Advertisement

An Overview of Plant Proteolytic Enzymes

  • D’Ipólito Sebastián
  • María Gabriela Guevara
  • Tito Florencia Rocío
  • Tonón Claudia Virginia
Chapter

Abstract

Enzymes are proteins that act as highly efficient catalysts in biochemical reactions. This catalytic capability is what makes enzymes unique and they work efficiently, rapidly, and are biodegradable. The use of enzymes frequently results in many benefits that cannot be obtained with traditional chemical treatments. These often include higher product quality and lower manufacturing cost, less waste, and reduced energy consumption. Industrial enzymes represent the heart of biotechnology processes and biotechnology (Whitehurst and van Oort 2009; Sabalza et al. 2014)

Keywords

Plant proteases Industrial enzymes Protein engineering Genetic engineering Applications 

References

  1. Agboola S, Chen S, Zhao J (2004) Formation of bitter peptides during ripening of ovine milk cheese made with different coagulants. Dairy Sci Technol 84:567–578.  https://doi.org/10.1051/lait:2004032CrossRefGoogle Scholar
  2. Almeida CM, Simões I (2018) Cardoon-based rennets for cheese production. Appl Microbiol Biotechnol 102:4675–4686.  https://doi.org/10.1007/s00253-018-9032-3CrossRefGoogle Scholar
  3. Andallu B, Varadacharyulu NC (2003) Antioxidant role of mulberry (Morus indica L. cv. Anantha) leaves in streptozotocin-diabetic rats. Clin Chim Acta 338:3–10.  https://doi.org/10.1016/S0009-8981(03)00322-XCrossRefGoogle Scholar
  4. Andallu B, Suryakantham V, Lakshmi Srikanthi B, Kesava Reddy G (2001) Effect of mulberry (Morus indica L.) therapy on plasma and erythrocyte membrane lipids in patients with type 2 diabetes. Clin Chim Acta 314:47–53.  https://doi.org/10.1016/S0009-8981(01)00632-5CrossRefGoogle Scholar
  5. Andreu D, Carreño C, Linde C et al (1999) Identification of an anti-mycobacterial domain in NK-lysin and granulysin. Biochem J 344(Pt 3):845–849CrossRefGoogle Scholar
  6. Antão CM, Malcata FX (2005) Plant serine proteases: biochemical, physiological and molecular features. Plant Physiol Biochem 43:637–650.  https://doi.org/10.1016/J.PLAPHY.2005.05.001CrossRefGoogle Scholar
  7. Arima K, Uchikoba T, Yonezawa H et al (2000a) Isolation and characterization of a serine protease from the sprouts of Pleioblastus hindsii Nakai. Phytochemistry 54:559–565.  https://doi.org/10.1016/S0031-9422(00)00075-3CrossRefGoogle Scholar
  8. Arima K, Uchikoba T, Yonezawa H et al (2000b) Cucumisin-like protease from the latex of Euphorbia supina. Phytochemistry 53:639–644.  https://doi.org/10.1016/S0031-9422(99)00605-6CrossRefGoogle Scholar
  9. Asakura T, Watanabe H, Abe K, Arai S (1997) Oryzasin as an aspartic proteinase occurring in rice seeds: purification, characterization, and application to milk clotting. J Agric Food Chem 45:1070–1075.  https://doi.org/10.1021/JF960582XCrossRefGoogle Scholar
  10. Asano N, Yamashita T, Yasuda K et al (2001) Polyhydroxylated alkaloids isolated from mulberry trees (Morus alba L.) and silkworms (Bombyx mori L.). J Agric Food Chem 49:4208–4213CrossRefGoogle Scholar
  11. Asif-Ullah M, Kim K-S, Yu YG (2006) Purification and characterization of a serine protease from Cucumis trigonus Roxburghi. Phytochemistry 67:870–875.  https://doi.org/10.1016/J.PHYTOCHEM.2006.02.020CrossRefGoogle Scholar
  12. Azarkan M, El Moussaoui A, van Wuytswinkel D et al (2003) Fractionation and purification of the enzymes stored in the latex of Carica papaya. J Chromatogr B 790:229–238.  https://doi.org/10.1016/S1570-0232(03)00084-9CrossRefGoogle Scholar
  13. Bailey AJ, Light ND (1989) Connective tissue in meat and meat products. Livest Prod Sci 27:263–264.  https://doi.org/10.1016/0301-6226(91)90102-VCrossRefGoogle Scholar
  14. Barrett AJ (1994) Classification of peptidases. Methods Enzymol 244:1–15.  https://doi.org/10.1016/0076-6879(94)44003-4CrossRefGoogle Scholar
  15. Barrett AJ, Rawlings ND, Woessner JF (1998) Handbook of proteolytic enzymes. Elsevier, AmsterdamGoogle Scholar
  16. Bartel B, Fink GR (1995) ILR1, an amidohydrolase that releases active indole-3-acetic acid from conjugates. Science 268:1745–1748CrossRefGoogle Scholar
  17. Bartling D, Nosek J (1994) Molecular and immunological characterization of leucine aminopeptidase in Arabidopsis thaliana: a new antibody suggests a semi-constitutive regulation of a phylogenetically old enzyme. Plant Sci 99:199–209.  https://doi.org/10.1016/0168-9452(94)90177-5CrossRefGoogle Scholar
  18. Batkin S, Taussig S, Szekerczes J (1988) Modulation of pulmonary metastasis (Lewis lung carcinoma) by bromelain, an extract of the pineapple stem (Ananas comosus). Cancer Investig 6:241–242.  https://doi.org/10.3109/07357908809077053CrossRefGoogle Scholar
  19. Beers EP, Woffenden BJ, Zhao C (2000) Plant proteolytic enzymes: possible roles during programmed cell death. Plant Mol Biol 44:399–415.  https://doi.org/10.1023/A:1026556928624CrossRefGoogle Scholar
  20. Bhalerao R, Keskitalo J, Sterky F et al (2003) Gene expression in autumn leaves. Plant Physiol 131:430–442.  https://doi.org/10.1104/pp.012732CrossRefGoogle Scholar
  21. Bölter B, Nada A, Fulgosi H, Soll J (2006) A chloroplastic inner envelope membrane protease is essential for plant development. FEBS Lett 580:789–794.  https://doi.org/10.1016/j.febslet.2005.12.098CrossRefGoogle Scholar
  22. Brodelius PE, Cordeiro MC, Pais MS (1995) Aspartic proteinases (cyprosins) from Cynara Cardunculus spp. Flavescens cv. cardoon; purification, characterisation, and tissue-specific expression. Springer, Boston, pp 255–266Google Scholar
