, Volume 249, Issue 5, pp 1503–1519 | Cite as

Gene expression and spatiotemporal localization of antifungal chitin-binding proteins during Moringa oleifera seed development and germination

  • Tarcymara B. Garcia
  • Arlete A. Soares
  • Jose H. Costa
  • Helen P. S. Costa
  • João X. S. Neto
  • Lady Clarissa B. Rocha-Bezerra
  • Fredy Davi A. Silva
  • Mariana R. Arantes
  • Daniele O. B. Sousa
  • Ilka M. VasconcelosEmail author
  • Jose T. A. OliveiraEmail author
Original Article


Main conclusion

Chitin-binding proteins behave as storage and antifungal proteins in the seeds of Moringa oleifera.

Moringa oleifera is a tropical multipurpose tree. Its seed constituents possess coagulant, bactericidal, fungicidal, and insecticidal properties. Some of these properties are attributed to a group of polypeptides denominated M. oleifera chitin-binding proteins (in short, Mo-CBPs). Within this group, Mo-CBP2, Mo-CBP3, and Mo-CBP4 were previously purified to homogeneity. They showed high amino acid similarity with the 2S albumin storage proteins. These proteins also presented antimicrobial activity against human pathogenic yeast and phytopathogenic fungi. In the present study, the localization and expression of genes that encode Mo-CBPs and the biosynthesis and degradation of the corresponding proteins during morphogenesis and maturation of M. oleifera seeds at 15, 30, 60, and 90 days after anthesis (DAA) and germination, respectively, were assessed. The Mo-CBP transcripts and corresponding proteins were not detected at 15 and 30 days after anthesis (DAA). However, they accumulated at the latter stages of seed maturation (60 and 90 DAA), reaching the maximum level at 60 DAA. The degradation kinetics of Mo-CBPs during seed germination by in situ immunolocalization revealed a reduction in the protein content 48 h after sowing (HAS). Moreover, Mo-CBPs isolated from seeds at 60 and 90 DAA prevented the spore germination of Fusarium spp. Taken together, these results suggest that Mo-CBPs play a dual role as storage and defense proteins in the seeds of M. oleifera.


Drumstick seed Mo-CBPs 2S albumin Biosynthesis Degradation Antifungal activity 



This work was supported by the Coordination for the Improvement of Higher Education Personnel (CAPES, Brazilian Ministry of Education, Process Number: 306202/2017-4, grant number 1280942/2014-2018); the CAPES - Toxinology Project, Process Number: 431511/2016-0; and the Brazilian National Council for Scientific and Technological Development (CNPq, Process number: 306202/2017-4). We are also grateful to the Central Analytical facilities of the Federal University of Ceara, Brazil, for the scanning electron micrograph (SEM) analysis.

Compliance with ethical standards

Conflict of interest

The authors hereby declare no conflicts of interest.


