1932

Abstract

Plants have emerged as commercially relevant production systems for pharmaceutical and nonpharmaceutical products. Currently, the commercially available nonpharmaceutical products outnumber the medical products of plant molecular farming, reflecting the shorter development times and lower regulatory burden of the former. Nonpharmaceutical products benefit more from the low costs and greater scalability of plant production systems without incurring the high costs associated with downstream processing and purification of pharmaceuticals. In this review, we explore the areas where plant-based manufacturing can make the greatest impact, focusing on commercialized products such as antibodies, enzymes, and growth factors that are used as research-grade or diagnostic reagents, cosmetic ingredients, and biosensors or biocatalysts. An outlook is provided on high-volume, low-margin proteins such as industrial enzymes that can be applied as crude extracts or unprocessed plant tissues in the feed, biofuel, and papermaking industries.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-anchem-071015-041706
2016-06-12
2024-06-25
Loading full text...

Full text loading...

/deliver/fulltext/anchem/9/1/annurev-anchem-071015-041706.html?itemId=/content/journals/10.1146/annurev-anchem-071015-041706&mimeType=html&fmt=ahah

Literature Cited

  1. Hiatt A, Cafferkey R, Bowdish K. 1.  1989. Production of antibodies in transgenic plants. Nature 342:76–78 [Google Scholar]
  2. Sijmons PC, Dekker BM, Schrammeijer B, Verwoerd TC, van den Elzen PJ, Hoekema A. 2.  1990. Production of correctly processed human serum albumin in transgenic plants. Biotechnology 8:217–21 [Google Scholar]
  3. Paul MJ, Teh AY, Twyman RM, Ma JK. 3.  2013. Target product selection—Where can molecular pharming make the difference?. Curr. Pharm. Des. 19:5478–85 [Google Scholar]
  4. Stöger E, Fischer R, Moloney M, Ma JK. 4.  2014. Plant molecular pharming for the treatment of chronic and infectious diseases. Annu. Rev. Plant Biol. 65:743–68 [Google Scholar]
  5. Tekoah Y, Shulman A, Kizhner T, Ruderfer I, Fux L. 5.  et al. 2015. Large-scale production of pharmaceutical proteins in plant cell culture-the protalix experience. Plant Biotechnol. J. 13:1199–208 [Google Scholar]
  6. Hood E, Witcher D, Maddock S, Meyer T, Baszczynski C. 6.  et al. 1997. Commercial production of avidin from transgenic maize: characterization of transformant, production, processing, extraction and purification. Mol. Breed. 3:291–306 [Google Scholar]
  7. Fischer R, Schillberg S, Buyel JF, Twyman RM. 7.  2013. Commercial aspects of pharmaceutical protein production in plants. Curr. Pharm. Des. 19:5471–77 [Google Scholar]
  8. Kolotilin I, Topp E, Cox E, Devriendt B, Conrad U. 8.  et al. 2014. Plant-based solutions for veterinary immunotherapeutics and prophylactics. Vet. Res. 45:117 [Google Scholar]
  9. MacDonald J, Doshi K, Dussault M, Hall JC, Holbrook L. 9.  et al. 2015. Bringing plant-based veterinary vaccines to market: Managing regulatory and commercial hurdles. Biotechnol. Adv. 33:81572–81 [Google Scholar]
  10. Clarke JL, Waheed MT, Lossl AG, Martinussen I, Daniell H. 10.  2013. How can plant genetic engineering contribute to cost-effective fish vaccine development for promoting sustainable aquaculture?. Plant Mol. Biol. 83:33–40 [Google Scholar]
  11. Avesani L, Merlin M, Gecchele E, Capaldi S, Brozzetti A. 11.  et al. 2014. Comparative analysis of different biofactories for the production of a major diabetes autoantigen. Transgenic Res. 23:281–91 [Google Scholar]
  12. Merlin M, Gecchele E, Capaldi S, Pezzotti M, Avesani L. 12.  2014. Comparative evaluation of recombinant protein production in different biofactories: the green perspective. Biomed. Res. Int. 2014:136419 [Google Scholar]
