The Use of Transgenic Plants Expressing Antimicrobial Peptide Genes as a Promising Strategy to Improve Plant Resistance to Phytopathogens

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

Plant diseases significantly reduce crop yields and deteriorate the quality of agricultural products. The review is devoted to the problem of increasing plant resistance to pathogens by creating transgenic plants expressing antimicrobial peptide (AMP) genes as one of the strategies for plant disease control. The review summarizes the main economically important plant diseases caused by pathogenic fungi and bacteria and describes methods of plant resistance against them. The need to develop new, environmentally friendly plant protection products from the defensive arsenal of the plants themselves, which could be incorporated into an integrated plant defense management instead of/alongside traditionally used chemical pesticides, is emphasized. Plant antimicrobial peptides could become such new biopesticides. The review outlines the main properties of AMPs that make them promising molecules for enhancing crop resistance to phytopathogens and provides numerous examples of transgenic plants developed under laboratory conditions in which incorporated AMP genes improved their resistance to infection. Thus, the described strategy may become an important component of integrated plant disease control strategy against phytopathogens in the future.

About the authors

T. I Odintsova

Vavilov Institute of General Genetics, Russian Academy of Sciences

Email: odintsova2005@rambler.ru
Moscow, Russia

A. N Shiyan

Vavilov Institute of General Genetics, Russian Academy of Sciences

Moscow, Russia

M. P Slezina

Vavilov Institute of General Genetics, Russian Academy of Sciences

Moscow, Russia

References

  1. Savary S., Willocquet L., Pethybridge S.J. et al. The global burden of pathogens and pests on major food crops // Nat. Ecol. Evol. 2019. V. 3. P. 430–439. https://doi.org/10.1038/s41559-018-0793-y
  2. Horbach R., Navarro-Quesada A.R., Knogge W., Deising H.B. When and how to kill a plant cell: Infection strategies of plant pathogenic fungi // J. Plant Physiol. 2011. V. 168. № 1. P. 51–62. https://doi.org/10.1016/j.jplph.2010.06.014
  3. Fisher M.C., Henk D.A., Briggs C.J. et al. Emerging fungal threats to animal, plant and ecosystem health // Nature. 2012. V. 484. P. 186–194. https://doi.org/10.1038/nature10947
  4. Avery S.V., Singleton I., Magan N., Goldman G.H. The fungal threat to global food security // Fungal Biol. 2019. V. 123. № 8. P. 555–557. https://doi.org/10.1016/j.funbio.2019.03.006
  5. Godfray H.C.J., Beddington J.R., Crute I.R. et al. Food security: The challenge of feeding 9 billion people // Science. 2010. V. 327. № 5967. P. 812–818. https://doi.org/10.1126/science.1185383
  6. Nazarov P.A., Baleev D.N., Ivanova M.I. et al. Infectious plant diseases: Etiology, current status, problems and prospects in plant protection // Acta Naturae. 2020. V. 12. № 3. P. 46–59. https://doi.org/10.32607/actanaturae.11026
  7. Dean R., Van Kan J.A., Pretorius Z.A. et al. The Top 10 fungal pathogens in molecular plant pathology // Mol. Plant Pathol. 2012. V. 13. № 4. P. 414–430. https://doi.org/10.1111/j.1364-3703.2011.00783.x
  8. Nalley L., Tsiboe F., Durand-Morat A. et al. Economic and environmental impact of rice blast pathogen (Magnaporthe oryzae) alleviation in the United States // PLoS One. 2016. V. 11. https://doi.org/10.1371/journal.pone.0167295
  9. Beddow J.M., Pardey P.G., Chai Y. et al. Research investment implications of shifts in the global geography of wheat stripe rust // Nat. Plants. 2015. V. 1. https://doi.org/10.1038/nplants.2015.132.
  10. Kayim M., Nawaz H., Alsalmo A. Fungal diseases of wheat // Wheat. London: IntechOpen, 2022. https://doi.org/10.5772/intechopen.102661
  11. Różewicz M., Wyzińska M., Grabiński J. The most important fungal diseases of cereals – Problems and possible solutions // Agronomy. 2021. V. 11. https://doi.org/10.3390/agronomy11040714
