Abstract
Fungi of the genus Colletotrichum are economically important and are used as models in plant-pathogen interaction studies. In this study, the complete mitochondrial genomes of two Colletotrichum lindemuthianum isolates were sequenced and compared with the mitochondrial genomes of seven species of Colletotrichum. The mitochondrial genome of C. lindemuthianum is a typical circular molecule 37,446 bp (isolate 89 A2 2-3) and 37,440 bp (isolate 83.501) in length. The difference of six nucleotides between the two genomes is the result of a deletion in the ribosomal protein S3 (rps3) gene in the 83.501 isolate. In addition, substitution of adenine for guanine within the rps3 gene in the mitochondrial genome of the 83.501 isolate was observed. Compared to the previously sequenced C. lindemuthianum mitochondrial genome, an exon no annotated in the cytochrome c oxidase I (cox1) gene and a non-conserved open reading frame (ncORF) were observed. The size of the mitochondrial genomes of the seven species of Colletotrichum was highly variable, being attributed mainly to the ncORF, ranging from one to 10 and also from introns ranging from one to 11 and which encode a total of up to nine homing endonucleases. This paper reports for the first time by means of transcriptome that then ncORFs are transcribed in Colletotrichum spp. Phylogeny data revealed that core mitochondrial genes could be used as an alternative in phylogenetic relationship studies in Colletotrichum spp. This work contributes to the genetic and biological knowledge of Colletotrichum spp., which is of great economic and scientific importance.
Similar content being viewed by others
References
Aguileta G, De Vienne DM, Ross ON, Hood ME, Giraud T, Petit E, Gabaldón T (2014) High variability of mitochondrial gene order among fungi. Genome Biol Evol 6(2):451–465. https://doi.org/10.1093/gbe/evu028
Al-Reedy RM, Malireddy R, Dillman CB, Kennell JC (2012) Comparative analysis of Fusarium mitochondrial genomes reveals a highly variable region that encodes an exceptionally large open reading frame. Fungal Genet Biol 49(1):2–14. https://doi.org/10.1016/j.fgb.2011.11.008
Alikhan NF, Petty NK, Ben Zakour NL, Beatson SA (2011) BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 12(1):402. https://doi.org/10.1186/1471-2164-12-402
Alzate-Marin AL, Gonçalves De Barros E, Moreira MA (1999) Co-evolution model of Colletotrichum lindemuthianum (Melanconiaceae, Melanconiales) races that occur in some Brazilian regions. Genet Mol Biol 22(1):115–118. https://doi.org/10.1590/S1415-47571999000100022
Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13(4):729–744. https://doi.org/10.1046/j.1365-294X.2003.02063.x
Bernt M, Donath A, Jühling F, Externbrink F, Florentz C, Fritzsch G, Pütz J, Middendorf M, Stadler PF (2013) MITOS: improved de novo metazoan mitochondrial genome annotation. Mol Phylogenet Evol 69(2):313–319. https://doi.org/10.1016/j.ympev.2012.08.023
Burger G, Gray MW, Lang BF (2003) Mitochondrial genomes: anything goes. Trends Genet 19(12):709–716. https://doi.org/10.1016/j.tig.2003.10.012
Cannon PF, Damm U, Johnston PR, Weir BS (2012) Colletotrichum—current status and future directions. Stud Mycol 73(1):181–213. https://doi.org/10.3114/sim0014
Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T (2009) trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25(15):1972–1973. https://doi.org/10.1093/bioinformatics/btp348
