The genome of opportunistic fungal pathogen Fusarium oxysporum carries a unique set of lineage-specific chromosomes.
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
31 01 2020
31 01 2020
Historique:
received:
19
03
2019
accepted:
10
01
2020
entrez:
2
2
2020
pubmed:
2
2
2020
medline:
11
5
2021
Statut:
epublish
Résumé
Fusarium oxysporum is a cross-kingdom fungal pathogen that infects plants and humans. Horizontally transferred lineage-specific (LS) chromosomes were reported to determine host-specific pathogenicity among phytopathogenic F. oxysporum. However, the existence and functional importance of LS chromosomes among human pathogenic isolates are unknown. Here we report four unique LS chromosomes in a human pathogenic strain NRRL 32931, isolated from a leukemia patient. These LS chromosomes were devoid of housekeeping genes, but were significantly enriched in genes encoding metal ion transporters and cation transporters. Homologs of NRRL 32931 LS genes, including a homolog of ceruloplasmin and the genes that contribute to the expansion of the alkaline pH-responsive transcription factor PacC/Rim1p, were also present in the genome of NRRL 47514, a strain associated with Fusarium keratitis outbreak. This study provides the first evidence, to our knowledge, for genomic compartmentalization in two human pathogenic fungal genomes and suggests an important role of LS chromosomes in niche adaptation.
Identifiants
pubmed: 32005944
doi: 10.1038/s42003-020-0770-2
pii: 10.1038/s42003-020-0770-2
pmc: PMC6994591
doi:
Substances chimiques
Fungal Proteins
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
50Subventions
Organisme : NEI NIH HHS
ID : R01 EY030150
Pays : United States
Références
Brown, G. D., Denning, D. W. & Levitz, S. M. Tackling human fungal infections. Science 336, 647 (2012).
pubmed: 22582229
doi: 10.1126/science.1222236
Mukherjee, S. The Emperor of All Maladies: A Biography of Cancer, Large Print edn (Thorndike Press, 2010).
Morris, P. J. Transplantation–a medical miracle of the 20th century. N. Engl. J. Med. 351, 2678–2680 (2004).
pubmed: 15616201
doi: 10.1056/NEJMp048256
Brandt, M. E. & Park, B. J. Think fungus—prevention and control of fungal infections. Emerg. Infect. Dis. https://doi.org/10.3201/eid1910131092 (2013).
Low, C. Y. & Rotstein, C. Emerging fungal infections in immunocompromised patients. F1000 Med. Rep. 3, 14 (2011).
pubmed: 21876720
pmcid: 3155160
doi: 10.3410/M3-14
Guarro, J. Fusariosis, a complex infection caused by a high diversity of fungal species refractory to treatment. Eur. J. Clin. Microbiol. Infect. Dis. 32, 1491–1500 (2013).
pubmed: 23934595
doi: 10.1007/s10096-013-1924-7
Nucci, M. et al. Improvement in the outcome of invasive fusariosis in the last decade. Clin. Microbiol. Infect. (2013).
Nucci, M. & Anaissie, E. Fusarium infections in immunocompromised patients. Clin. Microbiol. Rev. 20, 695–704 (2007).
pubmed: 17934079
pmcid: 2176050
doi: 10.1128/CMR.00014-07
Kredics, L., Narendran, V., Shobana, C. S., Vagvolgyi, C. & Manikandan, P. Indo-Hungarian Fungal Keratitis Working Group.Filamentous fungal infections of the cornea: a global overview of epidemiology and drug sensitivity. Mycoses 58, 243–260 (2015).
pubmed: 25728367
doi: 10.1111/myc.12306
Hassan, A. S. et al. Antifungal susceptibility and phylogeny of opportunistic members of the genus Fusarium causing human keratomycosis in South India. Med. Mycol. 54, 287–294 (2016).
pubmed: 26705832
doi: 10.1093/mmy/myv105
O’Donnell, K. et al. Phylogenetic diversity and microsphere array-based genotyping of human pathogenic Fusaria, including isolates from the multistate contact lens-associated U.S. keratitis outbreaks of 2005 and 2006. J. Clin. Microbiol. 45, 2235–2248 (2007).