  12. Mapuranga J., Chang J., Yang W. Combating powdery mildew: Advances in molecular interactions between Blumeria graminis f. sp. tritici and wheat // Front. Plant Sci. 2022. V. 13. https://doi.org/10.3389/fpls.2022.1102908
  13. Okungbowa F.I., Shittu H.O. Fusarium wilts: An overview // Environ. Res. J. 2012. V. 6. № 2. P. 83–102.
  14. Gordon T.R. Fusarium oxysporum and the Fusarium wilt syndrome // Annu. Rev. Phytopathol. 2017. V. 55. P. 23–39. https://doi.org/10.1146/annurev-phyto-080615-095919
  15. Cighir A., Mare A.D., Vultur F. et al. Fusarium spp. in human disease: Exploring the boundaries between commensalism and pathogenesis // Life (Basel). 2023. V. 13. № 7. https://doi.org/10.3390/life13071440
  16. McLaughlin C.S., Vaughan M.H., Campbell I.M. et al. Inhibition of protein synthesis by trichothecenes // Mycotoxins in Human and Animal Health / Eds. Rodricks J.V., Hesseltine C.W., Mehlman M.A. Park Forest South, IL, USA: Pathtox Publ., 1977. P. 263–273.
  17. Bin-Umer M.A., McLaughlin J.E., Basu D. et al. Trichothecene mycotoxins inhibit mitochondrial translation-implication for the mechanism of toxi-city // Toxins (Basel). 2011. V. 3. № 12. P. 1484–1501. https://doi.org/10.3390/toxins3121484
  18. Eskola M., Kos G., Elliott C.T. et al. Worldwide contamination of food-crops with mycotoxins: Validity of the widely cited 'FAO estimate' of 25 // Crit. Rev. Food Sci Nutr. 2020. V. 60. № 16. P. 2773–2789. https://doi.org/10.1080/10408398.2019.1658570
  19. Bradbury J.F. Guide to Plant Pathogenic Bacteria. Farnham Royal, Slough, UK: CAB Intern., 1986. 332 p.
  20. Mansfield J., Genin S., Magori S. et al. Top 10 plant pathogenic bacteria in molecular plant pathology // Mol. Plant Pathol. 2012. V. 13. № 6. P. 614–629. https://doi.org/10.1111/j.1364-3703.2012.00804.x
  21. Bonn W.G., Van der Zwet T. Distribution and economic importance of fire blight // Fire Blight: The Disease and its Causative Agent, Erwinia amylovora. Wallingford, UK: CABI, 2000. P. 37–54.
  22. Update of a database of host plants of Xylella fastidiosa // EFSA J. 2016. V. 14. № 2. https://doi.org/10.2903/j.efsa.2016.4378
  23. Wang N., Trivedi P. Citrus huanglongbing: A newly relevant disease presents unprecedented challenges // Phytopathology. 2013. V. 103. № 7. P. 652–665. https://doi.org/10.1094/PHYTO-12-12-0331-RVW
  24. Zheng Z., Chen J., Deng X. Historical perspectives, management, and current research of Citrus HLB in Guangdong province of China, where the disease has been endemic for over a hundred years // Phytopathology. 2018. V. 108. № 11. P. 1224–1236. https://doi.org/10.1094/PHYTO-07-18-0255-IA
  25. Jones J.D.G., Dangl J.L. The plant immune system // Nature. 2006. V. 444. № 7117. P. 323–329. https://doi.org/10.1038/nature05286
  26. Zasloff M. Antimicrobial peptides of multicellular organisms // Nature. 2002. V. 415. № 6870. P. 389–395. https://doi.org/10.1038/415389a
  27. Tam J.P., Wang S., Wong K.H., Tan W.L. Antimicrobial peptides from plants // Pharmaceuticals. 2015. V. 8. № 4. P. 711–757. https://doi.org/10.3390/ph8040711
  28. Lima A.M., Azevedo M.I.G., Sousa L.M. et al. Plant antimicrobial peptides: An overview about classification, toxicity and clinical applications // Int. J. Biol. Macromol. 2022. V. 214. P. 10–21. https://doi.org/10.1016/j.ijbiomac.2022.06.043
  29. Li J., Hu S., Jian W. et al. Plant antimicrobial peptides: Structures, functions, and applications // Bot. Stud. 2021. V. 62. https://doi.org/10.1186/s40529-021-00312-x
  30. Brogden K.A. Antimicrobial peptides: Pore formers or metabolic inhibitors in bacteria? // Nat. Rev. Microbiol. 2005. V. 3. № 3. P. 238–250. https://doi.org/10.1038/nrmicro1098
  31. Cardoso M.H., Meneguetti B.T., Costa B.O. et al. Non-lytic antibacterial peptides that translocate through bacterial membranes to act on intracellular targets // Int. J. Mol. Sci. 2019. V. 20. № 19. https://doi.org/10.3390/ijms20194877
  32. Montesinos E. Functional peptides for plant disease control // Annu. Rev. Phytopathol. 2023. V. 61. P. 301–324. https://doi.org/10.1146/annurev-phyto-021722-034312
  33. Kaur H., Garg H. Pesticides: Environmental impacts and management strategies // Pesticides – Toxic Aspects. London: IntechOpen, 2014. https://doi.org/10.5772/57399
