Assessment of antimicrobial phytopeptides: lipid transfer protein and hevein-like peptide in the prospect of structure, function and allergenic effect

Sarfuddin Azmi1, Shahnaaz Khatoon2, Mohd Kamil Hussain3
1Molecular Microbiology Biology Division, Scientific Research Centre (SRC), Prince Sultan Military Medical City (PSMMC), Sulaimaniyah, Saudi Arabia
2Department of Botany, DN College, Meerut, India
3Department of Chemistry, Govt. Raza P.G. College, Rampur, India

Tóm tắt

Antimicrobial peptides (AMPs) are unique natural antibiotics that are crucial effectors of innate immune systems in almost all living organisms. Several different plant antimicrobial peptides have been identified and isolated, demonstrating a high level of protection against various types of bacteria, insects, nematodes and other microbes. Along with antimicrobial function, these peptides play a wide range of crucial function in plants, such as regulation of stomata, ion channel, heavy metals and membrane fluidity. Antimicrobial peptides show a continuum of toxicity for a variety of plants and animals pathogenic microbes and even show cytotoxicity against cancer cells. Numerous studies have shown that transgenic plants have increased the expression of AMP-encoding genes in response to biotic and abiotic stresses, and plants that express transgenic AMP genes are more responsive to biotic, abiotic and other functions. In addition to being a molecule with protective properties, various allergic reactions are associated with some phytopeptides and proteins, in particular non-specific lipid transfer protein (nsLTP) and peptide-like hevein. Pru p3 from peach is the most clinically important allergen within the nsLTP family that cause real food allergies and also triggers extreme clinical reactions. Similarly, latex-fruit syndrome was primarily associated with well-studied latex allergen Hevein (Hev b8, Hev b6) and class I chitinases. Several findings have shown that, in the near future, transgenic plants based on AMPs against the verity of pathogenic fungi, bacteria and other abiotic stresses will be released without any adverse effects. Recent study reason that association of lipid with nsLTP enhances allergic sensitization and hevein-like domain of chitinase I essentially plays a role in cross-sensitivity of latex with different fruits and nuts. This review discusses the structures and various functions of lipid transfer protein and hevein-like peptide.

Tài liệu tham khảo

Aboitiz N, Vila-Perelló M, Groves P, Asensio JL, Andreu D, Cañada FJ, Jimenez-Barbero J (2004) NMR and modeling studies of protein–carbohydrate interactions: synthesis, three-dimensional structure, and recognition properties of a minimum hevein domain with binding affinity for chitooligosaccharides. Chem BioChem 5(9):1245–1255 Archer B (1960) The proteins of Hevea brasiliensis latex. 4. Isolation and characterization of crystalline hevein. Biochem J 75(2):236–240 Asensio JL, Cañada FJ, Siebert H-C, Laynez J, Poveda A, Nieto PM et al (2000) Structural basis for chitin recognition by defense proteins: GlcNAc residues are bound in a multivalent fashion by extended binding sites in hevein domains. Chem Biol 7(7):529–543 Beintema JJ (1994) Structural features of plant chitinases and chitin-binding proteins. FEBS Lett 350(2–3):159–163 Berecz B, Mills EN, Tamas L, Lang F, Shewry PR, Mackie AR (2010) Structural stability and surface activity of sunflower 2S albumins and nonspecific lipid transfer protein. J Agric Food Chem 58(10):6490–6497. https://doi.org/10.1021/jf100554d Bernhard WR, Thoma S, Botella J, Somerville CR (1991) Isolation of a cDNA clone for spinach lipid transfer protein and evidence that the protein is synthesized by the secretory pathway. Plant Physiol 95(1):164–170. https://doi.org/10.1104/pp.95.1.164 Blanco