Seed-derived defensins from Scots pine: structural and functional features.

Item request has been placed! ×
Item request cannot be made. ×
loading   Processing Request
  • Additional Information
    • Source:
      Publisher: Springer-Verlag [etc.] Country of Publication: Germany NLM ID: 1250576 Publication Model: Electronic Cited Medium: Internet ISSN: 1432-2048 (Electronic) Linking ISSN: 00320935 NLM ISO Abbreviation: Planta Subsets: MEDLINE
    • Publication Information:
      Original Publication: Berlin, New York, Springer-Verlag [etc.]
    • Subject Terms:
    • Abstract:
      Main Conclusion: The recombinant PsDef5.1 defensin inhibits the growth of phytopathogenic fungi, Gram-positive and Gram-negative bacteria, and human pathogen Candida albicans. Expression of seed-derived Scots pine defensins is tissue-specific and developmentally regulated. Plant defensins are ubiquitous antimicrobial peptides that possess a broad spectrum of activities and multi-functionality. The genes for these antimicrobial proteins form a multigenic family in the plant genome and are expressed in every organ. Most of the known defensins have been isolated from seeds of various monocot and dicot species, but seed-derived defensins have not yet been characterized in gymnosperms. This study presents the isolation of two new 249 bp cDNA sequences from Scots pine seeds with 97.9% nucleotide homology named PsDef5.1 and PsDef5.2. Their deduced amino acid sequences have typical plant defensin features, including an endoplasmic reticulum signal sequence of 31 amino acids (aa), followed by a characteristic defensin domain of 51 aa. To elucidate the functional activity of new defensins, we expressed the mature form of PsDef5.1 in a prokaryotic system. The purified recombinant peptide exhibited activity against the phytopathogenic fungi and Gram-negative and Gram-positive bacteria with the IC 50 of 5-18 µM. Moreover, it inhibited the growth of the human pathogen Candida albicans with the IC 50 of 6.0 µM. Expression analysis showed that transcripts of PsDef5.1-2 genes were present in immature and mature pine seeds and different parts of seedlings at the early stage of germination. In addition, unlike the PsDef5.2, the PsDef5.1 gene was expressed in the reproductive organs. Our findings indicate that novel defensins are promising candidates for transgenic application and the development of new antimicrobial drugs.
      (© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.)
    • References:
      Aerts AM, Carmona-Gutierrez D, Lefevre S, Govaert G, François IE, Madeo F, Santos R, Cammue BP, Thevissen K (2009) The antifungal plant defensin RsAFP2 from radish induces apoptosis in a metacaspase independent way in Candida albicans. FEBS Lett 583:2513–2516. https://doi.org/10.1016/j.febslet.2009.07.004. (PMID: 10.1016/j.febslet.2009.07.00419596007)
      Allen A, Snyder AK, Preuss M, Nielsen EE, Shah DM, Smith TJ (2008) Plant defensins and virally encoded fungal toxin KP4 inhibit plant root growth. Planta 227:331–339. https://doi.org/10.1007/s00425-007-0620-1. (PMID: 10.1007/s00425-007-0620-117849147)
      Armenteros JJ, Salvatore M, Emanuelsson O, Winther O, von Heijne G, Elofsson A, Nielsen H (2019) Detecting sequence signals in targeting peptides using deep learning. Life Sci Alliance 2:e201900429. https://doi.org/10.26508/lsa.201900429. (PMID: 10.26508/lsa.201900429)
      Balandín M, Royo J, Gómez E, Muniz LM, Molina A, Hueros G (2005) A protective role for the embryo surrounding region of the maize endosperm, as evidenced by the characterisation of ZmESR-6, a defensin gene specifically expressed in this region. Plant Mol Biol 58:269–282. https://doi.org/10.1007/s11103-005-3479-1. (PMID: 10.1007/s11103-005-3479-116027978)