  23. Bruhn H (2005) A short guided tour through functional and structural features of saposin-like proteins. Biochem J 389:249–257.  https://doi.org/10.1042/BJ20050051CrossRefGoogle Scholar
  24. Buchanan-Wollaston V (1997) The molecular biology of leaf senescence. J Exp Bot 48:181–199.  https://doi.org/10.1093/jxb/48.2.181CrossRefGoogle Scholar
  25. de Carvalho MHC, D’Arcy-Lameta A, Roy-Macauley H et al (2001) Aspartic protease in leaves of common bean (Phaseolus vulgaris L.) and cowpea (Vigna unguiculata L. Walp): enzymatic activity, gene expression and relation to drought susceptibility. FEBS Lett 492:242–246.  https://doi.org/10.1016/S0014-5793(01)02259-1CrossRefGoogle Scholar
  26. Casamitjana-Martınez E, Hofhuis HF, Xu J et al (2003) Root-specific CLE19 overexpression and the sol1/2 suppressors implicate a CLV-like pathway in the control of arabidopsis root meristem maintenance. Curr Biol 13:1435–1441.  https://doi.org/10.1016/S0960-9822(03)00533-5CrossRefGoogle Scholar
  27. Chao WS, Gu Y-Q, Pautot V et al (1999) Leucine aminopeptidase RNAs, proteins, and activities increase in response to water deficit, salinity, and the wound signals systemin, methyl jasmonate, and abscisic acid. Plant Physiol 120:979–992.  https://doi.org/10.1104/PP.120.4.979CrossRefGoogle Scholar
  28. Chao WS, Pautot V, Holzer FM, Walling LL (2000) Leucine aminopeptidases: the ubiquity of LAP-N and the specificity of LAP-A. Planta 210:563–573.  https://doi.org/10.1007/s004250050045CrossRefGoogle Scholar
  29. Chen M, Choi Y, Voytas DF, Rodermel S (2000) Mutations in the Arabidopsis VAR2 locus cause leaf variegation due to the loss of a chloroplast FtsH protease. Plant J 22:303–313.  https://doi.org/10.1046/j.1365-313x.2000.00738.xCrossRefGoogle Scholar
  30. Chen G, Bi YR, Li N (2005) EGY1 encodes a membrane-associated and ATP-independent metalloprotease that is required for chloroplast development. Plant J 41:364–375.  https://doi.org/10.1111/j.1365-313X.2004.02308.xCrossRefGoogle Scholar
  31. Chen J, Burke JJ, Velten J, Xin Z (2006) FtsH11 protease plays a critical role in Arabidopsis thermotolerance. Plant J 48:73–84.  https://doi.org/10.1111/j.1365-313X.2006.02855.xCrossRefGoogle Scholar
  32. Cheon BS, Kim YH, Son KS et al (2000) Effects of prenylated flavonoids and biflavonoids on lipopolysaccharide-induced nitric oxide production from the mouse macrophage cell line RAW 264.7. Planta Med 66:596–600.  https://doi.org/10.1055/s-2000-8621CrossRefGoogle Scholar
  33. Coffeen WC, Wolpert TJ (2004) Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with programmed cell death in Avena sativa. Plant Cell Online 16:857–873.  https://doi.org/10.1105/tpc.017947CrossRefGoogle Scholar
  34. Combier J-P, Vernié T, de Billy F et al (2007) The MtMMPL1 early nodulin is a novel member of the matrix metalloendoproteinase family with a role in Medicago truncatula infection by Sinorhizobium meliloti. Plant Physiol 144:703–716.  https://doi.org/10.1104/pp.106.092585CrossRefGoogle Scholar
  35. Cordeiro MC, Pais MS, Brodelius PE (1994) Tissue-specific expression of multiple forms of cyprosin (aspartic proteinase) in flowers of Cynara cardunculus. Physiol Plant 92:645–653.  https://doi.org/10.1111/j.1399-3054.1994.tb03035.xCrossRefGoogle Scholar
  36. Davies DR (1990) The structure and function of the aspartic proteinases. Annu Rev Biophys Biophys Chem 19:189–215.  https://doi.org/10.1146/annurev.bb.19.060190.001201CrossRefGoogle Scholar
  37. Davies RT, Goetz DH, Lasswell J et al (1999) IAR3 encodes an auxin conjugate hydrolase from Arabidopsis. Plant Cell 11:365–376.  https://doi.org/10.1105/TPC.11.3.365CrossRefGoogle Scholar
  38. Delorme VG, McCabe PF, Kim DJ, Leaver CJ (2000) A matrix metalloproteinase gene is expressed at the boundary of senescence and programmed cell death in cucumber. Plant Physiol 123:917–927CrossRefGoogle Scholar
  39. van der Hoorn RAL (2008) Plant proteases: from phenotypes to molecular mechanisms. Annu Rev Plant Biol 59:191–223.  https://doi.org/10.1146/annurev.arplant.59.032607.092835CrossRefGoogle Scholar
  40. Déry O, Corvera CU, Steinhoff M, Bunnett NW (1998) Proteinase-activated receptors: novel mechanisms of signaling by serine proteases. Am J Physiol Physiol 274:C1429–C1452.  https://doi.org/10.1152/ajpcell.1998.274.6.C1429CrossRefGoogle Scholar
  41. Distefano S, Palma J, McCarthy I, del Rio L (1999) Proteolytic cleavage of plant proteins by peroxisomal endoproteases from senescent pea leaves. Planta 209:308–313CrossRefGoogle Scholar
  42. Doi E, Shibata D, Matoba T, Yonezawa D (1980) Characterization of pepstatin-sensitive acid protease in resting rice seeds. Agric Biol Chem 44:741–747.  https://doi.org/10.1080/00021369.1980.10864028CrossRefGoogle Scholar
  43. Doi K, Kojima T, Fujimoto Y (2000) Mulberry leaf extract inhibits the oxidative modification of rabbit and human low density lipoprotein. Biol Pharm Bull 23:1066–1071.  https://doi.org/10.1248/bpb.23.1066CrossRefGoogle Scholar
  44. Doi K, Kojima T, Makino M et al (2001) Studies on the constituents of the leaves of Morus alba L. Chem Pharm Bull 49:151–153.  https://doi.org/10.1248/cpb.49.151CrossRefGoogle Scholar
  45. Domingos A, Cardoso PC, Xue Z et al (2000) Purification, cloning and autoproteolytic processing of an aspartic proteinase from Centaurea calcitrapa. Eur J Biochem 267:6824–6831.  https://doi.org/10.1046/j.1432-1327.2000.01780.xCrossRefGoogle Scholar
  46. Domsalla A, Melzig M (2008) Occurrence and properties of proteases in plant lattices. Planta Med 74:699–711.  https://doi.org/10.1055/s-2008-1074530CrossRefGoogle Scholar
