Abstract
The placement of Corynespora olivacea within the large genus Corynespora (Pleosporales) is controversial, because the species is distantly related to other congeners, including the type species C. cassiicola. Corynespora cassiicola is a polyphagous, cosmopolitan plant pathogen. Successful colonization of plant tissues requires the pathogen’s effector repertoire to modulate host cell physiology and facilitate the infection process. We sequenced and performed functional annotations on the genomes of C. cassiicola CC_29 (genome size about 44.8 Mb; isolated from soybean leaves) and C. olivacea CBS 114450 (32.3 Mb). Our phylogenomic approach showed that C. cassiicola is distantly related to C. olivacea, which clustered among the Massarinaceae family members, supporting a hypothesis that C. olivacea was originally misclassified. The predicted sizes for the proteome and secretome of C. cassiicola (18,487 and 1327, respectively) were larger than those of C. olivacea (13,501 and 920; respectively). Corynespora cassiicola had a richer repertoire of effector proteins (CAZymes, proteases, lipases, and effectors) and genes associated with secondary metabolism than did C. olivacea.
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References
Bankevich A, Nurk S, Antipov D et al (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477. https://doi.org/10.1089/cmb.2012.0021
Blin K, Shaw S, Steinke K et al (2019) antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res 47:W81–W87. https://doi.org/10.1093/nar/gkz310
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Buchfink B, Xie C, Huson DH (2014) Fast and sensitive protein alignment using DIAMOND. Nat Methods 12:59–60. https://doi.org/10.1038/nmeth.3176
Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25:1972–1973. https://doi.org/10.1093/bioinformatics/btp348
Crous PW, Summerell BA, Shivas RG et al (2011) Fungal planet description sheets: 92–106. Persoonia Mol Phylogeny Evol Fungi 27:130–162. https://doi.org/10.3767/003158511X617561
Dixon LJ, Schlub RL, Pernezny K, Datnoff LE (2009) Host specialization and phylogenetic diversity of Corynespora cassiicola. Phytopathology 99:1015–1027. https://doi.org/10.1094/PHYTO-99-9-1015
Doyle JJ, Doyle JL (1990) Isolation of plant DNA from fresh tissue. Focus 12:13–15
El-Gebali S, Mistry J, Bateman A et al (2019) The Pfam protein families database in 2019. Nucleic Acids Res 47:D427–D432. https://doi.org/10.1093/nar/gky995
Emms DM, Kelly S (2015) OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol 16:1–14. https://doi.org/10.1186/s13059-015-0721-2
Figaj D, Ambroziak P, Przepiora T, Skorko-Glonek J (2019) The role of proteases in the virulence of plant pathogenic bacteria. Int J Mol Sci. https://doi.org/10.3390/ijms20030672
Fischer M, Pleiss J (2003) The lipase engineering database: a navigation and analysis tool for protein families. Nucleic Acids Res 31:319–321. https://doi.org/10.1093/nar/gkg015
Flynn JM, Hubley R, Goubert C et al (2020) RepeatModeler2 for automated genomic discovery of transposable element families. Proc Natl Acad Sci USA 117:9451–9457. https://doi.org/10.1073/pnas.1921046117
Gao S, Zeng R, Xu L et al (2020) Genome sequence and spore germination-associated transcriptome analysis of Corynespora cassiicola from cucumber. BMC Microbiol 20:1–20. https://doi.org/10.1186/s12866-020-01873-w
Grigoriev IV, Nikitin R, Haridas S et al (2013) MycoCosm portal: gearing up for 1000 fungal genomes. Nucleic Acids Res 42:D699. https://doi.org/10.1093/nar/gkt1183
Hane JK, Lowe RGT, Solomon PS et al (2007) Dothideomycete-plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. Plant Cell 19:3347–3368. https://doi.org/10.1105/tpc.107.052829
Haridas S, Albert R, Binder M et al (2020) 101 Dothideomycetes genomes: a test case for predicting lifestyles and emergence of pathogens. Stud Mycol 96:141–153. https://doi.org/10.1016/j.simyco.2020.01.003
Huerta-Cepas J, Forslund K, Coelho LP et al (2017) Fast genome-wide functional annotation through orthology assignment by eggNOG-mapper. Mol Biol Evol 34:2115–2122. https://doi.org/10.1093/molbev/msx148
Huerta-Cepas J, Szklarczyk D, Heller D et al (2019) EggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res 47:D309–D314. https://doi.org/10.1093/nar/gky1085
Jones P, Binns D, Chang HY et al (2014) InterProScan 5: Genome-scale protein function classification. Bioinformatics 30:1236–1240. https://doi.org/10.1093/bioinformatics/btu031
Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780. https://doi.org/10.1093/molbev/mst010
Keller NP (2019) Fungal secondary metabolism: regulation, function and drug discovery. Nat Rev Microbiol 17:167–180. https://doi.org/10.1038/s41579-018-0121-1
Krogh A, Larsson B, Von Heijne G, Sonnhammer ELL (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580. https://doi.org/10.1006/jmbi.2000.4315
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25:1754–1760. https://doi.org/10.1093/bioinformatics/btp324
Lo Presti L, Lanver D, Schweizer G et al (2015) Fungal effectors and plant susceptibility. Annu Rev Plant Biol 66:513–545. https://doi.org/10.1146/annurev-arplant-043014-114623