pubmed: 17507522
pmcid: 1933018
doi: 10.1128/JCM.00533-07
Khor, W. B. et al. An outbreak of Fusarium keratitis associated with contact lens wear in Singapore. JAMA 295, 2867–2873 (2006).
pubmed: 16804153
doi: 10.1001/jama.295.24.2867
Mukherjee, P. K. et al. Characterization of Fusarium keratitis outbreak isolates: contribution of biofilms to antimicrobial resistance and pathogenesis. Invest. Ophthalmol. Vis. Sci. 53, 4450–4457 (2012).
pubmed: 22669723
pmcid: 3394686
doi: 10.1167/iovs.12-9848
Gower, E. W. et al. Trends in fungal keratitis in the United States, 2001 to 2007. Ophthalmology 117, 2263–2267 (2010).
pubmed: 20591493
doi: 10.1016/j.ophtha.2010.03.048
Al-Hatmi, A. M., Meis, J. F. & de Hoog, G. S. Fusarium: molecular diversity and intrinsic drug resistance. PLoS Pathog. 12, e1005464 (2016).
pubmed: 27054821
pmcid: 4824402
doi: 10.1371/journal.ppat.1005464
Nucci, M. & Anaissie, E. Cutaneous infection by Fusarium species in healthy and immunocompromised hosts: implications for diagnosis and management. Clin. Infect. Dis. 35, 909–920 (2002).
pubmed: 12355377
doi: 10.1086/342328
Boutati, E. I. & Anaissie, E. J. Fusarium, a significant emerging pathogen in patients with hematologic malignancy: ten years’ experience at a cancer center and implications for management. Blood 90, 999–1008 (1997).
pubmed: 9242529
doi: 10.1182/blood.V90.3.999.999_999_1008
Ibrahim, M. M. et al. Epidemiologic aspects and clinical outcome of fungal keratitis in southeastern Brazil. Eur. J. Ophthalmol. 19, 355–361 (2009).
pubmed: 19396778
doi: 10.1177/112067210901900305
Leal, S. M. Jr. et al. Fungal antioxidant pathways promote survival against neutrophils during infection. J. Clin. Invest 122, 2482–2498 (2012).
pubmed: 22706306
pmcid: 3534057
doi: 10.1172/JCI63239
Bell, B. P. & Khabbaz, R. F. Responding to the outbreak of invasive fungal infections: the value of public health to Americans. JAMA 309, 883–884 (2013).
pubmed: 23364868
doi: 10.1001/jama.2013.526
Kauffman, C. A., Pappas, P. G. & Patterson, T. F. Fungal infections associated with contaminated methylprednisolone injections. N. Engl. J. Med. 368, 2495–2500 (2013).
pubmed: 23083312
doi: 10.1056/NEJMra1212617
O’Donnell, K. et al. Genetic diversity of human pathogenic members of the Fusarium oxysporum complex inferred from multilocus DNA sequence data and amplified fragment length polymorphism analyses: evidence for the recent dispersion of a geographically widespread clonal lineage and nosocomial origin. J. Clin. Microbiol. 42, 5109–5120 (2004).
pubmed: 15528703
pmcid: 525153
doi: 10.1128/JCM.42.11.5109-5120.2004
Ma, L.-J. et al. Fusarium pathogenomics. Annu. Rev. Microbiol. 67, 399–416 (2013).
pubmed: 24024636
doi: 10.1146/annurev-micro-092412-155650
Ma, L. J. et al. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 464, 367–373 (2010).
pubmed: 20237561
pmcid: 3048781
doi: 10.1038/nature08850
O’Donnell, K. et al. A two-locus DNA sequence database for typing plant and human pathogens within the Fusarium oxysporum species complex. Fungal Genet. Biol. 46, 936–948 (2009).
pubmed: 19715767
doi: 10.1016/j.fgb.2009.08.006
O’Donnell, K., Kistler, H. C., Cigelnik, E. & Ploetz, R. C. Multiple evolutionary origins of the fungus causing Panama disease of banana: concordant evidence from nuclear and mitochondrial gene genealogies. Proc. Natl Acad. Sci. USA 95, 2044–2049 (1998).