  47. Dryjanski M, Otlewski J, Polanowski A, Wilusz T (1990) Serine proteinase from cucurbita ficifolia seed; purification, properties, substrate specificity and action on native squash trypsin inhibitor (CMTI I). Biol Chem Hoppe Seyler 371:889–896.  https://doi.org/10.1515/bchm3.1990.371.2.889CrossRefGoogle Scholar
  48. Dubey VK, Pande M, Singh BK, Jagannadham MV (2007) Papain-like proteases: applications of their inhibitors. Afr J Biotechnol 6:1077–1086.  https://doi.org/10.4314/ajb.v6i9.57108CrossRefGoogle Scholar
  49. Dunn BM (2002) Structure and mechanism of the pepsin-like family of aspartic peptidases. Chem Rev 102:4431–4458.  https://doi.org/10.1002/chin.200306266CrossRefGoogle Scholar
  50. Estelle M (2001) Proteases and cellular regulation in plants. Curr Opin Plant Biol 4:254–260.  https://doi.org/10.1016/S1369-5266(00)00169-2CrossRefGoogle Scholar
  51. Esteves CLC, Lucey JA, Pires EMV (2001) Mathematical modelling of the formation of rennet-induced gels by plant coagulants and chymosin. J Dairy Res 68(3):499–510.  https://doi.org/10.1017/S0022029901005027CrossRefGoogle Scholar
  52. Esteves CLC, Lucey JA, Wang T, Pires EMV (2003) Effect of pH on the gelation properties of skim milk gels made from plant coagulants and chymosin. J Dairy Sci 86:2558–2567.  https://doi.org/10.3168/JDS.S0022-0302(03)73850-8CrossRefGoogle Scholar
  53. Faro C, Gal S (2005) Aspartic proteinase content of the arabidopsis genome. Curr Protein Pept Sci 6:493–500.  https://doi.org/10.2174/138920305774933268CrossRefGoogle Scholar
  54. Faro CJ, Moir AJG, Pires EV (1992) Specificity of a milk clotting enzyme extracted from the thistle Cynara cardunculus L.: Action on oxidised insulin and k-casein. Biotechnol Lett 14:841–846.  https://doi.org/10.1007/BF01029150CrossRefGoogle Scholar
  55. Feijoo-Siota L, Villa TG (2011) Native and biotechnologically engineered plant proteases with industrial applications. Food Bioprocess Technol 4:1066–1088.  https://doi.org/10.1007/s11947-010-0431-4CrossRefGoogle Scholar
  56. Fernández-Salguero J, Prados F, Calixto F et al (2003) Use of recombinant cyprosin in the manufacture of Ewe’s milk cheese. J Agric Food Chem 51:7426–7430.  https://doi.org/10.1021/jf034573hCrossRefGoogle Scholar
  57. Fontanini D, Jones B (2002) SEP-1 - a subtilisin-like serine endopeptidase from germinated seeds of Hordeum vulgare L. cv. Morex. Planta 215:885–893.  https://doi.org/10.1007/s00425-002-0823-4CrossRefGoogle Scholar
  58. Foroughi F, Keshavarz T, Evans CS (2006) Specificities of proteases for use in leather manufacture. J Chem Technol Biotechnol 81:257–261.  https://doi.org/10.1002/jctb.1367CrossRefGoogle Scholar
  59. García-Lorenzo M, Sjödin A, Jansson S, Funk C (2006) Protease gene families in populus and arabidopsis. BMC Plant Biol 6:30.  https://doi.org/10.1186/1471-2229-6-30CrossRefGoogle Scholar
  60. Garcia-Martinez JL, Moreno J (1986) Proteolysis of ribulose-1,5-bisphosphate carboxylase/oxygenase in Citrus leaf extracts. Physiol Plant 66:377–383.  https://doi.org/10.1111/j.1399-3054.1986.tb05938.xCrossRefGoogle Scholar
  61. Genelhu MS, Zanini MS, Veloso IF et al (1998) Use of a cysteine proteinase from Carica candamarcensis as a protective agent during DNA extraction. Braz J Med Biol Res 31:1129–1132CrossRefGoogle Scholar
  62. Glathe S, Kervinen J, Nimtz M et al (1998) Transport and activation of the vacuolar aspartic proteinase phytepsin in barley (Hordeum vulgare L.). J Biol Chem 273:31230–31236.  https://doi.org/10.1074/JBC.273.47.31230CrossRefGoogle Scholar
  63. Golldack D, Popova OV, Dietz K-J (2002) Mutation of the matrix metalloproteinase At2-MMP inhibits growth and causes late flowering and early senescence in Arabidopsis. J Biol Chem 277:5541–5547.  https://doi.org/10.1074/jbc.M106197200CrossRefGoogle Scholar
  64. González-Rábade N, Badillo-Corona JA, Aranda-Barradas JS (2011) Production of plant proteases in vivo and in vitro--a review. Biotechnol Adv 29:983–996.  https://doi.org/10.1016/J.BIOTECHADV.2011.08.017CrossRefGoogle Scholar
  65. Graham JS, Xiong J, Gillikin JW (1991) Purification and developmental analysis of a metalloendoproteinase from the leaves of glycine max. Plant Physiol 97:786–792.  https://doi.org/10.1104/PP.97.2.786CrossRefGoogle Scholar
  66. Groover A, Jones A (1999) Tracheary element differentiation uses a novel mechanism coordinating programmed cell death and secondary cell wall synthesis. Plant Physiol 119:375–384CrossRefGoogle Scholar
  67. Gu Y-Q, Holzer FM, Walling LL (1999) Overexpression, purification and biochemical characterization of the wound-induced leucine aminopeptidase of tomato. Eur J Biochem 263:726–735.  https://doi.org/10.1046/j.1432-1327.1999.00548.xCrossRefGoogle Scholar
  68. Guevara MG, Oliva CR, Machinandiarena M, Daleo GR (1999) Purification and properties of an aspartic protease from potato tuber that is inhibited by a basic chitinase. Physiol Plant 106:164–169.  https://doi.org/10.1034/j.1399-3054.1999.106203.xCrossRefGoogle Scholar
  69. Guevara MG, Daleo GR, Oliva CR (2001) Purification and characterization of an aspartic protease from potato leaves. Physiol Plant 112:321–326.  https://doi.org/10.1034/j.1399-3054.2001.1120304.xCrossRefGoogle Scholar
  70. Guevara MG, Oliva CR, Huarte M, Daleo GR (2002) An aspartic protease with antimicrobial activity is induced after infection and wounding in intercellular fluids of potato tubers. Eur J Plant Pathol 108:131–137.  https://doi.org/10.1023/A:1015049629736CrossRefGoogle Scholar