  13. Baeshen NA, Baeshen MN, Sheikh A, Bora RS, Ahmed M. 13.  et al. 2014. Cell factories for insulin production. Microb. Cell Fact. 13:141 [Google Scholar]
  14. Ma JK, Hiatt A, Hein M, Vine ND, Wang F. 14.  et al. 1995. Generation and assembly of secretory antibodies in plants. Science 268:716–19 [Google Scholar]
  15. Loos A, Gruber C, Altmann F, Mehofer U, Hensel F. 15.  et al. 2014. Expression and glycoengineering of functionally active heteromultimeric IgM in plants. PNAS 111:6263–68 [Google Scholar]
  16. Hauptmann V, Weichert N, Rakhimova M, Conrad U. 16.  2013. Spider silks from plants - a challenge to create native-sized spidroins. Biotechnol. J. 8:1183–92 [Google Scholar]
  17. Stein H, Wilensky M, Tsafrir Y, Rosenthal M, Amir R. 17.  et al. 2009. Production of bioactive, post-translationally modified, heterotrimeric, human recombinant type-I collagen in transgenic tobacco. Biomacromolecules 10:2640–45 [Google Scholar]
  18. Komori R, Amano Y, Ogawa-Ohnishi M, Matsubayashi Y. 18.  2009. Identification of tyrosylprotein sulfotransferase in Arabidopsis. PNAS 106:15067–72 [Google Scholar]
  19. Matsubayashi Y. 19.  2011. Post-translational modifications in secreted peptide hormones in plants. Plant Cell Physiol. 52:5–13 [Google Scholar]
  20. Gomord V, Fitchette AC, Menu-Bouaouiche L, Saint-Jore-Dupas C, Plasson C. 20.  et al. 2010. Plant-specific glycosylation patterns in the context of therapeutic protein production. Plant Biotechnol. J. 8:564–87 [Google Scholar]
  21. Strasser R, Altmann F, Steinkellner H. 21.  2014. Controlled glycosylation of plant-produced recombinant proteins. Curr. Opin. Biotechnol. 30:95–100 [Google Scholar]
  22. Cox KM, Sterling JD, Regan JT, Gasdaska JR, Frantz KK. 22.  et al. 2006. Glycan optimization of a human monoclonal antibody in the aquatic plant Lemna minor. Nat. Biotechnol. 24:1591–97 [Google Scholar]
  23. Forthal DN, Gach JS, Landucci G, Jez J, Strasser R. 23.  et al. 2010. Fc-glycosylation influences Fcgamma receptor binding and cell-mediated anti-HIV activity of monoclonal antibody 2G12. J. Immunol. 185:6876–82 [Google Scholar]
  24. Ullrich KK, Hiss M, Rensing SA. 24.  2015. Means to optimize protein expression in transgenic plants. Curr. Opin. Biotechnol. 32:61–67 [Google Scholar]
  25. Twyman RM, Schillberg S, Fischer R. 25.  2013. Optimizing the yield of recombinant pharmaceutical proteins in plants. Curr. Pharm. Des. 19:5486–94 [Google Scholar]
  26. Kirchhoff J, Raven N, Boes A, Roberts JL, Russell S. 26.  et al. 2012. Monoclonal tobacco cell lines with enhanced recombinant protein yields can be generated from heterogeneous cell suspension cultures by flow sorting. Plant Biotechnol. J. 10:936–44 [Google Scholar]
  27. Hood EE, Devaiah SP, Fake G, Egelkrout E, Teoh KT. 27.  et al. 2012. Manipulating corn germplasm to increase recombinant protein accumulation. Plant Biotechnol. J. 10:20–30 [Google Scholar]
  28. Rademacher T, Sack M, Arcalis E, Stadlmann J, Balzer S. 28.  et al. 2008. Recombinant antibody 2G12 produced in maize endosperm efficiently neutralizes HIV-1 and contains predominantly single-GlcNAc N-glycans. Plant Biotechnol. J. 6:189–201 [Google Scholar]
  29. Fischer R, Vasilev N, Twyman RM, Schillberg S. 29.  2015. High-value products from plants: the challenges of process optimization. Curr. Opin. Biotechnol. 32:156–62 [Google Scholar]
  30. Buyel JF. 30.  2015. Process development strategies in plant molecular farming. Curr. Pharm. Biotechnol. 16:966–82 [Google Scholar]
  31. He Y, Ning T, Xie T, Qiu Q, Zhang L. 31.  et al. 2011. Large-scale production of functional human serum albumin from transgenic rice seeds. PNAS 108:19078–83 [Google Scholar]