C, Carrillo T, Castillo R, Quiralte J, Cuevas M (1994) Latex allergy: clinical features and cross-reactivity with fruits. Ann Allergy 73(4):309–314 Blanco C, Diaz-Perales A, Collada C, Sánchez-Monge R, Aragoncillo C, Castillo R et al (1999) Class I chitinases as potential panallergens involved in the latex-fruit syndrome. J Allergy Clin Immunol 103(3):507–513 Blein JP, Coutos-Thevenot P, Marion D, Ponchet M (2002) From elicitins to lipid-transfer proteins: a new insight in cell signalling involved in plant defence mechanisms. Trends Plant Sci 7(7):293–296. https://doi.org/10.1016/s1360-1385(02)02284-7 Bogdanov IV, Shenkarev ZO, Finkina EI, Melnikova DN, Rumynskiy EI, Arseniev AS, Ovchinnikova TV (2016) A novel lipid transfer protein from the pea Pisum sativum: isolation, recombinant expression, solution structure, antifungal activity, lipid binding, and allergenic properties. BMC Plant Biol 16(1):107 Broekaert I, Lee H-I, Kush A, Chua N-H, Raikhel N (1990) Wound-induced accumulation of mRNA containing a hevein sequence in laticifers of rubber tree (Hevea brasiliensis). Proc Natl Acad Sci 87(19):7633–7637 Broekaert WF, Marien W, Terras FR, De Bolle MF, Proost P, Van Damme J et al (1992) Antimicrobial peptides from Amaranthus caudatus seeds with sequence homology to the cysteine/glycine-rich domain of chitin-binding proteins. Biochemistry 31(17):4308–4314 Broekaert WF, Van Parijs J, Leyns F, Joos H, Peumans WJ (1989) A chitin-binding lectin from stinging nettle rhizomes with antifungal properties. Science 245(4922):1100–1102 Bublin M, Eiwegger T, Breiteneder H (2014) Do lipids influence the allergic sensitization process? J Allergy Clin Immunol 134(3):521–529 Carvalho Ade O, Gomes VM (2007) Role of plant lipid transfer proteins in plant cell physiology-a concise review. Peptides 28(5):1144–1153. https://doi.org/10.1016/j.peptides.2007.03.004 Chae K, Kieslich CA, Morikis D, Kim S-C, Lord EM (2009) A gain-of-function mutation of Arabidopsis lipid transfer protein 5 disturbs pollen tube tip growth and fertilization. Plant Cell 21(12):3902–3914 Chávez MI, Vila-Perelló M, Cañada FJ, Andreu D, Jiménez-Barbero J (2010) Effect of a serine-to-aspartate replacement on the recognition of chitin oligosaccharides by truncated hevein. A 3D view by using NMR. Carbohydr Res 345(10):1461–1468 Da Silva P, Landon C, Industri B, Marais A, Marion D, Ponchet M, Vovelle F (2005) Solution structure of a tobacco lipid transfer protein exhibiting new biophysical and biological features. Proteins 59(2):356–367. https://doi.org/10.1002/prot.20405 De Bolle MF, Osborn RW, Goderis IJ, Noe L, Acland D, Hart CA et al (1996) Antimicrobial peptides from Mirabilis jalapa and Amaranthus caudatus: expression, processing, localization and biological activity in transgenic tobacco. Plant Mol Biol 31(5):993–1008 Debono A, Yeats TH, Rose JK, Bird D, Jetter R, Kunst L, Samuels L (2009) Arabidopsis LTPG is a glycosylphosphatidylinositol-anchored lipid transfer protein required for export of lipids to the plant surface. Plant Cell 21(4):1230–1238. https://doi.org/10.1105/tpc.108.064451 Diaz-Perales A, Collada C, Blanco C, Sanchez-Monge R, Carrillo T, Aragoncillo C, Salcedo G (1999) Cross-reactions in the latex-fruit syndrome: a relevant role of chitinases but not of complex asparagine-linked glycans. J Allergy Clin Immunol 104(3):681–687 Dubovskii PV, Vassilevski AA, Slavokhotova AA, Odintsova TI, Grishin EV, Egorov TA, Arseniev AS (2011) Solution structure of a defense peptide from wheat with a 10-cysteine motif. Biochem Biophys Res Commun 411(1):14–18 Duwadi D, Shrestha A, Yilma B, Kozlovski I, Sa-Eed M, Dahal N, Jukosky J (2018) Identification and screening of potent antimicrobial peptides in arthropod genomes. Peptides 103:26–30 Edstam MM, Blomqvist K, Eklof A, Wennergren U, Edqvist J (2013) Coexpression