  71. Guevara MG, Veríssimo P, Pires E et al (2004) Potato aspartic proteases: induction, antimicrobial activity and substrate specificity. J Plant Pathol 86:233–238.  https://doi.org/10.2307/41992430CrossRefGoogle Scholar
  72. Guevara MG, Almeida C, Mendieta JR et al (2005) Molecular cloning of a potato leaf cDNA encoding an aspartic protease (StAsp) and its expression after P. infestans infection. Plant Physiol Biochem 43:882–889.  https://doi.org/10.1016/J.PLAPHY.2005.07.004CrossRefGoogle Scholar
  73. Guimarães-Ferreira CA, Rodrigues EG, Mortara RA et al (2007) Antitumor effects in vitro and in vivo and mechanisms of protection against melanoma B16F10-Nex2 cells by fastuosain, a cysteine proteinase from Bromelia fastuosa. Neoplasia 9:723–733CrossRefGoogle Scholar
  74. Hartley BS (1960) Proteolytic enzymes. Annu Rev Biochem 29:45–72.  https://doi.org/10.1146/annurev.bi.29.070160.000401CrossRefGoogle Scholar
  75. Headon DR, Walsh G (1994) The industrial production of enzymes. Biotechnol Adv 12:635–646.  https://doi.org/10.1016/0734-9750(94)90004-3CrossRefGoogle Scholar
  76. Heimgartner U, Pietrzak M, Geertsen R et al (1990) Purification and partial characterization of milk clotting proteases from flowers of Cynara cardunculus. Phytochemistry 29:1405–1410.  https://doi.org/10.1016/0031-9422(90)80090-4CrossRefGoogle Scholar
  77. Helliwell CA, Chin-Atkins AN, Wilson IW et al (2001) The arabidopsis AMP1 gene encodes a putative glutamate carboxypeptidase. Plant Cell 13:2115–2125CrossRefGoogle Scholar
  78. Hildmann T, Ebneth M, Peña-Cortés H et al (1992) General roles of abscisic and jasmonic acids in gene activation as a result of mechanical wounding. Plant Cell 4:1157–1170.  https://doi.org/10.1105/tpc.4.9.1157CrossRefGoogle Scholar
  79. Hiraiwa N, Kondo M, Nishimura M, Hara-Nishimura I (1997) An aspartic endopeptidase is involved in the breakdown of propeptides of storage proteins in protein-storage vacuoles of plants. Eur J Biochem 246:133–141.  https://doi.org/10.1111/j.1432-1033.1997.00133.xCrossRefGoogle Scholar
  80. Huang T-K, McDonald KA (2009) Bioreactor engineering for recombinant protein production in plant cell suspension cultures. Biochem Eng J 45:168–184.  https://doi.org/10.1016/J.BEJ.2009.02.008CrossRefGoogle Scholar
  81. Huffaker R (1990) Proteolytic activity during senescence of plants. New Phytol 116:199–231.  https://doi.org/10.1111/j.1469-8137.1990.tb04710.xCrossRefGoogle Scholar
  82. Jang M-H, Kim H, Shin M-C et al (2002) Administration of folium mori extract decreases nitric oxide synthase expression in the hypothalamus of streptozotocin-induced diabetic rats. Jpn J Pharmacol 90:189–192.  https://doi.org/10.1254/jjp.90.189CrossRefGoogle Scholar
  83. Kaneda M, Tominaga N (1975) J Biochem 78:1287–1296CrossRefGoogle Scholar
  84. Kelly GS (1996) Bromelain: a literature review and discussion of its therapeutic applications. Altern Med Rev 11:243–257Google Scholar
  85. Kervinen J, Tobin GJ, Costa J et al (1999) Crystal structure of plant aspartic proteinase prophytepsin: inactivation and vacuolar targeting. EMBO J 18:3947–3955.  https://doi.org/10.1093/emboj/18.14.3947CrossRefGoogle Scholar
  86. Kim K-M, Kim MY, Yun PY et al (2007) Production of multiple shoots and plant regeneration from leaf segments of fig tree (Ficus carica L.). J Plant Biol 50:440–446.  https://doi.org/10.1007/BF03030680CrossRefGoogle Scholar
  87. Kleef R, Delohery TM, Bovbjerg DH (1996) Selective modulation of cell adhesion molecules on lymphocytes by bromelain protease 5. Pathobiology 64:339–346.  https://doi.org/10.1159/000164070CrossRefGoogle Scholar
  88. La Valle JB, Krinsky DL, Hawkins EB (2000) Natural therapeutics pocket guide, 2nd edn. Lexi-Comp, HudsonGoogle Scholar
  89. Laplaze L, Ribeiro A, Franche C et al (2000) Characterization of a Casuarina glauca nodule-specific subtilisin-like protease gene, a homolog of Alnus glutinosa ag12. Mol Plant-Microbe Interact 13:113–117.  https://doi.org/10.1094/MPMI.2000.13.1.113CrossRefGoogle Scholar
  90. Lawrie R (1985) Meat science. Pergamon, LondonGoogle Scholar
  91. Lee KL, Albee KL, Bernasconi RJ, Edmunds T (1997) Complete amino acid sequence of ananain and a comparison with stem bromelain and other plant cysteine proteases. Biochem J 327(Pt 1):199–202CrossRefGoogle Scholar
  92. Leipner J, Iten F, Saller R (2001) Therapy with proteolytic enzymes in rheumatic disorders. BioDrugs 15:779–789CrossRefGoogle Scholar
  93. Lindholm P, Kuittinen T, Sorri O et al (2000) Glycosylation of phytepsin and expression of dad1, dad2 and ost1 during onset of cell death in germinating barley scutella. Mech Dev 93:169–173.  https://doi.org/10.1016/S0925-4773(00)00254-9CrossRefGoogle Scholar
  94. Liu Y, Dammann C, Bhattacharyya MK (2001) The matrix metalloproteinase gene GmMMP2 is activated in response to pathogenic infections in soybean. Plant Physiol 127:1788–1797CrossRefGoogle Scholar
  95. López LMI, Sequeiros C, Natalucci CL et al (2000) Purification and Characterization of Macrodontain I, a Cysteine Peptidase from Unripe Fruits of Pseudananas macrodontes (Morr.) Harms (Bromeliaceae). Protein Expr Purif 18:133–140.  https://doi.org/10.1006/prep.1999.1165CrossRefGoogle Scholar
  96. Losada Cosmes E (1999) Importancia de las enzimas en el asma ocupacional. http://www.alergoaragon.org/1999/tercera2.html. Accessed 1 Jun 2018
  97. Lotti T, Mirone V, Imbimbo C et al (1993) Controlled clinical studies of nimesulide in the treatment of urogenital inflammation. Drugs 46(Suppl 1):144–146CrossRefGoogle Scholar