pubmed: 9482835
doi: 10.1073/pnas.95.5.2044
Schmidt, S. M. et al. MITEs in the promoters of effector genes allow prediction of novel virulence genes in Fusarium oxysporum. BMC Genomics 14, 119 (2013).
pubmed: 23432788
pmcid: 3599309
doi: 10.1186/1471-2164-14-119
Imamura, Y. et al. Fusarium and Candida albicans biofilms on soft contact lenses: model development, influence of lens type, and susceptibility to lens care solutions. Antimicrob. Agents Chemother. 52, 171–182 (2008).
pubmed: 17999966
doi: 10.1128/AAC.00387-07
Alabouvette, C., Olivain, C., Migheli, Q. & Steinberg, C. Microbiological control of soil-borne phytopathogenic fungi with special emphasis on wilt-inducing Fusarium oxysporum. N. Phytol. 184, 529–544 (2009).
doi: 10.1111/j.1469-8137.2009.03014.x
Gnerre, S. et al. High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc. Natl Acad. Sci. USA 108, 1513–1518 (2011).
pubmed: 21187386
doi: 10.1073/pnas.1017351108
Grabherr, M. G. et al. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29, 644–652 (2011).
pubmed: 3571712
pmcid: 3571712
doi: 10.1038/nbt.1883
Chellapan, B. V., van Dam, P., Rep, M., Cornelissen, B. J. & Fokkens, L. Non-canonical helitrons in Fusarium oxysporum. Mob. DNA 7, 27 (2016).
pubmed: 27990178
pmcid: 5148889
doi: 10.1186/s13100-016-0083-7
van Dam, P. et al. Effector profiles distinguish formae speciales of Fusarium oxysporum. Environ. Microbiol. 18, 4087–4102 (2016).
pubmed: 27387256
doi: 10.1111/1462-2920.13445
van Dam, P. & Rep, M. The distribution of miniature impala elements and SIX genes in the Fusarium genus is suggestive of horizontal gene transfer. J. Mol. Evol. 85, 14–25 (2017).
pubmed: 28744785
pmcid: 5579170
doi: 10.1007/s00239-017-9801-0
Penalva, M. A., Tilburn, J., Bignell, E. & Arst, H. N. Jr. Ambient pH gene regulation in fungi: making connections. Trends Microbiol. 16, 291–300 (2008).
pubmed: 18457952
doi: 10.1016/j.tim.2008.03.006
Cornet, M. & Gaillardin, C. pH signaling in human fungal pathogens: a new target for antifungal strategies. Eukaryot. Cell 13, 342–352 (2014).
pubmed: 24442891
pmcid: 3957587
doi: 10.1128/EC.00313-13
Davis, D., Edwards, J. E. Jr., Mitchell, A. P. & Ibrahim, A. S. Candida albicans RIM101 pH response pathway is required for host-pathogen interactions. Infect. Immun. 68, 5953–5959 (2000).
pubmed: 10992507
pmcid: 101559
doi: 10.1128/IAI.68.10.5953-5959.2000
O’Meara, T. R. et al. The Cryptococcus neoformans Rim101 transcription factor directly regulates genes required for adaptation to the host. Mol. Cell. Biol. 34, 673–684 (2014).
pubmed: 24324006
pmcid: 3911494
doi: 10.1128/MCB.01359-13
Bignell, E. et al. The Aspergillus pH-responsive transcription factor PacC regulates virulence. Mol. Microbiol 55, 1072–1084 (2005).
pubmed: 15686555
doi: 10.1111/j.1365-2958.2004.04472.x
pmcid: 15686555
Ortoneda, M. et al. Fusarium oxysporum as a multihost model for the genetic dissection of fungal virulence in plants and mammals. Infect. Immun. 72, 1760–1766 (2004).
pubmed: 14977985
pmcid: 356063
doi: 10.1128/IAI.72.3.1760-1766.2004
Bertuzzi, M. et al. The pH-responsive PacC transcription factor of Aspergillus fumigatus governs epithelial entry and tissue invasion during pulmonary Aspergillosis. PLoS Pathog. 10, e1004413 (2014).
