Multifunctional regulation of NADPH oxidase in growth, microsclerotia formation and virulence in Metarhizium rileyi.
Hyphal polarity
Metarhizium rileyi
Microsclerotia
NADPH oxidase
Pathogenicity
Journal
Biotechnology letters
ISSN: 1573-6776
Titre abrégé: Biotechnol Lett
Pays: Netherlands
ID NLM: 8008051
Informations de publication
Date de publication:
Dec 2023
Dec 2023
Historique:
received:
24
03
2023
accepted:
19
07
2023
revised:
28
06
2023
medline:
10
11
2023
pubmed:
25
9
2023
entrez:
25
9
2023
Statut:
ppublish
Résumé
Microsclerotia (MS), anti-stress structures produced by many filamentous fungi, have been proven to be a great substitute for conidia in the production of insecticides within entomogenous fungi. NADPH oxidase (Nox) is a highly conserved ROS-response protein family that is widespread in eukaryotes and plays distinct roles in environmental fitness among various filamentous fungi. However, it is not clear whether the formation of MS and pathogenicity in entomogenous fungi is regulated by the Nox inside. In this study, we reported the presence of NADPH oxidase homologs in a great potential biocontrol fungus, Metarhizium rileyi, and further showed multiple biological functions. Three Nox homologous genes in M. rileyi showed high expression throughout the entire process of MS formation. Targeted deletion of MrNoxA, MrNoxB and MrNoxR all led to a decrease in MS yield and impaired morphology. Moreover, the anti-adversity assay showed that they are indispensable for growth, osmotic pressure and oxidative stress regulation in Metarhizium rileyi. Most importantly, △MrNoxR and △MrNoxA but not △MrNoxB showed a dramatic reduction in virulence via inoculation. The normality of appressoria might be unaffected in mutants since there are no striking differences in virulence compared with WT by topical injections. Our results revealed that NADPH oxidase plays important roles in growth regulation, MS formation and pathogenicity in M. rileyi, perhaps in the ROS response and hyphal polarity.
Identifiants
pubmed: 37747666
doi: 10.1007/s10529-023-03427-2
pii: 10.1007/s10529-023-03427-2
doi:
Substances chimiques
NADPH Oxidases
EC 1.6.3.-
Reactive Oxygen Species
0
Fungal Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1441-1455Subventions
Organisme : Department of Science and Technology Planning Project of Henan Province
ID : 222102110102
Organisme : Department of Science and Technology Planning Project of Henan Province
ID : 212102110142
Organisme : Department of Science and Technology Planning Project of Henan Province
ID : 222102110015
Organisme : Scientific Research Support Project of Zhoukou Normal University
ID : ZKNUC2021049
Organisme : Scientific Research Support Project of Zhoukou Normal University
ID : ZKNUC2020045
Organisme : Scientific Research Support Project of Zhoukou Normal University
ID : ZKNUC2021050
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Nature B.V.
Références
Aguirre J, Rios-Memberg M, Hewitt D, Hensberg W (2005) Reactive oxygen species and development in microbial eukaryotes. Trends Microbiol 13(3):111–118. https://doi.org/10.1016/j.tim.2005.01.007
doi: 10.1016/j.tim.2005.01.007
pubmed: 15737729
Bedard K, Krause KH (2007) The NOX family of ROS-generating NADPH oxidases: physiology and pathphysiology. Physiol Rev 87(1):245–313. https://doi.org/10.1152/physrev.00044.2005
doi: 10.1152/physrev.00044.2005
pubmed: 17237347