  1. Agizzio AP, Da Cunha M, Carvalho AO, Oliveira MA, Ribeiro SFF, Gomes VM (2006) The antifungal properties of a 2S albumin-homologous protein from passion fruit seeds involve plasma membrane permeabilization and ultrastructural alterations in yeast cells. Plant Sci 171:515–522. CrossRefPubMedGoogle Scholar
  2. Agrawal GK, Thelen JJ (2006) Large scale identification and quantitative profiling of phosphoproteins expressed during seed filling in oilseed rape. Mol Cell Proteomics 5:2044–2059. CrossRefPubMedGoogle Scholar
  3. Ahn YJ, Chen GQ (2007) Temporal and spatial expression of 2S albumin in castor (Ricinus communis L.). J Agric Food Chem 55:10043–10049. CrossRefPubMedGoogle Scholar
  4. Al-Asmari AK, Albalawi SM, Athar MT, Khan AQ, Al-Shahrani H, Islam M (2015) Moringa oleifera as an anti-cancer agent against breast and colorectal cancer cell lines. PLoS One 10:e0135814. CrossRefPubMedPubMedCentralGoogle Scholar
  5. Ali NF, El-Mohamedy RSR (2016) Evaluation of Moringa oleifera seed extract coagulation in removal of some dyes in textile wastewater. Int J ChemTech Res 9:538–545Google Scholar
  6. Al-Malki AL, El Rabey HA (2015) The antidiabetic effect of low doses of Moringa oleifera Lam. seeds on streptozotocin induced diabetes and diabetic nephropathy in male rats. Biomed Res Int 2015:381040. CrossRefPubMedPubMedCentralGoogle Scholar
  7. Araújo LCC, Aguiar JS, Napoleão TH, Mota FVB, Barros ALS, Moura MC, Coriolano MC, Coelho LCBB, Silva TG, Paiva PMG (2013) Evaluation of cytotoxic and anti-inflammatory activities of extracts and lectins from Moringa oleifera seeds. PLoS One 8:e81973. CrossRefPubMedPubMedCentralGoogle Scholar
  8. Batista AB, Oliveira JTA, Gifoni JM, Pereira ML, Almeida MGG, Gomes VM, Da Cunha M, Ribeiro SFF, Dias GB, Beltramini LM, Lopes JLS, Grangeiro TB, Vasconcelos IM (2014) New insights into the structure and mode of action of Mo-CBP3, an antifungal chitin-binding protein of Moringa oleifera seeds. PLoS One 9:e111427. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Baud S, Dubreucq B, Miquel M, Rochat C, Lepiniec L (2008) Storage reserve accumulation in Arabidopsis: metabolic and developmental control of seed filling. Arabidopsis Book 6:e0113. CrossRefPubMedPubMedCentralGoogle Scholar
  10. Becker-Ritt AB, Carlini CR (2012) Fungitoxic and insecticidal plant polypeptides. Biopolymers 98:367–384. CrossRefPubMedGoogle Scholar
  11. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. CrossRefPubMedGoogle Scholar
  12. Brilhante RSN, Sales JA, Pereira VS, Castelo-Branco DSCM, Cordeiro RA, Sampaio CM, Paiva MAN, Santos JBFD, Sidrim JJC, Rocha MFG (2017) Research advances on the multiple uses of Moringa oleifera: a sustainable alternative for socially neglected population. Asian Pac J Trop Med 10:621–630. CrossRefPubMedGoogle Scholar
  13. Cândido ES, Pinto MFS, Pelegrini PB, Lima TB, Silva ON, Pogue R, Grossi-de-Sá MF, Franco OL (2011) Plant storage proteins with antimicrobial activity: novel insights into plant defense mechanisms. FASEB J 25:3290–3305. CrossRefGoogle Scholar
  14. Chen GQ, He X, Liao LP, Mckeon TA (2004) 2S albumin gene expression in castor plant (Ricinus communis L.). J Am Oil Chem Soc 81:867–872. CrossRefGoogle Scholar