patterns indicate that GPI-anchored non-specific lipid transfer proteins are involved in accumulation of cuticular wax, suberin and sporopollenin. Plant Mol Biol 83(6):625–649. https://doi.org/10.1007/s11103-013-0113-5 Edstam MM, Laurila M, Hoglund A, Raman A, Dahlstrom KM, Salminen TA et al (2014) Characterization of the GPI-anchored lipid transfer proteins in the moss Physcomitrella patens. Plant Physiol Biochem 75:55–69. https://doi.org/10.1016/j.plaphy.2013.12.001 Edstam MM, Viitanen L, Salminen TA, Edqvist J (2011) Evolutionary history of the non-specific lipid transfer proteins. Mol Plant 4(6):947–964. https://doi.org/10.1093/mp/ssr019 Egorov T, Odintsova T (2012) Defense peptides of plant immune system. Bioorg Khim 38(1):7 Fernandez de Caleya R, Gonzalez-Pascual B, Garcia-Olmedo F, Carbonero P (1972) Susceptibility of phytopathogenic bacteria to wheat purothionins in vitro. Appl Microbiol 23(5):998–1000 Fujimura M, Minami Y, Watanabe K, Tadera K (2003) Purification, characterization, and sequencing of a novel type of antimicrobial peptides, Fa-AMP1 and Fa-AMP2, from seeds of buckwheat (Fagopyrum esculentum Moench.). Biosci Biotechnol Biochem 67(8):1636–1642 Galelli A, Truffa-Bachi P (1993) Urtica dioica agglutinin. A superantigenic lectin from stinging nettle rhizome. J Immunol 151(4):1821–1831 Gangadhar BH, Sajeesh K, Venkatesh J, Baskar V, Abhinandan K, Yu JW et al (2016) Enhanced tolerance of transgenic potato plants over-expressing non-specific lipid transfer protein-1 (StnsLTP1) against multiple abiotic stresses. Front Plant Sci 7:1228 Garcia-Olmedo F, Molina A, Alamillo JM, Rodriguez-Palenzuela P (1998) Plant defense peptides. Biopolymers 47(6):479–491. https://doi.org/10.1002/(SICI)1097-0282(1998)47:6%3c479::AID-BIP6%3e3.0.CO;2-K Gidrol X, Chrestin H, Tan H-L, Kush A (1994) Hevein, a lectin-like protein from Hevea brasiliensis (rubber tree) is involved in the coagulation of latex. J Biol Chem 269(12):9278–9283 Giordani T, Buti M, Natali L, Pugliesi C, Cattonaro F, Morgante M, Cavallini A (2011) An analysis of sequence variability in eight genes putatively involved in drought response in sunflower (Helianthus annuus L.). Theor Appl Genet 122(6):1039–1049. https://doi.org/10.1007/s00122-010-1509-0 Gomez-Casado C, Diaz-Perales A (2016) Allergen-associated immunomodulators: modifying allergy outcome. Arch Immunol Ther Exp (Warsz) 64(5):339–347. https://doi.org/10.1007/s00005-016-0401-2 Guzman-Rodriguez JJ, Ochoa-Zarzosa A, Lopez-Gomez R, Lopez-Meza JE (2015) Plant antimicrobial peptides as potential anticancer agents. Biomed Res Int 2015:735087. https://doi.org/10.1155/2015/735087 Han GW, Lee JY, Song HK, Chang C, Min K, Moon J et al (2001) Structural basis of non-specific lipid binding in maize lipid-transfer protein complexes revealed by high-resolution X-ray crystallography. J Mol Biol 308(2):263–278. https://doi.org/10.1006/jmbi.2001.4559 Harata K, Muraki M (2000) Crystal structures of Urtica dioica agglutinin and its complex with tri-N-acetylchitotriose. J Mol Biol 297(3):673–681 Huang R-H, Xiang Y, Liu X-Z, Zhang Y, Hu Z, Wang D-C (2002) Two novel antifungal peptides distinct with a five-disulfide motif from the bark of Eucommia ulmoides Oliv. FEBS Lett 521(1–3):87–90 Huang R-H, Xiang Y, Tu G-Z, Zhang Y, Wang D-C (2004) Solution structure of Eucommia antifungal peptide: a novel structural model distinct with a five-disulfide motif. Biochemistry 43(20):6005–6012 Huang X, Xie W-J, Gong Z-Z (2000) Characteristics and antifungal activity of a chitin binding protein from Ginkgo biloba. FEBS Lett 478(1–2):123–126 Iseli B, Boller T, Neuhaus J-M (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(1):221–226 James DJ, Passey AJ, Barbara DJ, Bevan M (1989) Genetic transformation of apple (Malus pumila Mill) using a disarmed Ti-binary vector. Plant Cell