      Bleackley MR, Payne JA, Hayes BM, Durek T, Craik DJ, Shafee TM, Poon IK, Hulett MD, van der Weerden NL, Anderson MA (2016) Nicotiana alata defensin chimeras reveal differences in the mechanism of fungal and tumor cell killing and an enhanced antifungal variant. Antimicrob Agents Chemother 60(10):6302–6312. https://doi.org/10.1128/AAC.01479-16. (PMID: 10.1128/AAC.01479-16275036515038239)
      Broekaert WF, Terras F, Cammue BP, Vandedeyden J (1990) An automated quantitative assay for fungal growth inhibition. FEMS Microbiol Lett 69:55–60. https://doi.org/10.1016/0378-1097(90)90412-J. (PMID: 10.1016/0378-1097(90)90412-J)
      Broekaert WF, Terras FR, Cammue BP, Osborn RW (1995) Plant defensins: novel antimicrobial peptides as components of the host defense system. Plant Physiol 108(4):1353–1358. https://doi.org/10.1104/pp.108.4.1353. (PMID: 10.1104/pp.108.4.13537659744157512)
      Broekaert WF, Cammue BPA, De Bolle MFC, Thevissen K, De Samblanx G, Osborn RW (1997) Antimicrobial peptides from plants. CRC Crit Rev Plant Sci 16:297–323. https://doi.org/10.1080/07352689709701952. (PMID: 10.1080/07352689709701952)
      Cairney J, Zheng L, Cowles A, Hsiao J, Zismann V, Liu J, Ouyang S, Thibaud-Nissen F, Hamilton J, Childs K, Pullman GS, Zhang Y, Oh T, Buell CR (2006) Expressed sequence tags from loblolly pine embryos reveal similarities with angiosperm embryogenesis. Plant Mol Biol 62:485–501. https://doi.org/10.1007/s11103-006-9035-9. (PMID: 10.1007/s11103-006-9035-917001497)
      Carvalho AO, Gomes VM (2011) Plant defensins and defensin-like peptides—biological activities and biotechnological applications. Curr Pharm Des 17:4270–4293. https://doi.org/10.2174/138161211798999447. (PMID: 10.2174/138161211798999447)
      Carvalho AO, Filho GA, Ferreira BS, Branco AT, Okorokova-Façanha AL, Gomes VM (2006) Cloning and characterization of a cDNA encoding a cowpea seed defensin and analysis of its expression. Protein Pept Lett 13:1029–1036. https://doi.org/10.2174/092986606778777515. (PMID: 10.2174/09298660677877751517168826)
      Cervantes S, Vuosku J, Paczesniak D, Pyhäjärvi T (2021) Atlas of tissue-specific and tissue-preferential gene expression in ecologically and economically significant conifer Pinus sylvestris. bioRxiv. http://biorxiv.org/content/early/2021/01/07/2020.10.22.350058.1.abstract . Accessed 21 June 2021.
      Chaturani G, Mir Z, Mishra P, Grover A (2019) Identification and characterization of defensin genes in Brassica juncea and Camelina sativa and analysis of their expression in response to biotic and abiotic stress. Acta Sci Agric 3:96–112. https://doi.org/10.31080/ASAG.2019.03.0732. (PMID: 10.31080/ASAG.2019.03.0732)
      Cools TL, Struyfs C, Cammue BP, Thevissen K (2017) Antifungal plant defensins: increased insight in their mode of action as a basis for their use to combat fungal infections. Future Microbiol 12:441–454. https://doi.org/10.2217/fmb-2016-0181. (PMID: 10.2217/fmb-2016-018128339295)
      Crooks GE, Hon G, Chandonia JM, Brenner SE (2004) WebLogo: a sequence logogenerator. Genome Res 14:1188–1190. https://doi.org/10.1101/gr.849004. (PMID: 10.1101/gr.84900415173120419797)
      De Oliveira MÉ, Taveira GB, de Oliveira CA, Gomes VM (2019) Improved smallest peptides based on positive charge increase of the γ-core motif from PνD 1 and their mechanism of action against Candida species. Int J Nanomed 14:407–420. https://doi.org/10.2147/IJN.S187957. (PMID: 10.2147/IJN.S187957)
      De Samblanx GW, Goderis IJ, Thevissen K, Raemaekers R, Fant F, Borremans F, Acland DP, Osborn RW, Patel S, Broekaert WF (1997) Mutational analysis of a plant defensin from radish (Raphanus sativus L.) reveals two adjacent sites important for antifungal activity. J Biol Chem 272:1171–1179. https://doi.org/10.1074/jbc.272.2.1171. (PMID: 10.1074/jbc.272.2.11718995418)