  15. Chen M, Zhang B, Li C, Kulaveerasingam H, Chew FT, Yu H (2015) Transparent TESTA GLABRA 1 regulates the accumulation of seed storage reserves in Arabidopsis. Plant Physiol 169:391–402. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Chuang PH, Lee CW, Chou JY, Murugan M, Shieh BJ, Chen HM (2007) Anti-fungal activity of crude extracts and essential oil of Moringa oleifera Lam. Bioresour Technol 98:232–236. CrossRefPubMedGoogle Scholar
  17. Costa TG, Franco OL, Migliolo L, Dias SC (2015) Identification of a novel 2S albumin with antitryptic activity from Caryocar brasiliense seeds. J Agr Sci 6:197–206. CrossRefGoogle Scholar
  18. Di Berardino J, Marmagne A, Berger A, Yoshimoto K, Cueff G, Chardon F, Masclaux-Daubresse C, Reisdorf-Cren M (2018) Autophagy controls resource allocation and protein storage accumulation in Arabidopsis seeds. J Exp Bot 69:1403–1414. CrossRefPubMedPubMedCentralGoogle Scholar
  19. Duan XH, Jiang R, Wen YJ, Bin JH (2013) Some 2S albumin from peanut seeds exhibits inhibitory activity against Aspergillus flavus. Plant Physiol Biochem 66:84–90. CrossRefPubMedGoogle Scholar
  20. Ferreira PMP, Farias DF, Oliveira JTA, Carvalho AFU (2008) Moringa oleifera: bioactive compounds and nutritional potential. Rev Nutr 21:431–437. CrossRefGoogle Scholar
  21. Fisher DB (1968) Protein staining of ribboned epon sections for light microscopy. Histochemie 16:92–96. CrossRefPubMedGoogle Scholar
  22. Fiume E, Guyon V, Remoué C, Magnani E, Miquel M, Grain D, Lepiniec L (2016) TWS1, a novel small protein, regulates various aspects of seed and plant development. Plant Physiol 172:1732–1745. CrossRefPubMedPubMedCentralGoogle Scholar
  23. Fotouo-M H, Toit ES, Robbertse PJ (2015) Germination and ultrastructural studies of seeds produced by a fast-growing, drought-resistant tree: implications for its domestication and seed storage. AoB Plants 7:plv016. CrossRefPubMedPubMedCentralGoogle Scholar
  24. Freire JEC, Vasconcelos IM, Moreno FBMB, Batista AB, Lobo MDP, Pereira ML, Lima JPMS, Almeida RVM, Sousa AJS, Monteiro-Moreira ACO, Oliveira JTA, Grangeiro TB (2015) Mo-CBP3, an antifungal chitin-binding protein from Moringa oleifera seeds, is a member of the 2S albumin family. PLoS One 10:e0119871. CrossRefPubMedPubMedCentralGoogle Scholar
  25. Gallão MI, Damasceno LF, Brito ES (2006) Chemical and structural evaluation of moringa seeds. Rev Ciênc Agron 37:106–109Google Scholar
  26. Garcia-Casado G, Collada C, Allona I, Casado R, Pacios LF, Aragoncillo C, Gomez L (1998) Site-directed mutagenesis of active site residues in a class I endochitinase from chestnut seeds. Glycobiology 8:1021–1028CrossRefPubMedGoogle Scholar
  27. Gerlach D (1984) Botanische Mikrotechnik: eine Einführung, 3rd edn. Georg Thieme, StuttgartGoogle Scholar
  28. Gifoni JM, Oliveira JTA, Oliveira HD, Batista AB, Pereira ML, Gomes AS, Oliveira HP, Grangeiro TB, Vasconcelos IM (2012) A novel chitin-binding protein from Moringa oleifera seed with potential for plant disease control. Biopolymers 98:406–415. CrossRefPubMedGoogle Scholar
  29. Guerche P, Tire C, Sa FG, Clercq A, Van Montagu M, Krebbers E (1990) Differential expression of the Arabidopsis 2S albumin genes and the effect of increasing gene family size. Plant Cell 2:469–478. CrossRefPubMedPubMedCentralGoogle Scholar