pubmed: 25329394
pmcid: 4199764
doi: 10.1371/journal.ppat.1004413
Orejas, M. et al. Activation of the Aspergillus PacC transcription factor in response to alkaline ambient pH requires proteolysis of the carboxy-terminal moiety. Genes Dev. 9, 1622–1632 (1995).
pubmed: 7628696
doi: 10.1101/gad.9.13.1622
Caracuel, Z. et al. The pH signalling transcription factor PacC controls virulence in the plant pathogen Fusarium oxysporum. Mol. Microbiol. 48, 765–779 (2003).
pubmed: 12694620
doi: 10.1046/j.1365-2958.2003.03465.x
Mingot, J. M., Espeso, E. A., Diez, E. & Penalva, M. A. Ambient pH signaling regulates nuclear localization of the Aspergillus nidulans PacC transcription factor. Mol. Cell. Biol. 21, 1688–1699 (2001).
pubmed: 11238906
pmcid: 86715
doi: 10.1128/MCB.21.5.1688-1699.2001
Caza, M. & Kronstad, J. W. Shared and distinct mechanisms of iron acquisition by bacterial and fungal pathogens of humans. Front. Cell. Infect. Microbiol. 3, 80 (2013).
pubmed: 24312900
pmcid: 3832793
doi: 10.3389/fcimb.2013.00080
Parente, A. F. et al. Proteomic analysis reveals that iron availability alters the metabolic status of the pathogenic fungus Paracoccidioides brasiliensis. PLoS ONE 6, e22810 (2011).
pubmed: 21829521
pmcid: 3145762
doi: 10.1371/journal.pone.0022810
Schrettl, M. & Haas, H. Iron homeostasis–Achilles’ heel of Aspergillus fumigatus? Curr. Opin. Microbiol. 14, 400–405 (2011).
pubmed: 21724450
pmcid: 3162135
doi: 10.1016/j.mib.2011.06.002
Lopez-Berges, M. S. et al. HapX-mediated iron homeostasis is essential for rhizosphere competence and virulence of the soilborne pathogen Fusarium oxysporum. Plant Cell 24, 3805–3822 (2012).
pubmed: 22968717
pmcid: 3480304
doi: 10.1105/tpc.112.098624
Musci, G., Polticelli, F. & Calabrese, L. Structure/function relationships in ceruloplasmin. Adv. Exp. Med. Biol. 448, 175–182 (1999).
pubmed: 10079825
doi: 10.1007/978-1-4615-4859-1_15
Teixeira, M. M. et al. Exploring the genomic diversity of black yeasts and relatives (Chaetothyriales, Ascomycota). Stud. Mycol. 86, 1–28 (2017).
pubmed: 28348446
pmcid: 5358931
doi: 10.1016/j.simyco.2017.01.001
Varga, J., Houbraken, J., Van Der Lee, H. A., Verweij, P. E. & Samson, R. A. Aspergillus calidoustus sp. nov., causative agent of human infections previously assigned to Aspergillus ustus. Eukaryot. Cell 7, 630–638 (2008).
pubmed: 18281596
pmcid: 2292628
doi: 10.1128/EC.00425-07
van Laarhoven, K. A., Huinink, H. P. & Adan, O. C. A microscopy study of hyphal growth of Penicillium rubens on gypsum under dynamic humidity conditions. Microb. Biotechnol. 9, 408–418 (2016).
pubmed: 26996401
pmcid: 4835577
doi: 10.1111/1751-7915.12357
Mosier, A. C. et al. Fungi contribute critical but spatially varying roles in nitrogen and carbon cycling in acid mine drainage. Front. Microbiol. 7, 238 (2016).
pubmed: 26973616
pmcid: 4776211
doi: 10.3389/fmicb.2016.00238
Denef, V. J., Mueller, R. S. & Banfield, J. F. AMD biofilms: using model communities to study microbial evolution and ecological complexity in nature. ISME J. 4, 599–610 (2010).
pubmed: 20164865
doi: 10.1038/ismej.2009.158
Bielli, P. & Calabrese, L. Structure to function relationships in ceruloplasmin: a ‘moonlighting’ protein. Cell. Mol. Life Sci. 59, 1413–1427 (2002).
pubmed: 12440766
doi: 10.1007/s00018-002-8519-2
Zaitseva, I. et al. The x-ray structure of human serum ceruloplasmin at 3.1 angstrom: nature of the copper centres. J. Biol. Inorg. Chem. 1, 15–23 (1996).
