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Aspergillus alliaceus infection fatally shifts Orobanche hormones and phenolic metabolism

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Abstract

In this study, the physio pathological effects of Aspergillus alliaceus (Aa, fungi, biocontrol agent) on Orobanche (parasitic plant) were investigated by hormone and phenolic substance tests. In experimental group, Orobanches were treated with the fungi, considering control group was fungus-free. Based on the hormonal tests, in the experimental group, salicylic acid (SA), jasmonic acid (JA), abscisic acid (ABA) and gibberellic acid (GA) levels significantly decreased, and only indole acetic acid (IAA) hormone levels were fairly higher than the control group. According to phenolic substance tests, it was found that only gallic acid, syringic acid and caffeic acid values significantly increased compared with control, and catechin and p-coumaric acid values were significantly lower. Consequently, it was determined that Aa pathogenesis (1) considerably reduces the effects of all defence hormones (JA, ABA, SA), (2) operates an inadequate defence based solely on the IAA hormone and several phenolic substances (gallic acid, syringic acid and caffeic acid), (3) and inevitably the fungi lead the Orobanche to a slow and continuous death. The results were evaluated in detail in the light of similar recent article and current literature in terms of biocontrol and pathology.

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References

  1. Qasem JR (2009) Parasitic weeds of the Orobanchaceae family and their natural hosts in Jordan. Weed Biol Manag 9(2):112–122

    Google Scholar 

  2. Parker C (2013) The parasitic weeds of the Orobanchaceae. In: Joel DM, Gressel J, Musselman LJ (eds) Parasitic Orobanchaceae: parasitic mechanisms and control strategies. Springer, Berlin, pp 313–344

    Google Scholar 

  3. Delavault P (2015) Knowing the parasite: biology and genetics of Orobanche. Helia 38(62):15–29

    Google Scholar 

  4. Fernandez-Aparicio M, Reboud X, Gibot-Leclerc S (2016) Broomrape weeds, underground mechanisms of parasitism and associated strategies for their control: a review. Front Plant Sci 7:1–23. https://doi.org/10.3389/fpls.2016.00135

    Article  Google Scholar 

  5. Ghannam I, Al-Masri M, Barakat R (2012) The effect of herbicides on the Egyptian broomrape (Orobanche aegyptiaca) in tomato fields. Am J Plant Sci 3:346–352

    CAS  Google Scholar 

  6. Qasem JR (2019) Branched broomrape (Orobanche ramosa L.) control in tomato (Lycopersicon esculentum Mill.) by trap crops and other plant species in rotation. Crop Prot 120:75–83

    Google Scholar 

  7. Mamdouh M, Yasser N, Shabana A, Mamdouh M et al (2008) Granular formulation of Fusarium oxysporum for biological control of faba bean and tomato Orobanche. Pest Manag Sci 64:1237–1249

    Google Scholar 

  8. Shabana YM, Müller-Stöver D, Sauerborn J (2003) Granular Pesta formulation of Fusarium oxysporum f.sp. orthoceras for biological control of sunflower broomrape: efficacy and shelf-life. Biol Control 26:189–201

    Google Scholar 

  9. Boari A, Vurro M (2004) Evaluation of Fusarium spp. and other fungi as biological control agents of broomrape (Orobanche ramosa). Biol Control 30:212–219

    Google Scholar 

  10. Kohlschmid E, Sauerborn J, Müller-Stöver D (2009) Impact of Fusarium oxysporum on the holoparasitic weed Phelipanche ramosa: biocontrol efficacy under field-grown conditions. Weed Res 49(Suppl. 1):56–65

    Google Scholar 

  11. Hodosy AS, Hornok L (1983) Occurrence of hyperparasite Fusarium species and their use for control of broomrape on tomato. Proc Internat Conf Integr Plant Prot 4:48–52

    Google Scholar 

  12. Aybeke M (2017) Fusarium infection causes genotoxic disorders and antioxidant-based damages in Orobanche spp. Microbiol Res 201:46–51. https://doi.org/10.1016/j.micres.2017.05.001