  30. Harboe N, Inglid A (1973) Immunization, isolation of immunoglobulins, estimation of antibody titre. In: Axelsen NH (ed) A manual quantitative immunoelectrophoresis. Blackwell Scientific Publications, London, pp 161–164Google Scholar
  31. Hellemans J, Mortier G, De Paepe A, Speleman F, Vandesompele J (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8:R19. CrossRefPubMedPubMedCentralGoogle Scholar
  32. Huang X, Xie WJ, Gong ZZ (2000) Characteristics and antifungal activity of a chitin binding protein from Ginkgo biloba. FEBS Lett 478:123–126. CrossRefPubMedGoogle Scholar
  33. Iseli B, Boller T, Neuhaus JM (1993) The N-terminal cysteine-rich domain of tobacco class I chitinase is essential for chitin binding but not for catalytic or antifungal activity. Plant Physiol 103:221–226. CrossRefPubMedPubMedCentralGoogle Scholar
  34. Jashni MK, Dols IHM, Iida Y, Boeren S, Beenen HG, Mehrabi R, Collemare J, Wit PJGM (2015) Synergistic action of a metalloprotease and a serine protease from Fusarium oxysporum f. sp. lycopersici cleaves chitin-binding tomato chitinases, reduces their antifungal activity, and enhances fungal virulence. Mol Plant Microbe Interact 28:996–1008. CrossRefPubMedGoogle Scholar
  35. Ji C, Kúc J (1996) Antifungal activity of cucumber β-1,3-glucanase and chitinase. Physiol Mol Plant Pathol 49:257–265. CrossRefGoogle Scholar
  36. Johansen DA (1940) Plant Microtechnique. McGraw-Hill, NewYorkGoogle Scholar
  37. Junqueira CU (1990) O uso de cortes finos de tecidos na Medicina e Biologia. Meios e Métodos 66:167–171Google Scholar
  38. Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27:137–138Google Scholar
  39. Keogh MB, Elmusharaf K, Borde P, Mc Guigan KG (2017) Evaluation of the natural coagulant Moringa oleifera as a pretreatment for SODIS in contaminated turbid water. Sol Energy 158:448–454. CrossRefGoogle Scholar
  40. Kim HT, Choi UK, Ryu HS, Lee SJ, Kwon OS (2011) Mobilization of storage proteins in soybean seed (Glycine max L.) during germination and seedling growth. Biochim Biophys Acta 1814:1178–1187. CrossRefPubMedGoogle Scholar
  41. Kim YJ, Lee HJ, Jang MG, Kwon WS, Kim SY, Yang DC (2014) Cloning and characterization of pathogenesis-related protein 4 gene from Panax ginseng. Russ J Plant Physiol 61:664–671. CrossRefGoogle Scholar
  42. Krügel U, Veenhoff LM, Langbein J, Wiederhold E, Liesche J, Friedrich T, Grimm B, Martinoia E, Poolman B, Kühn C (2008) Transport and sorting of the Solanum tuberosum sucrose transporter SUT1 is affected by posttranslational modification. Plant Cell 20:2497–2513. CrossRefPubMedPubMedCentralGoogle Scholar
  43. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the bacteriophage T4. Nature 227:680–685. CrossRefPubMedGoogle Scholar
  44. Lara P, Oñate-Sánchez L, Abraham Z, Ferrándiz C, Díaz I, Carbonero P, Vicente-Carbajosa J (2003) Synergistic activation of seed storage protein gene expression in Arabidopsis by ABI3 and two bZIPs related to OPAQUE2. J Biol Chem 278:21003–21011. CrossRefPubMedGoogle Scholar
  45. Leone A, Spada A, Battezzati A, Schiraldi A, Aristil J, Bertoli S (2015) Cultivation, genetic, ethnopharmacology, phytochemistry and pharmacology of Moringa oleifera leaves: an overview. Int J Mol Sci 16:12791–12835. CrossRefPubMedPubMedCentralGoogle Scholar
  46. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. CrossRefGoogle Scholar