Skalova, T. et al. The structure of the small laccase from Streptomyces coelicolor reveals a link between laccases and nitrite reductases. J. Mol. Biol. 385, 1165–1178 (2009).
pubmed: 19063896
doi: 10.1016/j.jmb.2008.11.024
Nairz, M., Schroll, A., Sonnweber, T. & Weiss, G. The struggle for iron - a metal at the host-pathogen interface. Cell. Microbiol. 12, 1691–1702 (2010).
pubmed: 20964797
doi: 10.1111/j.1462-5822.2010.01529.x
Potrykus, J., Ballou, E. R., Childers, D. S. & Brown, A. J. Conflicting interests in the pathogen-host tug of war: fungal micronutrient scavenging versus mammalian nutritional immunity. PLoS Pathog. 10, e1003910 (2014).
pubmed: 24626223
pmcid: 3953404
doi: 10.1371/journal.ppat.1003910
Kronstad, J. W., Hu, G. & Jung, W. H. An encapsulation of iron homeostasis and virulence in Cryptococcus neoformans. Trends Microbiol. 21, 457–465 (2013).
pubmed: 23810126
pmcid: 3769505
doi: 10.1016/j.tim.2013.05.007
Kim, B. E., Nevitt, T. & Thiele, D. J. Mechanisms for copper acquisition, distribution and regulation. Nat. Chem. Biol. 4, 176–185 (2008).
pubmed: 18277979
doi: 10.1038/nchembio.72
Zhu, X. & Williamson, P. R. Role of laccase in the biology and virulence of Cryptococcus neoformans. FEMS Yeast Res. 5, 1–10 (2004).
pubmed: 15381117
doi: 10.1016/j.femsyr.2004.04.004
DeIulio, G. A. et al. Kinome expansion in the Fusarium oxysporum species complex driven by accessory chromosomes. mSphere 3, e00231-18. (2018).
Mulet, J. M. et al. A novel mechanism of ion homeostasis and salt tolerance in yeast: the Hal4 and Hal5 protein kinases modulate the Trk1-Trk2 potassium transporter. Mol. Cell. Biol. 19, 3328–3337 (1999).
pubmed: 10207057
pmcid: 84126
doi: 10.1128/MCB.19.5.3328
Park, G. et al. Global analysis of serine-threonine protein kinase genes in Neurospora crassa. Eukaryot. Cell 10, 1553–1564 (2011).
pubmed: 21965514
pmcid: 3209061
doi: 10.1128/EC.05140-11
Siebel, C. W., Feng, L., Guthrie, C. & Fu, X. D. Conservation in budding yeast of a kinase specific for SR splicing factors. Proc. Natl Acad. Sci. USA 96, 5440–5445 (1999).
pubmed: 10318902
doi: 10.1073/pnas.96.10.5440
Giannakouros, T., Nikolakaki, E., Mylonis, I. & Georgatsou, E. Serine-arginine protein kinases: a small protein kinase family with a large cellular presence. FEBS J. 278, 570–586 (2011).
pubmed: 21205200
doi: 10.1111/j.1742-4658.2010.07987.x
Martinez, D. A. et al. Comparative genome analysis of Trichophyton rubrum and related dermatophytes reveals candidate genes involved in infection. MBio 3, e00259–00212 (2012).
pubmed: 22951933
pmcid: 3445971
doi: 10.1128/mBio.00259-12
Tortorano, A. M. et al. Species distribution and in vitro antifungal susceptibility patterns of 75 clinical isolates of Fusarium spp. from northern Italy. Antimicrob. Agents Chemother. 52, 2683–2685 (2008).