  34. Carmona M.J., Molina A., Fernández J.A. et al. Expression of the α-thionin gene from barley in tobacco confers enhanced resistance to bacterial pathogens // Plant J. 1993. V. 3. № 3. P. 4574–4562. https://doi.org/10.1111/j.1365-313x.1993.tb00165.x
  35. Terras F.R., Eggermont K., Kovaleva V. et al. Small cysteine-rich antifungal proteins from radish: Their role in host defense // Plant Cell. 1995. V. 7. № 5. P. 573–588. https://doi.org/10.1105/tpc.7.5.573
  36. Kostov K., Christova P., Slavov S., Batchvarova S. Constitutive expression of a radish defensin gene Rs-Afp2 in tomato increases the resistance to fungal pathogens // Biotechno. Biotechnol. Equip. 2009. V. 23. P. 1121–1125. https://doi.org/10.1080/13102818.2009.10817625
  37. Jha S., Chattoo B.B. Expression of a plant defensin in rice confers resistance to fungal phytopathogens // Transgenic Res. 2010. V. 19. № 3. P. 373–384. https://doi.org/10.1007/s11248-009-9315-7
  38. Li Z., Zhou M., Zhang Z. et al. Expression of a radish defensin in transgenic wheat confers increased resistance to Fusarium graminearum and Rhizoctonia cerealis // Funct. Integr. Genomics. 2011. V. 11. № 1. P. 63–70. https://doi.org/10.1007/s10142-011-0211-x
  39. Sadhu S., Jogam P., Gande K. et al. Expression of radish defensin (RsAFP2) gene in chickpea (Cicer arietinum L.) confers resistance to Fusarium wilt disease // Mol. Biol. Rep. 2023. V. 50. № 1. P. 11–18. https://doi.org/10.1007/s11033-022-08021-9
  40. Turrini A., Sbrana C., Pitto L. et al. The antifungal Dm-AMP1 protein from Dahlia merckii expressed in Solanum melongena is released in root exudates and differentially affects pathogenic fungi and mycorrhizal symbiosis // New Phytol. 2004. V. 163. № 2. P. 393–403. https://doi.org/10.1111/j.1469-8137.2004.01107.x
  41. Zhu Y.J., Agbayani R., Moore P.H. Ectopic expression of Dahlia merckii defensin DmAMP1 improves papaya resistance to Phytophthora palmivora by reducing pathogen vigor // Planta. 2007. V. 226. № 1. P. 87–97. https://doi.org/10.1007/s00425-006-0471-1
  42. Jha S., Tank H.G., Prasad B.D., Chattoo B.B. Expression of Dm-AMP1 in rice confers resistance to Magnaporthe oryzae and Rhizoctonia solani // Transgenic Res. 2009. V. 18. № 1. P. 59–69. https://doi.org/10.1007/s11248-008-9196-1
  43. Su Q., Wang K., Zhang Z. Ecotopic expression of the antimicrobial peptide DmAMP1W improves resistance of transgenic wheat to two diseases: Sharp eyespot and common root rot // Int. J. Mol. Sci. 2020. V. 21. № 2. https://doi.org/10.3390/ijms21020647
  44. Ghag S.B., Shekhawat U.K., Ganapathi T.R. Petunia floral defensins with unique prodomains as novel candidates for development of fusarium wilt resistance in transgenic banana plants // PLoS One. 2012. V. 7. № 6. https://doi.org/10.1371/journal.pone.0039557
  45. Gaspar Y.M., McKenna J.A., McGinness B.S. et al. Field resistance to Fusarium oxysporum and Verticillium dahliae in transgenic cotton expressing the plant defensin NaD1 // J. Exp. Bot. 2014. V. 65. № 6. P. 1541–1550. https://doi.org/10.1093/jxb/eru021
  46. Gao A.G., Hakimi S.M., Mittanck C.A. et al. Fungal pathogen protection in potato by expression of a plant defensin peptide // Nat. Biotechnol. 2000. V. 18. № 12. P. 1307–1310. https://doi.org/10.1038/82436
  47. Abdallah N.A., Shah D., Abbas D., Madkour M. Stable integration and expression of a plant defensin in tomato confers resistance to fusarium wilt // GM Crops. 2010. V. 1. № 5. P. 344–350. https://doi.org/10.4161/gmcr.1.5.15091
  48. Kaur J., Fellers J., Adholeya A. et al. Expression of apoplast targeted plant defensin MtDef4.2 confers resistance to leaf rust pathogen Puccinia triticina but does not affect mycorrhizal symbiosis in transgenic wheat // Transgenic Res. 2017. V. 26. № 1. P. 37–49. https://doi.org/10.1007/s11248-016-9978-9
  49. Park H.C., Kang Y.H., Chun H.J. et al. Charac-terization of a stamen-specific cDNA encoding a novel plant defensin in Chinese cabbage // Plant Mol. Biol. 2002. V. 50. P. 59–69. https://doi.org/10.1023/a:1016005231852