    Article  CAS  PubMed  Google Scholar 

  13. Aybeke M (2017) Fusarium infection causes phenolic accumulations and hormonal disorders in Orobanche spp. Indian J Microbiol 57(4):416–421. https://doi.org/10.1007/s12088-017-0669-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Aybeke M, Sen B, Okten S (2014) Aspergillus alliaceus, a new potential biological control of the root parasitic weed Orobanche. J Basic Microbiol 54:93–101. https://doi.org/10.1002/jobm.201300080

    Article  CAS  Google Scholar 

  15. Mycobank, 2020, http://www.mycobank.org/Biolomics.aspx?Table=Mycobank&MycoBankNr_=256402, acc.date: 9.3.2020

  16. Ozhak-Baysan B, Alastruey-Izquıerdo A, Saba R, Ogunc D, Ongut G, Tımuragaoglu A, Arslan G, Cuenca-Estrella M, Rodrıguez-Tudela JL (2010) Aspergillus alliaceus and Aspergillus flavus co-infection in an acute myeloid leukemia patient. Med Mycol 48:995–999

    PubMed  Google Scholar 

  17. Bayman P, Baker JL, Doster MA, Michailides TJ, Mahoney NE (2002) Ochratoxin production by the Aspergillus ochraceus group and Aspergillus alliaceus. Appl Environ Microbiol 68:2326–2329

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Wang Y, Wang L, Liu F, Wang Q, Selvaraj JN, Xing F, Zhao Y, Yang L (2016) Ochratoxin a producing fungi, biosynthetic pathway and regulatory mechanisms. Toxins (Basel) 8(3):83

    Google Scholar 

  19. Aybeke M, Şen B, Ökten S (2015) Pesta granule trials with Aspergillus alliaceus for the biocontrol of Orobanche spp. J Bioc Sci Technol 25(7):803–813

    Google Scholar 

  20. Aybeke M (2016) Several pesta tablet trials with Aspergillus alliaceus Thom & Church for effective underground and aboveground Orobanche L. Biocontrol. Trakya Uni J Nat Sci 17(1):65–70

    Google Scholar 

  21. Aybeke M (2018) Transcriptomic effects of Aspergillus alliaceus on Orobanche during its pathogenesis. J Plant Dis Prot 125:33–39

    Google Scholar 

  22. Herron DA, Wingfield MJ, Wingfield BD, Rodas CA, Marincowitz S, Steenkamp E (2015) Novel taxa in the Fusarium fujikuroi species complex from Pinus spp. Stud Mycol 80:131–150

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Klich MA (2002) Identification of common Aspergillus species, 1st edn. Centralbureau voor Schimmelcultures, Utrecht, p 122

    Google Scholar 

  24. Raper KB, Fennell DI (1965) The genus Aspergillus. Williams & Wilkins, Baltimore

    Google Scholar 

  25. Muller-Stover D, Kroschel J, Thomas H, Sauerborn J (2002) Chlamydospores of Fusarium oxysporum Schlecht f.sp. orthoceras (Appel & Wollenw.) Bilai as inoculum for wheat-flourkaolin granules to be used for biological control of Orobanche cumana Wallr. Eur J Plant Pathol 108:221–228

    Google Scholar 

  26. Nirenberg HI (1976) Untersuchungen u ber die morphologische und biologische Differenzierung in der Fusarien Sektion Liseola. Mitt Biol Bundesanstalt Land- und Forstwirtsch Berlin-Dahlem, Germany 169:1–117

    Google Scholar 

  27. Louarn J, Boniface M-C, Pouilly N, Velasco L, Pérez-Vich B, Vincourt P, Muños S (2016) Sunflower resistance to broomrape (Orobanche cumana) is controlled by specific QTLs for different parasitism stages. Front Plant Sci 7:590. https://doi.org/10.3389/fpls.2016.00590

    Article  PubMed  PubMed Central  Google Scholar 

  28. Muller M, Munne-Bosch S (2011) Rapid and sensitive hormonal profiling of complex plant samples by liquid chromatography coupled to electrospray ionization tandem mass spectrometry. Plant Methods 7:37. https://doi.org/10.1186/1746-4811-7-37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Doganlar ZB (2012) Physiological and genetic responses to pesticide mixture treatment of Veronica beccabunga. Water Air Soil Pollut doi 223:6201–6212. https://doi.org/10.1007/s11270-012-1350-y