pubmed: 18443107
pmcid: 2443921
doi: 10.1128/AAC.00272-08
Azor, M., Gene, J., Cano, J. & Guarro, J. Universal in vitro antifungal resistance of genetic clades of the Fusarium solani species complex. Antimicrob. Agents Chemother. 51, 1500–1503 (2007).
pubmed: 17220423
pmcid: 1855466
doi: 10.1128/AAC.01618-06
Parks, L. W. & Casey, W. M. Physiological implications of sterol biosynthesis in yeast. Annu. Rev. Microbiol. 49, 95–116 (1995).
pubmed: 8561481
doi: 10.1146/annurev.mi.49.100195.000523
Lupetti, A., Danesi, R., Campa, M., Del Tacca, M. & Kelly, S. Molecular basis of resistance to azole antifungals. Trends Mol. Med. 8, 76–81 (2002).
pubmed: 11815273
doi: 10.1016/S1471-4914(02)02280-3
Coste, A. et al. Genotypic evolution of azole resistance mechanisms in sequential Candida albicans isolates. Eukaryot. Cell 6, 1889–1904 (2007).
pubmed: 17693596
pmcid: 2043391
doi: 10.1128/EC.00151-07
Selmecki, A., Gerami-Nejad, M., Paulson, C., Forche, A. & Berman, J. An isochromosome confers drug resistance in vivo by amplification of two genes, ERG11 and TAC1. Mol. Microbiol. 68, 624–641 (2008).
pubmed: 18363649
doi: 10.1111/j.1365-2958.2008.06176.x
O’Donnell, K. et al. Phylogenetic analyses of RPB1 and RPB2 support a middle Cretaceous origin for a clade comprising all agriculturally and medically important fusaria. Fungal Genet. Biol. 52, 20–31 (2013).
pubmed: 23357352
doi: 10.1016/j.fgb.2012.12.004
Chowdhary, A., Sharma, C. & Meis, J. F. Candida auris: a rapidly emerging cause of hospital-acquired multidrug-resistant fungal infections globally. PLoS Pathog. 13, e1006290 (2017).
Berger, S., El Chazli, Y., Babu, A. F. & Coste, A. T. Azole resistance in Aspergillus fumigatus: a consequence of antifungal use in agriculture? Front. Microbiol. 8, 1024 (2017).
Coleman, J. J. et al. The genome of Nectria haematococca: contribution of supernumerary chromosomes to gene expansion. PLoS Genet. 5, e1000618 (2009).
pubmed: 19714214
pmcid: 2725324
doi: 10.1371/journal.pgen.1000618
Schafer, K., Di Pietro, A., Gow, N. A. & MacCallum, D. Murine model for Fusarium oxysporum invasive fusariosis reveals organ-specific structures for dissemination and long-term persistence. PLoS ONE 9, e89920 (2014).
pubmed: 24587124
pmcid: 3937399
doi: 10.1371/journal.pone.0089920
Dimalanta, E. T. et al. A microfluidic system for large DNA molecule arrays. Anal. Chem. 76, 5293–5301 (2004).
pubmed: 15362885
doi: 10.1021/ac0496401
pmcid: 15362885
Zhou, S., Herschleb, J. & Schwartz, D. C. In: New Methods for DNA Sequencing (ed. Mitchelson, K. R.) (Elsevier B. V., Amsterdam (2007).
Zhou, S. et al. A whole-genome shotgun optical map of Yersinia pestis strain KIM. Appl. Environ. Microbiol. 68, 6321–6331 (2002).
pubmed: 12450857
pmcid: 134435
doi: 10.1128/AEM.68.12.6321-6331.2002
Zhou, S. et al. Shotgun optical mapping of the entire Leishmania major Friedlin genome. Mol. Biochem. Parasitol. 138, 97–106 (2004).
pubmed: 15500921
doi: 10.1016/j.molbiopara.2004.08.002
pmcid: 15500921
Anantharaman, T. S., Mishra, B. & Schwartz, D. C. Genomics via optical mapping III: contiging genomic DNA and variations. Proc. Int. Conf. Intell. Syst. Mol. Biol. 18–27 (1999).