Carullo M, Xia X (2008) An extensive study of mutation and selection on the wobble nucleotide in tRNA anticodons in fungal mitochondrial genomes. J Mol Evol 66(5):484–493. https://doi.org/10.1007/s00239-008-9102-8
Chan PP, Lowe TM (2009) GtRNAdb: a database of transfer RNA genes detected in genomic sequence. Nucleic Acids Res 37(Database):93–97. https://doi.org/10.1093/nar/gkn787
Crouch JA, O’Connell R, Gan P, Buiate E, Torres MF, Beirn L, Shirasu K, Vaillancourt L (2014) The genomics of Colletotrichum. In: Dean RA, Lichens-Park A, Kole C (eds) Genomics of plant-associated fungi: monocot pathogens. Springer Verlag, Berlin, pp 69–102. https://doi.org/10.1007/978-3-662-44053-7_3
Deng Y, Zhang Q, Ming R, Lin L, Lin X, Lin Y, Li X, Xie B, Wen Z (2016) Analysis of the mitochondrial genome in Hypomyces aurantius reveals a novel twintron complex in fungi. Int J Mol Sci 17(7):1049. https://doi.org/10.3390/ijms17071049
dos Santos LV, de Queiroz MV, Santana MF, Soares MA, de Barros EG, de Araújo EF, Langin T (2012) Development of new molecular markers for the Colletotrichum genus using RetroCl1 sequences. World J Microbiol Biotechnol 28(3):1087–1095. https://doi.org/10.1007/s11274-011-0909-x
Ferandon C, Chatel SEK, Castandet B, Castroviejo M, Barroso G (2008) The Agrocybe aegerita mitochondrial genome contains two inverted repeats of the nad4 gene arisen by duplication on both sides of a linear plasmid integration site. Fungal Genet Biol 45(3):292–301. https://doi.org/10.1016/j.fgb.2007.10.012
Fernández MT, Fernández M, Casares A, Rodriguez R, Fueyo M (2000) Bean germplasm evaluation for anthracnose resistance and characterization of agronomic traits: a new physiological strain of Colletotrichum lindemuthianum infecting Phaseolus vulgaris L. Spain Euphytica 114(2):143–149. https://doi.org/10.1023/A:1003937812700
Ferreira JJ, Campa A, Kelly JD (2013) Organization of genes conferring resistance to anthracnose in common bean. Transl Genomics Crop Breed 1:151–176. https://doi.org/10.1002/9781118728475
Gan P, Narusaka M, Kumakura N, Tsushima A, Takano Y, Narusaka Y, Shirasu K (2016) Genus-wide comparative genome analyses of Colletotrichum species reveal specific gene family losses and gains during adaptation to specific infection lifestyles. Genome Biol Evol 8(5):1467–1481. https://doi.org/10.1093/gbe/evw089
Ghikas DV, Kouvelis VN, Typas MA (2006) The complete mitochondrial genome of the entomopathogenic fungus Metarhizium anisopliae var. anisopliae: gene order and trn gene clusters reveal a common evolutionary course for all Sordariomycetes, while intergenic regions show variation. Arch Microbiol 185(5):393–401. https://doi.org/10.1007/s00203-006-0104-x
González AM, Yuste-Lisbona FJ, Rodiño AP, De Ron AM, Capel C, García-Alcázar M, Lozano R, Santalla M (2015) Uncovering the genetic architecture of Colletotrichum lindemuthianum resistance through QTL mapping and epistatic interaction analysis in common bean. Front Plant Sci 6:13. https://doi.org/10.3389/fpls.2015.00141
Gutiérrez P, Alzate J, Yepes MS, Marín M (2016) Complete mitochondrial genome sequence of the common bean anthracnose pathogen Colletotrichum lindemuthianum. Mitochondrial DNA Part A 27(1):136–137. https://doi.org/10.3109/19401736.2013.878912
James TY, Pelin A, Bonen L, Ahrendt S, Sain D, Corradi N, Stajich JE (2013) Shared signatures of parasitism and phylogenomics unite Cryptomycota and microsporidia. Curr Biol 23(16):1548–1553. https://doi.org/10.1016/j.cub.2013.06.057