    Article  CAS  Google Scholar 

  30. Li JR, Yu K, Wei JR, Ma Q, Wang BQ, Yu D (2010) Gibberellin retards chlorophyll degradation during senescence of Paris polyphylla. Biol Plant 54(2):395–399

    CAS  Google Scholar 

  31. Colebrook EH, Thomas SG, Phillips AL, Hedden P (2014) The role of gibberellin signalling in plant responses to abiotic stress. J Exp Biol 217:67–75

    CAS  PubMed  Google Scholar 

  32. Xia X-J, Zhou Y-H, Shi K, Zhou J, Foyer CH, Yu J-Q (2015) Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. J Exp Bot 66(10):2839–2856

    CAS  PubMed  Google Scholar 

  33. Sung CL, Luan S (2012) ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant Cell Environ 35:53–60

    Google Scholar 

  34. Humplik JF, Bergougnoux V, Van Volkenburgh E (2017) To stimulate or inhibit? That is the question for the function of abscisic acid. Trends Plant Sci 22:830–841

    CAS  PubMed  Google Scholar 

  35. Chen L, Zhang L, Li D, Wang F, Yu D (2013) WRKY8 transcription factor functions in the TMV-cg defense response by mediating both abscisic acid and ethylene signaling in Arabidopsis. Proc Natl Acad Sci U S A 110:E1963–E1971

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Alazem M, Lin KY, Lin NS (2014) The abscisic acid pathway has multifaceted effects on the accumulation of Bamboo mosaic virus. Mol Plant-Microbe Interact 27:177–189

    CAS  PubMed  Google Scholar 

  37. Alazem M, Lin NS (2015) Roles of plant hormones in the regulation of host-virus interactions. Mol Plant Pathol 16:529–540. https://doi.org/10.1111/mpp.12204

    Article  CAS  PubMed  Google Scholar 

  38. Curvers KHS, Mouille G, de Rycke R, Asselbergh B, Van Hecke A, Vanderschaeghe D, Höfte H, Callewaert N, Van Breusegem F, Höfte M (2010) Abscisic acid deficiency causes changes in cuticle permeability and pectin composition that influence tomato resistance to Botrytis cinerea. Plant Physiol 154:847–860

    CAS  PubMed  PubMed Central  Google Scholar 

  39. Kaliff M, Staal J, Myrenås M, Dixelius C (2007) ABA is required for Leptosphaeria maculans resistance via ABI1- and ABI4-dependent signaling. Mol Plant-Microbe Interact 20:335–345

    CAS  PubMed  Google Scholar 

  40. Mbengue M, Navaud O, Peyraud R, Barascud M, Badet T, Vincent R et al (2016) Emerging trends in molecular interactions between plants and the broad host range fungal pathogens Botrytis cinerea and Sclerotinia sclerotiorum. Front Plant Sci 7:422

    PubMed  PubMed Central  Google Scholar 

  41. Stec N, Banasiak J, Jasinski M (2016) Abscisic acid–an overlooked player in plant-microbe symbioses formation? Acta Biochim Pol 63:53–58. https://doi.org/10.18388/abp.2015_1210

    Article  CAS  PubMed  Google Scholar 

  42. Sivakumaran A, Akinyemi A, Mandon J, Cristescu SM, Hall MA, Harren FJ et al (2016) ABA suppresses Botrytis cinerea elicited NO production in tomato to influence H2O2 generation and increase host susceptibility. Front Plant Sci 7:709

    PubMed  PubMed Central  Google Scholar 

  43. Zhou J, Zhang H, Yang Y, Zhang Z, Zhang H, Hu X, Chen J, Wang XC, Huang R (2008) Abscisic acid regulates TSRF1-mediated resistance to Ralstonia solanacearum by modifying the expression of GCC box-containing genes in tobacco. J Exp Bot 59:645–652. https://doi.org/10.1093/jxb/erm353

    Article  CAS  PubMed  Google Scholar 

  44. Sánchez-Vallet A, López G, Ramos B, Delgado-Cerezo M, Riviere M-P, Llorente F, Fernández PV, Miedes E, Estevez JM, Grant M, Molina A (2012) Disruption of abscisic acid signaling constitutively activates Arabidopsis resistance to the necrotrophic fungus Plectosphaerella cucumerina. Plant Physiol 160:2109–2124

