Tryptamine accumulation caused by deletion of MrMao-1 in Metarhizium genome significantly enhances insecticidal virulence


Autoři: Xiwen Tong aff001;  Yundan Wang aff001;  Pengcheng Yang aff003;  Chengshu Wang aff004;  Le Kang aff001
Působiště autorů: State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing, China aff001;  University of Chinese Academy of Sciences, Beijing, China aff002;  Beijing Institutes of Life Science, Chinese Academy of Sciences, Beijing, China aff003;  Key Laboratory of Insect Developmental and Evolutionary Biology, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, China aff004
Vyšlo v časopise: Tryptamine accumulation caused by deletion of MrMao-1 in Metarhizium genome significantly enhances insecticidal virulence. PLoS Genet 16(4): e32767. doi:10.1371/journal.pgen.1008675
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008675

Souhrn

Metarhizium is a group of insect-pathogenic fungi that can produce insecticidal metabolites, such as destruxins. Interestingly, the acridid-specific fungus Metarhizium acridum (MAC) can kill locusts faster than the generalist fungus Metarhizium robertsii (MAA) even without destruxin. However, the underlying mechanisms of different pathogenesis between host-generalist and host-specialist fungi remain unknown. This study compared transcriptomes and metabolite profiles to analyze the difference in responsiveness of locusts to MAA and MAC infections. Results confirmed that the detoxification and tryptamine catabolic pathways were significantly enriched in locusts after MAC infection compared with MAA infection and that high levels of tryptamine could kill locusts. Furthermore, tryptamine was found to be capable of activating the aryl hydrocarbon receptor of locusts (LmAhR) to produce damaging effects by inducing reactive oxygen species production and immune suppression. Therefore, reducing LmAhR expression by RNAi or inhibitor (SR1) attenuates the lethal effects of tryptamine on locusts. In addition, MAA, not MAC, possessed the monoamine oxidase (Mao) genes in tryptamine catabolism. Hence, deleting MrMao-1 could increase the virulence of generalist MAA on locusts and other insects. Therefore, our study provides a rather feasible way to design novel mycoinsecticides by deleting a gene instead of introducing any exogenous gene or domain.

Klíčová slova:

Fats – Fungal genetics – Fungi – Gene expression – Insects – Locusts – Metarhizium – Virulence factors


Zdroje

1. Lomer CJ, Bateman RP, Johnson DL, Langewald J, Thomas M (2001) Biological control of locusts and grasshoppers. Annu Rev of Entomol 46: 667–702.

2. Wang C, Wang S (2017) Insect Pathogenic Fungi: Genomics, Molecular Interactions, and Genetic Improvements. Annu Rev Entomol 62: 73–90. doi: 10.1146/annurev-ento-031616-035509 27860524

3. de Faria MR, Wraight SP (2007) Mycoinsecticides and Mycoacaricides: A comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43: 237–256.

4. Fornelli F, Minervini F, Logrieco A (2004) Cytotoxicity of fungal metabolites to lepidopteran (Spodoptera frugiperda) cell line (SF-9). J Invertebr Pathol 85: 74–79. doi: 10.1016/j.jip.2004.01.002 15050836

5. Wang CS, Skrobek A, Butt TM (2004) Investigations on the destruxin production of the entomopathogenic fungus Metarhizium anisopliae. J Invertebr Pathol 85: 168–174. doi: 10.1016/j.jip.2004.02.008 15109899

6. Branine M, Bazzicalupo A, Branco S (2019) Biology and applications of endophytic insect-pathogenic fungi. PLoS Pathog 15: e1007831. doi: 10.1371/journal.ppat.1007831 31318959

7. Gao QA, Jin K, Ying SH, Zhang YJ, Xiao GH, et al. (2011) Genome Sequencing and Comparative Transcriptomics of the Model Entomopathogenic Fungi Metarhizium anisopliae and M. acridum. PloS Genet 7: e1001264. doi: 10.1371/journal.pgen.1001264 21253567

8. Wang C, St Leger RJ (2005) Developmental and transcriptional responses to host and nonhost cuticles by the specific locust pathogen Metarhizium anisopliae var. acridum. Eukaryot Cell 4: 937–947. doi: 10.1128/EC.4.5.937-947.2005 15879528

9. Wang SB, Fang WG, Wang CS, Leger RJS (2011) Insertion of an Esterase Gene into a Specific Locust Pathogen (Metarhizium acridum) Enables It to Infect Caterpillars. PloS Pathog 7: e1002097. doi: 10.1371/journal.ppat.1002097 21731492

10. Hu X, Xiao GH, Zheng P, Shang YF, Su Y, et al. (2014) Trajectory and genomic determinants of fungal-pathogen speciation and host adaptation. Proc Natl Acad Sci U S A 111: 16796–16801. doi: 10.1073/pnas.1412662111 25368161

11. Xu YJ, Luo F, Li B, Shang Y, Wang C (2016) Metabolic Conservation and Diversification of Metarhizium Species Correlate with Fungal Host-Specificity. Front Microbiol 7: 2020. doi: 10.3389/fmicb.2016.02020 28018335

12. Gillespie JP, Bailey AM, Cobb B, Vilcinskas A (2000) Fungi as elicitors of insect immune responses. Arch Insect Biochem 44: 49–68.