Looi HK, Toh YF, Yew SM et al (2017) Genomic insight into pathogenicity of dematiaceous fungus Corynespora cassiicola. PeerJ 5:1–28. https://doi.org/10.7717/peerj.2841
Lopez D, Ribeiro S, Label P et al (2018) Genome-wide analysis of Corynespora cassiicola leaf fall disease putative effectors. Front Microbiol 9:1–21. https://doi.org/10.3389/fmicb.2018.00276
Mikheenko A, Prjibelski A, Saveliev V et al (2018) Versatile genome assembly evaluation with QUAST-LG. Bioinformatics 34:i142–i150. https://doi.org/10.1093/bioinformatics/bty266
Molina JPE, Paul PA, Amorim L et al (2019) Effect of target spot on soybean yield and factors affecting this relationship. Plant Pathol 68:107–115. https://doi.org/10.1111/ppa.12944
Nguyen LT, Schmidt HA, Von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274. https://doi.org/10.1093/molbev/msu300
Ohm RA, Feau N, Henrissat B et al (2012) Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen Dothideomycetes fungi. PLoS Pathog. https://doi.org/10.1371/journal.ppat.1003037
Petersen TN, Brunak S, Von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786. https://doi.org/10.1038/nmeth.1701
Rawlings ND, Barrett AJ, Bateman A (2012) MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Res 40:343–350. https://doi.org/10.1093/nar/gkr987
Rouxel T, Grandalbert J, Hane JK et al (2011) Effector diversification within compartments of the Leptosphaeria maculans genome affected by repeat-induced point mutations. Nat Commun 2:202. https://doi.org/10.1038/ncomms1189
Schoch CL, Crous PW, Groenewald JZ et al (2009) A class-wide phylogenetic assessment of Dothideomycetes. Stud Mycol 64:1–15. https://doi.org/10.3114/sim.2009.64.01
Simão FA, Waterhouse RM, Ioannidis P et al (2015) BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics 31:3210–3212. https://doi.org/10.1093/bioinformatics/btv351
Snelders NC, Kettles GJ, Rudd JJ, Thomma BPHJ (2018) Plant pathogen effector proteins as manipulators of host microbiomes? Mol Plant Pathol 19:257–259. https://doi.org/10.1111/mpp.12628
Sonah H, Deshmukh RK, Bélanger RR (2016) Computational prediction of effector proteins in fungi: opportunities and challenges. Front Plant Sci 7:1–14. https://doi.org/10.3389/fpls.2016.00126
Sperschneider J, Dodds PN, Gardiner DM et al (2018) Improved prediction of fungal effector proteins from secretomes with EffectorP 2.0. Mol Plant Pathol 19:2094–2110. https://doi.org/10.1111/mpp.12682
Stanke M, Morgenstern B (2005) AUGUSTUS: a web server for gene prediction in eukaryotes that allows user-defined constraints. Nucleic Acids Res 33:465–467. https://doi.org/10.1093/nar/gki458
Sumabat LG, Kemerait RC, Brewer MT (2018) Phylogenetic diversity and host specialization of Corynespora cassiicola responsible for emerging target spot disease of cotton and other crops in the southeastern United States. Phytopathology 108:892–901. https://doi.org/10.1094/PHYTO-12-17-0407-R
Tanaka K, Hirayama K, Yonezawa H et al (2015) Revision of the Massarineae (Pleosporales, Dothideomycetes). Stud Mycol 82:75–136. https://doi.org/10.1016/j.simyco.2015.10.002
Verma S, Gazara RK, Nizam S et al (2016) Draft genome sequencing and secretome analysis of fungal phytopathogen Ascochyta rabiei provides insight into the necrotrophic effector repertoire. Sci Rep 6:1–14. https://doi.org/10.1038/srep24638
Voglmayr H, Jaklitsch WM (2017) Corynespora, Exosporium and Helminthosporium revisited – new species and generic reclassification. Stud Mycol 87:43–76. https://doi.org/10.1016/j.simyco.2017.05.001
Wood DE, Lu J, Langmead B (2019) Improved metagenomic analysis with Kraken 2. Genome Biol 20:1–13. https://doi.org/10.1186/s13059-019-1891-0
Zeiner CA, Purvine SO, Zink EM et al (2016) Comparative analysis of secretome profiles of manganese(II)-oxidizing Ascomycete fungi. PLoS ONE. https://doi.org/10.1371/journal.pone.0157844
Zhang H, Yohe T, Huang L et al (2018) DbCAN2: a meta server for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 46:W95–W101. https://doi.org/10.1093/nar/gky418
Ziv C, Zhao Z, Gao YG, Xia Y (2018) Multifunctional roles of plant cuticle during plant–pathogen interactions. Front Plant Sci 9:1–8. https://doi.org/10.3389/fpls.2018.01088
Acknowledgements
This work was supported by The Minas Gerais State Foundation of Research Aid—FAPEMIG (grant number APQ-00150-17) and by The National Council of Scientific and Technological Development—CNPq (fellowship number PQ 302336/2019-2) to LOO. TCSD received student fellowships from the CAPES Foundation (PROEX—0487 No. 1684083) from Mar/2017 to Jul/2018 and CNPq (GM/GD 142400/2018-1) from Aug/2018 to Apr/2021. HVSR was supported by a PD fellowship from the São Paulo Research Foundation—FAPESP (2018/04555-0).
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Dal’Sasso, T.C.d.S., Rody, H.V.S., Grijalba, P.E. et al. Genome sequences and in silico effector mining of Corynespora cassiicola CC_29 and Corynespora olivacea CBS 114450. Arch Microbiol 203, 5257–5265 (2021). https://doi.org/10.1007/s00203-021-02456-7
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DOI: https://doi.org/10.1007/s00203-021-02456-7