  50. Portieles R., Ayra C., Gonzalez E. et al. NmDef02, a novel antimicrobial gene isolated from Nicotiana megalosiphon confers high-level pathogen resistance under greenhouse and field conditions // Plant Biotechnol. J. 2010. V. 8. № 6. P. 678–690. https://doi.org/10.1111/j.1467-7652.2010.00501.x
  51. Soto N., Hernández Y., Delgado C. et al. Field resistance to Phakopsora pachyrhizi and Colletotrichum truncatum of transgenic soybean expressing the NmDef02 plant defensin gene // Front. Plant Sci. 2020. V. 11. https://doi.org/10.3389/fpls.2020.00562
  52. Kanzaki H., Nirasawa S., Saitoh H. et al. Over-expression of the wasabi defensin gene confers enhanced resistance to blast fungus (Magnaporthe grisea) in transgenic rice // Theor. Appl. Genet. 2002. V. 105. № 6–7. P. 809–814. https://doi.org/10.1007/s00122-001-0817-9
  53. Ntui V.O., Thirukkumaran G., Azadi P. et al. Stable integration and expression of wasabi defensin gene in “Egusi” melon (Colocynthis citrullus L.) confers resistance to Fusarium wilt and Alternaria leaf spot // Plant Cell Rep. 2010. V. 29. № 9. P. 943–954. https://doi.org/10.1007/s00299-010-0880-2
  54. Khan R.S., Nakamura I., Mii M. Development of disease-resistant marker-free tomato by R/RS site-specific recombination // Plant Cell Rep. 2011. V. 30. № 6. P. 1041–1053. https://doi.org/10.1007/s00299-011-1011-4
  55. Muramoto N., Tanaka T., Shimamura T. et al. Transgenic sweet potato expressing thionin from barley gives resistance to black rot disease caused by Ceratocystis fimbriata in leaves and storage roots // Plant Cell Rep. 2012. V. 31. № 6. P. 9879–9897. https://doi.org/10.1007/s00299-011-1217-5
  56. Charity J.A., Hughes P., Anderson M.A. et al. Pest and disease protection conferred by expression of barley β-hordothionin and Nicotiana alata proteinase inhibitor genes in transgenic tobacco // Funct. Plant Biol. 2005. V. 32. № 1. P. 35–44. https://doi.org/10.1071/FP04105
  57. Oard S.V., Enright F.M. Expression of the antimi-crobial peptides in plants to control phytopathogenic bacteria and fungi // Plant Cell Rep. 2006. V. 25. № 6. P. 561–572. https://doi.org/10.1007/s00299-005-0102-5
  58. Epple P., Apel K., Bohlmann H. Overexpression of an endogenous thionin enhances resistance of Arabidopsis against Fusarium oxysporum // Plant Cell. 1997. V. 9. № 4. P. 509–520. https://doi.org/10.1105/tpc.9.4.509
  59. Chan Y.L., Prasad V., Sanjaya et al. Transgenic tomato plants expressing an Arabidopsis thionin (Thi2.1) driven by fruit-inactive promoter battle against phytopathogenic attack // Planta. 2005. V. 221. № 3. P. 386–393. https://doi.org/10.1007/s00425-004-1459-3
  60. Tawfik E., Hammad I., Bakry A. Production of transgenic Allium cepa by nanoparticles to resist Aspergillus niger infection // Mol. Biol. Rep. 2022. V. 49. № 3. P. 1783–1790. https://doi.org/10.1007/s11033-021-06988-5
  61. Hussien E.T. Production of transgenic Paulownia tomentosa (Thunb.) steud. using chitosan nanoparticles to express antimicrobial genes resistant to bacterial infection // Mol. Biol. Res. Commun. 2020. V. 9. № 2. P. 55–62. https://doi.org/10.22099/mbrc.2019.35331.1454
  62. Bouqellah N.A., Hussein E.T., Abdel Razik A.B. et al. Development of transgenic Paulownia trees expressing antimicrobial thionin genes for enhanced resistance to fungal infections using chitosan nanoparticles // Microb. Pathog. 2024. V. 191. https://doi.org/10.1016/j.micpath.2024.106659
  63. Iwai T., Kaku H., Honkura R. et al. Enhanced resistance to seed-transmitted bacterial diseases in transgenic rice plants overproducing an oat cell-wall-bound thionin // Mol. Plant Microbe Interact. 2002. V. 15. № 6. P. 515–521. https://doi.org/10.1094/MPMI.2002.15.6.515
  64. Hoshikawa K., Ishihara G., Takahashi H., Nakamura I. Enhanced resistance to gray mold (Botrytis cinerea) in transgenic potato plants expressing thionin genes isolated from Brassicaceae species // Plant Biothechnol. 2012. V. 29. P. 87–93. https://doi.org/10.5511/plantbiotechnology.12.0125a
  65. Kanrar S., Venkateswari J.C., Kirti P.B., Chopra V.L. Transgenic expression of hevein, the rubber tree lectin, in Indian mustard confers protection against Alternaria brassicae // Plant Sci. 2002. V. 162. № 3. P. 441–448. https://doi.org/10.1016/S0168-9452(01)00588-X
