Metabolism of plant-derived toxins from its insect host increases the success of the entomopathogenic fungus Beauveria bassiana.

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      Publisher: Nature Pub. Group Country of Publication: England NLM ID: 101301086 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1751-7370 (Electronic) Linking ISSN: 17517362 NLM ISO Abbreviation: ISME J Subsets: MEDLINE
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      Original Publication: London : Nature Pub. Group
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    • Abstract:
      Beauveria bassiana is a soil fungus that parasitizes a large number of arthropod species, including numerous crop pests, causing white muscardine disease and is therefore used as a biological insecticide. However, some insects, such as the cabbage aphid (Brevicoryne brassicae), defend themselves chemically by sequestering dietary pro-toxins (glucosinolates) from their Brassicales host plants. Glucosinolates are accumulated by cabbage aphids and activated to form toxic isothiocyanates when under attack. While isothiocyanate formation protects aphids against most attackers, B. bassiana is still able to infect the cabbage aphid under natural conditions. We therefore investigated how this fungus is able to circumvent the chemical defense system of the cabbage aphid. Here, we describe how B. bassiana infection activates the cabbage aphid defense system, but the resulting toxins are metabolized by B. bassiana via the mercapturic acid pathway, of which the first step is catalyzed by glutathione-S-transferases of low substrate specificity. This detoxification pathway enhances B. bassiana growth when isothiocyanates are present in natural concentrations, and so appears to be an important factor in fungal parasitization of these chemically defended aphids.
      (© 2023. The Author(s).)
    • References:
      Petschenka G, Agrawal AA. How herbivores coopt plant defenses: natural selection, specialization, and sequestration. Curr Opin Insect Sci. 2016;14:17–24. (PMID: 2743664210.1016/j.cois.2015.12.004)
      Hartmann T. Plant-derived secondary metabolites as defensive chemicals in herbivorous insects: a case study in chemical ecology. Planta. 2004;219:1–4. (PMID: 1504237010.1007/s00425-004-1249-y)
      Beran F, Petschenka G. Sequestration of plant defense compounds by insects: from mechanisms to insect–plant coevolution. Annu Rev Entomol. 2022;67:163–80. (PMID: 3499509110.1146/annurev-ento-062821-062319)
      Rask L, Andréasson E, Ekbom B, Eriksson S, Pontoppidan B, Meijer J. Myrosinase: gene family evolution and herbivore defense in Brassicaceae. Plant Mol Biol. 2000;42:93–114. (PMID: 1068813210.1023/A:1006380021658)
      Wittstock U, Kliebenstein DJ, Lambrix V, Reichelt M, Gershenzon J. Glucosinolate hydrolysis and its impact on generalist and specialist insect herbivores. Recent Adv Phytochem. 2003;37:101–25. (PMID: 10.1016/S0079-9920(03)80020-5)
      Sun R, Gols R, Harvey JA, Reichelt M, Gershenzon J, Pandit SS, et al. Detoxification of plant defensive glucosinolates by an herbivorous caterpillar is beneficial to its endoparasitic wasp. Mol Ecol. 2020;29:4014–31. (PMID: 3285346310.1111/mec.15613)