  47. Lopes TDP (2016). Anti-dermatophyte potential of Mo-CBP4, a chitin binding protein from Moringa oleifera seeds. Dissertation, Federal University of CearaGoogle Scholar
  48. Maria-Neto S, Honorato RV, Costa FT, Almeida RG, Amaro DS, Oliveira JTA, Vasconcelos IM, Franco OL (2011) Bactericidal activity identified in 2S albumin from sesame seeds and in silico studies of structure-function relations. Protein J 30:340–350. CrossRefPubMedGoogle Scholar
  49. Muhl QE, Dtoit ES, Steyn JM (2014) Irrigation amounts affect the compositional changes of Moringa oleifera seeds throughout different developmental stages. Int J Agric Biol 16:201–206Google Scholar
  50. Muhl QE, Toit ES, Steyn JM, Robbertse PJ (2016) The embryo, endosperm and seed coat structure of developing Moringa oleifera seed. South African J Bot 106:60–66. CrossRefGoogle Scholar
  51. Müntz K, Belozersky MA, Dunaevsky YE, Schlereth A, Tiedemann J (2001) Stored proteinases and the initiation of storage protein mobilization in seeds during germination and seedling growth. J Exp Bot 52:1741–1752. CrossRefPubMedGoogle Scholar
  52. Neto JXS, Pereira ML, Oliveira JTA, Rocha-Bezerra LCB, Lopes TDP, Costa HPS, Sousa DOB, Rocha BAM, Grangeiro TB, Freire JEC, Monteiro-Moreira ACO, Lobo MDP, Brilhante RSN, Vasconcelos IM (2017) A chitin-binding protein purified from Moringa oleifera seeds presents anticandidal activity by increasing cell membrane permeability and reactive oxygen species production. Front Microbiol 8:980. CrossRefPubMedPubMedCentralGoogle Scholar
  53. Odintsova TI, Rogozhin EA, Sklyar IV, Musolyamov AK, Kudryavtsev AM, Pukhalsky VA, Smirnov AN, Grishin EV, Egorov TA (2010) Antifungal activity of storage 2S albumins from seeds of the invasive weed dandelion Taraxacum officinale Wigg. Protein Pept Lett 17:522–529. CrossRefPubMedGoogle Scholar
  54. Oguri S, Kamoshida M, Nagata Y, Momonoki YS, Kamimura H (2003) Characterization and sequence of tomato 2S seed albumin: a storage protein with sequence similarities to the fruit lectin. Planta 216:976–984. CrossRefPubMedGoogle Scholar
  55. Oliveira JTA, Silveira SB, Vasconcelos IM, Cavada BS, Moreira RA (1999) Compositional and nutritional attributes of seeds from the multiple purpose tree Moringa oleifera Lamarck. J Sci Food Agric 79:815–820.;2-P CrossRefGoogle Scholar
  56. Oliveira EAP, Zucareli C, Fonseca ICB, Oliveira JC, Barros ASR (2014) Foliar fungicide and environments on the physiological quality of oat seeds. J Seed Sci 36:15–24. CrossRefGoogle Scholar
  57. Ouchterlony O, Nilsson LA (1986) Immunodiffusion and immunoelectrophoresis. In: Weir DM, Herzerberg LA, Blackwell C, Herzerberg LA (eds) Handbook of experimental immunology. Blackwell, Oxford, p 32.1–50Google Scholar
  58. Pandey A, Pradheep K, Gupta R, Nayar ER, Bhandari DC (2011) “Drumstick tree” (Moringa oleifera Lam.): a multipurpose potential species in India. Genet Resour Crop Evol 58:453–460. CrossRefGoogle Scholar
  59. Pavankumar AR, Kayathri R, Murugan NA, Zhang Q, Srivastava V, Okoli C, Bulone V, Rajarao GK, Ågren H (2014) Dimerization of a flocculent protein from Moringa oleifera: experimental evidence and in silico interpretation. J Biomol Struct Dyn 32:406–415. CrossRefPubMedGoogle Scholar