  66. Pujade-Renaud V., Sanier C., Cambillau L. et al. Molecular characterization of new members of the Hevea brasiliensis hevein multigene family and analysis of their promoter region in rice // Biochim. Biophys. Acta. 2005. V. 1727. № 3. P. 151–161. https://doi.org/10.1016/j.bbaexp.2004.12.013
  67. Shukurov R.R., Voblikova V.D., Nikonorova A.K. et al. Transformation of tobacco and Arabidopsis plants with Stellaria media genes encoding novel hevein-like peptides increases their resistance to fungal pathogens // Transgenic Res. 2012. V. 21. № 2. P. 313–325. https://doi.org/10.1007/s11248-011-9534-6
  68. Beliaev D.V., Yuorieva N.O., Tereshonok D.V. et al. High resistance of potato to early blight is achieved by expression of the Pro-SmAMP1 Gene for hevein-like antimicrobial peptides from common chickweed (Stellaria media) // Plants (Basel). 2021. V. 10. № 7. https://doi.org/10.3390/plants10071395
  69. Koo J.C., Chun H.J., Park H.C. et al. 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. 2002. V. 50. № 3. P. 441–452. https://doi.org/10.1023/a:1019864222515
  70. Lee O.S., Lee B., Park N. et al. Pn-AMPs, the hevein-like proteins from Pharbitis nil confers disease resistance against phytopathogenic fungi in tomato, Lycopersicum esculentum // Phytochemistry. 2003. V. 62. № 7. P. 1073–1079. https://doi.org/10.1016/s0031-9422(02)00668-4
  71. De Bolle M.F., Osborn R.W., Goderis I.J. et al. Antimicrobial peptides from Mirabilis jalapa and Amaranthus caudatus: Expression, processing, localization and biological activity in transgenic tobacco // Plant Mol. Biol. 1996. V. 31. № 5. P. 993–1008. https://doi.org/10.1007/BF00040718
  72. Jia Z., Gou J., Sun Y. et al. Enhanced resistance to fungal pathogens in transgenic Populus tomentosa Carr. by overexpression of an nsLTP-like antimicrobial protein gene from motherwort (Leonurus japonicus) // Tree Physiol. 2010. V. 30. № 12. P. 1599–1605. https://doi.org/10.1093/treephys/tpq093
  73. Zhu F., Cao M.Y., Zhu P.X. et al. Non-specific LIPID TRANSFER PROTEIN 1 enhances immunity against tobacco mosaic virus in Nicotiana benthamiana // J. Exp. Bot. 2023. V. 74. № 17. P. 5236–5254. https://doi.org/10.1093/jxb/erad202
  74. Molina A., García-Olmedo F. Enhanced tolerance to bacterial pathogens caused by the transgenic expression of barley lipid transfer protein LTP2 // Plant J. 1997. V. 12. № 3. P. 669–675. https://doi.org/10.1046/j.1365-313x.1997.00669.x
  75. Li X., Gasic K., Cammue B. et al. Transgenic rose lines harboring an antimicrobial protein gene, Ace-AMP1, demonstrate enhanced resistance to powdery mildew (Sphaerotheca pannosa) // Planta. 2003. V. 218. № 2. P. 226–232. https://doi.org/10.1007/s00425-003-1093-5
  76. Roy-Barman S., Sautter C., Chattoo B.B. Expression of the lipid transfer protein Ace-AMP1 in transgenic wheat enhances antifungal activity and defense responses // Transgenic Res. 2006. V. 15. № 4. P. 435–446. https://doi.org/10.1007/s11248-006-0016-1
  77. Zhao J., Bi W., Zhao S. et al. Wheat apoplast-localized lipid transfer protein TaLTP3 enhances defense responses against Puccinia triticina // Front. Plant Sci. 2021. V. 12. https://doi.org/10.3389/fpls.2021.771806
  78. Jung H.W., Kim K.D., Hwang B.K. Identification of pathogen-responsive regions in the promoter of a pepper lipid transfer protein gene (CALTPI) and the enhanced resistance of the CALTPI transgenic Arabidopsis against pathogen and environmental stresses // Planta. 2005. V. 221. № 3. P. 361–373. https://doi.org/10.1007/s00425-004-1461-9
  79. Almasia N.I., Bazzini A.A., Hopp H.E., Vazquez-Rovere C. Overexpression of snakin-1 gene enhances resistance to Rhizoctonia solani and Erwinia carotovora in transgenic potato plants // Mol. Plant Pathol. 2008. V. 9. № 3. P. 329–338. https://doi.org/10.1111/j.1364-3703.2008.00469.x
  80. Darqui F.S., Radonic L.M., Trotz P.M. et al. Potato snakin-1 gene enhances tolerance to Rhizoctonia solani and Sclerotinia sclerotiorum in transgenic lettuce plants // J. Biotechnol. 2018. V. 283. P. 62–69. https://doi.org/10.1016/j.jbiotec.2018.07.017