Chen H, Yin YP, Li Y, Mahmud MS, Wang ZK (2012) Identification and analysis of gene differentially expressed in the Spodoptera litura fat body in response to the biocontrol fungus, Nomuraea rileyi. Comp Biochem Physiol B Biochem Mol Biol 163(2):203–210. https://doi.org/10.1016/j.cbpb.2012.05.018
doi: 10.1016/j.cbpb.2012.05.018
pubmed: 22659052
Egan MJ, Wang ZY, Jones MA, Smirnoff N, Talbot NJ (2007) Generation of reactive oxygen species by fungal NADPH oxidases is required for rice blast disease. Proc Natl Acad Sci U S A 104(28):11772–11777. https://doi.org/10.1073/pnas.0700574104
doi: 10.1073/pnas.0700574104
pubmed: 17600089
pmcid: 1913907
Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JDG (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422(6930):442–446. https://doi.org/10.1038/nature01485
doi: 10.1038/nature01485
pubmed: 12660786
Georgiou CD (1997) Lipid peroxidation in Sclerotium rolfsii: a new look into the mechanism of sclerotial biogenesis in fungi. Mycol Res 101(4):460–464. https://doi.org/10.1017/S0953756296002882
doi: 10.1017/S0953756296002882
Georgiou CD, Pastsoukis N, Papapostolou I, Zervoudakis G (2006) Sclerotial metamorphosis in filamentous fungi is induced by oxidative stress. Integr Comp Biol 46(6):691–712. https://doi.org/10.1093/icb/icj034
doi: 10.1093/icb/icj034
pubmed: 21672779
Giesbert S, Schurg T, Scheele S, Tudzynski P (2008) The NADPH oxidase Cpnox1 is required for full pathogenicity of the ergot fungus Claviceps purpurea. Mol Plant Pathol 9(3):317–327. https://doi.org/10.1111/j.1364-3703.2008.00466.x
doi: 10.1111/j.1364-3703.2008.00466.x
pubmed: 18705873
pmcid: 6640299
Ipsilantis I, Samourelis C, Karpouzas DG (2012) The impact of biological pesticides on arbuscular mycorrhizal fungi. Soil Biol Biochem 45:147–155. https://doi.org/10.1016/j.soilbio.2011.08.007
doi: 10.1016/j.soilbio.2011.08.007
Jiang SS, Yin YP, Song ZY, Zhou GL, Wang ZK (2014) RacA and Cdc42 regulate polarized growth and microsclerotium formation in the dimorphic fungus Nomuraea rileyi. Res Microbiol 165(3):233–242. https://doi.org/10.1016/j.resmic.2014.03.003
doi: 10.1016/j.resmic.2014.03.003
pubmed: 24657749
Khachatourians GG, Uribe D (2008) Identification and characterization of an alternative oxidase in the entomopathogenic fungus Metarhizium anisopliae. Can J Microbiol 54(2):119–127. https://doi.org/10.1139/w07-127
doi: 10.1139/w07-127
pubmed: 18388981
Klimes A, Amyotte SG, Grant S, Kang S, Dobinson KF (2008) Microsclerotia development in Verticillium dahliae: regulation and differential expression of the hydrophobin gene VDH1. Fungal Genet Biol 45(12):1525–1532. https://doi.org/10.1016/j.fgb.2008.09.014
doi: 10.1016/j.fgb.2008.09.014
pubmed: 18951989
Kumar D, Yusuf MA, Singh P, Sardar M, Sarin NB (2014) Histochemical detection of superoxide and H
doi: 10.21769/BioProtoc.1108
Lambeth JD (2004) NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 4(3):81–89. https://doi.org/10.1038/nri1312
doi: 10.1038/nri1312
Lara-Ortiz T, Riveros-Rosas H, Aguirre J (2003) Reactive oxygen species generated by microbial NADPH oxidase NoxA regulates sexual development in Aspergillus nidulans. Mol Microbiol 50(4):1241–1255. https://doi.org/10.1046/j.1365-2958.2003.03800.x
doi: 10.1046/j.1365-2958.2003.03800.x
pubmed: 14622412
Leclerque A, Hong W, Abschütz A, Chen S, Mitina GV, Zimmermann G, Schairer HU (2004) Agrobacterium-mediated insertional mutagenesis (AIM) of the entomopathogenic fungus Beauveria bassiana. Curr Genet 45:111–119. https://doi.org/10.1111/j.1467-9280.2009.02408.x
