Plant defensin explained

Plant defensins (formerly gamma-thionins) are a family of primitive, highly stable, cysteine-rich defensins found in plants that function to defend them against pathogens and parasites.[1] Defensins are integral components of the innate immune system and belong to the ancient superfamily of antimicrobial peptides (AMPs). AMPs are also known as host defense peptides (HDPs),[2] and they are thought to have diverged about 1.4 billion years ago before the evolution of prokaryotes and eukaryotes.[3] [4] They are ubiquitous in almost all plant species, functionally diverse, and their primary structure varies significantly from one species to the next, except for a few cysteine residues, which stabilize the protein structure through disulfide bond formation. Plant defensins usually have a net positive charge due to the abundance of cationic amino acids[5] and are generally divided into two classes. Those in the class II category contain a C-terminal pro-peptide domain of approximately 33 amino acids and are targeted to the vacuole,[6] while the class I defensins lack this domain and mature in the cell wall. Unlike their class I counterparts, class II plant defensins are relatively smaller, and their acidic C-terminal prodomain is hypothesized to contribute to their vacuolar targeting.[7] The first plant defensins were discovered in barley and wheat in 1990 and were initially designated as γ-thionins.[8] [9] In 1995, the name was changed to 'plant defensin' when it was identified that they are evolutionarily unrelated to other thionins and were more similar to defensins from insects and mammals.[10] [11]

Tissue-specific localization

A large number of defensins were initially isolated from seeds, where they are linked to the defense of germinating seeds against fungal pathogens, but recent advances in bioinformatics and molecular biology techniques have revealed that these peptides are present in other parts of the plant, including flowers and roots.[12] Defensins can be expressed in two ways: constitutively or induced under certain stresses. For example, the defensin AtPDF2.2 from Arabidopsis thaliana is expressed constitutively,[13] while another defensin from the same plant is induced by methyl jasmonate and ethylene.[14]

Structure and evolution

Plant defensins are members of the protein superfamily called the cis-defensins or CSαβ fold.[15] This superfamily includes arthropod defensins and fungal defensins (but not defensins found in mammals). It also includes several families of proteins not involved in the immune system, including plant S-locus 11 proteins involved in self-incompatibility during reproduction and toxin proteins in scorpion venoms.[16] [17] Defensin proteins are produced as an amphipathic protein precursor with one or two pro-domains that are removed to make the final mature protein. In their mature form, they generally consist of about 45 to 50 amino acid residues. The folded globular structure is characterized by a well-defined 3-stranded anti-parallel beta-sheet and a short alpha-helix.[18] The structure of most plant defensins is cross-linked by four disulfide bridges: three in the core and one linking the N- and C-termini. Some plant defensins have only the core three disulfides, and a few have been found with an additional one (resulting in five total bridges).[19] Two of these bonds, those formed between the α-helix and the last β-strand, are arranged into the Cys-stabilized α-helix β-strand (CSαβ) motif, which play significant roles in their biological activities and stability.[20] [21] The globular structures of plant defensins make them resistant to degradation by proteolytic digestion and stable up to a pH and a temperature range of 10 and 90 degrees Celsius, respectively.[22] [23]

Functions

Plant defensins are a large component of the plant innate immune system. They are regarded as highly promiscuous molecules due to their diverse biological functions. A plant genome typically contains large numbers of different defensin genes[24] that vary in their efficacy against different pathogens and the amount they are expressed in different tissues.[25] In addition to their functions in the immune system, many of these low-molecular-weight peptides have developed additional roles in aiding reproduction and abiotic stress tolerance.

Antimicrobial activity

Plant defensins elicit diverse antimicrobial properties, including antibacterial, and antifungal[26] activities. The modes of action of different defensins depend on the type of organism and specific molecular targets,[27] although their exact mechanisms of action vary. For instance, their antifungal activities, which are their best-characterized property, are attributed to their ability to interact with lipid structures on pathogenic fungi surfaces. These include sphingolipids,[28] glucosyceramide,[29] and phosphatidic acid[30] Apart from their capacity to attack and damage fungal membranes, these peptides have also been extensively researched for their capacity to trigger apoptosis and target other intracellular structures and biomolecules.[31] Plant defensins can spread their lethality by interfering with important developmental and/or regulatory processes, such as the cell cycle, when they perturb or disrupt the membrane of the fungus they target.[32] On the other hand, their ability to induce apoptosis has been linked to the bioaccumulation of reactive oxygen species[33] and the recruitment of specific caspases and caspase-associated proteins/[34] In mediating their antibacterial mechanisms, plant defensin has been shown to cause loss of cell viability by inducing an unfavorable morphological change in the bacterial target via membrane targeting and permeation.[35] This defensin-membrane interaction has been linked to the presence of the cationic amino acid residues arginine, lysine, and histidine.[36] Furthermore, studies have shown that plant defensin inhibits in vitro protein synthesis in a cell-free system,[37] and their interactions with the DNA of bacterial pathogens have also been documented, hinting that they might have a lethal effect on DNA replication or transcription.