  60. Pelegrini PB, Noronha EF, Muniz MAR, Vasconcelos IM, Chiarello MD, Oliveira JTA, Franco OL (2006) An antifungal peptide from passion fruit (Passiflora edulis) seeds with similarities to 2S albumin proteins. Biochim Biophys Acta 1764:1141–1146. CrossRefPubMedGoogle Scholar
  61. Pereira ML (2014) Structural, pharmacological and toxicological aspects of Mo-CBP4, a Moringa oleifera chitin binding protein with anti-inflammatory and oral antinociceptive activity. Thesis, Federal University of CearaGoogle Scholar
  62. Pereira ML, Oliveira HD, Oliveira JTA, Gifoni JM, Oliveira RO, Sousa DOB, Vasconcelos IM (2011) Purification of a chitin-binding protein from Moringa oleifera seeds with potential to relieve pain and inflammation. Protein Pept Lett 18:1078–1085. CrossRefPubMedGoogle Scholar
  63. Ribeiro SFF, Taveira GB, Carvalho AO, Dias GB, Da Cunha M, Santa-Catarina C, Rodrigues R, Gomes VM (2012) Antifungal and other biological activities of two 2S albumin-homologous proteins against pathogenic fungi. Protein J 31:59–67. CrossRefPubMedGoogle Scholar
  64. Rios FJB, Cavada BS, Medeiros DA, Moreira RA, Vasconcelos IM, Oliveira JTA (1996) Digestibility of plant lectins from Canavalia, Cratylia, Dioclea and Artocarpus genera. In: Van Driessche E, Rougé P, Beeckmans S, Bog-Hansen TC (eds) Lectins: biology, biochemistry, clinical biochemistry. Textop, Denmark, pp 277–284Google Scholar
  65. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: A laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, PlainviewGoogle Scholar
  66. Sharma A, Kumar P, Kesari P, Neetua Katiki M, Mishra M, Singh PK, Gurjar BR, Sharma AK, Tomar S, Kumar P (2017) Purification and characterization of 2S albumin from seeds of Wrightia tinctoria exhibiting antibacterial and DNase activity. Protein Pept Lett 24:368–378. CrossRefPubMedGoogle Scholar
  67. Shebek K, Schantz AB, Sines I, Lauser K, Velegol S, Kumar M (2015) The flocculating cationic polypetide from Moringa oleifera seeds damages bacterial cell membranes by causing membrane fusion. Langmuir 31:4496–4502. CrossRefPubMedGoogle Scholar
  68. Shewry PR, Halford NG (2002) Cereal seed storage proteins: structures, properties and role in grain utilization. J Exp Bot 53:947–958. CrossRefGoogle Scholar
  69. Singh RSG, Negi PS, Radha C (2013) Phenolic composition, antioxidant and antimicrobial activities of free and bound phenolic extracts of Moringa oleifera seed flour. J Funct Foods 5:1883–1891. CrossRefGoogle Scholar
  70. Soares EL, Shah M, Soares AA, Costa JH, Carvalho P, Domont GB, Nogueira FCS, Campos FAP (2014) Proteome analysis of the inner integument from developing Jatropha curcas L. seeds. J Proteome Res 13:3562–3570. CrossRefPubMedGoogle Scholar
  71. Sutar NG, Bonde CG, Patil VV, Narkhede SB, Patil AP, Kakade RT (2008) Analgesic activity of seeds of Moringa oleifera Lam. Int J Green Pharm 2:108–110. CrossRefGoogle Scholar
  72. Tai SSK, Lee TTT, Tsai CCY, Yiu T-J, Tzen JTC (2001) Expression pattern and deposition of three storage proteins, 11S globulin, 2S albumin and 7S globulin in maturing sesame seeds. Plant Physiol Biochem 39:981–992. CrossRefGoogle Scholar
  73. Terras FRG, Schoofs HME, De Bolle MFC, Van Leuven F, Rees SB, Vanderleyden J, Cammue BPA, Broekaert WF (1992) Analysis of two novel classes of plant antifungal proteins from radish (Raphanus sativus L.) seeds. J Biol Chem 267:15301–15309. CrossRefPubMedGoogle Scholar
