivatized peptides. J Proteome Res 6:70–80PubMedCrossRefGoogle Scholar
  87. 87.
    Saravanan RS, Rose JK (2004) A critical evaluation of sample extraction techniques for enhanced proteomic analysis of recalcitrant plant tissues. Proteomics 4:2522–2532PubMedCrossRefGoogle Scholar
  88. 88.
    Sebastiana M, Figueiredo A, Monteiro F, Martins J, Franco C, Coelho AV, Vaz F, Simoes T, Penque D, Pais MS, Ferreira S (2013) A possible approach for gel-based proteomic studies in recalcitrant woody plants. SpringerPlus 2:210PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Shah P, Powell AL, Orlando R, Bergmann C, Gutierrez-Sanchez G (2012) Proteomic analysis of ripening tomato fruit infected by Botrytis cinerea. J Proteome Res 11:2178–2192PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Sharathchandra RG, Stander C, Jacobson D, Ndimba B, Vivier MA (2011) Proteomic analysis of grape berry cell cultures reveals that developmentally regulated ripening related processes can be studied using cultured cells. PLoS One 6:e14708PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Shen S, Sharma A, Komatsu S (2003) Characterization of proteins responsive to gibberellin in the leaf-sheath of rice (Oryza sativa L.) seedling using proteome analysis. Biol Pharm Bull 26:129–136PubMedCrossRefGoogle Scholar
  92. 92.
    Shi Y, Jiang L, Zhang L, Kang R, Yu Z (2014) Dynamic changes in proteins during apple (Malus x domestica) fruit ripening and storage. Hortic Res 1:6PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Shoresh M, Harman GE (2008) The molecular basis of shoot responses of maize seedlings to Trichoderma harzianum T22 inoculation of the root: a proteomic approach. Plant Physiol 147:2147–2163PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Silva-Sanchez C, Chen S, Zhu N, Li QB, Chourey PS (2013) Proteomic comparison of basal endosperm in maize miniature1 mutant and its wild-type Mn1. Front Plant Sci 4:211PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Sobhanian H, Razavizadeh R, Nanjo Y, Ehsanpour AA, Jazii FR, Motamed N, Komatsu S (2010) Proteome analysis of soybean leaves, hypocotyls and roots under salt stress. Proteome Sci 8:19PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Song J, Braun G, Bevis E, Doncaster K (2006) A simple protocol for protein extraction of recalcitrant fruit tissues suitable for 2-DE and MS analysis. Electrophoresis 27:3144–3151PubMedCrossRefGoogle Scholar
  97. 97.
    Sun J, Fu J, Zhou R (2014) Proteomic analysis of differentially expressed proteins induced by salicylic acid in suspension-cultured ginseng cells. Saudi J Biol Sci 21:185–190PubMedCrossRefGoogle Scholar
  98. 98.
    Swarbreck D, Wilks C, Lamesch P, Berardini TZ, Garcia-Hernandez M, Foerster H, Li D, Meyer T, Muller R, Ploetz L, Radenbaugh A, Singh S, Swing V, Tissier C, Zhang P, Huala E (2008) The Arabidopsis Information Resource (TAIR): gene structure and function annotation. Nucleic Acids Res 36:D1009–D1014PubMedCrossRefGoogle Scholar
  99. 99.
    Tsugama D, Liu S, Takano T (2011) A rapid chemical method for lysing Arabidopsis celss for protein analysis. Plant Methods 7:22PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Tsugita A, Kawakami T, Uchiyama Y, Kamo M, Miyatake N, Nozu Y (1994) Separation and characterization of rice proteins. Electrophoresis 15:708–720PubMedCrossRefGoogle Scholar
  101. 101.
    Vander Mijnsbrugge K, Meyermans H, Van Montagu M, Bauw G, Boerjan W (2000) Wood formation in poplar: identification, characterization, and seasonal variation of xylem proteins. Planta 210:589–598PubMedCrossRefGoogle Scholar
  102. 102.
    Verdonk JC, Hatfield RD, Sullivan ML (2012) Proteomic analysis of cell walls of two developmental stages of alfalfa stems. Front Plant Sci 3:279PubMedPubMedCentralCrossRefGoogle Scholar
  103. 103.
    Vincent D, Lapierre C, Pollet B, Cornic G, Negroni L, Zivy M (2005) Water deficits affect caffeate O-methyltransferase, lignification, and related enzymes in maize leaves. A proteomic investigation. Plant Physiol 137:949–960PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Wan J, Torres M, Ganapathy A, Thelen J, DaGue BB, Mooney B, Xu D, Stacey G (2005) Proteomic analysis of soybean root hairs after infection by Bradyrhizobium japonicum. Mol Plant-Microbe Interact MPMI 18:458–467PubMedCrossRefGoogle Scholar
  105. 105.
    Wang H, Alvarez S, Hicks LM (2012) Comprehensive comparison of iTRAQ and label-free LC-based quantitative proteomics approaches using two Chlamydomonas reinhardtii strains of interest for biofuels engineering. J Proteome Res 11:487–501PubMedCrossRefGoogle Scholar
  106. 106.