  98. Maidment JM, Moore D, Murphy GP et al (1999) Matrix metalloproteinase homologues from Arabidopsis thaliana. Expression and activity. J Biol Chem 274:34706–34710.  https://doi.org/10.1074/JBC.274.49.34706CrossRefGoogle Scholar
  99. Mandal MK, Fischer R, Schillberg S, Schiermeyer A (2010) Biochemical properties of the matrix metalloproteinase NtMMP1 from Nicotiana tabacum cv. BY-2 suspension cells. Planta 232:899–910.  https://doi.org/10.1007/s00425-010-1221-yCrossRefGoogle Scholar
  100. Massova I, Kotra LP, Fridman R, Mobashery S (1998) Matrix metalloproteinases: structures, evolution, and diversification. FASEB J 12:1075–1095.  https://doi.org/10.1096/fasebj.12.12.1075CrossRefGoogle Scholar
  101. McGeehan G, Burkhart W, Anderegg R et al (1992) Sequencing and characterization of the soybean leaf metalloproteinase: structural and functional similarity to the matrix metalloproteinase family. Plant Physiol 99:1179–1183.  https://doi.org/10.1104/PP.99.3.1179CrossRefGoogle Scholar
  102. Meichtry J, Amrhein N, Schaller A (1999) Characterization of the subtilase gene family in tomato (Lycopersicon esculentum Mill.). Plant Mol Biol 39:749–760.  https://doi.org/10.1023/A:1006193414434CrossRefGoogle Scholar
  103. Melis GB (1990) Clinical experience with methoxybutropate vs. bromelin in the treatment of female pelvic inflammation. Minerva Ginecol 42:309–312Google Scholar
  104. Mello VJ, Gomes MTR, Lemos FO et al (2008) The gastric ulcer protective and healing role of cysteine proteinases from Carica candamarcensis. Phytomedicine 15:237–244.  https://doi.org/10.1016/J.PHYMED.2007.06.004CrossRefGoogle Scholar
  105. Mendieta JR, Pagano MR, Muñoz FF et al (2006) Antimicrobial activity of potato aspartic proteases (StAPs) involves membrane permeabilization. Microbiology 152:2039–2047.  https://doi.org/10.1099/mic.0.28816-0CrossRefGoogle Scholar
  106. Michalek M, Leippe M (2015) Mechanistic insights into the lipid interaction of an ancient saposin-like protein. Biochemistry 54:1778–1786.  https://doi.org/10.1021/acs.biochem.5b00094CrossRefGoogle Scholar
  107. Miller A (1982) Improved sausage casing. US patent 3(666) 844Google Scholar
  108. Munford RS, Sheppard PO, O’Hara PJ (1995) Saposin-like proteins (SAPLIP) carry out diverse functions on a common backbone structure. J Lipid Res 36:1653–1663Google Scholar
  109. Muñoz FF, Mendieta JR, Pagano MR et al (2010) The swaposin-like domain of potato aspartic protease (StAsp-PSI) exerts antimicrobial activity on plant and human pathogens. Peptides 31:777–785.  https://doi.org/10.1016/J.PEPTIDES.2010.02.001CrossRefGoogle Scholar
  110. Mutlu A, Chen X, Reddy SM, Gal S (1999) The aspartic proteinase is expressed in Arabidopsis thaliana seeds and localized in the protein bodies. Seed Sci Res 9:75–84.  https://doi.org/10.1017/S0960258599000082CrossRefGoogle Scholar
  111. Nomura T (1999) The chemistry and biosynthesis of isoprenylated flavonoids from moraceous plants. Pure Appl Chem 71:1115–1118.  https://doi.org/10.1351/pac199971061115CrossRefGoogle Scholar
  112. O’Brien JS, Kishimoto Y (1991) Saposin proteins: structure, function, and role in human lysosomal storage disorders. FASEB J 5:301–308.  https://doi.org/10.1096/FASEBJ.5.3.2001789CrossRefGoogle Scholar
  113. Otsuki N, Dang NH, Kumagai E et al (2010) Aqueous extract of Carica papaya leaves exhibits anti-tumor activity and immunomodulatory effects. J Ethnopharmacol 127:760–767.  https://doi.org/10.1016/J.JEP.2009.11.024CrossRefGoogle Scholar
  114. Pak JH, Liu CY, Huangpu J, Graham JS (1997) Construction and characterization of the soybean leaf metalloproteinase cDNA 1. FEBS Lett 404:283–288.  https://doi.org/10.1016/S0014-5793(97)00141-5CrossRefGoogle Scholar
  115. Panavas T, Pikula A, Reid PD et al (1999) Identification of senescence-associated genes from daylily petals. Plant Mol Biol 40:237–248.  https://doi.org/10.1023/A:1006146230602CrossRefGoogle Scholar
  116. Pardo M, López LMI, Canals F et al (2000) Purification of balansain I, an endopeptidase from unripe fruits of Bromelia balansae Mez (Bromeliaceae). J Agric Food Chem 48:3795–3800.  https://doi.org/10.1021/JF0002488CrossRefGoogle Scholar
  117. Pautot V, Holzer FM, Reisch B, Walling LL (1993) Leucine aminopeptidase: an inducible component of the defense response in Lycopersicon esculentum (tomato). Proc Natl Acad Sci U S A 90:9906–9910.  https://doi.org/10.1073/PNAS.90.21.9906CrossRefGoogle Scholar
  118. Pautot V, Holzer FM, Chaufaux J, Walling LL (2001) The induction of tomato leucine aminopeptidase genes (LapA) after Pseudomonas syringae pv. tomato infection is primarily a wound response triggered by coronatine. Mol Plant-Microbe Interact 14:214–224.  https://doi.org/10.1094/MPMI.2001.14.2.214CrossRefGoogle Scholar
  119. Planta RJ, Calixto F, Pais MS (2000) Production by yeast of aspartic proteinases from plant origin with sheep’s, cow’s, goat’s milk, etc. clotting and proteolytic activity. Patent EP1196542 (WO0075283), Lisboa, PortugalGoogle Scholar
  120. Polanowski A, Wilusz T, Kolaczkowska M, Wieczorek M, Wilimowska-Pelc A (1985) Purification and characterization of aspartic proteinases from Cucumis sativus and Cucurbita maxima seeds. In: Kostka V (ed) Aspartic proteinases and their inhibitors. Walter de Gruyter, New York, pp 49–52Google Scholar
  121. Popovič T, Puizdar V, Brzin J (2002) A novel subtilase from common bean leaves. FEBS Lett 530:163–168.  https://doi.org/10.1016/S0014-5793(02)03453-1CrossRefGoogle Scholar