doi: 10.1111/j.1467-9280.2009.02408.x
pubmed: 14634789
Li Y, Wang Z, Liu X, Song Z, Li R, Shao C, Yin Y (2016) Siderophore biosynthesis but not reductive iron assimilation is essential for the dimorphic fungus Nomuraea rileyi conidiation, dimorphism transition, resistance to oxidative stress, pigmented microsclerotium formation, and virulence. Front Microbiol 7:931. https://doi.org/10.3389/fmicb.2016.00931
pubmed: 27379061
pmcid: 4909778
Lin YL, Fan LQ, Xia XH, Wang ZK, Yin YP, Cheng YL, Li ZG (2019) Melatonin decreases resistance to postharvest green mold on citrus fruit by scavenging defense-related reactive oxygen species. Postharvest Biol Tec 153:21–30. https://doi.org/10.1016/j.postharvbio.2019.03.01
doi: 10.1016/j.postharvbio.2019.03.01
Liu JJ, Yin YP, Song ZY, Li Y, Jiang SS, Shao CW, Wang ZK (2014) NADH:flavin oxidoreductase/NADH oxidase and ROS regulate microsclerotium development in Nomuraea rileyi. World J Microbiol Biotechnol 30(7):1927–1935. https://doi.org/10.1007/s11274-014-1610-7
doi: 10.1007/s11274-014-1610-7
pubmed: 24497186
Malagnac F, Lalucque H, Lepére G, Silar P (2004) Two NADPH oxidase isoforms are required for sexual reproduction and ascospore germination in the filamentous fungus Podospora anserina. Fungal Genet Biol 41(11):982–997. https://doi.org/10.1016/j.fgb.2004.07.008
doi: 10.1016/j.fgb.2004.07.008
pubmed: 15465387
Marcet-Houben M, Ballester AR, Fuente BDL, Harries E, Marcos JF, González-Candelas L, Gabaldón T (2012) Genome sequence of the necrotrophic fungus Penicillium digitatum, the main postharvest pathogen of citrus. BMC Genomics 13(1):646. https://doi.org/10.1186/1471-2164-13-646
doi: 10.1186/1471-2164-13-646
pubmed: 23171342
pmcid: 3532085
Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH oxidases. Trends Plant Sci 17(1):9–15. https://doi.org/10.1016/j.tplants.2011.10.001
doi: 10.1016/j.tplants.2011.10.001
pubmed: 22037416
Miranda-Fuentes P, García-Carneros AB, Molinero-Ruiz L (2021) Updated characterization of races of Plasmopara halstedii and Entomopathogenic fungi as endophytes of sunflower plants in axenic culture. Agronomy 11(2):268. https://doi.org/10.3390/agronomy11020268
doi: 10.3390/agronomy11020268
Mithofer A, Daxberger A, Fromhold-Treu D, Ebel J (1997) Involvement of an NAD(P)H oxidase in the elicitor-inducible oxidative burst of soybean. Phytochemistry 45(6):1101–1107. https://doi.org/10.1016/S0031-9422(97)00133-7
doi: 10.1016/S0031-9422(97)00133-7
Nevoigt E, Stahl U (1997) Osmoregulation and glycerol metabolism in the yeast Saccharomyces cerevisiae. Fems Microbiol Rev 21(3):231–241. https://doi.org/10.1111/j.1574-6976.1997.tb00352.x
doi: 10.1111/j.1574-6976.1997.tb00352.x
pubmed: 9451815
Page MJ, Cera ED (2006) Role of Na
doi: 10.1152/physrev.00008.2006
pubmed: 17015484
Rolke Y, Tudzynski P (2008) The small GTPase Rac and the p21-activated kinase Cla4 in Claviceps purpurea: interaction and impact on polarity, development and pathogenicity. Mol Microbiol 68(2):405–423. https://doi.org/10.1111/j.1365-2958.2008.06159.x
doi: 10.1111/j.1365-2958.2008.06159.x
pubmed: 18284596
Ryder LS, Dagdas YF, Mentlak TA, Kershaw MJ, Thornton CR, Schuster M, Chen JS, Wang ZH, Talbot NJ (2013) NADPH oxidases regulate septin-mediated cytoskeletal remodeling during plant infection by the rice blast fungus. Proc Natl Acad Sci U S A 110(8):3179–3184. https://doi.org/10.1073/pnas.1217470110
doi: 10.1073/pnas.1217470110
pubmed: 23382235
pmcid: 3581893