Valouev, A., Zhang, Y., Schwartz, D. C. & Waterman, M. S. Refinement of optical map assemblies. Bioinformatics 22, 1217–1224 (2006).
pubmed: 16500933
doi: 10.1093/bioinformatics/btl063
Zhou, S. et al. Validation of rice genome sequence by optical mapping. BMC Genomics 8, 278 (2007).
pubmed: 17697381
pmcid: 2048515
doi: 10.1186/1471-2164-8-278
Ayhan, D. H., Lopez-Diaz, C., Di Pietro, A. & Ma L. J. Improved assembly of reference genome Fusarium oxysporum f. sp. lycopersici strain Fol4287. Microbiol. Resour. Announc. 7, pii: e00910-18 (2018).
Seppey, M., Manni, M. & Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness. Methods Mol. Biol. 1962, 227–245 (2019).
pubmed: 31020564
pmcid: 31020564
doi: 10.1007/978-1-4939-9173-0_14
Haas, B. J. et al. Improving the Arabidopsis genome annotation using maximal transcript alignment assemblies. Nucleic Acids Res. 31, 5654–5666 (2003).
pubmed: 14500829
pmcid: 14500829
doi: 10.1093/nar/gkg770
Haas, B. J. et al. Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. Genome Biol. 9, 1 (2008).
doi: 10.1186/gb-2008-9-1-r7
Ter-Hovhannisyan, V., Lomsadze, A., Chernoff, Y. O. & Borodovsky, M. Gene prediction in novel fungal genomes using an ab initio algorithm with unsupervised training. Genome Res. 18, 1979–1990 (2008).
Parra, G., Blanco, E. & Guigó, R. Geneid in Drosophila. Genome Res. 10, 511–515 (2000).
pubmed: 10779490
pmcid: 310871
doi: 10.1101/gr.10.4.511
Stanke, M., Steinkamp, R., Waack, S. & Morgenstern, B. AUGUSTUS: a web server for gene finding in eukaryotes. Nucleic Acids Res. 32, W309–W312 (2004).
pubmed: 15215400
pmcid: 441517
doi: 10.1093/nar/gkh379
Majoros, W. H., Pertea, M. & Salzberg, S. L. TigrScan and GlimmerHMM: two open source ab initio eukaryotic gene-finders. Bioinformatics 20, 2878–2879 (2004).
pubmed: 15145805
doi: 10.1093/bioinformatics/bth315
Korf, I. Gene finding in novel genomes. BMC Bioinformatics 5, 59 (2004).
pubmed: 15144565
pmcid: 421630
doi: 10.1186/1471-2105-5-59
Birney, E., Clamp, M. & Durbin, R. GeneWise and genomewise. Genome Res. 14, 988–995 (2004).
pubmed: 15123596
pmcid: 479130
doi: 10.1101/gr.1865504
Bolger, A. M., Lohse, M. & Usadel, B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120 (2014).
pubmed: 24695404
pmcid: 24695404
doi: 10.1093/bioinformatics/btu170
Burge, S. W. et al. Rfam 11.0: 10 years of RNA families. Nucleic Acids Res. 41, D226–D232 (2013).
pubmed: 23125362
doi: 10.1093/nar/gks1005
Price, A. L., Jones, N. C. & Pevzner, P. A. De novo identification of repeat families in large genomes. Bioinformatics 21, i351–i358 (2005).
pubmed: 15961478
doi: 10.1093/bioinformatics/bti1018
Chen, N. Using RepeatMasker to identify repetitive elements in genomic sequences. Curr. Protoc. Bioinformatics. 5, 4.10. 11–14.10. 14 (2004).
doi: 10.1002/0471250953.bi0410s05
Lawton, T. J., Sayavedra-Soto, L. A., Arp, D. J. & Rosenzweig, A. C. Crystal structure of a two-domain multicopper oxidase: implications for the evolution of multicopper blue proteins. J. Biol. Chem. 284, 10174–10180 (2009).
pubmed: 19224923
pmcid: 2665071
doi: 10.1074/jbc.M900179200
Gill, S. R. et al. Metagenomic analysis of the human distal gut microbiome. Science 312, 1355–1359 (2006).
pubmed: 16741115
pmcid: 3027896
doi: 10.1126/science.1124234