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Molecular insight into the endophytic growth of Beauveria bassiana within Phaseolus vulgaris in the presence or absence of Tetranychus urticae

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Abstract

Entomopathogenic fungi are an important factor in the natural regulation of arthropod populations. Moreover, some can exist as an endophyte in many plant species and establish a mutualistic relationship. In this study, we have investigated the endophytic growth of Beauveria bassiana within different tissues of Phaseolus vulgaris in the presence and absence of Tetranuychus urticae. After the colonization of the B. bassiana within the internal tissues of P. vulgaris. The susceptibility of T. urticae appeared to depend on the life stage where high, moderate, and low mortalities were recorded among adults, nymphs, and eggs, respectively. In addition, this study provided, for the first time, molecular insight into the endophytic growth of B. bassiana by analyzing the expression of several genes involved in the development of the entomopathogenic fungi at 0-, 2-, and 7- days post-inoculation. B. bassiana displayed preferential tissue colonization within P. vulgaris that can be put into the following order based on the detection rate: leaf > stem > root. After analyzing the development-implicated genes (degrading enzymes, sugar transporter, hydrophobins, cell wall synthesis, secondary metabolites, stress management), the most remarkable finding is the detection of behavioral change between parasitic and endophytic Beauveria during post-penetration events. This study elucidates the tri-trophic interaction between fungus-plant-herbivore.

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References

  1. Smith GS, O'Day MH, Reid W (2019) Pecan pest management: insects and diseases. Department of entomology, Kansas State University. https://extension2.missouri.edu/mp711. Accessed July 2020

  2. Aktar W, Sengupta D, Chowdhury A (2009) Impact of pesticides use in agriculture: their benefits and hazards. Interdiscip Toxicol 2:1–12

    PubMed  PubMed Central  Google Scholar 

  3. Plant R, Freudenberger D (2005) Changes in global agriculture: a framework for diagnosing ecosystem effects and identifying response options. WWF Macroeconomics Program Office Washington, DC, USA

  4. 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

    Google Scholar 

  5. Cafarchia C, Immediato D, Iatta R, Ramos RAN, Lia RP, Porretta D, Figueredo LA, Dantas-Torres F, Otranto D (2015) Native strains of Beauveriabassiana for the control of Rhipicephalussanguineus sensu lato. Parasite Vectors 8:80

    CAS  Google Scholar 

  6. Chandler D, Davidson G, Jacobson RJ (2005) Laboratory and glasshouse evaluation of entomopathogenic fungi against the two-spotted spider mite, Tetranychusurticae (Acari: Tetranychidae), on tomato, Lycopersicon esculentum. Biocontrol Sci Technol 15:37–54

    Google Scholar 

  7. Immediato D, Camarda A, Iatta R, Puttilli MR, Ramos RAN, Di Paola G, Giangaspero A, Otranto D, Cafarchia C (2015) Laboratory evaluation of a native strain of Beauveriabassiana for controlling Dermanyssusgallinae (De Geer, 1778)(Acari: Dermanyssidae). Vet Parasitol 212:478–482

    PubMed  Google Scholar 

  8. Kaiser D, Handschin S, Rohr RP, Bacher S, Grabenweger G (2020) Co-formulation of Beauveriabassiana with natural substances to control pollen beetles–synergy between fungal spores and colza oil. Biol Control 140:104106

    CAS  Google Scholar 

  9. Morales AD, Castillo A, Cisneros J, Valle JF, Gómez J (2019) Effect of spinosad combined with Beauveriabassiana (Hypocreales: Clavicipitaceae) on Hypothenemushampei (Coleoptera: Curculionidae) under laboratory conditions. J Entomol Sci 54:106–109

    Google Scholar 

  10. Mwamburi LA, Laing MD, Miller RM (2019) External development of the entomopathogenic fungus beauveria bassiana on the housefly (Muscadomestica). Proc Natl Acad Sci India B 89:833–839

    CAS  Google Scholar 

  11. Yanar Y, Yanar D, Demir B, Karan YB (2019) Effects of local entomopathogen Beauveriabassiana isolates against Sitophilusgranaries (Coleoptera). Poljoprivreda i Sumarstvo 65:49–55

    Google Scholar 

  12. Feng MG, Poprawski TJ, Khachatourians GG (1994) Production, formulation and application of the entomopathogenic fungus Beauveriabassiana for insect control: current status. Biocontrol Sci Technol 4:3–34