  122. Priolo N, del Valle SM, Arribére MC et al (2000) Isolation and characterization of a cysteine protease from the latex of Araujia hortorum fruits. J Protein Chem 19:39–49.  https://doi.org/10.1023/A:1007042825783CrossRefGoogle Scholar
  123. Puente XS, Sánchez LM, Overall CM, López-Otín C (2003) Human and mouse proteases: a comparative genomic approach. Nat Rev Genet 4:544–558.  https://doi.org/10.1038/nrg1111CrossRefGoogle Scholar
  124. Radlowski M, Kalinowski A, Adamczyk J et al (1996) Proteolytic activity in the maize pollen wall. Physiol Plant 98:172–178.  https://doi.org/10.1111/j.1399-3054.1996.tb00689.xCrossRefGoogle Scholar
  125. Ragster LV, Chrispeels MJ (1979) Azocoll-digesting proteinases in soybean leaves: characteristics and changes during leaf maturation and senescence. Plant Physiol 64:857–862.  https://doi.org/10.1104/PP.64.5.857CrossRefGoogle Scholar
  126. Ramalho-Santos M, Veríssimo P, Faro C, Pires E (1996) Action on bovine αs1-casein of cardosins A and B, aspartic proteinases from the flowers of the cardoon Cynara cardunculus L. Biochim Biophys Acta 1297:83–89.  https://doi.org/10.1016/0167-4838(96)00103-3CrossRefGoogle Scholar
  127. Ramalho-Santos M, Pissarra J, Veríssimo P et al (1997) Cardosin A, an abundant aspartic proteinase, accumulates in protein storage vacuoles in the stigmatic papillae of Cynara cardunculus L. Planta 203:204–212.  https://doi.org/10.1007/s004250050183CrossRefGoogle Scholar
  128. Rao MB, Tanksale AM, Ghatge MS, Deshpande VV (1998) Molecular and biotechnological aspects of microbial proteases. Microbiol Mol Biol Rev 62:597–635Google Scholar
  129. Ratnaparkhe SM, Egertsdotter EMU, Flinn BS (2009) Identification and characterization of a matrix metalloproteinase (Pta1-MMP) expressed during Loblolly pine (Pinus taeda) seed development, germination completion, and early seedling establishment. Planta 230:339–354.  https://doi.org/10.1007/s00425-009-0949-8CrossRefGoogle Scholar
  130. Rawlings ND, Barrett AJ (1994) Families of serine peptidases. Methods Enzymol 244:19–61.  https://doi.org/10.1016/0076-6879(94)44004-2CrossRefGoogle Scholar
  131. Rawlings ND, Salvesen G (2013) Handbook of proteolytic enzymes, 3rd edn. Academic, CambridgeGoogle Scholar
  132. Rawlings ND, Barrett AJ, Bateman A (2010) MEROPS: the peptidase database. Nucleic Acids Res 38:D227–D233.  https://doi.org/10.1093/nar/gkp971CrossRefGoogle Scholar
  133. Rawlings ND, Waller M, Barrett AJ, Bateman A (2014) MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 42:D503–D509.  https://doi.org/10.1093/nar/gkt953CrossRefGoogle Scholar
  134. Reis PJM, Malcata FX (2011) Current state of Portuguese dairy products from ovine and caprine milks. Small Rumin Res 101:122–133.  https://doi.org/10.1016/j.smallrumres.2011.09.032CrossRefGoogle Scholar
  135. Ribeiro A, Akkermans AD, van Kammen A et al (1995) A nodule-specific gene encoding a subtilisin-like protease is expressed in early stages of actinorhizal nodule development. Plant Cell 7:785–794.  https://doi.org/10.1105/TPC.7.6.785CrossRefGoogle Scholar
  136. Rodrigo I, Vera P, Conejero V (1989) Degradation of tomato pathogenesis-related proteins by an endogenous 37-kDa aspartyl endoproteinase. Eur J Biochem 184:663–669.  https://doi.org/10.1111/j.1432-1033.1989.tb15064.xCrossRefGoogle Scholar
  137. Rodrigo I, Vera P, Van Loon LC, Conejero V (1991) Degradation of tobacco pathogenesis-related proteins: evidence for conserved mechanisms of degradation of pathogenesis-related proteins in plants. Plant Physiol 95:616–622.  https://doi.org/10.1104/PP.95.2.616CrossRefGoogle Scholar
  138. Roseiro LB, Andrew Wilbey R, Barbosa M (2003a) Serpa Cheese: technological, biochemical and microbiological characterisation of a PDO ewe’s milk cheese coagulated with Cynara cardunculus L. Lait 83:469–481.  https://doi.org/10.1051/lait:2003026CrossRefGoogle Scholar
  139. Roseiro LB, Barbosa M, Ames JM, Wilbey RA (2003b) Cheesemaking with vegetable coagulants-the use of Cynara L. for the production of ovine milk cheeses. Int J Dairy Technol 56:76–85.  https://doi.org/10.1046/j.1471-0307.2003.00080.xCrossRefGoogle Scholar
  140. Rowan AD, Buttle DJ, Barrett AJ (1990) The cysteine proteinases of the pineapple plant. Biochem J 266:869–875Google Scholar
  141. Rudenskaya GN, Bogdanova EA, Revina LP et al (1995) Macluralisin - a serine proteinase from fruits of Maclura pomifera (Raf.) Schneid. Planta 196:174–179.  https://doi.org/10.1007/BF00193231CrossRefGoogle Scholar
  142. Rudenskaya GN, Bogacheva AM, Preusser A et al (1998) Taraxalisin - a serine proteinase from dandelion Taraxacum officinale Webb s.l. FEBS Lett 437:237–240.  https://doi.org/10.1016/S0014-5793(98)01243-5CrossRefGoogle Scholar
  143. Runeberg-Roos P, Törmakängas K, Östman A (1991) Primary structure of a barley-grain aspartic proteinase. A plant aspartic proteinase resembling mammalian cathepsin D. Eur J Biochem 202:1021–1027.  https://doi.org/10.1111/j.1432-1033.1991.tb16465.xCrossRefGoogle Scholar
  144. Runeberg-Roos P, Kervinen J, Kovaleva V et al (1994) The aspartic proteinase of barley is a vacuolar enzyme that processes probarley lectin in vitro. Plant Physiol 105:321–329.  https://doi.org/10.1104/PP.105.1.321CrossRefGoogle Scholar
  145. Sabalza M, Christou P, Capell T (2014) Recombinant plant-derived pharmaceutical proteins: current technical and economic bottlenecks. Biotechnol Lett 36:2367–2379.  https://doi.org/10.1007/s10529-014-1621-3CrossRefGoogle Scholar
  146. Sakamoto W, Tamura T, Hanba-Tomita Y et al (2002) The VAR1 locus of Arabidopsis encodes a chloroplastic FtsH and is responsible for leaf variegation in the mutant alleles. Genes Cells 7:769–780.  https://doi.org/10.1046/j.1365-2443.2002.00558.xCrossRefGoogle Scholar