Rep 7(8):658–661 Ji H, Gheysen G, Ullah C, Verbeek R, Shang C, De Vleesschauwer D et al (2015) The role of thionins in rice defence against root pathogens. Mol Plant Pathol 16(8):870–881. https://doi.org/10.1111/mpp.12246 Jimenez-Barbero J, Cañada FJ, Asensio JL, Aboitiz N, Vidal P, Canales A et al (2006) Hevein domains: an attractive model to study carbohydrate–protein interactions at atomic resolution. Adv Carbohydr Chem Biochem 60:303–354 Joly V, Matton DP (2015) KAPPA, a simple algorithm for discovery and clustering of proteins defined by a key amino acid pattern: a case study of the cysteine-rich proteins. Bioinformatics 31(11):1716–1723. https://doi.org/10.1093/bioinformatics/btv047 Jose-Estanyol M, Gomis-Ruth FX, Puigdomenech P (2004) The eight-cysteine motif, a versatile structure in plant proteins. Plant Physiol Biochem 42(5):355–365. https://doi.org/10.1016/j.plaphy.2004.03.009 Jung HW, Kim W, Hwang BK (2003) Three pathogen-inducible genes encoding lipid transfer protein from pepper are differentially activated by pathogens, abiotic, and environmental stresses. Plant Cell Environ 26(6):915–928. https://doi.org/10.1046/j.1365-3040.2003.01024.x Kader JC (1975) Proteins and the intracellular exchange of lipids. I. Stimulation of phospholipid exchange between mitochondria and microsomal fractions by proteins isolated from potato tuber. Biochim Biophys Acta 380(1):31–44 Kader JC, Julienne M, Vergnolle C (1984) Purification and characterization of a spinach-leaf protein capable of transferring phospholipids from liposomes to mitochondria or chloroplasts. Eur J Biochem 139(2):411–416. https://doi.org/10.1111/j.1432-1033.1984.tb08020.x Kalla R, Shimamoto K, Potter R, Nielsen PS, Linnestad C, Olsen OA (1994) The promoter of the barley aleurone-specific gene encoding a putative 7 kDa lipid transfer protein confers aleurone cell-specific expression in transgenic rice. Plant J 6(6):849–860. https://doi.org/10.1046/j.1365-313x.1994.6060849.x Kim H, Lee SB, Kim HJ, Min MK, Hwang I, Suh MC (2012) Characterization of -anchored lipid transfer protein 2 (LTPG2) and overlapping function between LTPG/LTPG1 and LTPG2 in cuticular wax export or accumulation in Arabidopsis thaliana. Plant Cell Physiol 53(8):1391–1403. https://doi.org/10.1093/pcp/pcs083 Kini SG, Nguyen PQ, Weissbach S, Mallagaray A, Shin J, Yoon HS, Tam JP (2015) Studies on the chitin binding property of novel cysteine-rich peptides from Alternanthera sessilis. Biochemistry 54(43):6639–6649 Kini SG, Wong KH, Tan WL, Xiao T, Tam JP (2017) Morintides: cargo-free chitin-binding peptides from Moringa oleifera. BMC Plant Biol 17(1):68 Koo JC, Chun HJ, Park HC, Kim MC, Koo YD, Koo SC et al (2002) Over-expression of a seed specific hevein-like antimicrobial peptide from Pharbitis nil enhances resistance to a fungal pathogen in transgenic tobacco plants. Plant Mol Biol 50(3):441–452 Koo JC, Lee SY, Chun HJ, Cheong YH, Choi JS, Kawabata S et al (1998) Two hevein homologs isolated from the seed of Pharbitis nil L. exhibit potent antifungal activity. Protein Struct Mol Enzymol 1382(1):80–90 Kristensen AK, Brunstedt J, Nielsen KK, Roepstorff P, Mikkelsen JD (2000) Characterization of a new antifungal non-specific lipid transfer protein (nsLTP) from sugar beet leaves. Plant Sci 155(1):31–40. https://doi.org/10.1016/s0168-9452(00)00190-4 Lagier F, Vervloet D, Lhermet I, Poyen D, Charpin D (1992) Prevalence of latex allergy in operating room nurses. J Allergy Clin Immunol 90(3):319–322 Lee H, Broekaert W, Raikhel N, Lee H (1991) Co-and post-translational processing of the hevein preproprotein of latex of the rubber tree (Hevea brasiliensis). J Biol Chem 266(24):15944–15948 Lee H, Raikhel N (1995) Prohevein is poorly processed but shows enhanced resistance to a chitin-binding fungus in transgenic tomato plants. Br J Medical