    Google Scholar 

  13. Butt TM, Coates CJ, Dubovskiy IM, Ratcliffe NA (2016) Entomopathogenic fungi: new insights into host–pathogen interactions. Anonymous advances in genetics, vol 94. Elsevier, Amsterdam, pp 307–364

    Google Scholar 

  14. Mondal S, Baksi S, Koris A, Vatai G (2016) Journey of enzymes in entomopathogenic fungi. Pac Sci Rev A 18:85–99

    Google Scholar 

  15. Zhang S, Xia YX, Kim B, Keyhani NO (2011) Two hydrophobins are involved in fungal spore coat rodlet layer assembly and each play distinct roles in surface interactions, development and pathogenesis in the entomopathogenic fungus, Beauveriabassiana. Mol Microbiol 80:811–826

    CAS  PubMed  Google Scholar 

  16. Tartar A, Shapiro AM, Scharf DW, Boucias DG (2005) Differential expression of chitin synthase (CHS) and glucan synthase (FKS) genes correlates with the formation of a modified, thinner cell wall in in vivo-produced Beauveriabassiana cells. Mycopathologia 160:303–314

    CAS  PubMed  Google Scholar 

  17. Xu Y, Orozco R, Wijeratne EK, Espinosa-Artiles P, Gunatilaka AL, Stock SP, Molnár I (2009) Biosynthesis of the cyclooligomer depsipeptide bassianolide, an insecticidal virulence factor of Beauveriabassiana. Fungal Genet Biol 46:353–364

    CAS  PubMed  Google Scholar 

  18. Xu Y, Orozco R, Wijeratne EK, Gunatilaka AL, Stock SP, Molnár I (2008) Biosynthesis of the cyclooligomer depsipeptide beauvericin, a virulence factor of the entomopathogenic fungus Beauveriabassiana. Chem Biol 15:898–907

    CAS  PubMed  Google Scholar 

  19. Xiao G, Ying S, Zheng P, Wang Z, Zhang S, Xie X, Shang Y, Leger RJS, Zhao G, Wang C (2012) Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveriabassiana. Sci Rep 2:483

    PubMed  PubMed Central  Google Scholar 

  20. Zhang Y, Zhao J, Fang W, Zhang J, Luo Z, Zhang M, Fan Y, Pei Y (2009) Mitogen-activated protein kinase hog1 in the entomopathogenic fungus Beauveriabassiana regulates environmental stress responses and virulence to insects. Appl Environ Microbiol 75:3787–3795

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Ramakuwela T, Hatting J, Bock C, Vega FE, Wells L, Mbata GN, Shapiro-Ilan D (2020) Establishment of Beauveriabassiana as a fungal endophyte in pecan (Caryaillinoinensis) seedlings and its virulence against pecan insect pests. Biol Control 140:104102

    CAS  Google Scholar 

  22. Ownley BH, Griffin MR, Klingeman WE, Gwinn KD, Moulton JK, Pereira RM (2008) Beauveriabassiana: endophytic colonization and plant disease control. J Invertebr Pathol 98:267–270

    CAS  PubMed  Google Scholar 

  23. Russo ML, Scorsetti AC, Vianna MF, Allegrucci N, Ferreri NA, Cabello MN, Pelizza SA (2019) Effects of endophytic Beauveriabassiana (Ascomycota: Hypocreales) on biological, reproductive parameters and food preference of the soybean pest Helicoverpagelotopoeon. J King Saud Univ Sci 31:1077–1082

    Google Scholar 

  24. Vega FE (2018) The use of fungal entomopathogens as endophytes in biological control: a review. Mycologia 110:4–30

    PubMed  Google Scholar 

  25. Barra-Bucarei L, France Iglesias A, Gerding González M, Silva Aguayo G, Carrasco-Fernández J, Castro JF, Ortiz Campos J (2020) Antifungal activity of Beauveriabassiana endophyte against botrytis cinerea in two solanaceae crops. Microorganisms 8:65

    CAS  Google Scholar 

  26. Afandhi A, Widjayanti T, Emi AAL, Tarno H, Afiyanti M, Handoko RNS (2019) Endophytic fungi Beauveriabassiana Balsamo accelerates growth of common bean (Phaeseolusvulgaris L.). Chem Biol 6:11