  147. Salas CE, Gomes MTR, Hernandez M, Lopes MTP (2008) Plant cysteine proteinases: evaluation of the pharmacological activity. Phytochemistry 69:2263–2269.  https://doi.org/10.1016/J.PHYTOCHEM.2008.05.016CrossRefGoogle Scholar
  148. Sampaio PN, Fortes AM, Cabral JMS et al (2008) Production and characterization of recombinant cyprosin B in Saccharomyces cerevisiae (W303-1A) strain. J Biosci Bioeng 105:305–312.  https://doi.org/10.1263/JBB.105.305CrossRefGoogle Scholar
  149. Sanchez-Moran E, Jones GH, Franklin FCH, Santos JL (2004) A puromycin-sensitive aminopeptidase is essential for meiosis in Arabidopsis thaliana. Plant Cell Online 16:2895–2909.  https://doi.org/10.1105/tpc.104.024992CrossRefGoogle Scholar
  150. Sarkkinen P, Kalkkinen N, Tilgmann C et al (1992) Aspartic proteinase from barley grains is related to mammalian lysosomal cathepsin D. Planta 186:317–323.  https://doi.org/10.1007/BF00195311CrossRefGoogle Scholar
  151. Schall VT, Vasconcellos MC, Rocha RS et al (2001) The control of the schistosome-transmitting snail Biomphalaria glabrata by the plant Molluscicide Euphorbia splendens var. hislopii (syn milli Des. Moul): a longitudinal field study in an endemic area in Brazil. Acta Trop 79:165–170.  https://doi.org/10.1016/S0001-706X(01)00126-7CrossRefGoogle Scholar
  152. Schaller A (2004) A cut above the rest: the regulatory function of plant proteases. Planta 220:183–197.  https://doi.org/10.1007/s00425-004-1407-2CrossRefGoogle Scholar
  153. Schaller A, Bergey DR, Ryan CA (1995) Induction of wound response genes in tomato leaves by bestatin, an inhibitor of aminopeptidases. Plant Cell 7:1893–1898.  https://doi.org/10.1105/tpc.7.11.1893CrossRefGoogle Scholar
  154. Schiermeyer A, Hartenstein H, Mandal MK et al (2009) A membrane-bound matrix metalloproteinase from Nicotiana tabacum cv. BY-2 is induced by bacterial pathogens. BMC Plant Biol 9:83.  https://doi.org/10.1186/1471-2229-9-83CrossRefGoogle Scholar
  155. Seker S, Beyenal H, Tanyolac A (1999) Modeling milk clotting activity in the continuous production of microbial rennet from Mucor miehei. J Food Sci 64:525–529.  https://doi.org/10.1111/j.1365-2621.1999.tb15076.xCrossRefGoogle Scholar
  156. Silva SV, Malcata FX (1999) On the activity and specificity of cardosin B, a plant proteinase, on ovine caseins. Food Chem 67:373–378.  https://doi.org/10.1016/S0308-8146(99)00126-0CrossRefGoogle Scholar
  157. Silva SV, Malcata FX (2000) Action of cardosin A from Cynara humilis on ovine and caprine caseinates. J Dairy Res 67:449–454CrossRefGoogle Scholar
  158. Silva SV, Malcata FX (2005) Partial identification of water-soluble peptides released at early stages of proteolysis in sterilized ovine cheese-like systems: influence of type of coagulant and starter. J Dairy Sci 88:1947–1954.  https://doi.org/10.3168/jds.S0022-0302(05)72870-8CrossRefGoogle Scholar
  159. Silva SV, Xavier Malcata F (1998) Proteolysis of ovine caseins by cardosin A, an aspartic acid proteinase from Cynara cardunculus L. Lait 78:513–519.  https://doi.org/10.1051/lait:1998548CrossRefGoogle Scholar
  160. Silva SV, Allmere T, Xavier Malcata F, Andrén A (2003) Comparative studies on the gelling properties of cardosins extracted from Cynara cardunculus and chymosin on cow’s skim milk. Int Dairy J 13:559–564.  https://doi.org/10.1016/S0958-6946(03)00075-XCrossRefGoogle Scholar
  161. Simões I, Faro C (2004) Structure and function of plant aspartic proteinases. Eur J Biochem 271:2067–2075.  https://doi.org/10.1111/j.1432-1033.2004.04136.xCrossRefGoogle Scholar
  162. Singh VK, Patel AK, Moir AJ, Jagannadham MV (2008) Indicain, a dimeric serine protease from Morus indica cv. K2. Phytochemistry 69:2110–2119.  https://doi.org/10.1016/J.PHYTOCHEM.2008.05.005CrossRefGoogle Scholar
  163. Sjögren LLE, Stanne TM, Zheng B et al (2006) Structural and functional insights into the chloroplast ATP-dependent Clp protease in arabidopsis. Plant Cell Online 18:2635–2649.  https://doi.org/10.1105/tpc.106.044594CrossRefGoogle Scholar
  164. Sousa M, Malcata F (1997) Comparison of plant and animal rennets in terms of microbiological, chemical, and proteolysis characteristics of ovine cheese. J Agric Food Chem 45:74–81.  https://doi.org/10.1021/JF9506601CrossRefGoogle Scholar
  165. Sousa MJ, Malcata FX (1998) Proteolysis of ovine and caprine caseins in solution by enzymatic extracts from flowers of cynara cardunculus. Enzym Microb Technol 22:305–314.  https://doi.org/10.1016/S0141-0229(97)00173-7CrossRefGoogle Scholar
  166. Sousa M, Malcata F (2002) Advances in the role of a plant coagulant (Cynara cardunculus) in vitro and during ripening of cheeses from several milk species. Lait 82:151–170.  https://doi.org/10.1051/lait:2002001CrossRefGoogle Scholar
  167. Souza CAM, de-Carvalho RR, Kuriyama SN et al (1997) Study of the embryofeto-toxicity of Crown-of-Thorns (Euphorbia milii) latex, a natural molluscicide. Braz J Med Biol Res 30:1325–1332.  https://doi.org/10.1590/S0100-879X1997001100011CrossRefGoogle Scholar
  168. St. Angelo AJ, Ory RL, Hansen HJ (1969) Localization of an acid proteinase in hempseed. Phytochemistry 8:1135–1138.  https://doi.org/10.1016/S0031-9422(00)85547-8CrossRefGoogle Scholar
  169. St. Angelo AJ, Ory RL, Hansen HJ (1970) Properties of a purified proteinase from hempseed. Phytochemistry 9:1933–1938.  https://doi.org/10.1016/S0031-9422(00)85342-XCrossRefGoogle Scholar