  81. Balaji V., Smart C.D. Over-expression of snakin-2 and extensin-like protein genes restricts pathogen invasiveness and enhances tolerance to Clavibacter michiganensis subsp. michiganensis in transgenic tomato (Solanum lycopersicum) // Transgenic. Res. 2012. V. 21. № 1. P. 23–37. https://doi.org/10.1007/s11248-011-9506-x
  82. Nahirñak V., Almasia N.I., Lia V.V. et al. Unveiling the defensive role of Snakin-3, a member of the subfamily III of Snakin/GASA peptides in potatoes // Plant Cell Rep. 2024. V. 43. № 2. https://doi.org/10.1007/s00299-023-03108-4
  83. Bouteraa M.T., Ben Romdhane W., Wiszniewska A. et al. Functional analysis of durum wheat GASA1 protein as a biotechnological alternative against plant fungal pathogens and a positive regulator of biotic stress defense // Plants (Basel). 2025. V. 14. № 1. https://doi.org/10.3390/plants14010112
  84. Weinhold A., Karimi Dorcheh E., Li R. et al. Antimicrobial peptide expression in a wild tobacco plant reveals the limits of host-microbe-manipulations in the field // eLife. 2018. V. 7. https://doi.org/10.7554/eLife.28715
  85. Jha S., Chattoo B.B. Transgene stacking and coordinated expression of plant defensins confer fungal resistance in rice // Rice. 2009. V. 2. P. 143–154. https://doi.org/10.1007/s12284-009-9030-2
  86. Nalluri N., Karri V. Over-expression of Tfgd2-RsAFP2 fusion gene isolated from fenugreek and radish shows enhanced disease resistance against Alternaria blight disease caused by Alternaria alternata in transgenic pigeonpea // Mol. Biol. Rep. 2025. V. 52. № 1. https://doi.org/10.1007/s11033-025-10471-w
  87. Rustagi A., Kumar D., Shekhar S. et al. Transgenic Brassica juncea plants expressing MsrA1, a synthetic cationic antimicrobial peptide, exhibit resistance to fungal phytopathogens // Mol. Biotechnol. 2014. V. 56. № 6. P. 535–545. https://doi.org/10.1007/s12033-013-9727-8
  88. Cary J.W., Rajasekaran K., Jaynes J.M., Cleveland T.E. Transgenic expression of a gene encoding a synthetic antimicrobial peptide results in inhibition of fungal growth in vitro and in planta // Plant Sci. 2000. V. 154. № 2. P. 171–181. https://doi.org/10.1016/s0168-9452(00)00189-8
  89. Rajasekaran K., Cary J.W., Jaynes J.M., Cleveland T.E. Disease resistance conferred by the expression of a gene encoding a synthetic peptide in transgenic cotton (Gossypium hirsutum L.) plants // Plant Biotechnol. J. 2005. V. 3. № 6. P. 545–554. https://doi.org/10.1111/j.1467-7652.2005.00145.x
  90. Núñez-Muñoz L.A., Sánchez-García M.E., Calderón-Pérez B. et al. Metagenomic analysis of rhizospheric bacterial community of citrus trees expressing phloem-directed antimicrobials // Microb. Ecol. 2024. V. 87. № 1. https://doi.org/10.1007/s00248-024-02408-w
  91. Hao G., Bakker M.G., Kim H.S. Enhanced resistance to Fusarium graminearum in transgenic Arabidopsis plants expressing a modified plant thionin // Phytopathology. 2020. V. 110. № 5. P. 1056–1066. https://doi.org/10.1094/PHYTO-12-19-0447-R
  92. Parisi K., Shafee T.M.A., Quimbar P. et al. The evolution, function and mechanisms of action for plant defensins // Semin. Cell Dev. Biol. 2019. V. 88. P. 107–118. https://doi.org/10.1016/j.semcdb.2018.02.004
  93. Cools T.L., Struyfs C., Cammue B.P., Thevissen K. Antifungal plant defensins: Increased insight in their mode of action as a basis for their use to combat fungal infections // Future Microbiol. 2017. V. 12. P. 441−454. https://doi.org/10.2217/fmb-2016-0181
  94. Sathoff A.E., Samac D.A. Antibacterial activity of plant defensins // Mol. Plant Microbe Interact. 2019. V. 32. № 5. P. 507−514. https://doi.org/10.1094/MPMI-08-18-0229-CR
  95. Mirouze M., Sels J., Richard O. et al. A putative novel role for plant defensins: A defensin from the zinc hyper-accumulating plant, Arabidopsis halleri, confers zinc tolerance // Plant J. 2006. V. 47. № 3. P. 329−342. https://doi.org/10.1111/j.1365-313X.2006.02788.x
  96. Sasaki K., Kuwabara C., Umeki N. et al. The cold-induced defensin TAD1 confers resistance against snow mold and Fusarium head blight in transgenic wheat // J. Biotechnol. 2016. V. 228. P. 3−7. https://doi.org/10.1016/j.jbiotec.2016.04.015