Enzyme inhibition

Some plant defensins have also been identified as enzyme inhibitors of α-amylase or trypsin.[38] [39] [40] It is believed that these are antifeedant activities to deter insects. Typically, molecular modeling analysis of defensin expressed in Vigna unguiculata revealed that defensin inhibits α-amylase in the weevils Acanthoscelides obtectus and Zabrotes subfasciatus by binding via its N-terminal to the active site of the enzyme. Defensins with alpha-amylase-inhibitory activity have also been identified in Sorghum bicolor,[41] suggesting defensins might interfere with carbohydrate metabolism in insect targets. Beyond their ability to inhibit alpha-amylases, defensins also demonstrate inhibitory properties toward trypsin and chymotrypsin. For instance, two defensins from the seeds of Cassia fistula have been documented to inhibit the activity of trypsin,[42] and Capsicum annuum (CanDef-20) defensin has been reported to alter insect metabolism and retard growth in a number of ways, such as upregulation of lipase, serine endopeptidase, glutathione S-transferase, cadherin, alkaline phosphatase, and aminopeptidases and triggering transposon mobilization in Helicoverpa armigera.[43]

Anti-cancer

An additional promiscuous activity of some plant defensins is stopping the growth or disrupting the membranes of cancer cells in in vitro experiments.[44] [45] This interaction is basically facilitated and made stable due to the negatively charged membrane components on cancer cells relative to the positive charge of defensin.[46] [47] Typically, in addition to reducing the viability of melanoma and leukemia cells, Nicotiana alata defensin 1 (NaD1) reportedly induces the death of tumor cells within 30 minutes of contact.[48] This necrotic-like cell killing was facilitated by the binding of NaD1 to the plasma membrane lipid, phosphatidylinositol 4,5-bisphosphate (PIP2), which resulted in subsequent cell lysis. Defensins from plant origins have also shown potent toxicity towards colon and breast cancer.[49]

Abiotic stress tolerance

Plant defensins are expressed in diverse organelles and tissues in plants, and exposure of plants to specific environmental stresses has been associated with increased expression of defensin, suggesting their function in abiotic stress defense.[50] By means of endoplasmic reticulum adaptive activity, plant defensins AhPDF1.1 and AhPDF1.2 were recently found to exhibit metal (Zn) tolerance in yeast and plants.[51] Also, a defensin from paddy has been documented to sequester cadmium in rice, preventing its intracellular distribution. Overexpression of chickpea defensin gene also confers tolerance to water-deficit stress in Arabidopsis thaliana.[52]

Examples

The following plant proteins belong to this family:

Databases

A database for antimicrobial peptides, including defensins is available: PhytAMP (http://phytamp.hammamilab.org).[57]

