Enrichment of G4DNA and a Large Inverted Repeat Coincide in the Mitochondrial Genomes of Termitomyces

Overview

Journal Genome Biol Evol

Publisher Oxford University Press

Specialties Biology
Genetics
Molecular Biology

Date 2019 Jun 19

PMID 31209489

Citations 11

Authors

Mathijs Nieuwenhuis

Lennart J J van de Peppel

Freek T Bakker

Bas J Zwaan

Duur K Aanen

Affiliations

Soon will be listed here.

Abstract

Mitochondria retain their own genome, a hallmark of their bacterial ancestry. Mitochondrial genomes (mtDNA) are highly diverse in size, shape, and structure, despite their conserved function across most eukaryotes. Exploring extreme cases of mtDNA architecture can yield important information on fundamental aspects of genome biology. We discovered that the mitochondrial genomes of a basidiomycete fungus (Termitomyces spp.) contain an inverted repeat (IR), a duplicated region half the size of the complete genome. In addition, we found an abundance of sequences capable of forming G-quadruplexes (G4DNA); structures that can disrupt the double helical formation of DNA. G4DNA is implicated in replication fork stalling, double-stranded breaks, altered gene expression, recombination, and other effects. To determine whether this occurrence of IR and G4DNA was correlated within the genus Termitomyces, we reconstructed the mitochondrial genomes of 11 additional species including representatives of several closely related genera. We show that the mtDNA of all sampled species of Termitomyces and its sister group, represented by the species Tephrocybe rancida and Blastosporella zonata, are characterized by a large IR and enrichment of G4DNA. To determine whether high mitochondrial G4DNA content is common in fungi, we conducted the first broad survey of G4DNA content in fungal mtDNA, revealing it to be a highly variable trait. The results of this study provide important direction for future research on the function and evolution of G4DNA and organellar IRs.

Citing Articles

Genetic differentiation of Oncomelania hupensis robertsoni in hilly regions of China: Using the complete mitochondrial genome.

Song J, Wang H, Li S, Qian P, Wang W, Shen M PLoS Negl Trop Dis. 2024; 18(11):e0012094.

PMID: 39591469 PMC: 11630586. DOI: 10.1371/journal.pntd.0012094.

Genetic population structure of the agaric () reveals cryptic species and different roles for sexual and asexual spores in dispersal.

van de Peppel L, Baroni T, Franco-Molano A, Aanen D Persoonia. 2024; 49:195-200.

PMID: 38234378 PMC: 10792229. DOI: 10.3767/persoonia.2022.49.06.

The mitochondrial genome of the bioluminescent fish Ayres, 1848 (Stomiidae, Actinopterygii) is large and complex, and contains an inverted-repeat structure.

Gastineau R, Otis C, Boyle B, Lemieux C, Turmel M, St-Cyr J Zookeys. 2023; 1157:177-191.

PMID: 37234952 PMC: 10206720. DOI: 10.3897/zookeys.1157.97921.

Co-evolution of large inverted repeats and G-quadruplex DNA in fungal mitochondria may facilitate mitogenome stability: the case of Malassezia.

Christinaki A, Theelen B, Zania A, Coutinho S, Cabanes J, Boekhout T Sci Rep. 2023; 13(1):6308.

PMID: 37072481 PMC: 10113387. DOI: 10.1038/s41598-023-33486-4.

A genetic linkage map and improved genome assembly of the termite symbiont Termitomyces cryptogamus.

Vreeburg S, Auxier B, Jacobs B, Bourke P, van den Heuvel J, Zwaan B BMC Genomics. 2023; 24(1):123.

PMID: 36927388 PMC: 10021994. DOI: 10.1186/s12864-023-09210-x.