  97. Stotz H.U., Spence B., Wang Y. A defensin from tomato with dual function in defense and development // Plant Mol. Biol. 2009. V. 71. № 1−2. P. 131−143. https://doi.org/10.1007/s11103-009-9512-z
  98. Terras F.R., Schoofs H.M., De Bolle M.F. et al. Analysis of two novel classes of plant antifungal proteins from radish (Raphanus sativus L.) seeds // J. Biol. Chem. 1992. V. 267. P. 15301–15309. https://doi.org/10.1016/S0021-9258(19)49534-3
  99. Osborn R.W., De Samblanx G.W., Thevissen K. et al. Isolation and characterisation of plant defensins from seeds of Asteraceae, Fabaceae, Hippocastanaceae and Saxifragaceae // FEBS Lett. 1995. V. 368. P. 257–262. https://doi.org/10.1016/0014-5793(95)00666-W
  100. Stec B. Plant thionins – the structural perspective // Cell. Mol. Life Sci. 2006. V. 63. P. 1370–1385. https://doi.org/10.1007/s00018-005-5574-5
  101. Höng K., Austerlitz T., Bohlmann T., Bohlmann H. The thionin family of antimicrobial peptides // PLoS One. 2021. V. 16. № 7. https://doi.org/10.1371/journal.pone.0254549
  102. Slavokhotova A.A., Shelenkov A.A., Andreev Y.A., Odintsova T.I. Hevein-like antimicrobial peptides of plants // Biochemistry (Moscow). 2017. V. 82. № 13. P. 1659−1674. https://doi.org/10.1134/S0006297917130065
  103. Slavokhotova A.A., Naumann T.A., Price N.P. et al. Novel mode of action of plant defense peptides – hevein-like antimicrobial peptides from wheat inhibit fungal metalloproteases // FEBS J. 2014. V. 281. № 20. P. 4754−4764. https://doi.org/10.1111/febs.13015
  104. Van den Bergh K.P., Rougé P., Proost P. et al. Synergistic antifungal activity of two chitin-binding proteins from spindle tree (Euonymus europaeus L.) // Planta. 2004. V. 219. № 2. P. 221−232. https://doi.org/10.1007/s00425-004-1238-1
  105. Loo S., Tay S.V., Kam A. et al. Anti-fungal hevein-like peptides biosynthesized from quinoa cleavable hololectins // Molecules. 2021. V. 26. № 19. https://doi.org/10.3390/molecules26195909
  106. Ляпкова Н.С., Лоскутова Н.А., Майсурян А.Н. и др. Получение генетически модифицированных растений картофеля, несущих ген защитного пептида амаранта // Прикл. биохимия и микробиология. 2001. Т. 37. С. 349–354.
  107. Salminen T.A., Blomqvist K., Edqvist J. Lipid transfer proteins: classification, nomenclature, structure, and function // Planta. 2016. V. 244. № 5. P. 971−997. https://doi.org/10.1007/s00425-016-2585-4
  108. Yang Y., Li P., Liu C. et al. Systematic analysis of the non-specific lipid transfer protein gene family in Nicotiana tabacum reveal its potential roles in stress responses // Plant Physiol. Biochem. 2022. V. 172. P. 33−47. https://doi.org/10.1016/j.plaphy.2022.01.002
  109. Fahlberg P., Buhot N., Johansson O.N., Andersson M.X. Involvement of lipid transfer proteins in resistance against a non-host powdery mildew in Arabidopsis thaliana // Mol. Plant Pathol. 2019. V. 20. № 1. P. 69−77. https://doi.org/10.1111/mpp.12740
  110. Edstam M.M., Blomqvist K., Eklöf A. et al. Coexpression patterns indicate that GPI-anchored non-specific lipid transfer proteins are involved in accumulation of cuticular wax, suberin and sporopollenin // Plant Mol. Biol. 2013. V. 83. № 6. P. 625−649. https://doi.org/10.1007/s11103-013-0113-5
  111. Santos-Silva C.A.D., Ferreira-Neto J.R.C., Amador V.C. et al. From gene to transcript and peptide: A deep overview on non-specific lipid transfer proteins (nsLTPs) // Antibiotics (Basel). 2023. V. 12. № 5. 939. https://doi.org/10.3390/antibiotics12050939
  112. Segura A., Moreno M., Madueño F. et al. Snakin-1, a peptide from potato that is active against plant pathogens // Mol. Plant Microbe Interact. 1999. V. 12. № 1. P. 16−23. https://doi.org/10.1094/MPMI.1999.12.1.16
  113. Oliveira-Lima M., Benko-Iseppon A.M., Neto J.R.C.F. et al. Snakin: Structure, roles and applications of a plant antimicrobial peptide // Curr. Protein Pept. Sci. 2017. V. 18. № 4. P. 368–374. https://doi.org/10.2174/1389203717666160619183140
  114. Nahirñak V., Almasia N.I., Fernandez P.V. et al. Potato snakin-1 gene silencing affects cell division, primary metabolism, and cell wall composition // Plant Physiol. 2012. V. 158. P. 252–263. https://doi.org/10.1104/pp.111.186544