      Sun R, Jiang X, Reichelt M, Gershenzon J, Vassão DG. The selective sequestration of glucosinolates by the cabbage aphid severely impacts a predatory lacewing. J Pest Sci. 2021;94:1147–60. (PMID: 10.1007/s10340-020-01319-2)
      Louis J, Singh V, Shah J. Arabidopsis thaliana-aphid interaction. The Arabidopsis book. 2012;10:e0159. (PMID: 22666177336562310.1199/tab.0159)
      Kazana E, Pope TW, Tibbles L, Bridges M, Pickett JA, Bones AM, et al. The cabbage aphid: a walking mustard oil bomb. Proc Royal Soc B. 2007;274:2271–7. (PMID: 10.1098/rspb.2007.0237)
      Kos M, Kabouw P, Noordam R, Hendriks K, Vet LEM, Van Loon JJA, et al. Prey-mediated effects of glucosinolates on aphid predators. Ecol Entomol. 2011;36:377–88. (PMID: 10.1111/j.1365-2311.2011.01282.x)
      Sporer T, Körnig J, Beran F. Ontogenetic differences in the chemical defence of flea beetles influence their predation risk. Funct Ecol. 2020;34:1370–9. (PMID: 10.1111/1365-2435.13548)
      Kawakishi S, Namiki M. Oxidative cleavage of the disulfide bond of cystine by allyl isothiocyanate. J Agric Food Chem. 1982;30:618–20. (PMID: 10.1021/jf00111a056)
      Sotelo T, Lema M, Soengas P, Cartea ME, Velasco P. In vitro activity of glucosinolates and their degradation products against brassica-pathogenic bacteria and fungi. Appl Environ Microbiol. 2015;81:432–40. (PMID: 2536205810.1128/AEM.03142-14)
      Aires A, Mota VR, Saavedra MJ, Monteiro AA, Simões M, Rosa EA, et al. Initial in vitro evaluations of the antibacterial activities of glucosinolate enzymatic hydrolysis products against plant pathogenic bacteria. J Appl Microbiol. 2009;106:2096–105. (PMID: 1929123910.1111/j.1365-2672.2009.04181.x)
      Manici LM, Lazzeri L, Palmieri S. In vitro fungitoxic activity of some glucosinolates and their enzyme-derived products toward plant pathogenic fungi. J Agric Food Chem. 1997;45:2768–73. (PMID: 10.1021/jf9608635)
      Pratt C, Pope TW, Powell G, Rossiter JT. Accumulation of glucosinolates by the cabbage aphid Brevicoryne brassicae as a defense against two Coccinellid species. J Chem Ecol. 2008;34:323–9. (PMID: 1827078010.1007/s10886-007-9421-z)
      Zhang WQ, Hassan SA. Use of the parasitoid Diaeretiella rapae (McIntoch) to control the cabbage aphid Brevicoryne brassicae (L.). J Appl Entomol. 2003;127:522–6. (PMID: 10.1046/j.1439-0418.2003.00792.x)
      Asi MR, Bashir MH, Afzal M, Imran S. Effect of conidial concentration of entomopathogenic fungi on mortality of cabbage aphid, Brevicoryne brassicae L. Pak J Life Soc Sci. 2009;2:175–80.
      Wraight SP, Carruthers RI, Jaronski ST, Bradley CA, Garza CJ, Galaini-Wraight S. Evaluation of the entomopathogenic fungi Beauveria bassiana and Paecilomyces fumosoroseus for microbial control of the silverleaf whitefly, Bemisia argentifolii. Biol Control. 2000;17:203–17. (PMID: 10.1006/bcon.1999.0799)
      Islam MT, Castle SJ, Ren S. Compatibility of the insect pathogenic fungus Beauveria bassiana with neem against sweetpotato whitefly, Bemisia tabaci, on eggplant. Entomol Exp Appl. 2010;134:28–34. (PMID: 10.1111/j.1570-7458.2009.00933.x)
      Akbari S, Ali Safavi S, Ghosta Y. Efficacy of Beauveria bassiana (Blas.) Vuill. against cabbage aphid Brevicoryne brassicae L. (Hem.: Aphididae) in laboratory condition. Arch Phytopathol Pflanzenschutz. 2014;47:1454–8. (PMID: 10.1080/03235408.2013.845972)
      Milner RJ. Prospects for biopesticides for aphid control. Entomophaga. 1997;42:227–39.