Schürmann J, Buttermann D, Herrmann A, Giesbert S, Tudzynski P (2013) Molecular characterization of the NADPH oxidase complex in the ergot fungus Claviceps purpurea:CpNox2 and CpPls1 are important for a balanced host-pathogen interaction. Mol Plant Microbe Interact 26(10):1151–1164. https://doi.org/10.1094/MPMI-03-13-0064-R
doi: 10.1094/MPMI-03-13-0064-R
pubmed: 23777432
Segmuller N, Kokkelink L, Giesbert S, Odinius D, Kan JV, Tudzynski P (2008) NADPH oxidases are involved in differentiation and pathogenicity in Botrytis cinerea. Mol Plant Microbe Interact 21(6):808–819. https://doi.org/10.1094/MPMI-21-6-0808
doi: 10.1094/MPMI-21-6-0808
pubmed: 18624644
Song ZY, Yin YP, Jiang SS, Liu JJ, Chen H, Wang ZK (2013) Comparative transcriptome analysis of microsclerotia development in Nomuraea rileyi. BMC Genomics 14:411. https://doi.org/10.1186/1471-2164-14-411
doi: 10.1186/1471-2164-14-411
pubmed: 23777366
pmcid: 3698084
Song ZY, Yin YP, Jiang SS, Liu JJ, Wang ZK (2014) Optimization of culture medium for microsclerotia production by Nomuraea rileyi and analysis of their viability for use as a mycoinsecticide. Biocontrol 59(5):597–605. https://doi.org/10.1007/s10526-014-9589-4
doi: 10.1007/s10526-014-9589-4
Srisukchayakul P, ChanpenW SP (2005) Studies on the pathogenesis of the local isolates of Nomuraea rileyi against Spodoptera litura. ScienceAsia 31(3):273–276. https://doi.org/10.2306/scienceasia1513-1874.2005.31.273
doi: 10.2306/scienceasia1513-1874.2005.31.273
Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R (2011) Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol 14(6):691–699. https://doi.org/10.1016/j.pbi.2011.07.014
doi: 10.1016/j.pbi.2011.07.014
pubmed: 21862390
Takano Y, Kubo Y, Kuroda I, Furusawa I (1997) Temporal transcriptional pattern of three melanin biosynthesis genes, PKS1, SCD1, and THR1, in appressorium-differentiating and nondifferentiating conidia of colletotrichum lagenarium. Appl Environ Microbiol 63(1):351–354. https://doi.org/10.1016/S0065-2164(08)70266-1
doi: 10.1016/S0065-2164(08)70266-1
pubmed: 16535499
pmcid: 1389113
Takemoto D, Tanaka A, Scott B (2007) NADPH oxidase in fungi: diverse roles of reactive oxygen species in fungal cellular differentiation. Fungal Genet Biol 44(11):1065–1067. https://doi.org/10.1016/j.fgb.2007.04.011
doi: 10.1016/j.fgb.2007.04.011
pubmed: 17560148
Wang L, Mogg C, Walkowiak S, Joshi M, Subramaniam R (2014) Characterization of NADPH oxidase genes NoxA and NoxB in Fusarium graminearum. Can J Plant Pathol 36(1):12–21. https://doi.org/10.1080/07060661.2013.868370
doi: 10.1080/07060661.2013.868370
Wang HH, Wang JL, Li YP, Liu X, Wen JZ, Lei ZR (2011) Liquid culturing of microsclerotia of Beauveria bassiana, an entomopathgeonic fungus to control western flower thrip,Frankliniella occidentalis. Chinese J Appl Entomol 48(3):588—595. http://www.ent-bull.com.cn/viewmulu.aspx?qi_id=624&mid=15668
Wei H, Huang Y, Du J (2004) Sex pheromones and reproductive behavior of Spodoptera litura (Fabricius) moths reared from larvae treated with four insecticides. J Chem Ecol 30(7):1457–1466. https://doi.org/10.1023/B:JOEC.0000037751.86203.10
doi: 10.1023/B:JOEC.0000037751.86203.10
pubmed: 15503531
Zhang CK, Lin YH, Wang JQ, Wang Y, Chen MP, Norvienyeku J, Li GP, Yu WY, Wang ZH (2016) FgNoxR, a regulatory subunit of NADPH oxidases, is required for female fertility and pathogenicity in Fusarium graminearum. FEMS Microbiol Lett 363(1):1–8. https://doi.org/10.1093/femsle/fnv223
doi: 10.1093/femsle/fnv223