13. Rohlfs M, Churchill ACL (2011) Fungal secondary metabolites as modulators of interactions with insects and other arthropods. Fungal Genet Biol 48: 23–34. doi: 10.1016/j.fgb.2010.08.008 20807586

14. Fan AL, Mi WB, Liu ZG, Zeng GH, Zhang P, et al. (2017) Deletion of a Histone Acetyltransferase Leads to the Pleiotropic Activation of Natural Products in Metarhizium robertsii. Org Lett 19: 1686–1689. doi: 10.1021/acs.orglett.7b00476 28301168

15. Pal S, St Leger RJ, Wu LP (2007) Fungal Peptide Destruxin A Plays a Specific Role in Suppressing the Innate Immune Response in Drosophila melanogaster. J Biol Chem 282, 8969–8977. doi: 10.1074/jbc.M605927200 17227774

16. Wang Y, Yang P, Cui F, Kang L (2013) Altered immunity in crowded locust reduced fungal (Metarhizium anisopliae) pathogenesis. PLoS Pathog 9: e1003102. doi: 10.1371/journal.ppat.1003102 23326229

17. Thomas JC, Adams DG, Nessler CL, Brown JK, Bohnert HJ (1995) Tryptophan Decarboxylase, Tryptamine, and Reproduction of the Whitefly. Plant Physiol 109: 717–720. doi: 10.1104/pp.109.2.717 12228625

18. Thomas JC, Saleh EF, Akroush AM (1996) Tryptamine: Plant-synthesized compounds for self defense against insects. Plant Physiol 111: 303–303.

19. Oliveira RRB, Brito TB, Nepel A, Costa EV, Barison A, et al. (2014) Synthesis, Activity, and QSAR Studies of Tryptamine Derivatives on Third-instar Larvae of Aedes Aegypti Linn. Med Chem 10: 580–587. doi: 10.2174/1573406409666131202144010 24295020

20. Ali S E, Abdel-Aty A S (2010) Insecticidal activity of some indole derivatives against Spodoptera littoralis (Boisd.). Alex J Agric Res 55: 1–11.

21. Liao XG, Lovett B, Fang WG, St Leger RJ (2017) Metarhizium robertsii produces indole-3-acetic acid, which promotes root growth in Arabidopsis and enhances virulence to insects. Microbiology 163: 980–991. doi: 10.1099/mic.0.000494 28708056

22. Wat CK, Towers GHN (1979) Metabolism of the Aromatic Amino Acids by Fungi. Biochemistry of Plant Phenolics. Biochemistry of Plant Phenolics. Springer, Boston, MA, 1979: 371–432.

23. Stockinger B, Di Meglio P, Gialitakis M, Duarte JH (2014) The Aryl Hydrocarbon Receptor: Multitasking in the Immune System. Annu Rev Immunol 32: 403–432. doi: 10.1146/annurev-immunol-032713-120245 24655296

24. Gill RIS, Ellis BE (2006) Over-expression of tryptophan decarboxylase gene in poplar and its possible role in resistance against Malacosoma disstria. New Forests 31: 195–209.

25. Gill RI, Ellis BE, Isman MB (2003) Tryptamine-induced resistance in tryptophan decarboxylase transgenic poplar and tobacco plants against their specific herbivores. J Chem Ecol 29: 779–793. doi: 10.1023/a:1022983529555 12775143

26. Thomas JC, Saleh EF, Alammar N, Akroush AM (1998) The indole alkaloid tryptamine impairs reproduction in Drosophila melanogaster. J Econ Entomol 91: 841–846. doi: 10.1093/jee/91.4.841 9725032

27. Radwanski ER, Last RL (1995) Tryptophan biosynthesis and metabolism: biochemical and molecular genetics. Plant Cell 7: 921–934. doi: 10.1105/tpc.7.7.921 7640526

28. Clarke AJ, Mann PJ (1957) The oxidation of tryptamine to 3-indolylacetaldehyde by plant amine oxidase. Biochem J 65: 763–774. doi: 10.1042/bj0650763 13426099

29. Behie SW, Zelisko PM, Bidochka MJ1 (2012) Endophytic Insect-Parasitic Fungi Translocate Nitrogen Directly from Insects to Plants. Science 336:1576–1577. doi: 10.1126/science.1222289 22723421