Biol Res 28(7):743 Lee OS, Lee B, Park N, Koo JC, Kim YH, Karigar C et al (2003) Pn-AMPs, the hevein-like proteins from Pharbitis nil confers disease resistance against phytopathogenic fungi in tomato Lycopersicum esculentum. Phytochemistry 62(7):1073–1079 Lee SB, Go YS, Bae HJ, Park JH, Cho SH, Cho HJ et al (2009) Disruption of glycosylphosphatidylinositol-anchored lipid transfer protein gene altered cuticular lipid composition, increased plastoglobules, and enhanced susceptibility to infection by the fungal pathogen Alternaria brassicicola. Plant Physiol 150(1):42–54. https://doi.org/10.1104/pp.109.137745 Li S-S, Claeson P (2003) Cys/Gly-rich proteins with a putative single chitin-binding domain from oat (Avena sativa) seeds. Phytochemistry 63(3):249–255 Liapkova N, Loskutova N, Maĭsurian A, Mazin V, Korableva N, Platonova T et al (2001) Isolation of genetically modified potato plant containing the gene of defensive peptide from Am. Prikl Biokhim Mikrobiol 37(3):349–354 Lin P, Xia L, Ng T (2007) First isolation of an antifungal lipid transfer peptide from seeds of a Brassica species. Peptides 28(8):1514–1519 Lipkin A, Anisimova V, Nikonorova A, Babakov A, Krause E, Bienert M et al (2005) An antimicrobial peptide Ar-AMP from amaranth (Amaranthus retroflexus L.) seeds. Phytochemistry 66(20):2426–2431 Liu F, Zhang X, Lu C, Zeng X, Li Y, Fu D, Wu G (2015) Non-specific lipid transfer proteins in plants: presenting new advances and an integrated functional analysis. J Exp Bot 66(19):5663–5681. https://doi.org/10.1093/jxb/erv313 Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK (2002) A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419(6905):399–403. https://doi.org/10.1038/nature00962 Mareška V, Tvaroška I, Králová B, Spiwok V (2015) Molecular simulations of hevein/(GlcNAc) 3 complex with weakened OH/O and CH/π hydrogen bonds: Implications for their role in complex stabilization. Carbohyd Res 408:1–7 Martins JC, Maes D, Loris R, Pepermans HA, Wyns L, Willem R, Verheyden P (1996) 1H NMR study of the solution structure of Ac-AMP2, a sugar binding antimicrobial protein isolated from Amaranthus caudatus. J Mol Biol 258(2):322–333 Mohan S, Meiyalaghan S, Latimer JM, Gatehouse ML, Monaghan KS, Vanga BR et al (2014) GSL2 over-expression confers resistance to Pectobacterium atrosepticum in potato. Theor Appl Genet 127(3):677–689. https://doi.org/10.1007/s00122-013-2250-2 Molina A, Segura A, Garcia-Olmedo F (1993) Lipid transfer proteins (nsLTPs) from barley and maize leaves are potent inhibitors of bacterial and fungal plant pathogens. FEBS Lett 316(2):119–122. https://doi.org/10.1016/0014-5793(93)81198-9 Nielsen KK, Nielsen JE, Madrid SM, Mikkelsen JD (1997) Characterization of a new antifungal chitin-binding peptide from sugar beet leaves. Plant Physiol 113(1):83–91 Nieuwland J, Feron R, Huisman BA, Fasolino A, Hilbers CW, Derksen J, Mariani C (2005) Lipid transfer proteins enhance cell wall extension in tobacco. Plant Cell 17(7):2009–2019 Nordstrom R, Malmsten M (2017) Delivery systems for antimicrobial peptides. Adv Colloid Interface Sci 242:17–34. https://doi.org/10.1016/j.cis.2017.01.005 Odintsova TI, Vassilevski AA, Slavokhotova AA, Musolyamov AK, Finkina EI, Khadeeva NV et al (2009) A novel antifungal hevein-type peptide from Triticum kiharae seeds with a unique 10-cysteine motif. FEBS J 276(15):4266–4275 Pan Y, Li J, Jiao L, Li C, Zhu D, Yu J (2016) A non-specific Setaria italica lipid transfer protein gene plays a critical role under abiotic stress. Front Plant Sci 7:1752 Pasquato N, Berni R, Folli C, Folloni S, Cianci M, Pantano S et al (2006) Crystal structure of peach Pru p3, the prototypic member of the family of plant non-specific lipid transfer protein pan-allergens. J Mol Biol 356(3):684–694. https://doi.org/10.1016/j.jmb.2005.11.063 Petersen