  32. Devaiah SP, Requesens DV, Chang YK, Hood KR, Flory A. 32.  et al. 2013. Heterologous expression of cellobiohydrolase II (Cel6A) in maize endosperm. Transgenic Res. 22:477–88 [Google Scholar]
  33. De Jaeger G, Scheffer S, Jacobs A, Zambre M, Zobell O. 33.  et al. 2002. Boosting heterologous protein production in transgenic dicotyledonous seeds using Phaseolus vulgaris regulatory sequences. Nat. Biotechnol. 20:1265–68 [Google Scholar]
  34. Oey M, Lohse M, Kreikemeyer B, Bock R. 34.  2009. Exhaustion of the chloroplast protein synthesis capacity by massive expression of a highly stable protein antibiotic. Plant J. 57:436–45 [Google Scholar]
  35. Twyman RM, Stöger E, Schillberg S, Christou P, Fischer R. 35.  2003. Molecular farming in plants: host systems and expression technology. Trends Biotechnol. 21:570–78 [Google Scholar]
  36. Doran PM. 36.  2006. Foreign protein degradation and instability in plants and plant tissue cultures. Trends Biotechnol. 24:426–32 [Google Scholar]
  37. Hofbauer A, Stöger E. 37.  2013. Subcellular accumulation and modification of pharmaceutical proteins in different plant tissues. Curr. Pharm. Des. 19:5495–502 [Google Scholar]
  38. Martoglio B, Dobberstein B. 38.  1998. Signal sequences: more than just greasy peptides. Trends Cell Biol. 8:410–15 [Google Scholar]
  39. Schouten A, Roosien J, van Engelen FA, de Jong GA, Borst-Vrenssen AW. 39.  et al. 1996. The C-terminal KDEL sequence increases the expression level of a single-chain antibody designed to be targeted to both the cytosol and the secretory pathway in transgenic tobacco. Plant Mol. Biol. 30:781–93 [Google Scholar]
  40. Neuhaus JM, Rogers JC. 40.  1998. Sorting of proteins to vacuoles in plant cells. Plant Mol. Biol. 38:127–44 [Google Scholar]
  41. Robinson DG, Oliviusson P, Hinz G. 41.  2005. Protein sorting to the storage vacuoles of plants: a critical appraisal. Traffic 6:615–25 [Google Scholar]
  42. Takaiwa F. 42.  2013. Update on the use of transgenic rice seeds in oral immunotherapy. Immunotherapy 5:301–12 [Google Scholar]
  43. Hood E, Cramer C, Medrano G, Xu J. 43.  2012. Protein targeting: strategic planning for optimizing protein products through plant biotechnology. Plant Biotechnology and Agriculture A Arie, MH Paul 35–54 San Diego, CA: Academic [Google Scholar]
  44. Llop-Tous I, Ortiz M, Torrent M, Ludevid MD. 44.  2011. The expression of a xylanase targeted to ER-protein bodies provides a simple strategy to produce active insoluble enzyme polymers in tobacco plants. PLOS ONE 6:e19474 [Google Scholar]
  45. Ma JK, Drossard J, Lewis D, Altmann F, Boyle J. 45.  et al. 2015. Regulatory approval and a first-in-human phase I clinical trial of a monoclonal antibody produced in transgenic tobacco plants. Plant Biotechnol. J. 131106–20 [Google Scholar]
  46. Wilken LR, Nikolov ZL. 46.  2012. Recovery and purification of plant-made recombinant proteins. Biotechnol. Adv. 30:419–33 [Google Scholar]
  47. Buyel JF, Twyman RM, Fischer R. 47.  2015. Extraction and downstream processing of plant-derived recombinant proteins. Biotechnol. Adv. 33:902–13 [Google Scholar]
  48. Tuse D, Tu T, McDonald KA. 48.  2014. Manufacturing economics of plant-made biologics: case studies in therapeutic and industrial enzymes. Biomed. Res. Int. 2014:256135 [Google Scholar]
  49. Ou J, Guo Z, Shi J, Wang X, Liu J. 49.  et al. 2014. Transgenic rice endosperm as a bioreactor for molecular pharming. Plant Cell Rep. 33:585–94 [Google Scholar]
  50. Walwyn DR, Huddy SM, Rybicki EP. 50.  2014. Techno-economic analysis of horseradish peroxidase production using a transient expression system in Nicotiana benthamiana. Appl. Biochem. Biotechnol. 175:841–54 [Google Scholar]