Subfamilies

Notes and References

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  2. Sathoff AE, Samac DA . Antibacterial Activity of Plant Defensins . Molecular Plant-Microbe Interactions . 32 . 5 . 507–514 . May 2019 . 30501455 . 10.1094/mpmi-08-18-0229-cr . 205343360 . free .
  3. Carvalho A, Gomes VM . Plant defensins and defensin-like peptides - biological activities and biotechnological applications . Current Pharmaceutical Design . 17 . 38 . 4270–4293 . December 2011 . 22204427 . 10.2174/138161211798999447 .
  4. Javaux EJ, Knoll AH, Walter MR . Morphological and ecological complexity in early eukaryotic ecosystems . Nature . 412 . 6842 . 66–69 . July 2001 . 11452306 . 10.1038/35083562 . 205018792 .
  5. Tavares LS, Santos M, Viccini LF, Moreira JS, Miller RN, Franco OL . Biotechnological potential of antimicrobial peptides from flowers . Peptides . 29 . 10 . 1842–1851 . October 2008 . 18602431 . 10.1016/j.peptides.2008.06.003 . 25750244 .
  6. Lay FT, Poon S, McKenna JA, Connelly AA, Barbeta BL, McGinness BS, Fox JL, Daly NL, Craik DJ, Heath RL, Anderson MA . 6 . The C-terminal propeptide of a plant defensin confers cytoprotective and subcellular targeting functions . BMC Plant Biology . 14 . 1 . 41 . February 2014 . 24495600 . 3922462 . 10.1186/1471-2229-14-41 . free .
  7. Azmi S, Hussain MK . 2021-01-14 . Analysis of structures, functions, and transgenicity of phytopeptides defensin and thionin: a review . Beni-Suef University Journal of Basic and Applied Sciences . 10 . 1 . 10.1186/s43088-020-00093-5 . 2314-8543 . free .
  8. Mendez E, Moreno A, Colilla F, Pelaez F, Limas GG, Mendez R, Soriano F, Salinas M, de Haro C . 6 . Primary structure and inhibition of protein synthesis in eukaryotic cell-free system of a novel thionin, gamma-hordothionin, from barley endosperm . European Journal of Biochemistry . 194 . 2 . 533–539 . December 1990 . 2176600 . 10.1111/j.1432-1033.1990.tb15649.x . free .
  9. Colilla FJ, Rocher A, Mendez E . gamma-Purothionins: amino acid sequence of two polypeptides of a new family of thionins from wheat endosperm . FEBS Letters . 270 . 1–2 . 191–194 . September 1990 . 2226781 . 10.1016/0014-5793(90)81265-p . 9260786 . free .
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  14. Penninckx IA, Eggermont K, Terras FR, Thomma BP, De Samblanx GW, Buchala A, Métraux JP, Manners JM, Broekaert WF . 6 . Pathogen-induced systemic activation of a plant defensin gene in Arabidopsis follows a salicylic acid-independent pathway . The Plant Cell . 8 . 12 . 2309–2323 . December 1996 . 8989885 . 10.1105/tpc.8.12.2309 . 161354 .
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  19. Janssen BJ, Schirra HJ, Lay FT, Anderson MA, Craik DJ . Structure of Petunia hybrida defensin 1, a novel plant defensin with five disulfide bonds . Biochemistry . 42 . 27 . 8214–8222 . July 2003 . 12846570 . 10.1021/bi034379o .
  20. Cornet B, Bonmatin JM, Hetru C, Hoffmann JA, Ptak M, Vovelle F . Refined three-dimensional solution structure of insect defensin A . Structure . 3 . 5 . 435–448 . May 1995 . 7663941 . 10.1016/s0969-2126(01)00177-0 . free .
  21. Bontems F, Roumestand C, Boyot P, Gilquin B, Doljansky Y, Menez A, Toma F . Three-dimensional structure of natural charybdotoxin in aqueous solution by 1H-NMR. Charybdotoxin possesses a structural motif found in other scorpion toxins . European Journal of Biochemistry . 196 . 1 . 19–28 . February 1991 . 1705886 . 10.1111/j.1432-1033.1991.tb15780.x . free .
  22. Wong JH, Ng TB . Sesquin, a potent defensin-like antimicrobial peptide from ground beans with inhibitory activities toward tumor cells and HIV-1 reverse transcriptase . Peptides . 26 . 7 . 1120–1126 . July 2005 . 15949629 . 10.1016/j.peptides.2005.01.003 . 39557168 .
  23. Wong JH, Ng TB . Vulgarinin, a broad-spectrum antifungal peptide from haricot beans (Phaseolus vulgaris) . The International Journal of Biochemistry & Cell Biology . 37 . 8 . 1626–1632 . August 2005 . 15896669 . 10.1016/j.biocel.2005.02.022 .
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  28. Thevissen K, François IE, Takemoto JY, Ferket KK, Meert EM, Cammue BP . DmAMP1, an antifungal plant defensin from dahlia (Dahlia merckii), interacts with sphingolipids from Saccharomyces cerevisiae . FEMS Microbiology Letters . 226 . 1 . 169–173 . September 2003 . 13129623 . 10.1016/S0378-1097(03)00590-1 . free .
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  30. Kvansakul M, Lay FT, Adda CG, Veneer PK, Baxter AA, Phan TK, Poon IK, Hulett MD . 6 . Binding of phosphatidic acid by NsD7 mediates the formation of helical defensin-lipid oligomeric assemblies and membrane permeabilization . Proceedings of the National Academy of Sciences of the United States of America . 113 . 40 . 11202–11207 . October 2016 . 27647905 . 5056070 . 10.1073/pnas.1607855113 . free . 2016PNAS..11311202K .
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  32. Lobo DS, Pereira IB, Fragel-Madeira L, Medeiros LN, Cabral LM, Faria J, Bellio M, Campos RC, Linden R, Kurtenbach E . 6 . Antifungal Pisum sativum defensin 1 interacts with Neurospora crassa cyclin F related to the cell cycle . Biochemistry . 46 . 4 . 987–996 . January 2007 . 17240982 . 10.1021/bi061441j .
  33. Aerts AM, Bammens L, Govaert G, Carmona-Gutierrez D, Madeo F, Cammue BP, Thevissen K . The Antifungal Plant Defensin HsAFP1 from Heuchera sanguinea Induces Apoptosis in Candida albicans . Frontiers in Microbiology . 2 . 47 . 2011 . 21993350 . 3128936 . 10.3389/fmicb.2011.00047 . free .
  34. Thevissen K, de Mello Tavares P, Xu D, Blankenship J, Vandenbosch D, Idkowiak-Baldys J, Govaert G, Bink A, Rozental S, de Groot PW, Davis TR, Kumamoto CA, Vargas G, Nimrichter L, Coenye T, Mitchell A, Roemer T, Hannun YA, Cammue BP . 6 . The plant defensin RsAFP2 induces cell wall stress, septin mislocalization and accumulation of ceramides in Candida albicans . Molecular Microbiology . 84 . 1 . 166–180 . April 2012 . 22384976 . 3405362 . 10.1111/j.1365-2958.2012.08017.x .
  35. Velivelli SL, Islam KT, Hobson E, Shah DM . Modes of Action of a Bi-domain Plant Defensin MtDef5 Against a Bacterial Pathogen Xanthomonas campestris . Frontiers in Microbiology . 9 . 934 . 2018-05-16 . 29867843 . 5964164 . 10.3389/fmicb.2018.00934 . free .
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