    Wang W, Scali M, Vignani R, Spadafora A, Sensi E, Mazzuca S, Cresti M (2003) Protein extraction for two-dimensional electrophoresis from olive leaf, a plant tissue containing high levels of interfering compounds. Electrophoresis 24:2369–2375PubMedCrossRefGoogle Scholar
  107. 107.
    Wang W, Vignani R, Scali M, Cresti M (2006) A universal and rapid protocol for protein extraction from recalcitrant plant tissues for proteomic analysis. Electrophoresis 27:2782–2786PubMedCrossRefGoogle Scholar
  108. 108.
    Watson BS, Lei Z, Dixon RA, Sumner LW (2004) Proteomics of Medicago sativa cell walls. Phytochemistry 65:1709–1720PubMedCrossRefGoogle Scholar
  109. 109.
    Watson BS, Sumner LW (2007) Isolation of cell wall proteins from Medicago sativa stems. Methods Mol Biol 355:79–92PubMedGoogle Scholar
  110. 110.
    Witzel K, Weidner A, Surabhi GK, Borner A, Mock HP (2009) Salt stress-induced alterations in the root proteome of barley genotypes with contrasting response towards salinity. J Exp Bot 60:3545–3557PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Wu FS, Wang MY (1984) Extraction of proteins for sodium dodecyl sulfate-polyacrylamide gel electrophoresis from protease-rich plant tissues. Anal Biochem 139:100–103PubMedCrossRefGoogle Scholar
  112. 112.
    Wu X, Xiong E, Wang W, Scali M, Cresti M (2014) Universal sample preparation method integrating trichloroacetic acid/acetone precipitation with phenol extraction for crop proteomic analysis. Nat Protoc 9:362–374PubMedCrossRefGoogle Scholar
  113. 113.
    Xi J, Wang X, Li S, Zhou X, Yue L, Fan J, Hao D (2006) Polyethylene glycol fractionation improved detection of low-abundant proteins by two-dimensional electrophoresis analysis of plant proteome. Phytochemistry 67:2341–2348PubMedCrossRefGoogle Scholar
  114. 114.
    Yan S, Tang Z, Su W, Sun W (2005) Proteomic analysis of salt stress-responsive proteins in rice root. Proteomics 5:235–244PubMedCrossRefGoogle Scholar
  115. 115.
    Yan SP, Zhang QY, Tang ZC, Su WA, Sun WN (2006) Comparative proteomic analysis provides new insights into chilling stress responses in rice. Mol Cell Proteomics MCP 5:484–496PubMedCrossRefGoogle Scholar
  116. 116.
    Yang L, Zhang Y, Zhu N, Koh J, Ma C, Pan Y, Yu B, Chen S, Li H (2013) Proteomic analysis of salt tolerance in sugar beet monosomic addition line M14. J Proteome Res 12:4931–4950PubMedCrossRefGoogle Scholar
  117. 117.
    Zhang H, Lian C, Shen Z (2009) Proteomic identification of small, copper-responsive proteins in germinating embryos of Oryza sativa. Ann Bot 103:923–930PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Zhang Y, Gao P, Xing Z, Jin S, Chen Z, Liu L, Constantino N, Wang X, Shi W, Yuan JS, Dai SY (2013) Application of an improved proteomics method for abundant protein cleanup: molecular and genomic mechanisms study in plant defense. Mol Cell Proteomics MCP 12:3431–3442PubMedCrossRefGoogle Scholar
  119. 119.
    Zhao X, Ren J, Cui N, Fan H, Yu G, Li T (2013) Preparation of protein extraction from flower buds of Solanum lycopersicum for two-dimensional gel electrophoresis. Br Biotechnol J 3:183–190CrossRefGoogle Scholar
  120. 120.
    Zheng Q, Song J, Campbell-Palmer L, Thompson K, Li L, Walker B, Cui Y, Li X (2013) A proteomic investigation of apple fruit during ripening and in response to ethylene treatment. J Proteome 93:276–294CrossRefGoogle Scholar
  121. 121.
    Zhong B, Karibe H, Komatsu S, Ichimura H, Nagamura Y, Sasaki T, Hirano H (1997) Screening of rice genes from a cDNA catalog based on the sequence data-file of proteins separated by two-dimensional electrophoresis. Breed Sci 47:245–251Google Scholar
  122. 122.
    Zhou X, Wang K, Lv D, Wu C, Li J, Zhao P, Lin Z, Du L, Yan Y, Ye X (2013) Global analysis of differentially expressed genes and proteins in the wheat callus infected by Agrobacterium tumefaciens. PLoS One 8:e79390PubMedPubMedCentralCrossRefGoogle Scholar
  123. 123.
    Zhu J, Chen S, Alvarez S, Asirvatham VS, Schachtman DP, Wu Y, Sharp RE (2006) Cell wall proteome in the maize primary root elongation zone. I. Extraction and identification of water-soluble and lightly ionically bound proteins. Plant Physiol 140:311–325PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Center for BiotechnologyUniversity of Nebraska–Lincoln, Beadle CenterLincolnUSA

Personalised recommendations