  51. Buyel JF, Kaever T, Buyel JJ, Fischer R. 51.  2013. Predictive models for the accumulation of a fluorescent marker protein in tobacco leaves according to the promoter/5′UTR combination. Biotechnol. Bioeng. 110:471–82 [Google Scholar]
  52. Hood EE, Kusnadi A, Nikolov Z, Howard JA. 52.  1999. Molecular farming of industrial proteins from transgenic maize. Adv. Exp. Med. Biol. 464:127–47 [Google Scholar]
  53. Witcher D, Hood E, Peterson D, Bailey M, Bond D. 53.  et al. 1998. Commercial production of β-glucuronidase (GUS): a model system for the production of proteins in plants. Mol. Breeding 4:301–12 [Google Scholar]
  54. Howard JA, Hood E. 54.  2005. Bioindustrial and biopharmaceutical products produced in plants. Advances in Agronomy 85 D Sparks 91–124 San Diego, CA: Academic [Google Scholar]
  55. Loos R, Carvalho R, Antonio DC, Comero S, Locoro G. 55.  et al. 2013. EU-wide monitoring survey on emerging polar organic contaminants in wastewater treatment plant effluents. Water Res. 47:6475–87 [Google Scholar]
  56. Creminon C, Taran F. 56.  2015. Enzyme immunoassays as screening tools for catalysts and reaction discovery. Chem. Commun. 51:7996–8009 [Google Scholar]
  57. Collins KD, Gensch T, Glorius F. 57.  2014. Contemporary screening approaches to reaction discovery and development. Nat. Chem. 6:859–71 [Google Scholar]
  58. De Meyer T, Muyldermans S, Depicker A. 58.  2014. Nanobody-based products as research and diagnostic tools. Trends Biotechnol. 32:263–70 [Google Scholar]
  59. Geering B, Fussenegger M. 59.  2015. Synthetic immunology: modulating the human immune system. Trends Biotechnol. 33:65–79 [Google Scholar]
  60. Skerra A. 60.  2007. Alternative non-antibody scaffolds for molecular recognition. Curr. Opin. Biotechnol. 18:295–304 [Google Scholar]
  61. Richter A, Eggenstein E, Skerra A. 61.  2014. Anticalins: exploiting a non-Ig scaffold with hypervariable loops for the engineering of binding proteins. FEBS Lett. 588:213–18 [Google Scholar]
  62. Schiefner A, Skerra A. 62.  2015. The menagerie of human lipocalins: a natural protein scaffold for molecular recognition of physiological compounds. Acc. Chem. Res. 48:976–85 [Google Scholar]
  63. Justino CIL, Duarte AC, Rocha-Santos TAP. 63.  2015. Analytical applications of affibodies. Trac-Trends Anal. Chem. 65:73–82 [Google Scholar]
  64. Robinson MP, Ke N, Lobstein J, Peterson C, Szkodny A. 64.  et al. 2015. Efficient expression of full-length antibodies in the cytoplasm of engineered bacteria. Nat. Commun. 6:8072 [Google Scholar]
  65. Orzaez D, Granell A, Blazquez MA. 65.  2009. Manufacturing antibodies in the plant cell. Biotechnol. J. 4:1712–24 [Google Scholar]
  66. Julve JM, Gandia A, Fernandez-del-Carmen A, Sarrion-Perdigones A, Castelijns B. 66.  et al. 2013. A coat-independent superinfection exclusion rapidly imposed in Nicotiana benthamiana cells by tobacco mosaic virus is not prevented by depletion of the movement protein. Plant Mol. Biol. 81:553–64 [Google Scholar]
  67. Pujol M, Ramirez NI, Ayala M, Gavilondo JV, Valdes R. 67.  et al. 2005. An integral approach towards a practical application for a plant-made monoclonal antibody in vaccine purification. Vaccine 23:1833–37 [Google Scholar]
  68. Ritala A, Leelavathi S, Oksman-Caldentey KM, Reddy VS, Laukkanen ML. 68.  2014. Recombinant barley-produced antibody for detection and immunoprecipitation of the major bovine milk allergen, beta-lactoglobulin. Transgenic Res. 23:477–87 [Google Scholar]
  69. Hood E, Howard J. 69.  2014. Commercial plant-produced recombinant avidin. Commercial Plant-Produced Recombinant Protein Products: Case Studies JA Howard, EE Hood 15–25 Berlin: Springer [Google Scholar]