    Google Scholar 

  27. Gange AC, Koricheva J, Currie AF, Jaber LR, Vidal S (2019) Meta-analysis of the role of entomopathogenic and unspecialized fungal endophytes as plant bodyguards. New Phytol 223:2002–2010

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Vidal S, Jaber LR (2015) Entomopathogenic fungi as endophytes: plant–endophyte–herbivore interactions and prospects for use in biological control. Curr Sci 109:46–54

    Google Scholar 

  29. Jaber LR, Ownley BH (2018) Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? Biol Control 116:36–45

    Google Scholar 

  30. Quesada-Moraga E (2020) Entomopathogenic fungi as endophytes: their broader contribution to IPM and crop production. Biocontrol Sci Technol. https://doi.org/10.1080/09583157.2020.1771279

    Article  Google Scholar 

  31. Quesada-Moraga E, Yousef-Naef M, Garrido-Jurado I (2020) Advances in the use of entomopathogenic fungi as biopesticides in suppressing crop insect pests. In: Nick Birch N, Glare T (eds) Biopesticides for sustainable agriculture. Burleigh Dodds Science Publishing, Cambridge, pp 63–98

    Google Scholar 

  32. González-Mas N, Sánchez-Ortiz A, Valverde-García P, Quesada-Moraga E (2019) Effects of endophytic entomopathogenic ascomycetes on Aphisgossypii glover life-history traits and interaction with melon plants. Insects 10:165

    PubMed Central  Google Scholar 

  33. Gurulingappa P, Sword GA, Murdoch G, McGee PA (2010) Colonization of crop plants by fungal entomopathogens and their effects on two insect pests when in planta. Biol Control 55:34–41

    Google Scholar 

  34. Akutse KS, Maniania NK, Fiaboe K, Van den Berg J, Ekesi S (2013) Endophytic colonization of Viciafaba and Phaseolusvulgaris (Fabaceae) by fungal pathogens and their effects on the life-history parameters of Liriomyzahuidobrensis (Diptera: Agromyzidae). Fungal Ecol 6:293–301

    Google Scholar 

  35. Behie SW, Zelisko PM, Bidochka MJ (2012) Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants. Science 336:1576–1577

    CAS  PubMed  Google Scholar 

  36. Behie SW, Jones SJ, Bidochka MJ (2015) Plant tissue localization of the endophytic insect pathogenic fungi Metarhizium and Beauveria. Fungal Ecol 13:112–119

    Google Scholar 

  37. Wagner BL, Lewis LC (2000) Colonization of corn, Zeamays, by the entomopathogenic fungus Beauveriabassiana. Appl Environ Microbiol 66:3468–3473

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Myers JR, Kmiecik K (2017) Common bean: economic importance and relevance to biological science research. Anonymous the common bean genome. Springer, Cham, pp 1–20

    Google Scholar 

  39. Capinera L (2008) Twospotted spider mite, Tetranychusurticae Koch (Acari: Tetranychidae). In: Capinera JL (ed) Encyclopedia of entomology. Springer, Dordrecht

    Google Scholar 

  40. Boubou A, Migeon A, Roderick GK, Navajas M (2011) Recent emergence and worldwide spread of the red tomato spider mite, Tetranychusevansi: genetic variation and multiple cryptic invasions. Biol Invasions 13:81–92

    Google Scholar 

  41. Dagli F, Tunc I (2001) Dicofol resistance in Tetranychus cinnabarinus: resistance and stability of resistance in populations from Antalya, Turkey. Pest Manag Sci 57:609–614

    CAS  PubMed  Google Scholar 

  42. Van Leeuwen T, Vontas J, Tsagkarakou A, Dermauw W, Tirry L (2010) Acaricide resistance mechanisms in the two-spotted spider mite Tetranychusurticae and other important Acari: a review. Insect Biochem Mol 40:563–572

    Google Scholar 

  43. Goettel MS, Inglis GD (1997) Fungi: hyphomycetes. Manual of techniques in insect pathology. Elsevier, Amsterdam, pp 213–249

    Google Scholar 

  44. Posada F, Aime MC, Peterson SW, Rehner SA, Vega FE (2007) Inoculation of coffee plants with the fungal entomopathogen Beauveriabassiana (Ascomycota: Hypocreales). Mycol Res 111:748–757

    CAS  PubMed  Google Scholar 

  45. Rehner SA, Minnis AM, Sung G, Luangsa-ard JJ, Devotto L, Humber RA (2011) Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia 103:1055–1073