Jang CY, Lee JY, Kim J (2004) RpS3, a DNA repair endonuclease and ribosomal protein, is involved in apoptosis. FEBS Lett 560(1-3):81–85. https://doi.org/10.1016/S0014-5793(04)00074-2
Jelen V, De Jonge R, Van De Peer Y, Javornik B, Jakše J (2016) Complete mitochondrial genome of the Verticillium-wilt causing plant pathogen Verticillium nonalfalfae. PLoS One 11(2):e0148525. https://doi.org/10.1371/journal.pone.0148525
Kang D, Hamasaki N (2002) Maintenance of mitochondrial DNA integrity: repair and degradation. Curr Genet 41(5):311–322. https://doi.org/10.1007/s00294-002-0312-0
Kim J-O, Choi K-Y, Han J-H, Choi I-Y, Lee Y-H, Kim KS (2016) The complete mitochondrial genome sequence of the ascomycete plant pathogen Colletotrichum acutatum. Mitochondrial DNA Part A 27(6):4547–4548. https://doi.org/10.3109/19401736.2015.1101556
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874. https://doi.org/10.1093/molbev/msw054
Lang BF, Laforest MJ, Burger G (2007) Mitochondrial introns: a critical view. Trends Genet 23(3):119–125. https://doi.org/10.1016/j.tig.2007.01.006
Laslett D, Canbäck B (2008) ARWEN: a program to detect tRNA genes in metazoan mitochondrial nucleotide sequences. Bioinformatics 24(2):172–175. https://doi.org/10.1093/bioinformatics/btm573
Li Y, Hu X-D, Yang R-H, Hsiang T, Wang K, Liang D-Q, Liang F, Cao D-M, Zhou F, Wen G, Yao Y-J (2015) Complete mitochondrial genome of the medicinal fungus Ophiocordyceps sinensis. Sci Rep 5(1):13892. https://doi.org/10.1038/srep13892
Liang X, Tian X, Liu W, Wei T, Wang W, Dong Q, Wang B, Meng Y, Zhang R, Gleason ML, Sun G (2017) Comparative analysis of the mitochondrial genomes of Colletotrichum gloeosporioides sensu lato: insights into the evolution of a fungal species complex interacting with diverse plants. BMC Genomics 18(1):171. https://doi.org/10.1186/s12864-016-3480-x
Losada L, Pakala SB, Fedorova ND, Joardar V, Shabalina SA, Hostetler J, Pakala SM, Zafar N, Thomas E, Rodriguez-Carres M, Dean R, Vilgalys R, Nierman WC, Cubeta MA (2014) Mobile elements and mitochondrial genome expansion in the soil fungus and potato pathogen Rhizoctonia solani AG-3. FEMS Microbiol Lett 352(2):165–173. https://doi.org/10.1111/1574-6968.12387
Maddison WP, Maddison DR (2017) Mesquite: a modular system for evolutionary analysis. Version 3.2. http://mequiteproject.org
Mota SF, Barcelos QL, Dias MA, Souza EA (2016) Variability of Colletotrichum spp in common bean. Genet Mol Res 15(2):. https://doi.org/10.4238/gmr.15027176
Nadimi M, Stefani FOP, Hijri M (2016) The large (134.9 kb) mitochondrial genome of the glomeromycete Funneliformis mosseae. Mycorrhiza 26(7):747–755. https://doi.org/10.1007/s00572-016-0710-7
Novoa EM, Ribas de Pouplana L (2012) Speeding with control: codon usage, tRNAs, and ribosomes. Trends Genet 28(11):574–581. https://doi.org/10.1016/j.tig.2012.07.006
Nylander JAA (2004) MrModeltest v. 2. Program distributed by the author. Uppsala: Evolutionary Biology Center, Uppsala University
O’Connell RJ, Thon MR, Hacquard S, Amyotte SG, Kleemann J, Torres MF, Damm U, Buiate EA, Epstein L, Alkan N, Altmüller J, Alvarado-Balderrama L, Bauser CA, Becker C, Birren BW, Chen Z, Choi J, Crouch JA, Duvick JP, Farman MA, Gan P, Heiman D, Henrissat B, Howard RJ, Kabbage M, Koch C, Kracher B, Kubo Y, Law AD, Lebrun M-H, Lee Y-H, Miyara I, Moore N, Neumann U, Nordström K, Panaccione DG, Panstruga R, Place M, Proctor RH, Prusky D, Rech G, Reinhardt R, Rollins JA, Rounsley S, Schardl CL, Schwartz DC, Shenoy N, Shirasu K, Sikhakolli UR, Stüber K, Sukno SA, Sweigard JA, Takano Y, Takahara H, Trail F, van der Does HC, Voll LM, Will I, Young S, Zeng Q, Zhang J, Zhou S, Dickman MB, Schulze-Lefert P, Ver Loren van Themaat E, Ma L-J, Vaillancourt LJ (2012) Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat Genet 44(9):1060–1065. https://doi.org/10.1038/ng.2372
