Six type-I PKS classes and highly conserved melanin and elsinochrome gene clusters found in diverse Elsinoë species.
Perylenequinone
Phylogenetic analysis
Polyketide synthase
Secondary metabolites
Synteny analysis
Journal
BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258
Informations de publication
Date de publication:
22 Oct 2024
22 Oct 2024
Historique:
received:
23
07
2024
accepted:
18
10
2024
medline:
23
10
2024
pubmed:
23
10
2024
entrez:
22
10
2024
Statut:
epublish
Résumé
Elsinoë species are phytopathogenic fungi that cause serious scab diseases on economically important plants. The disease symptoms arise from the effects of a group of phytotoxins known as elsinochromes, produced via a type-I polyketide synthase (PKS) biosynthetic pathway. The elsinochrome gene cluster was first annotated in Elsinoë fawcettii where the main type-I PKS gene was characterized as EfPKS1. A later study showed that this gene and the associated cluster had not been correctly annotated, and that EfPKS1 was actually the anchor gene of the melanin biosynthetic pathway. A new type-I PKS gene EfETB1 associated with elsinochrome production was also identified. The aim of this study was to identify all type-I PKS genes in the genomes of seven Elsinoë species with the goal of independently verifying the PKS containing clusters for both melanin and elsinochrome production. A total of six type-I PKS classes were identified, although there was variation between the species in the number and type of classes present. Genes similar to the E. fawcettii EfPKS1 and EfETB1 type-I PKS genes were associated with melanin and elsinochrome production respectively in all species. The complete melanin and elsinochrome PKS containing clusters were subsequently annotated in all the species with high levels of synteny across Elsinoë species. This study provides a genus-level overview of type-I PKS distribution in Elsinoë species, including an additional line of support for the annotation of the melanin and elsinochrome PKS containing clusters in these important plant pathogens.
Identifiants
pubmed: 39438784
doi: 10.1186/s12864-024-10920-z
pii: 10.1186/s12864-024-10920-z
doi:
Substances chimiques
Melanins
0
Polyketide Synthases
79956-01-7
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
990Informations de copyright
© 2024. The Author(s).
Références
Fan XL, Barreto RW, Groenewald JZ, Bezerra JD, Pereira OL, Cheewangkoon R, Mostert L, Tian CM, Crous PW. Phylogeny and taxonomy of the scab and spot anthracnose fungus Elsinoë (Myriangiales, Dothideomycetes). Stud Mycol. 2017;87:1–41.
pubmed: 28373739
pmcid: 5367849
doi: 10.1016/j.simyco.2017.02.001
Chung KR. Elsinoë fawcettii and Elsinoë australis: the fungal pathogens causing citrus scab. Mol Plant Pathol. 2011;12(2):123–35.
pubmed: 21199563
doi: 10.1111/j.1364-3703.2010.00663.x
Jenkins AE. Sphaceloma perseae, the cause of avocado scab. J Agric Res. 1934;49:859–69.
Magarey RD, Emmett RW, Magarey PA, Franz PR. Evaluation of control of grapevine anthracnose caused by Elsinoë ampelina by pre-infection fungicides. Australas Plant Pathol. 1993;22(2):48–52.
doi: 10.1071/APP9930048
Pham NQ, Marincowitz S, Solís M, Duong TA, Wingfield BD, Barnes I, Slippers B, Muro Abad JI, Durán A, Wingfield MJ. Eucalyptus scab and shoot malformation: a new and serious foliar disease of Eucalyptus caused by Elsinoë necatrix sp. nov. Plant Pathol. 2021;70(5):1230–42.
doi: 10.1111/ppa.13348
Roux J, Wingfield MJ, Marincowitz S, Solís M, Phungula S, Pham NQ. Eucalyptus scab and shoot malformation: a new disease in South Africa caused by a novel species, Elsinoë masingae. Forestry: Int J For Res. 2023;97(2):327–38.
doi: 10.1093/forestry/cpad031
Swart L, Crous PW, Kang J-C, McHau GRA, Pascoe I, Palm ME. Differentiation of species of Elsinoë associated with scab disease of Proteaceae based on morphology, symptomatology, and ITS sequence phylogeny. Mycologia. 2001;93(2):366–79.