      Do HM, Lee SC, Jung HW, Sohn KH, Hwang BK (2004) Differential expression and in situ localization of a pepper defensin (CADEF1) gene in response to pathogen infection, abiotic elicitors and environmental stresses in Capsicum annuum. Plant Sci 166:1297–1305. https://doi.org/10.1016/j.plantsci.2004.01.008. (PMID: 10.1016/j.plantsci.2004.01.008)
      Doughty J, Dixon S, Hiscock SJ, Willis AC, Parkin IA, Dickinson HG (1998) PCP-A1, a defensin-like Brassica pollen coat protein that binds the S locus glycoprotein, is the product of gametophytic gene expression. Plant Cell 10:1333–1347. https://doi.org/10.1105/tpc.10.8.1333. (PMID: 10.1105/tpc.10.8.13339707533144068)
      Endo A, Tatematsu K, Hanada K, Duermeyer L, Okamoto M, Yonekura-Sakakibara K, Saito K, Toyoda T, Kawakami N, Kamiya Y, Seki M, Nambara E (2012) Tissue-specific transcriptome analysis reveals cell wall metabolism, flavonol biosynthesis and defense responses are activated in the endosperm of germinating Arabidopsis thaliana seeds. Plant Cell Physiol 53:16–27. https://doi.org/10.1093/pcp/pcr171. (PMID: 10.1093/pcp/pcr17122147073)
      Ermakova EA, Faizullin DA, Idiyatullin BZ, Khairutdinov BI, Mukhamedova LN, Tarasova NB, Toporkova YY, Osipova EV, Kovaleva V, Gogolev YV, Zuev YF, Nesmelova IV (2016) Structure of Scots pine defensin 1 by spectroscopic methods and computational modeling. Int J Biol Macromol 84:142–152. https://doi.org/10.1016/j.ijbiomac.2015.12.011. (PMID: 10.1016/j.ijbiomac.2015.12.01126687241)
      Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. https://doi.org/10.2307/2408678. (PMID: 10.2307/24086782856135928561359)
      Fossdal CG, Nagy NE, Sharma P, Lönneborg A (2003) The putative gymnosperm plant defensin polypeptide (SPI1) accumulates after seed germination, is not readily released, and the SPI1 levels are reduced in Pythium dimorphum-infected spruce roots. Plant Mol Biol 52:291–302. https://doi.org/10.1023/a:1023915230129. (PMID: 10.1023/a:102391523012912856937)
      Francisco GC, Georgina E (2017) Structural motifs in class I and class II plant defensins for phospholipid interactions: intriguing role of ligand binding and modes of action. J Plant Physiol Pathol 5:1. https://doi.org/10.4172/2329-955X.1000159. (PMID: 10.4172/2329-955X.1000159)
      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 67:1636–1642. https://doi.org/10.1271/bbb.67.1636. (PMID: 10.1271/bbb.67.163612951494)
      Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. In: Walker JM (ed) The proteomics protocols handbook. Humana Press, Totowa, pp 571–607. (PMID: 10.1385/1-59259-890-0:571)
      Germain H, Lachance D, Pelletier G, Fossdal CG, Solheim H, Séguin A (2012) The expression pattern of the Picea glauca Defensin 1 promoter is maintained in Arabidopsis thaliana, indicating the conservation of signalling pathways between angiosperms and gymnosperms. J Exp Bot 63:785–795. https://doi.org/10.1093/jxb/err303. (PMID: 10.1093/jxb/err30322048038)
      Giacomelli L, Nanni V, Lenzi L, Zhuang J, Dalla Serra M, Banfield MJ, Town CD, Silverstein KA, Baraldi E, Moser C (2012) Identification and characterization of the defensin-like gene family of grapevine. Mol Plant Microb Interact 25:1118–1131. https://doi.org/10.1094/MPMI-12-11-0323. (PMID: 10.1094/MPMI-12-11-0323)
      Graham MA, Silverstein KAT, Cannon SB, Vanden Bosch KA (2004) Computational identification and characterization of novel genes from legumes. Plant Physiol 135:1179–1197. https://doi.org/10.1104/pp.104.037531. (PMID: 10.1104/pp.104.03753115266052519039)
      Hanks JN, Snyder AK, Graham MA, Shah RK, Blaylock LA, Harrison MJ, Shah DM (2005) Defensin gene family in Medicago truncatula: structure, expression and induction by signal molecules. Plant Mol Biol 58:385–399. https://doi.org/10.1007/s11103-005-5567-7. (PMID: 10.1007/s11103-005-5567-716021402)