Padder BA, Sharma PN, Sharma OP, Kapoor V (2007) Genetic diversity and gene flow estimates among five populations of Colletotrichum lindemuthianum across Himachal Pradesh. Physiol Mol Plant Pathol 70:8–12. https://doi.org/10.1016/j.pmpp.2007.05.003
Pasharawipas T, Thaikua S, Flegel TW (2009) Intriguing phylogenetic arrangement of tailed bacteriophages based on putative DNA polymerase sequences. ScienceAsia 35(2):125. https://doi.org/10.2306/scienceasia1513-1874.2009.35.125
Pastor-Corrales MA, Tu JC (1989) Anthracnose. In: Schwartz HF, Pastor-Corrales MA (eds) Bean production problems in the tropics, 2nd edn. Centro Internacional de Agricultura Tropical (CIAT), Cali, Colombia, pp 77–104
Queiroz CB, Correia HLN, Menicucci RP, Vidigal PMP, Queiroz MV (2017) Draft genome sequences of two isolates of Colletotrichum lindemuthianum, the causal agent of anthracnose in common beans. Genome Announc 5(18):e00214–e00217. https://doi.org/10.1128/genomeA.00214-17
Robicheau BM, Young AP, Labutti K, Grigoriev IV, Walker AK (2017) The complete mitochondrial genome of the conifer needle endophyte, Phialocephala scopiformis DAOMC 229536 confirms evolutionary division within the fungal Phialocephala fortinii s.l.—Acephala appalanata species complex. Fungal Biol 121(3):212–221. https://doi.org/10.1016/j.funbio.2016.11.007
Rodríguez-Guerra R, Acosta-Gallegos JA, González-Chavira MM, Simpson J (2006) Patotipos de Colletotrichum lindemuthianum y su implicación en la generación de cultivares resistentes de frijol. Agric técnica en México 32:101–114
Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) Mrbayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61(3):539–542. https://doi.org/10.1093/sysbio/sys029
Salavirta H, Oksanen I, Kuuskeri J, Mäkelä M, Laine P, Paulin L, Lundell T (2014) Mitochondrial genome of Phlebia radiata is the second largest (156 kbp) among fungi and features signs of genome flexibility and recent recombination events. PLoS One 9(5):e97141. https://doi.org/10.1371/journal.pone.0097141
Santaquiteria A, Nielsen J, Klemetsen T, Willassen NP, Præbel K (2017) The complete mitochondrial genome of the long-lived Greenland shark (Somniosus microcephalus): characterization and phylogenetic position. Conserv Genet Resour 9(3):351–355. https://doi.org/10.1007/s12686-016-0676-y
Saraste M (1999) Oxidative phosphorylation at the fin de siècle. Science 283(5407):1488–1493. https://doi.org/10.1126/science.283.5407.1488
Schneider A (2011) Mitochondrial tRNA import and its consequences for mitochondrial translation. Annu Rev Biochem 80(1):1033–1053. https://doi.org/10.1146/annurev-biochem-060109-092838
Sethuraman J, Majer A, Iranpour M, Hausner G (2009) Molecular evolution of the mtDNA encoded rps3 gene among filamentous ascomycetes fungi with an emphasis on the ophiostomatoid fungi. J Mol Evol 69(4):372–385. https://doi.org/10.1007/s00239-009-9291-9
Sharma P, Sharma O, Padder BA, Kapil R (2008) Yield loss assessment in common bean due to anthracnose (Colletotrichum lindemuthianum) under sub temperate conditions of North-Western Himalayas. Indian Phytopathol 61:323–330