doi: 10.1080/00275514.2001.12063168
Weiss U, Ziffer H, Batterham TJ, Blumer M, Hackeng WH, Copier H, Salemink CA. Pigments of Elsinoë species. i. Pigment production by Elsinoë species; isolation of pure elsinochromes a, b, and c. Can J Microbiol. 1965;11:57–66.
pubmed: 14290960
doi: 10.1139/m65-008
Liao HL, Chung KR. Cellular toxicity of elsinochrome phytotoxins produced by the pathogenic fungus, Elsinoë fawcettii causing citrus scab. New Phytol. 2008;177(1):239–50.
pubmed: 17953652
doi: 10.1111/j.1469-8137.2007.02234.x
Liao HL, Chung KR. Genetic dissection defines the roles of elsinochrome Phytotoxin for fungal pathogenesis and conidiation of the citrus pathogen Elsinoë fawcettii. Mol Plant Microbe Interact. 2008;21(4):469–79.
pubmed: 18321192
doi: 10.1094/MPMI-21-4-0469
Jiao W, Liu L, Zhou R, Xu M, Xiao D, Xue C. Elsinochrome phytotoxin production and pathogenicity of Elsinoë arachidis isolates in China. PLoS ONE. 2019;14(6):e0218391.
pubmed: 31194853
pmcid: 6564019
doi: 10.1371/journal.pone.0218391
Daub ME, Herrero S, Chung KR. Photoactivated perylenequinone toxins in fungal pathogenesis of plants. FEMS Microbiol Lett. 2005;252(2):197–206.
pubmed: 16165316
doi: 10.1016/j.femsle.2005.08.033
Lund NA, Robertson A, Whalley WB. The chemistry of fungi. Part XXI. Asperxanthone and a preliminary examination of aspergillin. J Chem Soc. 1953;494:2434–9.
doi: 10.1039/jr9530002434
Liu WZ, Shen YX, Liu XF, Chen YT, Xie JL. A new perylenequinone from Hypomyces sp. Chin Chem Lett. 2001;12:431–2.
Cordero RJ, Casadevall A. Functions of fungal melanin beyond virulence. Fungal Biol Rev. 2017;31(2):99–112.
pubmed: 31649746
pmcid: 6812541
doi: 10.1016/j.fbr.2016.12.003
Belozerskaya TA, Gessler NN, Aver‘yanov AA. Melanin pigments of fungi. In: Merillon JM, Ramawat KG, editors. Fungal Metabolites. Cham: Springer International Publishing; 2016. p. 1–29.
Suthar M, Dufossé L, Singh SK. The enigmatic world of fungal melanin: a comprehensive review. J Fungi (Basel). 2023;9(9):891.
pubmed: 37754999
doi: 10.3390/jof9090891
Hu J, Sarrami F, Li H, Zhang G, Stubbs KA, Lacey E, Stewart SG, Karton A, Piggott AM, Chooi YH. Heterologous biosynthesis of elsinochrome A sheds light on the formation of the photosensitive perylenequinone system. Chem Sci. 2019;10(5):1457–65.
pubmed: 30809363
doi: 10.1039/C8SC02870B
Sabatini M, Comba S, Altabe S, Recio-Balsells AI, Labadie GR, Takano E, Gramajo H, Arabolaza A. Biochemical characterization of the minimal domains of an iterative eukaryotic polyketide synthase. Febs j. 2018;285(23):4494–511.
pubmed: 30300504
pmcid: 6334511
doi: 10.1111/febs.14675
Chung KR, Liao HL. Determination of a transcriptional regulator-like gene involved in biosynthesis of elsinochrome phytotoxin by the citrus scab fungus, Elsinoë fawcettii. Microbiol (Reading). 2008;154(Pt 11):3556–66.
doi: 10.1099/mic.0.2008/019414-0
Ebert MK, Spanner RE, de Jonge R, Smith DJ, Holthusen J, Secor GA, Thomma B, Bolton MD. Gene cluster conservation identifies melanin and perylenequinone biosynthesis pathways in multiple plant pathogenic fungi. Environ Microbiol. 2019;21(3):913–27.