    PubMed  Google Scholar 

  46. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118

    CAS  PubMed  Google Scholar 

  47. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols 18:315–322

    Google Scholar 

  48. Landa BB, López-Díaz C, Jiménez-Fernández D, Montes-Borrego M, Muñoz-Ledesma FJ, Ortiz-Urquiza A, Quesada-Moraga E (2013) In-planta detection and monitorization of endophytic colonization by a Beauveriabassiana strain using a new-developed nested and quantitative PCR-based assay and confocal laser scanning microscopy. J Invertebr Pathol 114:128–138

    CAS  PubMed  Google Scholar 

  49. Batta YA (2018) Efficacy of two species of entomopathogenic fungi against the stored-grain pest, Sitophilusgranarius L. (Curculionidae: Coleoptera), via oral ingestion. Egypt J Biol Pest Control 28:44–52

    Google Scholar 

  50. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods 25:402–408

    CAS  PubMed  Google Scholar 

  51. Zhou Y, Zhang Y, Luo Z, Fan Y, Tang G, Liu L, Pei Y (2012) Selection of optimal reference genes for expression analysis in the entomopathogenic fungus Beauveriabassiana during development, under changing nutrient conditions, and after exposure to abiotic stresses. Appl Microbiol Biotechnol 93:679–685

    CAS  PubMed  Google Scholar 

  52. Fang W, Feng J, Fan Y, Zhang Y, Bidochka MJ, Leger RJS, Pei Y (2009) Expressing a fusion protein with protease and chitinase activities increases the virulence of the insect pathogen Beauveriabassiana. J Invertebr Pathol 102:155–159

    CAS  PubMed  Google Scholar 

  53. Fang W, Leng B, Xiao Y, Jin K, Ma J, Fan Y, Feng J, Yang X, Zhang Y, Pei Y (2005) Cloning of Beauveriabassiana chitinase gene Bbchit1 and its application to improve fungal strain virulence. Appl Environ Microbiol 71:363–370

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Abdo C, Nemer N, Nemer G, Jawdah YA, Atamian H, Kawar NS (2008) Isolation of Beauveria species from Lebanon and evaluation of its efficacy against the cedar web-spinning sawfly, Cephalciatannourinensis. Biocontrol 53:341–352

    Google Scholar 

  55. Parsa S, García-Lemos AM, Castillo K, Ortiz V, López-Lavalle LAB, Braun J, Vega FE (2016) Fungal endophytes in germinated seeds of the common bean, Phaseolusvulgaris. Fungal Biol 120:783–790

    PubMed  PubMed Central  Google Scholar 

  56. Parsa S, Ortiz V, Vega FE (2013) Establishing fungal entomopathogens as endophytes: towards endophytic biological control. J Vis Exp. https://doi.org/10.3791/50360

    Article  PubMed  PubMed Central  Google Scholar 

  57. McKinnon AC, Saari S, Moran-Diez ME, Meyling NV, Raad M, Glare TR (2017) Beauveriabassiana as an endophyte: a critical review on associated methodology and biocontrol potential. Biocontrol 62:1–17

    CAS  Google Scholar 

  58. Healey A, Furtado A, Cooper T, Henry RJ (2014) Protocol: a simple method for extracting next-generation sequencing quality genomic DNA from recalcitrant plant species. Plant Methods 10:21

    PubMed  PubMed Central  Google Scholar 

  59. Al Khoury C, Guillot J, Nemer N (2020) Susceptibility and development of resistance of the mite Tetranychusurticae to aerial conidia and blastospores of the entomopathogenic fungus Beauveriabassiana. Syst App Acarol 25:429–443

    Google Scholar 

  60. Tehri K, Gulati R, Geroh M, Dhankhar SK (2015) Dry weather: a crucial constraint in the field efficacy of entomopathogenic fungus BeauveriaBassiana against Tetranychusurticae Koch (Acari: Tetranychidae). J Entomol 3:287–291

    Google Scholar 

  61. Ortucu S, Algur OF (2017) A laboratory assessment of two local strains of the Beauveriabassiana (Bals.) Vuill. against the Tetranychusurticae (acari: Tetranychidae) and their potential as a mycopesticide. J Pathog 2107:1–7

    Google Scholar 

  62. Gómez-Vidal S, Lopez-Llorca LV, Jansson H, Salinas J (2006) Endophytic colonization of date palm (Phoenixdactylifera L.) leaves by entomopathogenic fungi. Micron 37:624–632