Shen XY, Li T, Chen S, Fan L, Gao J, Hou CL (2015) Characterization and phylogenetic analysis of the mitochondrial genome of Shiraia bambusicola reveals special features in the order of Pleosporales. PLoS One 10(3):e0116466. https://doi.org/10.1371/journal.pone.0116466
Slack KE, Delsuc F, Mclenachan PA, Arnason U, Penny D (2007) Resolving the root of the avian mitogenomic tree by breaking up long branches. Mol Phylogenet Evol 42(1):1–13. https://doi.org/10.1016/j.ympev.2006.06.002
Stone CL, Buitrago MLP, Boore JL, Frederick RD (2010) Analysis of the complete mitochondrial genome sequences of the soybean rust pathogens Phakopsora pachyrhizi and P. meibomiae. Mycologia 102(4):887–897. https://doi.org/10.3852/09-198
Sun Z, Wang D, Murphy R, Ma L, Zhang X, Huang D (2009) Comparison of base composition and codon usage in insect mitochondrial genomes. Genes Genomics 31:67–67. https://doi.org/10.1007/BF03191139
Torriani SFF, Goodwin SB, Kema GHJ, Pangilinan JL, McDonald BA (2008) Intraspecific comparison and annotation of two complete mitochondrial genome sequences from the plant pathogenic fungus Mycosphaerella graminicola. Fungal Genet Biol 45(5):628–637. https://doi.org/10.1016/j.fgb.2007.12.005
Torriani SFF, Penselin D, Knogge W, Felder M, Taudien S, Platzer M, McDonald BA, Brunner PC (2014) Comparative analysis of mitochondrial genomes from closely related Rhynchosporium species reveals extensive intron invasion. Fungal Genet Biol 62:34–42. https://doi.org/10.1016/j.fgb.2013.11.001
van de Sande WWJ (2012) Phylogenetic analysis of the complete mitochondrial genome of Madurella mycetomatis confirms its taxonomic position within the order Sordariales. PLoS One 7(6):e38654. https://doi.org/10.1371/journal.pone.0038654
Wei L, He J, Jia X, Qi Q, Liang Z, Zheng H, Ping Y, Liu S, Sun J (2014) Analysis of codon usage bias of mitochondrial genome in Bombyx mori and its relation to evolution. BMC Evol Biol 14(1):262. https://doi.org/10.1186/s12862-014-0262-4
Xia X (2005) Mutation and selection on the anticodon of tRNA genes in vertebrate mitochondrial genomes. Gene 345(1):13–20. https://doi.org/10.1016/j.gene.2004.11.019
Yadavilli S, Mayo LD, Higgins M, Lain S, Hegde V, Deutsch WA (2009) Ribosomal protein S3: A multifunctional protein that interacts with both p53 and MDM2 through its KH domain. DNA Repair (Amst) 8(10):1215–1224. https://doi.org/10.1016/j.dnarep.2009.07.003
Yang X, Cameron SL, Lees DC, Xue D, Han H (2015) A mitochondrial genome phylogeny of owlet moths (Lepidoptera: Noctuoidea), and examination of the utility of mitochondrial genomes for lepidopteran phylogenetics. Mol Phylogenet Evol 85:230–237. https://doi.org/10.1016/j.ympev.2015.02.005
Zhang S, Wang X-N, Zhang X-L, Liu X-Z, Zhang Y-J (2017) Complete mitochondrial genome of the endophytic fungus Pestalotiopsis fici: features and evolution. Appl Microbiol Biotechnol 101(4):1593–1604. https://doi.org/10.1007/s00253-017-8112-0
Funding
This work was supported by the Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Electronic supplementary material
ESM 1
(PDF 106 kb).
Rights and permissions
About this article
Cite this article
de Queiroz, C.B., Santana, M.F., Pereira Vidigal, P.M. et al. Comparative analysis of the mitochondrial genome of the fungus Colletotrichum lindemuthianum, the causal agent of anthracnose in common beans. Appl Microbiol Biotechnol 102, 2763–2778 (2018). https://doi.org/10.1007/s00253-018-8812-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00253-018-8812-0