pubmed: 30421572
doi: 10.1111/1462-2920.14475
Jeffress S, Arun-Chinnappa K, Stodart B, Vaghefi N, Tan YP, Ash G. Genome mining of the citrus pathogen Elsinoë fawcettii; prediction and prioritisation of candidate effectors, cell wall degrading enzymes and secondary metabolite gene clusters. PLoS ONE. 2020;15(5):e0227396.
pubmed: 32469865
pmcid: 7259788
doi: 10.1371/journal.pone.0227396
Jiao W, Xu M, Zhou R, Fu Y, Li Z, Xue C. Genomic analysis of Elsinoë arachidis reveals its potential pathogenic mechanism and the biosynthesis pathway of elsinochrome toxin. PLoS ONE. 2021;16(12):e0261487.
pubmed: 34914789
pmcid: 8675698
doi: 10.1371/journal.pone.0261487
Wingfield BD, Berger DK, Coetzee MPA, Duong TA, Martin A, Pham NQ, van den Berg N, Wilken PM, Arun-Chinnappa KS, Barnes I, et al. IMA genome-F17. IMA Fungus. 2022;13(1):19.
pubmed: 36411457
pmcid: 9677705
doi: 10.1186/s43008-022-00104-3
Pham NQ, Duong TA, Wingfield BD, Barnes I, Durán A, Wingfield MJ. Characterisation of the mating-type loci in species of Elsinoë causing scab diseases. Fungal Biol. 2023;127(12):1484–90.
pubmed: 38097322
doi: 10.1016/j.funbio.2023.11.003
Cequeña RCM, Sumabat-Dacones LG. Presence of elsinochrome and other putative effectors in select genomes of the plant pathogen Elsinoë spp. based on in silico analysis. SciEnggJ. 2024;17(1):59–70.
doi: 10.54645/2024171LLY-35
Sayers EW, Bolton EE, Brister JR, Canese K, Chan J, Comeau DC, Connor R, Funk K, Kelly C, Kim S, et al. Database resources of the national center for biotechnology information. Nucleic Acids Res. 2022;50(D1):D20–d26.
pubmed: 34850941
doi: 10.1093/nar/gkab1112
The Galaxy platform for accessible. reproducible, and collaborative data analyses: 2024 update. Nucleic Acids Res. 2024;52(W1):W83–w94.
doi: 10.1093/nar/gkae410
Gurevich A, Saveliev V, Vyahhi N, Tesler G. QUAST: quality assessment tool for genome assemblies. Bioinformatics. 2013;29(8):1072–5.
pubmed: 23422339
pmcid: 3624806
doi: 10.1093/bioinformatics/btt086
Simão FA, Waterhouse RM, Ioannidis P, Kriventseva EV, Zdobnov EM. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics. 2015;31(19):3210–2.
pubmed: 26059717
doi: 10.1093/bioinformatics/btv351
Ter-Hovhannisyan V, Lomsadze A, Chernoff YO, Borodovsky M. Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training. Genome Res. 2008;18(12):1979–90.
pubmed: 18757608
pmcid: 2593577
doi: 10.1101/gr.081612.108
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28(12):1647–9.
pubmed: 22543367
pmcid: 3371832
doi: 10.1093/bioinformatics/bts199
Blin K, Shaw S, Kloosterman AM, Charlop-Powers Z, van Wezel GP, Medema MH, Weber T. antiSMASH 6.0: improving cluster detection and comparison capabilities. Nucleic Acids Res. 2021;49(W1):W29–w35.
pubmed: 33978755
pmcid: 8262755
doi: 10.1093/nar/gkab335
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–10.
pubmed: 2231712
doi: 10.1016/S0022-2836(05)80360-2
Li Z, Fan Y, Chang P, Gao L, Wang X. Genome sequence resource for Elsinoë ampelina, the causal organism of grapevine anthracnose. Mol Plant-Microbe Interact. 2020;33(4):576–9.