    PubMed  PubMed Central  Google Scholar 

  45. Ulferts S, Delventhal R, Splivallo R, Karlovsky P, Schaffrath U (2015) Abscisic acid negatively interferes with basal defence of barley against Magnaporthe oryzae. BMC Plant Biol 15:7

    PubMed  PubMed Central  Google Scholar 

  46. Joshi JR, Burdman S, Lipsky A, Yariv S, Yedidia I (2016) Plant phenolic acids affect the virulence of Pectobacterium aroidearum and P. carotovorum ssp. brasiliense via quorum sensing regulation. Mol Plant Pathol 17:487–500

    CAS  PubMed  Google Scholar 

  47. Qi G, Chen J, Chang M, Chen H, Hall K, Korin J, Liu F, Wang D, Fu ZQ (2018) Pandemonium breaks out: disruption of salicylic acid-mediated defense by plant pathogens. Mol Plant 11:1427–1439

    CAS  PubMed  Google Scholar 

  48. Schweiger R, Heise A, Persicke M, Muller C (2014) Interactions between the jasmonic and salicylic acid pathway modulate the plant metabolome and affect herbivores of different feeding types. Plant Cell Environ 37:1574–1585

    CAS  PubMed  Google Scholar 

  49. Shoresh M, Harman GE, Mastouri F (2010) Induced systemic resistance and plant responses to fungal biocontrol agents. Annu Rev Phytopathol 48:21–43

    CAS  PubMed  Google Scholar 

  50. Wasternack C (2014) Action of jasmonates in plant stress responses and development—applied aspects. Biotechnol Adv 32:31–39

    CAS  PubMed  Google Scholar 

  51. Zhao S, Ma Q, Xu X, Li G, Hao L (2016) Tomato jasmonic acid-deficient mutant spr2 seedling response to cadmium stress. J Plant Growth Regul 35(3):603–610

    CAS  Google Scholar 

  52. Taylor-Teeples M, Lanctot A, Nemhauser JL (2016) As above, so below: auxin’s role in lateral organ development. Dev Biol 419:156–164

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Zhao Y (2018) Essential roles of local auxin biosynthesis in plant development and in adaptation to environmental changes. Annu Rev Plant Biol 69:417–435

    CAS  PubMed  Google Scholar 

  54. Potters G, Pasternak TP, Guise Y, Palme KJ, Jansen MAK (2007) Stress-induced morphogenic responses: growing out of trouble? Trends Plant Sci 12:98–105

    CAS  PubMed  Google Scholar 

  55. Kazan K (2013) Auxin and the integration of environmental signals into plant root development. Ann Bot 112:1655–1665

    PubMed  PubMed Central  Google Scholar 

  56. Petti C, Reiber K, Ali SS, Berney M, Doohan FM (2012) Auxin as a player in the biocontrol of Fusarium head blight disease of barley and its potential as a disease control agent. BMC Plant Biol 12:224

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Liu X, Lin Y, Liu D, Wang C, Zhao Z, Cui X et al (2017) MAPKmediated auxin signal transduction pathways regulate the malic acid secretion under aluminum stress in wheat (Triticum aestivum L.). Sci Rep 7:1620

    PubMed  PubMed Central  Google Scholar 

  58. Benjamins R, Scheres B (2008) Auxin: the looping star in plant development. Annu Rev Plant Biol 59:443–465

    CAS  PubMed  Google Scholar 

  59. Kolachevskaya OO, Lomin SN, Arkhipov DV, Romanov GA (2019) Auxins in potato: molecular aspects and emerging roles in tuber formation and stress resistance. Plant Cell Rep 38:681–698

    CAS  PubMed  Google Scholar 

  60. Bieleszová K, Pařízková B, Kubeš M et al (2018) New fluorescently labeled auxins exhibit promising anti-auxin activity. New Biotechnol. https://doi.org/10.1016/j.nbt.2018.06.003

  61. Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC (2009) Networking by small molecule hormones in plant immunity. Nat Chem Biol 5(5):308–316