      Harrison SJ, Marcus JP, Goulter KC, Green JL, Maclean DJ, Manners JM (1997) An antimicrobial peptide from the Australian native Hardenbergia violacea provides the first functionally characterised member of a subfamily of plant defensins. Aust J Plant Physiol 24:571–578. https://doi.org/10.1071/PP97075. (PMID: 10.1071/PP97075)
      He X, Kermode AR (2010) Programmed cell death of the megagametophyte during post-germinative growth of white spruce (Picea glauca) seeds is regulated by reactive oxygen species and the ubiquitin-mediated proteolytic system. Plant Cell Physiol 51:1707–1720. https://doi.org/10.1093/pcp/pcq130. (PMID: 10.1093/pcp/pcq13020833629)
      Higashiyama T (2010) Peptide signaling in pollen-pistil interactions. Plant Cell Physiol 51:177–189. https://doi.org/10.1093/pcp/pcq008. (PMID: 10.1093/pcp/pcq00820081210)
      Hrunyk N, Gout R, Kovaleva V (2017) Regulation of gene expression for defensins and lipid transfer protein in Scots pine seedlings by necrotrophic pathogen Alternaria alternata (Fr.). Folia Forestalia Polonica 59:152–158. https://doi.org/10.1515/ffp-2017-0015. (PMID: 10.1515/ffp-2017-0015)
      Hrunyk NI, Shalovylo YI, Yusypovych YM, Roman II, Nesmelova IV, Kovaleva VA (2019) Prokaryotic expression and purification of bioactive defension 2 from Pinus sylvestris L. Studia Biologica 13:29–40. https://doi.org/10.30970/sbi.1302.603. (PMID: 10.30970/sbi.1302.603)
      Islam KT, Velivelli SLS, Berg RH, Oakley B, Shah D (2017) A novel bi-domain plant defensin MtDef5 with potent broad-spectrum antifungal activity binds to multiple phospholipids and forms oligomers. Sci Rep 7:16157. https://doi.org/10.1038/s41598-017-16508-w. (PMID: 10.1038/s41598-017-16508-w291704455700942)
      Järvå M, Lay FT, Phan TK, Humble C, Poon IKH, Bleackley MR, Anderson MA, Hulett MD, Kvansakul M (2018) X-ray structure of a carpet-like antimicrobial defensin-phospholipid membrane disruption complex. Nat Commun 9:1962. https://doi.org/10.1038/s41467-018-04434-y. (PMID: 10.1038/s41467-018-04434-y297738005958116)
      Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJ (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10:845–858. https://doi.org/10.1038/nprot.2015.053. (PMID: 10.1038/nprot.2015.053259502375298202)
      Kerenga BK, McKenna JA, Harvey PJ, Quimbar P, Garcia-Ceron D, Lay FT, Phan TK, Veneer PK, Vasa S, Parisi K, Shafee TMA, van der Weerden NL, Hulett MD, Craik DJ, Anderson MA, Bleackley MR (2019) Salt-tolerant antifungal and antibacterial activities of the corn defensin ZmD32. Front Microbiol 10:795. https://doi.org/10.3389/fmicb.2019.00795. (PMID: 10.3389/fmicb.2019.00795310317396474387)
      Khairutdinov BI, Ermakova EA, Yusypovych YM, Bessolicina EK, Tarasova NB, Toporkova YY, Kovaleva V, Zuev YF, Nesmelova IV (2017) NMR structure, conformational dynamics, and biological activity of PsDef1 defensin from Pinus sylvestris. Biochim Biophys Acta Proteins Proteom 1865:1085–1094. https://doi.org/10.1016/j.bbapap.2017.05.012. (PMID: 10.1016/j.bbapap.2017.05.01228528214)
      Koike M, Okamoto T, Tsuda S, Imai R (2002) A novel plant defensin-like gene of winter wheat is specifically induced during cold acclimation. Biochem Biophys Res Commun 298:46–53. https://doi.org/10.1016/s0006-291x(02)02391-4. (PMID: 10.1016/s0006-291x(02)02391-412379218)
      Kovaleva V, Kiyamova R, Cramer R, Krynytskyy H, Gout I, Filonenko V, Gout R (2009) Purification and molecular cloning of antimicrobial peptides from Scots pine seedlings. Peptides 30:2136–2143. https://doi.org/10.1016/j.peptides.2009.08.007. (PMID: 10.1016/j.peptides.2009.08.00719683554)