  70. Neurath H, Walsh KA. 70.  1976. Role of proteolytic enzymes in biological regulation (a review). PNAS 73:3825–32 [Google Scholar]
  71. Merten OW. 71.  2002. Virus contaminations of cell cultures—biotechnological view. Cytotechnology 39:91–116 [Google Scholar]
  72. Yee L, Blanch HW. 72.  1993. Recombinant trypsin production in high cell density fed-batch cultures in Escherichia coli. Biotechnol. Bioeng. 41:781–90 [Google Scholar]
  73. Mattanovich D, Katinger H, Hohenblum H, Naschberger S, Weik R. 73.  2008. Method for the manufacture of recombinant trypsin. US Patent No. 20030157634 A1
  74. Muller R, Glaser S, Geipel F, Thalhofer JP, Rexer B. 74.  et al. 2010. Method for producing recombinant trypsin. US Patent No. 20080064084 A1
  75. Hanquier J, Sorlet Y, Desplancq D, Baroche L, Ebtinger M. 75.  et al. 2003. A single mutation in the activation site of bovine trypsinogen enhances its accumulation in the fermentation broth of the yeast Pichia pastoris. Appl. Environ. Microbiol. 69:1108–13 [Google Scholar]
  76. Woodard SL, Mayor JM, Bailey MR, Barker DK, Love RT. 76.  et al. 2003. Maize (Zea mays)-derived bovine trypsin: characterization of the first large-scale, commercial protein product from transgenic plants. Biotechnol. Appl. Biochem. 38:123–30 [Google Scholar]
  77. Zhang H, Huang RY, Jalili PR, Irungu JW, Nicol GR. 77.  et al. 2010. Improved mass spectrometric characterization of protein glycosylation reveals unusual glycosylation of maize-derived bovine trypsin. Anal. Chem. 82:10095–101 [Google Scholar]
  78. Krishnan A, Woodard S. 78.  2014. TryZean™: an animal-free alternative to bovine trypsin. See Ref. 69 43–63
  79. Kim NS, Yu HY, Chung ND, Kwon TH, Yang MS. 79.  2014. High-level production of recombinant trypsin in transgenic rice cell culture through utilization of an alternative carbon source and recycling system. Enzyme Microb. Technol. 63:21–27 [Google Scholar]
  80. Bornke F, Broer I. 80.  2010. Tailoring plant metabolism for the production of novel polymers and platform chemicals. Curr. Opin. Plant Biol. 13:354–62 [Google Scholar]
  81. Canty EG, Kadler KE. 81.  2005. Procollagen trafficking, processing and fibrillogenesis. J. Cell Sci. 118:1341–53 [Google Scholar]
  82. Scheller J, Guhrs KH, Grosse F, Conrad U. 82.  2001. Production of spider silk proteins in tobacco and potato. Nat. Biotechnol. 19:573–77 [Google Scholar]
  83. Hauptmann V, Menzel M, Weichert N, Reimers K, Spohn U, Conrad U. 83.  2015. In planta production of ELPylated spidroin-based proteins results in non-cytotoxic biopolymers. BMC Biotechnol. 15:9 [Google Scholar]
  84. Weichert N, Hauptmann V, Menzel M, Schallau K, Gunkel P. 84.  et al. 2014. Transglutamination allows production and characterization of native-sized ELPylated spider silk proteins from transgenic plants. Plant Biotechnol. J. 12:265–75 [Google Scholar]
  85. Bhavsar K, Khire JM. 85.  2014. Current research and future perspectives of phytase bioprocessing. RSC Adv. 4:26677–91 [Google Scholar]
  86. Gupta RK, Gangoliya SS, Singh NK. 86.  2015. Reduction of phytic acid and enhancement of bioavailable micronutrients in food grains. J. Food Sci. Technol. 52:676–84 [Google Scholar]
  87. Xu X, Zhang Y, Meng Q, Meng K, Zhang W. 87.  et al. 2013. Overexpression of a fungal beta-mannanase from Bispora sp. MEY-1 in maize seeds and enzyme characterization. PLOS ONE 8:e56146 [Google Scholar]
  88. Lv JN, Chen YQ, Guo XJ, Piao XS, Cao YH, Dong B. 88.  2013. Effects of supplementation of beta-mannanase in corn-soybean meal diets on performance and nutrient digestibility in growing pigs. Asian-Australas. J. Anim. Sci. 26:579–87 [Google Scholar]