      Mann AJ, Davis TS. Plant secondary metabolites and low temperature are the major limiting factors for Beauveria bassiana (Bals.-Criv.) Vuill. (Ascomycota: Hypocreales) growth and virulence in a bark beetle system. Biol Control. 2020;141:104130. (PMID: 10.1016/j.biocontrol.2019.104130)
      Posada F, Vega FE, Rehner SA, Blackwell M, Weber D, Suh S-O, et al. Syspastospora parasitica, a mycoparasite of the fungus Beauveria bassiana attacking the Colorado potato beetle Leptinotarsa decemlineata: a tritrophic association. J Insect Sci. 2004;4:24. (PMID: 15861239528884)
      Mascarin GM, Jaronski S. The production and uses of Beauveria bassiana as a microbial insecticide. World J Microbiol Biotechnol. 2016;32:177. (PMID: 2762833710.1007/s11274-016-2131-3)
      Inyang EN, Butt TM, Doughty KJ, Todd AD, Archer S. The effects of isothiocyanates on the growth of the entomopathogenic fungus Metarhizium anisopliae and its infection of the mustard beetle. Mycol Res. 1999;103:974–80. (PMID: 10.1017/S0953756298007989)
      Atsumi A, Saito T. Volatiles from wasabi inhibit entomopathogenic fungi: implications for tritrophic interactions and biological control. J Plant Interact. 2015;10:152–7. (PMID: 10.1080/17429145.2015.1039613)
      Ramanujam B, Japur K, Poornesha B. Field evaluation of entomopathogenic fungi against cabbage aphid, Brevicoryne brassicae (L.) and their effect on coccinellid predator, Coccinella septempunctata (Linnaeus). J Biol Control. 2018;31:168–71. (PMID: 10.18311/jbc/2017/16350)
      Pacheco JC, Poltronieri AS, Porsani MV, Zawadneak MAC, Pimentel IC. Entomopathogenic potential of fungi isolated from intertidal environments against the cabbage aphid Brevicoryne brassicae (Hemiptera: aphididae). Biocontrol Sci Technol. 2017;27:496–509. (PMID: 10.1080/09583157.2017.1315053)
      Blažević I, Montaut S, Burčul F, Olsen CE, Burow M, Rollin P, et al. Glucosinolate structural diversity, identification, chemical synthesis and metabolism in plants. Phytochem. 2020;169:112100. (PMID: 10.1016/j.phytochem.2019.112100)
      Brown PD, Tokuhisa JG, Reichelt M, Gershenzon J. Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana. Phytochem. 2003;62:471–81. (PMID: 10.1016/S0031-9422(02)00549-6)
      Ratzka A, Vogel H, Kliebenstein DJ, Mitchell-Olds T, Kroymann J. Disarming the mustard oil bomb. Proc Natl Acad Sci USA. 2002;99:11223–8. (PMID: 1216156312323710.1073/pnas.172112899)
      Wittstock U, Agerbirk N, Stauber EJ, Olsen CE, Hippler M, Mitchell-Olds T, et al. Successful herbivore attack due to metabolic diversion of a plant chemical defense. Proc Natl Acad Sci USA. 2004;101:4859–64. (PMID: 1505187838733910.1073/pnas.0308007101)
      Jeschke V, Kearney EE, Schramm K, Kunert G, Shekhov A, Gershenzon J, et al. How glucosinolates affect generalist lepidopteran larvae: growth, development and glucosinolate metabolism. Front Plant Sci. 2017;8:1995. (PMID: 29209354570229310.3389/fpls.2017.01995)
      Chen J, Ullah C, Reichelt M, Beran F, Yang Z-L, Gershenzon J, et al. The phytopathogenic fungus Sclerotinia sclerotiorum detoxifies plant glucosinolate hydrolysis products via an isothiocyanate hydrolase. Nat Commun. 2020;11:3090. (PMID: 32555161730311310.1038/s41467-020-16921-2)
      Fan J, Crooks C, Creissen G, Hill L, Fairhurst S, Doerner P, et al. Pseudomonas sax genes overcome aliphatic isothiocyanate-mediated non-host resistance in Arabidopsis. Science. 2011;331:1185–8. (PMID: 2138571410.1126/science.1199707)
      Gloss AD, Vassão DG, Hailey AL, Dittrich ACN, Schramm K, Reichelt M, et al. Evolution in an ancient detoxification pathway Is coupled with a transition to herbivory in the Drosophilidae. Mol Biol Evol. 2014;31:2441–56. (PMID: 24974374413771810.1093/molbev/msu201)
      Lekberg Y, Arnillas CA, Borer ET, Bullington LS, Fierer N, Kennedy PG, et al. Nitrogen and phosphorus fertilization consistently favor pathogenic over mutualistic fungi in grassland soils. Nat Commun. 2021;12:3484. (PMID: 34108462819009610.1038/s41467-021-23605-y)