      Kovaleva V, Krynytskyy H, Gout I, Gout R (2011) Recombinant expression, affinity purification and functional characterization of Scots pine defensin 1. Appl Microbiol Biotechnol 89:1093–1101. https://doi.org/10.1007/s00253-010-2935-2. (PMID: 10.1007/s00253-010-2935-220957359)
      Kovaleva V, Cramer R, Krynytskyy H, Gout I, Gout R (2013) Analysis of tyrosine phosphorylation and phosphotyrosine-binding proteins in germinating seeds from Scots pine. Plant Physiol Biochem 67:33–40. https://doi.org/10.1016/j.plaphy.2013.02.008. (PMID: 10.1016/j.plaphy.2013.02.00823542181)
      Kovaleva V, Bukhteeva I, Kit OY, Nesmelova IV (2020) Plant defensins from a structural perspective. Int J Mol Sci 21:5307. https://doi.org/10.3390/ijms21155307. (PMID: 10.3390/ijms211553077432377)
      Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096. (PMID: 10.1093/molbev/msy096297228875967553)
      Lacerda AF, Vasconcelos EA, Pelegrini PB, Grossi de Sa MF (2014) Antifungal defensins and their role in plant defense. Front Microbiol 5(459):1–10. https://doi.org/10.3389/fmicb.2014.00116. (PMID: 10.3389/fmicb.2014.00116)
      Lay FT, Anderson MA (2005) Defensins—components of the innate immune system in plants. Curr Protein Pept Sci 6:85–101. https://doi.org/10.2174/1389203053027575. (PMID: 10.2174/138920305302757515638771)
      Lay FT, Brugliera F, Anderson MA (2003) Isolation and properties of floral defensins from ornamental tobacco and petunia. Plant Physiol 131:1283–1293. https://doi.org/10.1104/pp.102.016626. (PMID: 10.1104/pp.102.01662612644678166888)
      Mello-Ede O, dos Santos IS, Carvalho-Ade O, de Souza LS, de Souza-Filho GA, do Nascimento VV, Machado OL, Zottich U, Gomes VM (2014) Functional expression and activity of the recombinant antifungal defensin PvD1r from Phaseolus vulgaris L. (common bean) seeds. BMC Biochem 15:7. https://doi.org/10.1186/1471-2091-15-7. (PMID: 10.1186/1471-2091-15-724690228)
      Mendez E, Moreno A, Colilla F, Pelaez F, Limas GG, Mendez R, Soriano F, Salinas M, de Haro C (1990) Primary structure and inhibition of protein synthesis in eukaryotic cell-free system of a novel thionin, gamma-hordothionin, from barley endosperm. Eur J Biochem 194:533–539. https://doi.org/10.1111/j.1432-1033.1990.tb15649.x. (PMID: 10.1111/j.1432-1033.1990.tb15649.x2176600)
      Nanni V, Schumacher J, Giacomelli L, Brazzale D, Sbolci L, Moser C, Tudzynski P, Baraldi E (2014) VvAMP2, a grapevine flower-specific defensin capable of inhibiting Botrytis cinerea growth: insights into its mode of action. Plant Pathol 63:899–910. https://doi.org/10.1111/ppa.12170. (PMID: 10.1111/ppa.12170)
      Ochiai A, Ogawa K, Fukuda M, Ohori M, Kanaoka T, Tanaka T, Taniguchi M, Sagehashi Y (2018) Rice defensin OsAFP1 is a new drug candidate against human pathogenic fungi. Sci Rep 8(1):11434. https://doi.org/10.1038/s41598-018-29715-w. (PMID: 10.1038/s41598-018-29715-w300617246065317)
      Ochiai A, Ogawa K, Fukuda M, Suzuki M, Ito K, Tanaka T, Sagehashi Y, Taniguchi M (2020) Crystal structure of rice defensin OsAFP1 and molecular insight into lipid-binding. J Biosci Bioeng 130:6–13. https://doi.org/10.1016/j.jbiosc.2020.02.011. (PMID: 10.1016/j.jbiosc.2020.02.01132192842)
      Ojeda DI, Mattila TM, Ruttink T, Kujala ST, Kärkkäinen K, Verta JP, Pyhäjärvi T (2019) Utilization of tissue ploidy level variation in de novo transcriptome assembly of Pinus sylvestris. G3 Gene Genom Genet (bethesda) 9:3409–3421. https://doi.org/10.1534/g3.119.400357. (PMID: 10.1534/g3.119.400357)
      Ong ST, Bajaj S, Tanner MR, Chang SC, Krishnarjuna B, Ng XR, Morales RAV, Chen MW, Luo D, Patel D, Yasmin S, Ng JJH, Zhuang Z, Nguyen HM, El Sahili A, Lescar J, Patil R, Charman SA, Robins EG, Goggi JL, Tan PW, Sadasivam P, Ramasamy B, Hartimath SV, Dhawan V, Bednenko J, Colussi P, Wulff H, Pennington MW, Kuyucak S, Norton RS, Beeton C (2020) Chandy KG (2020) Modulation of lymphocyte potassium channel KV1.3 by membrane-penetrating, joint-targeting immunomodulatory plant defensin. ACS Pharmacol Transl Sci 3(4):720–736. https://doi.org/10.1021/acsptsci.0c00035. (PMID: 10.1021/acsptsci.0c00035328328737432667)