A, Kleine-Tebbe J, Scheurer S (2017). Stable plant food allergens I: lipid-transfer proteins. In: Molecular Allergy Diagnostics. Springer, pp 57–75 Regente MC, De La Canal L (2000) Purification, characterization and antifungal properties of a lipid-transfer protein from sunflower (Helianthus annuus) seeds. Physiol Plant 110(2):158–163 Rivillas-Acevedo LA, Soriano-García M (2007) Isolation and biochemical characterization of an antifungal peptide from Amaranthus hypochondriacus seeds. J Agric Food Chem 55(25):10156–10161 Shukurov RR, Voblikova VD, Nikonorova AK, Komakhin RA, Komakhina VV, Egorov TA et al (2012) Transformation of tobacco and Arabidopsis plants with Stellaria media genes encoding novel hevein-like peptides increases their resistance to fungal pathogens. Transgenic Res 21(2):313–325 Sohal AK, Pallas JA, Jenkins GI (1999) The promoter of a Brassica napus lipid transfer protein gene is active in a range of tissues and stimulated by light and viral infection in transgenic Arabidopsis. Plant Mol Biol 41(1):75–87. https://doi.org/10.1023/a:1006232700835 Souza AA, Costa AS, Campos DCO, Batista AHM, Sales GWP, Nogueira NAP et al (2018) Lipid transfer protein isolated from noni seeds displays antibacterial activity in vitro and improves survival in lethal sepsis induced by CLP in mice. Biochimie 149:9–17. https://doi.org/10.1016/j.biochi.2018.03.011 Sterk P, Booij H, Schellekens GA, Van Kammen A, De Vries SC (1991) Cell-specific expression of the carrot EP2 lipid transfer protein gene. Plant Cell 3(9):907–921 Sy D, Le Gravier Y, Goodfellow J, Vovelle F (2003) Protein stability and plasticity of the hydrophobic cavity in wheat ns-LTP. J Biomol Struct Dyn 21(1):15–29. https://doi.org/10.1080/07391102.2003.10506902 Terras FR, Goderis IJ, Van Leuven F, Vanderleyden J, Cammue BP, Broekaert WF (1992) In vitro antifungal activity of a radish (Raphanus sativus L.) seed protein homologous to nonspecific lipid transfer proteins. Plant Physiol 100(2):1055–1058. https://doi.org/10.1104/pp.100.2.1055 Thomas WR (2014) Allergen ligands in the initiation of allergic sensitization. Curr Allergy Asthma Rep 14(5):432 Tian N, Liu F, Wang P, Yan X, Gao H, Zeng X, Wu G (2018) Overexpression of BraLTP2, a lipid transfer protein of Brassica napus, results in increased trichome density and altered concentration of secondary metabolites. Int J Mol Sci 19(6):1733 Tordesillas L, Gómez-Casado C, Garrido-Arandia M, Murua-García A, Palacin A, Varela J et al (2013) Transport of Pru p3 across gastrointestinal epithelium—an essential step towards the induction of food allergy? Clin Exp Allergy 43(12):1374–1383 Van den Bergh KP, Proost P, Van Damme J, Coosemans J, Van Damme EJ, Peumans WJ (2002) Five disulfide bridges stabilize a hevein-type antimicrobial peptide from the bark of spindle tree (Euonymus europaeus L.). FEBS Lett 530(1–3):181–185 Volpicella M, Leoni C, Fanizza I, Rinalducci S, Placido A, Ceci LR (2015) Expression and characterization of a new isoform of the 9 kDa allergenic lipid transfer protein from tomato (variety San Marzano). Plant Physiol Biochem 96:64–71 Wong KH, Tan WL, Serra A, Xiao T, Sze SK, Yang D, Tam JP (2016) Ginkgotides: proline-rich hevein-like peptides from gymnosperm Ginkgo biloba. Front Plant Sci 7:1639 Xiang Y, Huang R-H, Liu X-Z, Zhang Y, Wang D-C (2004) Crystal structure of a novel antifungal protein distinct with five disulfide bridges from Eucommia ulmoides Oliver at an atomic resolution. J Struct Biol 148(1):86–97 Zasloff M (2002) Antimicrobial peptides of multicellular organisms. Nature 415(6870):389–395. https://doi.org/10.1038/415389a Zhang D, Liang W, Yin C, Zong J, Gu F, Zhang D (2010) OsC6, encoding a lipid transfer protein, is required for postmeiotic anther development in rice. Plant Physiol 154(1):149–162. https://doi.org/10.1104/pp.110.158865