  170. Stenger S, Hanson DA, Teitelbaum R et al (1998) An antimicrobial activity of cytolytic T cells mediated by granulysin. Science 282:121–125.  https://doi.org/10.1126/SCIENCE.282.5386.121CrossRefGoogle Scholar
  171. Sutoh K, Kato H, Minamikawa T (1999) Identification and possible roles of three types of endopeptidase from germinated wheat Seeds. J Biochem 126:700–707.  https://doi.org/10.1093/oxfordjournals.jbchem.a022506CrossRefGoogle Scholar
  172. Takahashi K, Matsumoto K, Nishii W, Muramatsu M, Kubota K, Shibata C, Athauda SBP (2009) Comparative studies on the acid proteinase activities in the digestive fluids of Nepenthes, Cephalotus, Dionaea, and Drosera. Carniv Plant Newsl 38:75–82Google Scholar
  173. Takeda N, Kistner C, Kosuta S et al (2007) Proteases in plant root symbiosis. Phytochemistry 68:111–121.  https://doi.org/10.1016/J.PHYTOCHEM.2006.09.022CrossRefGoogle Scholar
  174. Tan-Wilson AL, Liu X, Chen R et al (1996) An acidic amino acid-specific protease from germinating soybeans. Phytochemistry 42:313–319.  https://doi.org/10.1016/0031-9422(95)00896-9CrossRefGoogle Scholar
  175. Targoni OS, Tary-Lehmann M, Lehmann PV (1999) Prevention of murine EAE by oral hydrolytic enzyme treatment. J Autoimmun 12:191–198.  https://doi.org/10.1006/JAUT.1999.0271CrossRefGoogle Scholar
  176. Taylor AA, Horsch A, Rzepczyk A et al (1997) Maturation and secretion of a serine proteinase is associated with events of late microsporogenesis. Plant J 12:1261–1271.  https://doi.org/10.1046/j.1365-313x.1997.12061261.xCrossRefGoogle Scholar
  177. Tökés ZA, Woon WC, Chambers SM (1974) Digestive enzymes secreted by the carnivorous plant Nepenthes macferlanei L. Planta 119:39–46.  https://doi.org/10.1007/BF00390820CrossRefGoogle Scholar
  178. Törmäkangas K, Hadlington JL, Pimpl P et al (2001) A vacuolar sorting domain may also influence the way in which proteins leave the endoplasmic reticulum. Plant Cell 13:2021–2032CrossRefGoogle Scholar
  179. Tornero P, Conejero V, Vera P (1997) Identification of a new pathogen-induced member of the subtilisin-like processing protease family from plants. J Biol Chem 272:14412–14419.  https://doi.org/10.1074/JBC.272.22.14412CrossRefGoogle Scholar
  180. Uchikoba T, Horita H, Kaneda M (1990) Proteases from the sarcocarp of yellow snake-gourd. Phytochemistry 29:1879–1881.  https://doi.org/10.1016/0031-9422(90)85032-BCrossRefGoogle Scholar
  181. Uchikoba T, Hosoyamada S, Onjyo M et al (2001) A serine endopeptidase from the fruits of Melothria japonica (Thunb.) Maxim. Phytochemistry 57:1–5.  https://doi.org/10.1016/S0031-9422(00)00511-2CrossRefGoogle Scholar
  182. Uhlig H, Linsmaier-Bednar EM (1998) Industrial enzymes and their applications. Wiley, New YorkGoogle Scholar
  183. Vaccaro AM, Salvioli R, Tatti M, Ciaffoni F (1999) Saposins and their interaction with lipids. Neurochem Res 24:307–314.  https://doi.org/10.1023/A:1022530508763CrossRefGoogle Scholar
  184. Varshavsky A (1996) The N-end rule: functions, mysteries, uses. Proc Natl Acad Sci U S A 93:12142–12149.  https://doi.org/10.1073/PNAS.93.22.12142CrossRefGoogle Scholar
  185. Verissimo P, Faro C, Moir AJG et al (1996) Purification, characterization and partial amino acid sequencing of two new aspartic proteinases from fresh flowers of Cynara cardunculus L. Eur J Biochem 235:762–768.  https://doi.org/10.1111/j.1432-1033.1996.00762.xCrossRefGoogle Scholar
  186. Vincent JL, Brewin NJ (2000) Immunolocalization of a cysteine protease in vacuoles, vesicles, and symbiosomes of pea nodule cells. Plant Physiol 123:521–530CrossRefGoogle Scholar
  187. Vioque M, Gómez R, Sánchez E et al (2000) Chemical and microbiological characteristics of ewes’ milk cheese manufactured with extracts from flowers of Cynara cardunculus and Cynara humilis as coagulants. J Agric Food Chem 48:451–456CrossRefGoogle Scholar
  188. White PC, Cordeiro MC, Arnold D et al (1999) Processing, activity, and inhibition of recombinant cyprosin, an aspartic proteinase from cardoon (Cynara cardunculus). J Biol Chem 274:16685–16693.  https://doi.org/10.1074/JBC.274.24.16685CrossRefGoogle Scholar
  189. Whitehurst RJ, van Oort M (2009) Enzymes in food technology. Wiley-Blackwell, OxfordCrossRefGoogle Scholar
  190. Yadav SC, Pande M, Jagannadham MV (2006) Highly stable glycosylated serine protease from the medicinal plant Euphorbia milii. Phytochemistry 67:1414–1426.  https://doi.org/10.1016/J.PHYTOCHEM.2006.06.002CrossRefGoogle Scholar
  191. Yamagata H, Masuzawa T, Nagaoka Y et al (1994) Cucumisin, a serine protease from melon fruits, shares structural homology with subtilisin and is generated from a large precursor. J Biol Chem 269:32725–32731Google Scholar
  192. Ye Z-H, Varner JE (1996) Induction of cysteine and serine proteases during xylogenesis in Zinnia elegans. Plant Mol Biol 30:1233–1246.  https://doi.org/10.1007/BF00019555CrossRefGoogle Scholar
  193. Zasloff M (2002) Antimicrobial peptides of multicellular organisms. Nature 415:389–395.  https://doi.org/10.1038/415389aCrossRefGoogle Scholar
  194. Zhao C, Johnson BJ, Kositsup B, Beers EP (2000) Exploiting secondary growth in Arabidopsis. Construction of xylem and bark cDNA libraries and cloning of three xylem endopeptidases. Plant Physiol 123:1185–1196CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Biological Research Institute, National Council of Scientific and Technique Research (CONICET)University of Mar del Plata (UNMDP)Mar del PlataArgentina
  2. 2.Scientific Research Commission of the Province of Buenos Aires (CIC)Buenos AiresArgentina

Personalised recommendations