  89. Zhang Y, Xu X, Zhou X, Chen R, Yang P. 89.  et al. 2013. Overexpression of an acidic endo-beta-1,3-1,4-glucanase in transgenic maize seed for direct utilization in animal feed. PLOS ONE 8:e81993 [Google Scholar]
  90. Ranum P, Pena-Rosas JP, Garcia-Casal MN. 90.  2014. Global maize production, utilization, and consumption. Ann. N. Y. Acad. Sci. 1312:105–12 [Google Scholar]
  91. Hood E, Requesens D. 91.  2014. Commercial plant-produced recombinant cellulases for biomass conversion. See Ref. 69 231–46
  92. Li Q, Song J, Peng S, Wang JP, Qu GZ. 92.  et al. 2014. Plant biotechnology for lignocellulosic biofuel production. Plant Biotechnol. J. 12:1174–92 [Google Scholar]
  93. Zhang D, VanFossen A, Pagano R, Johnson J, Parker M. 93.  et al. 2011. Consolidated pretreatment and hydrolysis of plant biomass expressing cell wall degrading enzymes. BioEnergy Res. 4:276–86 [Google Scholar]
  94. Shen B, Sun X, Zuo X, Shilling T, Apgar J. 94.  et al. 2012. Engineering a thermoregulated intein-modified xylanase into maize for consolidated lignocellulosic biomass processing. Nat. Biotechnol. 30:1131–36 [Google Scholar]
  95. Blaylock MJ, Ferguson BW, Lee DA. 95.  2012. Energy crops for improved biofuel feedstocks. US Patent No. 20070250961 A1
  96. Hood EE, Love R, Lane J, Bray J, Clough R. 96.  et al. 2007. Subcellular targeting is a key condition for high-level accumulation of cellulase protein in transgenic maize seed. Plant Biotechnol. J. 5:709–19 [Google Scholar]
  97. Urbanchuk JM, Kowalski DJ, Dale B, Kim S. 97.  2009. Corn amylase: improving the efficiency and environmental footprint of corn to ethanol through plant biotechnology. AgBioForum 12:149–54 [Google Scholar]
  98. van der Maarel MJ, van der Veen B, Uitdehaag JC, Leemhuis H, Dijkhuizen L. 98.  2002. Properties and applications of starch-converting enzymes of the alpha-amylase family. J. Biotechnol. 94:137–55 [Google Scholar]
  99. Widsten P, Kandelbauer A. 99.  2008. Laccase applications in the forest products industry: a review. Enzyme Microb. Technol. 42:293–307 [Google Scholar]
  100. Hood EE, Bailey MR, Beifuss K, Magallanes-Lundback M, Horn ME. 100.  et al. 2003. Criteria for high-level expression of a fungal laccase gene in transgenic maize. Plant Biotechnol. J. 1:129–40 [Google Scholar]
  101. Bailey MR, Woodard SL, Callaway E, Beifuss K, Magallanes-Lundback M. 101.  et al. 2004. Improved recovery of active recombinant laccase from maize seed. Appl. Microbiol. Biotechnol. 63:390–97 [Google Scholar]
  102. Juturu V, Wu JC. 102.  2012. Microbial xylanases: engineering, production and industrial applications. Biotechnol. Adv. 30:1219–27 [Google Scholar]
  103. Sharma A, Thakur VV, Shrivastava A, Jain RK, Mathur RM. 103.  et al. 2014. Xylanase and laccase based enzymatic kraft pulp bleaching reduces adsorbable organic halogen (AOX) in bleach effluents: a pilot scale study. Bioresour. Technol. 169:96–102 [Google Scholar]
  104. Singh Arora D, Kumar Sharma R. 104.  2010. Ligninolytic fungal laccases and their biotechnological applications. Appl. Biochem. Biotechnol. 160:1760–88 [Google Scholar]
  105. Wang GD, Li QJ, Luo B, Chen XY. 105.  2004. Ex planta phytoremediation of trichlorophenol and phenolic allelochemicals via an engineered secretory laccase. Nat. Biotechnol. 22:893–97 [Google Scholar]
  106. Singh R, Cabrera ML, Radcliffe DE, Zhang H, Huang Q. 106.  2015. Laccase mediated transformation of 17beta-estradiol in soil. Environ. Pollut. 197:28–35 [Google Scholar]
  107. Li S, Yang X, Yang S, Zhu M, Wang X. 107.  2012. Technology prospecting on enzymes: Application, marketing and engineering. Comput. Struct. Biotechnol. J. 2:1–11 [Google Scholar]