  74. Terras FRG, Torrekens S, Van Leuven F, Osborn RW, Vanderleyden J, Cammue BPA, Broekaert WF (1993) A new family of basic cysteine-rich plant antifungal proteins from Brassicaceae species. FEBS Lett 316:233–240. CrossRefPubMedGoogle Scholar
  75. Theis T, Stahl U (2004) Antifungal proteins: targets, mechanisms and prospective applications. Cell Mol Life Sci 61:437–455. CrossRefGoogle Scholar
  76. Tomar PPS, Chaudhary NS, Mishra P, Gahloth D, Patel GK, Selvakumar P, Kumar P, Sharma AK (2014a) Purification, characterisation and cloning of a 2S albumin with DNase, RNase and antifungal activities from Putranjiva roxburghii. Appl Biochem Biotechnol 174:471–482. CrossRefPubMedGoogle Scholar
  77. Tomar PPS, Nikhil K, Singh A, Selvakumar P, Roy P, Sharma AK (2014b) Characterization of anticancer, DNase and antifungal activity of pumpkin 2S albumin. Biochem Biophys Res Commun 448:349–354. CrossRefPubMedGoogle Scholar
  78. Ullah A, Mariutti RB, Masood R, Caruso IP, Costa GHG, Freita CM, Santos CR, Zanphorlin LM, Mutton MJR, Murakami MT, Arni RK (2015) Crystal structure of mature 2S albumin from Moringa oleifera seeds. Biochem Biophys Res Commun 468:365–371. CrossRefPubMedGoogle Scholar
  79. Van den Bergh KPB, Rougé P, Proost P, Coosemans J, Krouglova T, Engelborghs Y, Peumans WJ, Van Damme EJM (2004) Synergistic antifungal activity of two chitin-binding proteins from spindle tree (Euonymus europaeus L.). Planta 219:221–232. CrossRefPubMedGoogle Scholar
  80. Vasconcelos IM, Morais JKS, Siebra EA, Carlini CR, Sousa DOB, Beltramini LM, Melo VMM, Oliveira JTA (2008) SBTX, a new toxic protein distinct from soyatoxin and other toxic soybean [Glycine max] proteins, and its inhibitory effect on Cercospora sojina growth. Toxicon 51:952–963. CrossRefPubMedGoogle Scholar
  81. Verdier J, Thompson RD (2008) Transcriptional regulation of storage protein synthesis during dicotyledon seed filling. Plant Cell Physiol 49:1263–1271. CrossRefPubMedGoogle Scholar
  82. Wang X, Bunkers GJ (2000) Potent heterologous antifungal proteins from cheeseweed (Malva parviflora). Biochem Biophys Res Commun 279:669–673. CrossRefPubMedGoogle Scholar
  83. Wang X, Bunkers GJ, Walters MR, Thoma RS (2001) Purification and characterization of three antifungal proteins from cheeseweed (Malva parviflora). Biochem Biophys Res Commun 282:1224–1228. CrossRefPubMedGoogle Scholar
  84. Zhang Y, Peng L, Wu Y, Shen Y, Wu X, Wang J (2014) Analysis of global gene expression profiles to identify differentially expressed genes critical for embryo development in Brassica rapa. Plant Mol Biol 86:425–442. CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Tarcymara B. Garcia
    • 1
  • Arlete A. Soares
    • 2
  • Jose H. Costa
    • 1
  • Helen P. S. Costa
    • 1
  • João X. S. Neto
    • 1
  • Lady Clarissa B. Rocha-Bezerra
    • 1
  • Fredy Davi A. Silva
    • 1
  • Mariana R. Arantes
    • 1
  • Daniele O. B. Sousa
    • 1
  • Ilka M. Vasconcelos
    • 1
    Email author
  • Jose T. A. Oliveira
    • 1
    Email author
  1. 1.Department of Biochemistry and Molecular BiologyFederal University of CearaFortalezaBrazil
  2. 2.Department of BiologyFederal University of CearaFortalezaBrazil

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