pubmed: 32013763
doi: 10.1094/MPMI-12-19-0337-A
Zhang X, Zou H, Yang Y, Fang B, Huang L. Genome Resource for Elsinoë batatas, the causal agent of stem and foliage scab disease of sweet potato. Phytopathology. 2022;112(4):973–5.
pubmed: 34645321
doi: 10.1094/PHYTO-08-21-0344-A
Shanmugam G, Jeon J, Hyun J-W. Draft Genome sequences of Elsinoë fawcettii and Elsinoë australis causing scab diseases on citrus. Mol Plant-Microbe Interact. 2020;33(2):135–7.
pubmed: 31577163
doi: 10.1094/MPMI-06-19-0169-A
Haridas S, Albert R, Binder M, Bloem J, LaButti K, Salamov A, Andreopoulos B, Baker SE, Barry K, Bills G, et al. 101 Dothideomycetes genomes: a test case for predicting lifestyles and emergence of pathogens. Stud Mycol. 2020;96:141–53.
pubmed: 32206138
pmcid: 7082219
doi: 10.1016/j.simyco.2020.01.003
Gostinčar C, Ohm RA, Kogej T, Sonjak S, Turk M, Zajc J, Zalar P, Grube M, Sun H, Han J, et al. Genome sequencing of four Aureobasidium pullulans varieties: biotechnological potential, stress tolerance, and description of new species. BMC Genomics. 2014;15:549.
pubmed: 24984952
pmcid: 4227064
doi: 10.1186/1471-2164-15-549
Jones P, Binns D, Chang HY, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, et al. InterProScan 5: genome-scale protein function classification. Bioinformatics. 2014;30(9):1236–40.
pubmed: 24451626
pmcid: 3998142
doi: 10.1093/bioinformatics/btu031
Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30(14):3059–66.
pubmed: 12136088
pmcid: 135756
doi: 10.1093/nar/gkf436
Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33(7):1870–4.
pubmed: 27004904
pmcid: 8210823
doi: 10.1093/molbev/msw054
Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30(9):1312–3.
pubmed: 24451623
pmcid: 3998144
doi: 10.1093/bioinformatics/btu033
Miller MA, Pfeiffer W, Schwartz T. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. New Orleans; 2010. p. 1–8. https://doi.org/10.1109/GCE.2010.5676129 .
Gilchrist C, Chooi YH. clinker & clustermap.js: Automatic generation of gene cluster comparison figures. Bioinformatics. 2020;37(16):2473–5 https://cagecat.bioinformatics.nl/tools/clinker .
doi: 10.1093/bioinformatics/btab007
Collemare J, Billard A, Böhnert HU, Lebrun MH. Biosynthesis of secondary metabolites in the rice blast fungus Magnaporthe grisea: the role of hybrid PKS-NRPS in pathogenicity. Mycol Res. 2008;112(Pt 2):207–15.
pubmed: 18272356
doi: 10.1016/j.mycres.2007.08.003
Ren J, Wen L, Gao X, Jin C, Xue Y, Yao X. DOG 1.0: illustrator of protein domain structures. Cell Res. 2009;19(2):271–3.
pubmed: 19153597
doi: 10.1038/cr.2009.6
Christiansen JV, Isbrandt T, Petersen C, Sondergaard TE, Nielsen MR, Pedersen TB, Sørensen JL, Larsen TO, Frisvad JC. Fungal quinones: diversity, producers, and applications of quinones from Aspergillus, Penicillium, Talaromyces, Fusarium, and Arthrinium. Appl Microbiol Biotechnol. 2021;105(21):8157–93.
pubmed: 34625822
doi: 10.1007/s00253-021-11597-0
Fan Y, Liu X, Keyhani NO, Tang G, Pei Y, Zhang W, Tong S. Regulatory cascade and biological activity of Beauveria bassiana oosporein that limits bacterial growth after host death. Proc Natl Acad Sci U S A. 2017;114(9):E1578–e1586.
pubmed: 28193896
pmcid: 5338512
doi: 10.1073/pnas.1616543114
Uchimiya M, Stone AT. Reversible redox chemistry of quinones: Impact on biogeochemical cycles. Chemosphere. 2009;77(4):451–8.