30. Bergander LV, Cai W, Klocke B, Seifert M, Pongratz I (2012) Tryptamine Serves As a Proligand of the AhR Transcriptional Pathway Whose Activation Is Dependent of Monoamine Oxidases. Mol Endocrinol 26: 1542–1551. doi: 10.1210/me.2011-1351 22865928

31. Schulenburg H, Kurtz J, Moret Y, Siva-Jothy MT (2009) Introduction. Ecological immunology. Philos Trans R Soc Lond B Biol Sci 364: 3–14. doi: 10.1098/rstb.2008.0249 18926970

32. Xu C, Li CY, Kong AN (2005) Induction of phase I, II and III drug metabolism/transport by xenobiotics. Arch Pharm Res 28: 249–268. doi: 10.1007/bf02977789 15832810

33. Lu AR, Zhang QL, Zhang J, Yang B, Wu K, et al. (2014) Insect prophenoloxidase: the view beyond immunity. Front Physiol 5: 525. doi: 10.3389/fphys.2014.00525

34. Patel S (2017) A critical review on serine protease: Key immune manipulator and pathology mediator. Allergol Immunopath 45: 579–591.

35. Zhang Z, Yuan Y, Liu Q, Yin H (2019) Plant nitrogen acquisition from inorganic and organic sources via root and mycelia pathways in ectomycorrhizal alpine forests. Soil Biol Biochem 136: 107517.

36. Näsholm T, Kielland K, Ganeteg U (2009) Uptake of organic nitrogen by plants. New Phytol 182: 31–48. doi: 10.1111/j.1469-8137.2008.02751.x 19210725

37. St Leger RJ, Nelson JO, Screen SE (1999) The entomopathogenic fungus Metarhizium anisopliae alters ambient pH, allowing extracellular protease production and activity. Microbiology 145: 2691–2699. doi: 10.1099/00221287-145-10-2691 10537191

38. de Bekker C, Smith PB, Patterson AD, Hughes DP (2013) Metabolomics reveals the heterogeneous secretome of two entomopathogenic fungi to ex vivo cultured insect tissues. PLoS One 8: e70609. doi: 10.1371/journal.pone.0070609 23940603

39. Lovett B, Bilgo E, Millogo SA, Ouattarra AK, Sare I, et al. (2019) Transgenic Metarhizium rapidly kills mosquitoes in a malaria-endemic region of Burkina Faso. Science 364, 894–897. doi: 10.1126/science.aaw8737 31147521

40. Floch GL, Rey P, Benizri E, Benhamou N, Tirilly Y (2003) Impact of auxin-compounds produced by the antagonistic fungus Pythium oligandrum or the minor pathogen Pythium group F on plant growth. Plant and Soil 257: 459–470.

41. Ma ZY, Guo W, Guo XJ, Wang XH, Kang L (2011) Modulation of behavioral phase changes of the migratory locust by the catecholamine metabolic pathway. Proc Natl Acad Sci U S A 108: 3882–3887. doi: 10.1073/pnas.1015098108 21325054

42. Xu J, Chi F, Guo TS, Punj V, Lee WNP, et al. (2015) NOTCH reprograms mitochondrial metabolism for proinflammatory macrophage activation. J Clin Invest 125: 1579–1590. doi: 10.1172/JCI76468 25798621

43. Yildirim HK, Uren A, Yucel U (2007) Evaluation of biogenic amines in organic and non-organic wines by HPLC OPA derivatization. Food Technol Biotech 45: 62–68.

44. Chen YX, Duan ZB, Chen PL, Shang YF, Wang CS (2015) The Bax inhibitor MrBI-1 regulates heat tolerance, apoptotic-like cell death, and virulence in Metarhizium robertsii. Scientific Reports 5: 10625. doi: 10.1038/srep10625 26023866

45. Rangel DEN, Alston DG, Roberts DW (2008) Effects of physical and nutritional stress conditions during mycelial growth on conidial germination speed, adhesion to host cuticle, and virulence of Metarhizium anisopliae, an entomopathogenic fungus. Mycol Res 112: 1355–1361. doi: 10.1016/j.mycres.2008.04.011 18947989

46. Shan LT, Feng MG (2010) Evaluation of the biocontrol potential of various Metarhizium isolates against green peach aphid Myzus persicae (Homoptera: Aphididae). Pest Manag Sci 66: 669–675. doi: 10.1002/ps.1928 20201034

47. Scholte EJ, Takken W, Knols BGJ (2007) Infection of adult Aedes aegypti and Ae. albopictus mosquitoes with the entomopathogenic fungus Metarhizium anisopliae. Acta Tropica 102: 151–158. doi: 10.1016/j.actatropica.2007.04.011 17544354

Štítky
Genetika Reprodukční medicína

Článek vyšel v časopise

PLOS Genetics


2020 Číslo 4

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

VIRTUÁLNÍ ČEKÁRNA ČR Jste praktický lékař nebo pediatr? Zapojte se! Jste praktik nebo pediatr? Zapojte se!

×