      Parisi K, Shafee TMA, Quimbar P, van der Weerden NL, Bleackley MR, Anderson MA (2019) The evolution, function and mechanisms of action for plant defensins. Semin Cell Dev Biol 88:107–118. https://doi.org/10.1016/j.semcdb.2018.02.004. (PMID: 10.1016/j.semcdb.2018.02.00429432955)
      Pelegrini PB, Del Sarto RP, Silva ON, Franco OL, Grossi-De-Sa MF (2011) Antibacterial peptides from plants: what they are and how they probably work. Biochem Res Int 2011:250349. https://doi.org/10.1155/2011/250349. (PMID: 10.1155/2011/250349)
      Penninckx IA, Eggermont K, Terras FR, Thomma BP, De Samblanx GW, Buchala A, Métraux JP, Manners JM, Broekaert WF (1996) Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway. Plant Cell 8:2309–2323. https://doi.org/10.1105/tpc.8.12.2309. (PMID: 10.1105/tpc.8.12.23098989885161354)
      Penninckx IA, Thomma BP, Buchala A, Métraux JP, Broekaert WF (1998) Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10:2103–2113. https://doi.org/10.1105/tpc.10.12.2103. (PMID: 10.1105/tpc.10.12.21039836748143966)
      Pervieux I, Bourassa M, Laurans F, Hamelin R, Séguin A (2004) A spruce defensin showing strong antifungal activity and increased transcript accumulation after wounding and jasmonate treatments. Physiol Mol Plant Pathol 64:331–341. https://doi.org/10.1016/j.pmpp.2004.09.008. (PMID: 10.1016/j.pmpp.2004.09.008)
      Picart P, Pirttilä AM, Raventos D, Kristensen HH, Sahl HG (2012) Identification of defensin-encoding genes of Picea glauca: characterization of PgD5, a conserved spruce defensin with strong antifungal activity. BMC Plant Biol 12:180. https://doi.org/10.1186/1471-2229-12-180. (PMID: 10.1186/1471-2229-12-180230357763502332)
      Poon IKh, Baxter AA, Lay FT, Mills GD, Adda CG, Payne JA, Phan TK, Ryan GF, White JA, Veneer PK, van der Weerden NL, Anderson MA, Kvansakul M, Hulett MD (2014) Phosphoinositide-mediated oligomerization of a defensin induces cell lysis. Elife 3:e01808. https://doi.org/10.7554/eLife.01808. (PMID: 10.7554/eLife.01808246924463968744)
      Pothana A, Bhatnagar-Mathur P, Yeshvekar RK, Sharma KK (2019) Plant defensins: tissue specific expression leading to distinctive functions. Curr Trends Biotechnol Pharm 13:212–231. http://oar.icrisat.org/id/eprint/11164.
      Ramamoorthy V, Cahoon EB, Li J, Thokala M, Minto RE, Shah DM (2007) Glucosylceramide synthase is essential for alfalfa defensin-mediated growth inhibition but not for pathogenicity of Fusarium graminearum. Mol Microbiol 66(3):771–786. https://doi.org/10.1111/j.1365-2958.2007.05955.x. (PMID: 10.1111/j.1365-2958.2007.05955.x17908205)
      Rogozhin EA, Oshchepkova YI, Odintsova TI, Khadeeva NV, Veshkurova ON, Egorov TA, Grishin EV, Salikhov SI (2011) Novel antifungal defensins from Nigella sativa L. seeds. Plant Physiol Biochem 49:131–1317. https://doi.org/10.1016/j.plaphy.2010.10.008. (PMID: 10.1016/j.plaphy.2010.10.00821144761)
      Sagaram US, Pandurangi R, Kaur J, Smith TJ, Shah DM (2011) Structure-activity determinants in antifungal plant defensins MsDef1 and MtDef4 with different modes of action against Fusarium graminearum. PLoS ONE 6:e18550. https://doi.org/10.1371/journal.pone.0018550. (PMID: 10.1371/journal.pone.0018550215332493076432)
      Sagaram US, El-Mounadi K, Buchko GW, Berg HR, Kaur J, Pandurangi RS, Smith TJ, Shah DM (2013) Structural and functional studies of a phosphatidic acid-binding antifungal plant defensin MtDef4: identification of an RGFRRR motif governing fungal cell entry. PLoS ONE 8:e82485. https://doi.org/10.1371/journal.pone.0082485. (PMID: 10.1371/journal.pone.0082485243247983853197)