pubmed: 19665164
doi: 10.1016/j.chemosphere.2009.07.025
Daub ME, Herrero S, Chung KR. Reactive oxygen species in plant pathogenesis: the role of perylenequinone photosensitizers. Antioxid Redox Signal. 2013;19(9):970–89.
pubmed: 23259634
doi: 10.1089/ars.2012.5080
Mazur M, Masłowiec D. Antimicrobial activity of lactones. Antibiotics (Basel). 2022;11(10):1327.
pubmed: 36289985
doi: 10.3390/antibiotics11101327
Evidente A. Fungal bioactive macrolides. Nat Prod Rep. 2022;39(8):1591–621.
pubmed: 35723218
doi: 10.1039/D2NP00025C
Lenz KD, Klosterman KE, Mukundan H, Kubicek-Sutherland JZ. Macrolides: From toxins to therapeutics. Toxins (Basel). 2021;13(5):347.
pubmed: 34065929
doi: 10.3390/toxins13050347
Markham JE, Hille J. Host-selective toxins as agents of cell death in plant–fungus interactions. Mol Plant Pathol. 2001;2(4):229–39.
pubmed: 20573011
doi: 10.1046/j.1464-6722.2001.00066.x
Pusztahelyi T, Holb IJ, Pócsi I. Secondary metabolites in fungus-plant interactions. Front Plant Sci. 2015;6:573.
pubmed: 26300892
pmcid: 4527079
doi: 10.3389/fpls.2015.00573
Weiss U, Flon H, Burger WC. The photodynamic pigment of some species of Elsinoë and Sphaceloma. Arch Biochem Biophys. 1957;69:311–9.
pubmed: 13445204
doi: 10.1016/0003-9861(57)90497-6
Wisecaver JH, Rokas A. Fungal metabolic gene clusters-caravans traveling across genomes and environments. Front Microbiol. 2015;6:161.
pubmed: 25784900
pmcid: 4347624
doi: 10.3389/fmicb.2015.00161
Hurst LD, Pál C, Lercher MJ. The evolutionary dynamics of eukaryotic gene order. Nat Rev Genet. 2004;5(4):299–310.
pubmed: 15131653
doi: 10.1038/nrg1319
Keller NP, Turner G, Bennett JW. Fungal secondary metabolism – from biochemistry to genomics. Nat Rev Microbiol. 2005;3(12):937–47.
pubmed: 16322742
doi: 10.1038/nrmicro1286
Wong S, Wolfe KH. Birth of a metabolic gene cluster in yeast by adaptive gene relocation. Nat Genet. 2005;37(7):777–82.
pubmed: 15951822
doi: 10.1038/ng1584
Cary JW, Ehrlich KC. Aflatoxigenicity in Aspergillus: molecular genetics, phylogenetic relationships and evolutionary implications. Mycopathologia. 2006;162(3):167–77.
pubmed: 16944284
doi: 10.1007/s11046-006-0051-8
Batada NN, Urrutia AO, Hurst LD. Chromatin remodelling is a major source of coexpression of linked genes in yeast. Trends Genet. 2007;23(10):480–4.
pubmed: 17822800
doi: 10.1016/j.tig.2007.08.003
Khaldi N, Collemare J, Lebrun MH, Wolfe KH. Evidence for horizontal transfer of a secondary metabolite gene cluster between fungi. Genome Biol. 2008;9(1):R18.
pubmed: 18218086
pmcid: 2395248
doi: 10.1186/gb-2008-9-1-r18
Sieber CM, Lee W, Wong P, Münsterkötter M, Mewes HW, Schmeitzl C, Varga E, Berthiller F, Adam G, Güldener U. The Fusarium graminearum genome reveals more secondary metabolite gene clusters and hints of horizontal gene transfer. PLoS ONE. 2014;9(10):e110311.
pubmed: 25333987
pmcid: 4198257
doi: 10.1371/journal.pone.0110311
Mann CWG, Sawyer A, Gardiner DM, Mitter N, Carroll BJ, Eamens AL. RNA-based control of fungal pathogens in plants. Int J Mol Sci. 2023;24(15):12391.
pubmed: 37569766
pmcid: 10418863
doi: 10.3390/ijms241512391