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2025 Russian Academy of Sciences

Согласие на обработку персональных данных с помощью сервиса «Яндекс.Метрика»

1. Я (далее – «Пользователь» или «Субъект персональных данных»), осуществляя использование сайта https://journals.rcsi.science/ (далее – «Сайт»), подтверждая свою полную дееспособность даю согласие на обработку персональных данных с использованием средств автоматизации Оператору - федеральному государственному бюджетному учреждению «Российский центр научной информации» (РЦНИ), далее – «Оператор», расположенному по адресу: 119991, г. Москва, Ленинский просп., д.32А, со следующими условиями.

2. Категории обрабатываемых данных: файлы «cookies» (куки-файлы). Файлы «cookie» – это небольшой текстовый файл, который веб-сервер может хранить в браузере Пользователя. Данные файлы веб-сервер загружает на устройство Пользователя при посещении им Сайта. При каждом следующем посещении Пользователем Сайта «cookie» файлы отправляются на Сайт Оператора. Данные файлы позволяют Сайту распознавать устройство Пользователя. Содержимое такого файла может как относиться, так и не относиться к персональным данным, в зависимости от того, содержит ли такой файл персональные данные или содержит обезличенные технические данные.

3. Цель обработки персональных данных: анализ пользовательской активности с помощью сервиса «Яндекс.Метрика».

4. Категории субъектов персональных данных: все Пользователи Сайта, которые дали согласие на обработку файлов «cookie».

5. Способы обработки: сбор, запись, систематизация, накопление, хранение, уточнение (обновление, изменение), извлечение, использование, передача (доступ, предоставление), блокирование, удаление, уничтожение персональных данных.

6. Срок обработки и хранения: до получения от Субъекта персональных данных требования о прекращении обработки/отзыва согласия.

7. Способ отзыва: заявление об отзыве в письменном виде путём его направления на адрес электронной почты Оператора: info@rcsi.science или путем письменного обращения по юридическому адресу: 119991, г. Москва, Ленинский просп., д.32А

8. Субъект персональных данных вправе запретить своему оборудованию прием этих данных или ограничить прием этих данных. При отказе от получения таких данных или при ограничении приема данных некоторые функции Сайта могут работать некорректно. Субъект персональных данных обязуется сам настроить свое оборудование таким способом, чтобы оно обеспечивало адекватный его желаниям режим работы и уровень защиты данных файлов «cookie», Оператор не предоставляет технологических и правовых консультаций на темы подобного характера.

9. Порядок уничтожения персональных данных при достижении цели их обработки или при наступлении иных законных оснований определяется Оператором в соответствии с законодательством Российской Федерации.

10. Я согласен/согласна квалифицировать в качестве своей простой электронной подписи под настоящим Согласием и под Политикой обработки персональных данных выполнение мною следующего действия на сайте: https://journals.rcsi.science/ нажатие мною на интерфейсе с текстом: «Сайт использует сервис «Яндекс.Метрика» (который использует файлы «cookie») на элемент с текстом «Принять и продолжить».