      Zagrobelny M, Bak S, Ekstrøm CT, Olsen CE, Møller BL. The cyanogenic glucoside composition of Zygaena filipendulae (Lepidoptera: Zygaenidae) as effected by feeding on wild-type and transgenic lotus populations with variable cyanogenic glucoside profiles. Insect Biochem Mol Biol. 2007;37:10–18. (PMID: 1717544210.1016/j.ibmb.2006.09.008)
      Beran F, Pauchet Y, Kunert G, Reichelt M, Wielsch N, Vogel H, et al. Phyllotreta striolata flea beetles use host plant defense compounds to create their own glucosinolate-myrosinase system. Proc Natl Acad Sci USA. 2014;111:7349–54. (PMID: 24799680403419810.1073/pnas.1321781111)
      Bramer C, Friedrich F, Dobler S. Defence by plant toxins in milkweed bugs (Heteroptera: Lygaeinae) through the evolution of a sophisticated storage compartment. Syst Entomol. 2017;42:15–30. (PMID: 10.1111/syen.12189)
      Thorpe KW, Barbosa P. Effects of comsumption of high and low nicotine tobacco by Manduca sexta (Lepidoptera: Sphingidae) on survival of gregarious endoparasitoid Cotesia congregata (Hymenoptera: Braconidae). J Chem Ecol. 1986;12:1329–37. (PMID: 2430711210.1007/BF01012352)
      Bramer C, Dobler S, Deckert J, Stemmer M, Petschenka G. Na+/K+-ATPase resistance and cardenolide sequestration: basal adaptations to host plant toxins in the milkweed bugs (Hemiptera: Lygaeidae: Lygaeinae). Proc Royal Soc B. 2015;282:20142346. (PMID: 10.1098/rspb.2014.2346)
      Zagrobelny M, Bak S, Møller BL. Cyanogenesis in plants and arthropods. Phytochem. 2008;69:1457–68. (PMID: 10.1016/j.phytochem.2008.02.019)
      Yang ZL, Nour-Eldin HH, Hänniger S, Reichelt M, Crocoll C, Seitz F, et al. Sugar transporters enable a leaf beetle to accumulate plant defense compounds. Nat Commun. 2021;12:2658. (PMID: 33976202811346810.1038/s41467-021-22982-8)
      Friedrichs J, Schweiger R, Müller C. Unique metabolism of different glucosinolates in larvae and adults of a leaf beetle specialised on Brassicaceae. Sci Rep. 2022;12:10905. (PMID: 35764778924007910.1038/s41598-022-14636-6)
      Thungrabeab M, Blaeser P, Sengonca C. Effect of temperature and host plant on the efficacy of different entomopathogenic fungi from Thailand against Frankliniella occidentalis (Pergande) and Thrips tabaci Lindeman (Thysanoptera: Thripidae) in the laboratory. J Plant Dis Prot. 2006;113:181–7. (PMID: 10.1007/BF03356177)
      Santiago-Álvarez C, Maranhão EA, Maranhão E, Quesada-Moraga E. Host plant influences pathogenicity of Beauveria bassiana to Bemisia tabaci and its sporulation on cadavers. Biocontrol. 2006;51:519–32. (PMID: 10.1007/s10526-005-5737-1)
      Ugine TA, Wraight SP, Sanderson JP. A tritrophic effect of host plant on susceptibility of western flower thrips to the entomopathogenic fungus Beauveria bassiana. J Invertebr Pathol. 2007;96:162–72. (PMID: 1757243810.1016/j.jip.2007.05.004)
      Poprawski TJ, Jones WJ. Host plant effects on activity of the mitosporic fungi Beauveria bassiana and Paecilomyces fumosoroseus against two populations of Bemisia whiteflies (Homoptera: Aleyrodidae). Mycopathologia. 2001;151:11–20. (PMID: 1150205810.1023/A:1010835224472)
      Soth S, Glare TR, Hampton JG, Card SD, Brookes JJ, Narciso JO. You are what you eat: fungal metabolites and host plant affect the susceptibility of diamondback moth to entomopathogenic fungi. PeerJ. 2022;10:e14491. (PMID: 36570000977400510.7717/peerj.14491)
      Brown KK, Hampton MB. Biological targets of isothiocyanates. Biochim Biophys Acta. 2011;1810:888–94. (PMID: 2170412710.1016/j.bbagen.2011.06.004)
      Schramm K, Vassão DG, Reichelt M, Gershenzon J, Wittstock U. Metabolism of glucosinolate-derived isothiocyanates to glutathione conjugates in generalist lepidopteran herbivores. Insect Biochem Mol Biol. 2012;42:174–82. (PMID: 2219339210.1016/j.ibmb.2011.12.002)
      Zhang YS, Kolm RH, Mannervik B, Talalay P. Reversible conjugation of isothiocyanates with glutathione catalyzed by human glutathione transferases. Biochem Biophys Res Commun. 1995;206:748–55. (PMID: 782639610.1006/bbrc.1995.1106)