      Sano N, Ono H, Murata K, Yamada T, Hirasawa T, Kanekatsu M (2015) Accumulation of long-lived mRNAs associated with germination in embryos during seed development of rice. J Exp Bot 66:4035–4046. https://doi.org/10.1093/jxb/erv209. (PMID: 10.1093/jxb/erv209259413264473999)
      Sathoff AE, Velivelli S, Shah DM, Samac DA (2019) Plant defensin peptides have antifungal and antibacterial activity against human and plant pathogens. Phytopathology 109:402–408. https://doi.org/10.1094/PHYTO-09-18-0331-R. (PMID: 10.1094/PHYTO-09-18-0331-R30252607)
      Sathoff AE, Lewenza S, Samac DA (2020) Plant defensin antibacterial mode of action against Pseudomonas species. BMC Microbiol 20:173. https://doi.org/10.1186/s12866-020-01852-1. (PMID: 10.1186/s12866-020-01852-1325606767304088)
      Schopfer CR, Nasrallah ME, Nasrallah JB (1999) The male determinant of self-incompatibility in Brassica. Science 286:1697–1700. https://doi.org/10.1126/science.286.5445. (PMID: 10.1126/science.286.544510576728)
      Segura A, Moreno M, Molina A, García-Olmedo F (1998) Novel defensin subfamily from spinach (Spinacia oleracea). FEBS Lett 435:159–162. https://doi.org/10.1016/s0014-5793(98)01060-6. (PMID: 10.1016/s0014-5793(98)01060-69762899)
      Shafee TM, Lay FT, Phan TK, Anderson MA, Hulett MD (2017) Convergent evolution of defensin sequence, structure and function. Cell Mol Life Sci 74:663–682. https://doi.org/10.1007/s00018-016-2344-5. (PMID: 10.1007/s00018-016-2344-527557668)
      Sharma P, Lönneborg A (1996) Isolation and characterization of a cDNA encoding a plant defensin-like protein from roots of Norway spruce. Plant Mol Biol 31:707–712. https://doi.org/10.1007/BF00042244. (PMID: 10.1007/BF000422448790304)
      Silverstein KAT, Graham MA, Paape TD, Vanden Bosch KA (2005) Genome organization of more than 300 defensin-like genes in Arabidopsis. Plant Physiol 138:600–610. https://doi.org/10.1104/pp.105.060079. (PMID: 10.1104/pp.105.060079159559241150381)
      Stotz HU, Spence B, Wang Y (2009) A defensin from tomato with dual function in defense and development. Plant Mol Biol 71:131–143. https://doi.org/10.1007/s11103-009-9512-z. (PMID: 10.1007/s11103-009-9512-z19533379)
      Takayama S, Shiba H, Iwano M, Shimosato H, Che FS, Kai N, Watanabe M, Suzuki G, Hinata K, Isogai A (2000) The pollen determinant of self-incompatibility in Brassica campestris. Proc Natl Acad Sci USA 97:1920–1925. https://doi.org/10.1073/pnas.040556397. (PMID: 10.1073/pnas.0405563971067755626537)
      Tantong S, Pringsulaka O, Weerawanich K, Meeprasert A, Rungrotmongkol T, Sarnthima R, Roytrakul S, Sirikantaramas S (2016) Two novel antimicrobial defensins from rice identified by gene coexpression network analyses. Peptides 84:7–16. https://doi.org/10.1016/j.peptides.2016.07.005. (PMID: 10.1016/j.peptides.2016.07.00527527801)
      Terras FR, Eggermont K, Kovaleva V, Raikhel NV, Osborn RW, Kester A, Rees SB, Torrekens S, Van Leuven F, Vanderleyden J et al (1995) Small cysteine-rich antifungal proteins from radish: their role in host defense. Plant Cell 7:573–588. https://doi.org/10.1105/tpc.7.5.573. (PMID: 10.1105/tpc.7.5.5737780308160805)
      Tesfaye M, Silverstein KA, Nallu S, Wang L, Botanga CJ, Gomez SK, Katagiri F (2013) Spatio-temporal expression patterns of A. thaliana and M. truncatula defensin-like genes. PLoS ONE 8:e58992. https://doi.org/10.1371/journal.pone.0058992. (PMID: 10.1371/journal.pone.0058992235270673601123)
      Thevissen K, Warnecke DC, François IE, Leipelt M, Heinz E, Ott C, Zähringer U, Thomma BP, Ferket KK, Cammue BP (2004) Defensins from insects and plants interact with fungal glucosylceramides. J Biol Chem 279:3900–3905. https://doi.org/10.1074/jbc.M311165200. (PMID: 10.1074/jbc.M31116520014604982)