  108. Howard J, Nikolov Z, Hood E. 108.  2011. Enzyme production systems for biomass conversion. Plant Biomass Conversion E Hood, P Nelson, R Powell 227–53 Hoboken, NJ: Wiley-Blackwell [Google Scholar]
  109. Ranganathan SV, Narasimhan SL, Muthukumar K. 109.  2008. An overview of enzymatic production of biodiesel. Bioresour. Technol. 99:3975–81 [Google Scholar]
  110. Du W, Li W, Sun T, Chen X, Liu D. 110.  2008. Perspectives for biotechnological production of biodiesel and impacts. Appl. Microbiol. Biotechnol. 79:331–37 [Google Scholar]
  111. Yang B, Wang Y-H, Yang J-G. 111.  2006. Optimization of enzymatic degumming process for rapeseed oil. J. Am. Oil Chem. Soc. 83:653–58 [Google Scholar]
  112. Bussamra BC, Freitas S, Costa AC. 112.  2015. Improvement on sugar cane bagasse hydrolysis using enzymatic mixture designed cocktail. Bioresour. Technol. 187:173–81 [Google Scholar]
  113. Clough RC, Pappu K, Thompson K, Beifuss K, Lane J. 113.  et al. 2006. Manganese peroxidase from the white-rot fungus Phanerochaete chrysosporium is enzymatically active and accumulates to high levels in transgenic maize seed. Plant Biotechnol. J. 4:53–62 [Google Scholar]
  114. Hayes TL, Zimmerman N, Hackle A. 114.  2014. World enzymes: industry study with forecasts for 2011 & 2016 Rep. 2229, Freedonia Group, Cleveland, OH [Google Scholar]
  115. Hood EE, Love R, Lane J, Bray J, Clough R. 115.  et al. 2007. Subcellular targeting is a key condition for high-level accumulation of cellulase protein in transgenic maize seed. Plant Biotechnol. J. 5:709–19 [Google Scholar]
  116. Hood EE, Devaiah SP, Fake G, Egelkrout E, Teoh K. 116.  et al. 2012. Manipulating corn germplasm to increase recombinant protein accumulation. Plant Biotechnol. J. 10:20–30 [Google Scholar]
  117. Hood NC, Hood KR, Woodard SL, Devaiah SP, Jeoh T. 117.  et al. 2014. Purification and characterization of recombinant cel7a from maize seed. Appl. Biochem. Biotechnol. 174:2864–74 [Google Scholar]
  118. Sparrow P, Broer I, Hood EE, Eversole K, Hartung F, Schiemann J. 118.  2013. Risk assessment and regulation of molecular farming—a comparison between Europe and US. Curr. Pharm. Des. 19:5513–30 [Google Scholar]
  119. Bock R. 119.  2015. Engineering plastid genomes: methods, tools, and applications in basic research and biotechnology. Annu. Rev. Plant Biol. 66:211–41 [Google Scholar]
  120. Whaley KJ, Hiatt A, Zeitlin L. 120.  2011. Emerging antibody products and Nicotiana manufacturing. Hum. Vaccines 7:349–56 [Google Scholar]
  121. D'Aoust MA, Couture MM, Charland N, Trepanier S, Landry N. 121.  et al. 2010. The production of hemagglutinin-based virus-like particles in plants: a rapid, efficient and safe response to pandemic influenza. Plant Biotechnol. J. 8:607–19 [Google Scholar]
  122. Vezina LP, Faye L, Lerouge P, D'Aoust MA, Marquet-Blouin E. 122.  et al. 2009. Transient co-expression for fast and high-yield production of antibodies with human-like N-glycans in plants. Plant Biotechnol. J. 7:442–55 [Google Scholar]
  123. Yusibov V, Rabindran S, Commandeur U, Twyman RM, Fischer R. 123.  2006. The potential of plant virus vectors for vaccine production. Drugs Res. Dev. 7:203–17 [Google Scholar]
  124. Yusibov V, Rabindran S. 124.  2008. Recent progress in the development of plant derived vaccines. Expert Rev. Vaccines 7:1173–83 [Google Scholar]
  125. Yusibov V, Streatfield SJ, Kushnir N, Roy G, Padmanaban A. 125.  2013. Hybrid viral vectors for vaccine and antibody production in plants. Curr. Pharm. Des. 19:5574–86 [Google Scholar]
  126. Canizares MC, Lomonossoff GP, Nicholson L. 126.  2005. Development of cowpea mosaic virus-based vectors for the production of vaccines in plants. Expert Rev. Vaccines 4:687–97 [Google Scholar]