    CAS  PubMed  Google Scholar 

  62. Kazan K, Manners JM (2013) MYC2: the master in action. Mol Plant 6:686–703

    CAS  PubMed  Google Scholar 

  63. Wasternack C, Hause B (2013) Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Ann of Botany. Ann Bot 111:1021–1058

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Pieterse CMJ, Van Der D, Zamioudis DC, Leon-Reyes A, Van Wees SCM (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:489–521. https://doi.org/10.1146/annurev-cellbio-092910-154055

    Article  CAS  PubMed  Google Scholar 

  65. Maggio A, Barbieri G, Raimondi G, De Pascale S (2010) Contrasting effects of GA3 treatments on tomato plants exposed to increasing salinity. J Plant Growth Regul 29:63–72

    CAS  Google Scholar 

  66. Shahzad S, Mateen S, Naeem SS, Akhtar K, Rizvi W, Moin S (2019) Syringic acid protects from isoproterenol induced cardiotoxicity in rats. Europ J of Pharmac 849:135–145

    CAS  Google Scholar 

  67. Fang W, Zhu S, Niu Z, Yin Y (2019) The protective effect of syringic acid on dextran sulfate sodium induced experimental colitis in BALB/c mice. Drug Dev Res. 2019 Sep;80(6):731-740. https://doi.org/10.1002/ddr.21524

  68. Babak G, Houshmand G, Hosseinzadeh A, Kalantar M, Mehrzadi S, Goudarzi M (2019) Gallic acid ameliorates sodium arsenite-induced renal and hepatic toxicity in rats. Drug Chem Toxicol:1–12. https://doi.org/10.1080/01480545.2019.1591434

  69. Safaei F, Mehrzadi S, Khadem Haghighian H, Hosseinzadeh A, Nesari A, Dolatshahi M, Esmaeilizadeh M, Goudarzi M (2018) Protective effects of gallic acid against methotrexate-induced toxicity in rats. Acta Chir Belg 118(3):152–160

    PubMed  Google Scholar 

  70. Prudêncio ER, Cardoso CM, Castro RN, Riger CJ (2019) Antioxidant effect of caffeic acid derivatives on sod and glutathione defective yeasts. Appl Biochem Microbiol 55(3):264–269

    Google Scholar 

  71. Pelinson LP, Assmann CE, Palma TV, da Cruz IBM et al (2019) Antiproliferative and apoptotic effects of caffeic acid on SK-Mel-28 human melanoma cancer cells. Mol Biol Rep 46:2085–2092

    CAS  PubMed  Google Scholar 

  72. Jing X, Zhang J, Huang Z, Sheng Y, Ji L (2018) The involvement of Nrf2 antioxidant signalling pathway in the protection of monocrotaline-induced hepatic sinusoidal obstruction syndrome in rats by (+)-catechin hydrate. Free Radic Res 52:402–414

    CAS  PubMed  Google Scholar 

  73. Yue Y, Shen P, Xu Y, Park Y (2019) p-Coumaric acid improves oxidative and osmosis stress responses in Caenorhabditis elegans. J Sci Food Agric 99:1190–1197

    CAS  PubMed  Google Scholar 

  74. Rossetti A, Mazzaglia A, Muganu M, Paolocci M, Sguizzato M, Esposito E, Cortesi R, Balestr GM (2017) Microparticles containing gallic and ellagic acids for the biological control of bacterial diseases of kiwifruit plants. J Plant Dis Prot 124:563–575

    Google Scholar 

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Acknowledgements

I thank Prof. Dr. Oguzhan Doganlar for his valuable comments, TUBAP (Trakya University, Scientific Researches Foundations) with the project number TUBAP 2016-15, and Assoc. Prof. Dr. Burhan Sen for cultivation and identification efforts of fungal material.

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  1. Faculty of Science, Department of Biology, Balkan Campus, Trakya University, 22030, Edirne, Turkey

    Mehmet Aybeke

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Aybeke, M. Aspergillus alliaceus infection fatally shifts Orobanche hormones and phenolic metabolism. Braz J Microbiol 51, 883–892 (2020). https://doi.org/10.1007/s42770-020-00283-4

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