      Thevissen K, de Mello TP, Xu D, Blankenship J et al (2012) The plant defensin RsAFP2 induces cell wall stress, septin mislocalization and accumulation of ceramides in Candida albicans. Mol Microbiol 84:166–180. https://doi.org/10.1111/j.1365-2958.2012.08017.x. (PMID: 10.1111/j.1365-2958.2012.08017.x223849763405362)
      Thomma BPHJ, Broekaert WF (1998) Tissue-specific expression of plant defensin genes PDF2.1 and PDF2.2 in Arabidopsis thaliana. Plant Physiol Biochem 36:533–537. https://doi.org/10.1016/S0981-9428(98)80179-4. (PMID: 10.1016/S0981-9428(98)80179-4)
      Thomma BP, Cammue BP, Thevissen K (2002) Plant defensins. Planta 216:193–202. https://doi.org/10.1007/s00425-002-0902-6. (PMID: 10.1007/s00425-002-0902-612447532)
      Thompson JD, Gibson TJ, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinform 2(2):3. https://doi.org/10.1002/0471250953.bi0203s00. (PMID: 10.1002/0471250953.bi0203s00)
      van den Heuvel KJ, Hulzink JM, Barendse GW, Wullems GJ (2001) The expression of tgas118, encoding a defensin in Lycopersicon esculentum, is regulated by gibberellin. J Exp Bot 52:1427–1436. https://doi.org/10.1093/jexbot/52.360.1427. (PMID: 10.1093/jexbot/52.360.142711457902)
      van der Weerden NL, Anderson MA (2013) Plant defensins: common fold, multiple functions. Fungal Biol Rev 26:121–131. https://doi.org/10.1016/j.fbr.2012.08.004. (PMID: 10.1016/j.fbr.2012.08.004)
      Velivelli SLS, Islam KT, Hobson E, Shah DM (2018) Modes of action of a Bi-domain plant defensin MtDef5 against a bacterial pathogen Xanthomonas campestris. Front Microbiol 9:934. https://doi.org/10.3389/fmicb.2018.00934. (PMID: 10.3389/fmicb.2018.00934298678435964164)
      Veronese P, Ruiz MT, Coca MA, Hernandez-Lopez A, Lee H, Ibeas JI, Damsz B, Pardo JM, Hasegawa PM, Bressan RA, Narasimhan ML (2003) In defense against pathogens. Both plant sentinels and foot soldiers need to know the enemy. Plant Physiol 131:1580–1590. https://doi.org/10.1104/pp.102.013417. (PMID: 10.1104/pp.102.013417126923171540302)
      Waghu FH, Barai RS, Gurung P, Idicula-thomas S (2016) CAMPR3: a database on sequences, structures and signatures of antimicrobial peptides. Nucleic Acids Res 44:1094–1097. https://doi.org/10.1093/nar/gkv1051. (PMID: 10.1093/nar/gkv1051)
      Wong JH, Ng TB (2005) Sesquin, a potent defensin-like antimicrobial peptide from ground beans with inhibitory activities toward tumor cells and HIV-1 reverse transcriptase. Peptides 26:1120–1126. https://doi.org/10.1016/j.peptides.2005.01.003. (PMID: 10.1016/j.peptides.2005.01.00315949629)
      Yan D, Duermeyer L, Leoveanu C, Nambara E (2014) The functions of the endosperm during seed germination. Plant Cell Physiol 55:1521–1533. https://doi.org/10.1093/pcp/pcu089. (PMID: 10.1093/pcp/pcu08924964910)
      Young N, Debellé F, Oldroyd G, Geurts R et al (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480:520–524. https://doi.org/10.1038/nature10625. (PMID: 10.1038/nature10625220891323272368)
      Zhu S, Gao B, Tytgat J (2005) Phylogenetic distribution, functional epitopes and evolution of the CSαβ superfamily. Cell Mol Life Sci 62:2257–2269. https://doi.org/10.1007/s00018-005-5200-6. (PMID: 10.1007/s00018-005-5200-616143827)
    • Grant Information:
      FSA-19-65490-0 crdf global; FSA-19-65490-1 crdf global; M52-2020 ministry of education and science of ukraine
    • Contributed Indexing:
      Keywords: Antifungal and antibacterial activities; Antimicrobial peptide; Cloning; Expression pattern; Heterological expression; Pinus sylvestris L.
    • Accession Number:
      0 (Anti-Bacterial Agents)
      0 (Defensins)
    • Publication Date:
      Date Created: 20211124 Date Completed: 20211126 Latest Revision: 20220428
    • Publication Date:
      20240105
    • Accession Number:
      10.1007/s00425-021-03788-w
    • Accession Number:
      34817648