  127. Lico C, Chen Q, Santi L. 127.  2008. Viral vectors for production of recombinant proteins in plants. J. Cell Physiol. 216:366–77 [Google Scholar]
  128. Sainsbury F, Lavoie PO, D'Aoust MA, Vezina LP, Lomonossoff GP. 128.  2008. Expression of multiple proteins using full-length and deleted versions of cowpea mosaic virus RNA-2. Plant Biotechnol. J. 6:82–92 [Google Scholar]
  129. Marillonnet S, Thoeringer C, Kandzia R, Klimyuk V, Gleba Y. 129.  2005. Systemic Agrobacterium tumefaciens-mediated transfection of viral replicons for efficient transient expression in plants. Nat. Biotechnol. 23:718–23 [Google Scholar]
  130. Gleba Y, Klimyuk V, Marillonnet S. 130.  2005. Magnifection—a new platform for expressing recombinant vaccines in plants. Vaccine 23:2042–48 [Google Scholar]
  131. Gleba Y, Klimyuk V, Marillonnet S. 131.  2007. Viral vectors for the expression of proteins in plants. Curr. Opin. Biotechnol. 18:134–41 [Google Scholar]
  132. Sainsbury F, Lomonossoff GP. 132.  2008. Extremely high-level and rapid transient protein production in plants without the use of viral replication. Plant Physiol. 148:1212–18 [Google Scholar]
  133. Phan HT, Hause B, Hause G, Arcalis E, Stöger E. 133.  et al. 2014. Influence of elastin-like polypeptide and hydrophobin on recombinant hemagglutinin accumulations in transgenic tobacco plants. PLOS ONE 9:e99347 [Google Scholar]
  134. Reuter LJ, Bailey MJ, Joensuu JJ, Ritala A. 134.  2014. Scale-up of hydrophobin-assisted recombinant protein production in tobacco BY-2 suspension cells. Plant Biotechnol. J. 12:402–10 [Google Scholar]
  135. Gutierrez SP, Saberianfar R, Kohalmi SE, Menassa R. 135.  2013. Protein body formation in stable transgenic tobacco expressing elastin-like polypeptide and hydrophobin fusion proteins. BMC Biotechnol. 13:40 [Google Scholar]
  136. van Rooijen GJ, Moloney MM. 136.  1995. Plant seed oil-bodies as carriers for foreign proteins. Biotechnology 13:72–77 [Google Scholar]
  137. Nykiforuk CL, Boothe JG, Murray EW, Keon RG, Goren HJ. 137.  et al. 2006. Transgenic expression and recovery of biologically active recombinant human insulin from Arabidopsis thaliana seeds. Plant Biotechnol. J. 4:77–85 [Google Scholar]
  138. Nykiforuk CL, Boothe JG. 138.  2012. Transgenic expression of therapeutic proteins in Arabidopsis thaliana seed. Methods Mol. Biol. 899:239–64 [Google Scholar]
  139. Anfossi L, Baggiani C, Giovannoli C, D'Arco G, Giraudi G. 139.  2013. Lateral-flow immunoassays for mycotoxins and phycotoxins: a review. Anal. Bioanal. Chem. 405:467–80 [Google Scholar]
  140. Taranova NA, Berlina AN, Zherdev AV, Dzantiev BB. 140.  2015. ‘Traffic light’ immunochromatographic test based on multicolor quantum dots for the simultaneous detection of several antibiotics in milk. Biosens. Bioelectron. 63:255–61 [Google Scholar]
  141. Cho IH, Radadia AD, Farrokhzad K, Ximenes E, Bae E. 141.  et al. 2014. Nano/micro and spectroscopic approaches to food pathogen detection. Annu. Rev. Anal. Chem. 7:65–88 [Google Scholar]
  142. Warriner K, Reddy SM, Namvar A, Neethirajan S. 142.  2014. Developments in nanoparticles for use in biosensors to assess food safety and quality. Trends Food Sci. Technol. 40:183–99 [Google Scholar]
  143. Knopp D, Tang D, Niessner R. 143.  2009. Review: bioanalytical applications of biomolecule-functionalized nanometer-sized doped silica particles. Anal. Chim. Acta 647:14–30 [Google Scholar]
/content/journals/10.1146/annurev-anchem-071015-041706
Loading
/content/journals/10.1146/annurev-anchem-071015-041706
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error