    PubMed  Google Scholar 

  63. Quesada-Moraga E, Ruiz-García A, Santiago-Alvarez C (2006) Laboratory evaluation of entomopathogenic fungi Beauveriabassiana and Metarhiziumanisopliae against puparia and adults of Ceratitiscapitata (Diptera: Tephritidae). J Econ Entomol 99:1955–1966

    CAS  PubMed  Google Scholar 

  64. Bensoussan N, Zhurov V, Yamakawa S, O’Neil CH, Suzuki T, Grbić M, Grbić V (2018) The digestive system of the two-spotted spider mite, Tetranychusurticae Koch, in the context of the mite-plant interaction. Front Plant Sci 9:1206

    PubMed  PubMed Central  Google Scholar 

  65. Charnley AK, Leger RS (1991) The role of cuticle-degrading enzymes in fungal pathogenesis in insects. In: Ann R (ed) The fungal spore and disease initiation in plants and animals. Springer, Boston, p 267

    Google Scholar 

  66. Mannino MC, Huarte-Bonnet C, Davyt-Colo B, Pedrini N (2019) Is the insect cuticle the only entry gate for fungal infection? insights into alternative modes of action of entomopathogenic fungi. J Fungi 5:33

    CAS  Google Scholar 

  67. Wan J, Zhang X, Neece D, Ramonell KM, Clough S, Kim S, Stacey MG, Stacey G (2008) A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. Plant Cell 20:471–481

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Behie SW, Moreira CC, Sementchoukova I, Barelli L, Zelisko PM, Bidochka MJ (2017) Carbon translocation from a plant to an insect-pathogenic endophytic fungus. Nat Commun 8:1–5

    Google Scholar 

  69. Branine M, Bazzicalupo A, Branco S (2019) Biology and applications of endophytic insect-pathogenic fungi. PLoS Pathog 15:e1007831

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Holder DJ, Kirkland BH, Lewis MW, Keyhani NO (2007) Surface characteristics of the entomopathogenic fungus Beauveria (Cordyceps) bassiana. Microbiology 153:3448–3457

    CAS  PubMed  Google Scholar 

  71. Pieterse CM, Zamioudis C, Berendsen RL, Weller DM, Van Wees SC, Bakker PA (2014) Induced systemic resistance by beneficial microbes. Ann Rev Phytopathol 52:347–375

    CAS  Google Scholar 

  72. Wu Q, Patocka J, Nepovimova E, Kuca K (2018) A review on the synthesis and bioactivity aspects of beauvericin, a fusarium mycotoxin. Front Pharmacol 9:1338

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Barelli L, Moonjely S, Behie SW, Bidochka MJ (2016) Fungi with multifunctional lifestyles: endophytic insect pathogenic fungi. Plant Mol Biol 90:657–664

    CAS  PubMed  Google Scholar 

  74. Zimmermann G (2007) Review on safety of the entomopathogenic fungi Beauveriabassiana and Beauveriabrongniartii. Biocontrol Sci Technol 17:553–596

    Google Scholar 

  75. Strasser H, Vey A, Butt TM (2000) Are there any risks in using entomopathogenic fungi for pest control, with particular reference to the bioactive metabolites of Metarhizium, Tolypocladium and Beauveria species? Biocontrol Sci Technol 10:717–735

    Google Scholar 

  76. Mascarin GM, Jaronski ST (2016) The production and uses of Beauveriabassiana as a microbial insecticide. World J Microbiol Biotechnol 32:177

    PubMed  Google Scholar 

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Funding

This work was funded by the Lebanese National Council for Scientific Research (CNRS), grant name (CNRS-L/USEK) and “Coopération pour l'évaluation et le développement de la recherche” CEDRE grant number 37349SA.

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  1. Department of Natural Sciences, School of Arts and Sciences, Lebanese American University, Byblos Campus, P.O. Box 36, Byblos, Lebanon

    Charbel Al Khoury

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The study conception and design, material preparation, data collection and analysis were performed by Charbel Al Khoury.

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Al Khoury, C. Molecular insight into the endophytic growth of Beauveria bassiana within Phaseolus vulgaris in the presence or absence of Tetranychus urticae. Mol Biol Rep 48, 2485–2496 (2021). https://doi.org/10.1007/s11033-021-06283-3

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