      Sun R, Jiang XC, Reichelt M, Gershenzon J, Pandit SS, Vassão DG. Tritrophic metabolism of plant chemical defenses and its effects on herbivore and predator performance. eLife. 2019;8:e51029. (PMID: 31841109693438110.7554/eLife.51029)
      Li X. Molecular mechanisms of metabolic resistance to synthetic and natural xenobiotics. Annu Rev Entomol. 2007;52:231–53. (PMID: 1692547810.1146/annurev.ento.51.110104.151104)
      Frova C. Glutathione transferases in the genomics era: new insights and perspectives. Biomol Eng. 2006;23:149–69. (PMID: 1683981010.1016/j.bioeng.2006.05.020)
      Sheehan D, Meade G, Foley VM, Dowd CA. Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochem. 2001;360:1–16. (PMID: 10.1042/bj3600001)
      McGoldrick S, O’Sullivan SM, Sheehan D. Glutathione transferase-like proteins encoded in genomes of yeasts and fungi: insights into evolution of a multifunctional protein superfamily. FEMS Microbiol Lett. 2005;242:1–12. (PMID: 1562141410.1016/j.femsle.2004.10.033)
      Morel M, Ngadin AA, Droux M, Jacquot J-P, Gelhaye E. The fungal glutathione S-transferase system. Evidence of new classes in the wood-degrading basidiomycete Phanerochaete chrysosporium. Cell Mol Life Sci. 2009;66:3711–25. (PMID: 1966250010.1007/s00018-009-0104-5)
      Morel M, Meux E, Mathieu Y, Thuillier A, Chibani K, Harvengt L, et al. Xenomic networks variability and adaptation traits in wood decaying fungi. Microb Biotechnol. 2013;6:248–63. (PMID: 23279857381592010.1111/1751-7915.12015)
      Shen M, Zhao D-K, Qiao Q, Liu L, Wang J-L, Cao G-H, et al. Identification of glutathione S-transferase (GST) genes from a dark septate endophytic fungus (Exophiala pisciphila) and their expression patterns under varied metals stress. PLoS One. 2015;10:e0123418. (PMID: 25884726440168510.1371/journal.pone.0123418)
      Zou X, Xu Z, Zou H, Liu J, Chen S, Feng Q, et al. Glutathione S-transferase SlGSTE1 in Spodoptera litura may be associated with feeding adaptation of host plants. Insect Biochem Mol Biol. 2016;70:32–43. (PMID: 2663159910.1016/j.ibmb.2015.10.005)
      Mazari AMA, Dahlberg O, Mannervik B, Mannervik M. Overexpression of glutathione transferase E7 in Drosophila differentially impacts toxicity of organic isothiocyanates in males and females. PLoS One. 2014;9:e110103. (PMID: 25329882419963110.1371/journal.pone.0110103)
      Gonzalez D, Fraichard S, Grassein P, Delarue P, Senet P, Nicolaï A, et al. Characterization of a Drosophila glutathione transferase involved in isothiocyanate detoxification. Insect Biochem Mol Biol. 2018;95:33–43. (PMID: 2957804710.1016/j.ibmb.2018.03.004)
      Heidel-Fischer HM, Kirsch R, Reichelt M, Ahn S-J, Wielsch N, Baxter SW, et al. An insect counteradaptation against host plant defenses evolved through concerted neofunctionalization. Mol Biol Evol. 2019;36:930–41. (PMID: 30715408650187410.1093/molbev/msz019)
      Manivannan A, Israni B, Luck K, Götz M, Seibel E, Easson MLAE, et al. Identification of a sulfatase that detoxifies glucosinolates in the phloem-feeding insect Bemisia tabaci and prefers indolic glucosinolates. Front Plant Sci. 2021;12:671286. (PMID: 34149771821212910.3389/fpls.2021.671286)
      Jeschke V, Gershenzon J, Vassão DG. A mode of action of glucosinolate-derived isothiocyanates: detoxification depletes glutathione and cysteine levels with ramifications on protein metabolism in Spodoptera littoralis. Insect Biochem Mol Biol. 2016;71:37–48. (PMID: 2685519710.1016/j.ibmb.2016.02.002)
    • Accession Number:
      0 (Glucosinolates)
      0 (Insecticides)
      0 (Isothiocyanates)
    • Publication Date:
      Date Created: 20230721 Date Completed: 20230918 Latest Revision: 20230922
    • Publication Date:
      20240829
    • Accession Number:
      PMC10504261
    • Accession Number:
      10.1038/s41396-023-01480-3
    • Accession Number:
      37479887