References

Aanen D, Eggleton P, Rouland-Lefevre C, Rosendahl S, Boomsma J . The evolution of fungus-growing termites and their mutualistic fungal symbionts. Proc Natl Acad Sci U S A. 2002; 99(23):14887-92. PMC: 137514. DOI: 10.1073/pnas.222313099. View

Valton A, Hassan-Zadeh V, Lema I, Boggetto N, Alberti P, Saintome C . G4 motifs affect origin positioning and efficiency in two vertebrate replicators. EMBO J. 2014; 33(7):732-46. PMC: 4000090. DOI: 10.1002/embj.201387506. View

Nguyen L, Schmidt H, von Haeseler A, Minh B . IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2014; 32(1):268-74. PMC: 4271533. DOI: 10.1093/molbev/msu300. View

Court D, Bertrand H . Genetic organization and structural features of maranhar, a senescence-inducing linear mitochondrial plasmid of Neurospora crassa. Curr Genet. 1992; 22(5):385-97. DOI: 10.1007/BF00352440. View

Hudspeth M, Shumard D, Bradford C, Grossman L . Organization of Achlya mtDNA: a population with two orientations and a large inverted repeat containing the rRNA genes. Proc Natl Acad Sci U S A. 1983; 80(1):142-6. PMC: 393326. DOI: 10.1073/pnas.80.1.142. View

OBrien M, Misner I, Lane C . Mitochondrial genome sequences and comparative genomics of Achlya hypogyna and Thraustotheca clavata. J Eukaryot Microbiol. 2013; 61(2):146-54. DOI: 10.1111/jeu.12092. View

Shrivastav M, De Haro L, Nickoloff J . Regulation of DNA double-strand break repair pathway choice. Cell Res. 2007; 18(1):134-47. DOI: 10.1038/cr.2007.111. View

Cui Y, Kong D, Ghimire C, Xu C, Mao H . Mutually Exclusive Formation of G-Quadruplex and i-Motif Is a General Phenomenon Governed by Steric Hindrance in Duplex DNA. Biochemistry. 2016; 55(15):2291-9. DOI: 10.1021/acs.biochem.6b00016. View

Wolters J, Chiu K, Fiumera H . Population structure of mitochondrial genomes in Saccharomyces cerevisiae. BMC Genomics. 2015; 16:451. PMC: 4464245. DOI: 10.1186/s12864-015-1664-4. View

10.

Xu J, Zhang Y, Pun N . Mitochondrial recombination in natural populations of the button mushroom Agaricus bisporus. Fungal Genet Biol. 2012; 55:92-7. DOI: 10.1016/j.fgb.2012.09.004. View

11.

Koole W, van Schendel R, Karambelas A, van Heteren J, Okihara K, Tijsterman M . A Polymerase Theta-dependent repair pathway suppresses extensive genomic instability at endogenous G4 DNA sites. Nat Commun. 2014; 5:3216. DOI: 10.1038/ncomms4216. View

12.

Peris D, Arias A, Orlic S, Belloch C, Perez-Traves L, Querol A . Mitochondrial introgression suggests extensive ancestral hybridization events among Saccharomyces species. Mol Phylogenet Evol. 2017; 108:49-60. DOI: 10.1016/j.ympev.2017.02.008. View

13.

Zaug A, Podell E, Cech T . Human POT1 disrupts telomeric G-quadruplexes allowing telomerase extension in vitro. Proc Natl Acad Sci U S A. 2005; 102(31):10864-9. PMC: 1180509. DOI: 10.1073/pnas.0504744102. View

14.

Gerhold J, Aun A, Sedman T, Joers P, Sedman J . Strand invasion structures in the inverted repeat of Candida albicans mitochondrial DNA reveal a role for homologous recombination in replication. Mol Cell. 2010; 39(6):851-61. DOI: 10.1016/j.molcel.2010.09.002. View

15.

Biffi G, Tannahill D, Miller J, Howat W, Balasubramanian S . Elevated levels of G-quadruplex formation in human stomach and liver cancer tissues. PLoS One. 2014; 9(7):e102711. PMC: 4102534. DOI: 10.1371/journal.pone.0102711. View

16.

Hansel-Hertsch R, Di Antonio M, Balasubramanian S . DNA G-quadruplexes in the human genome: detection, functions and therapeutic potential. Nat Rev Mol Cell Biol. 2017; 18(5):279-284. DOI: 10.1038/nrm.2017.3. View

17.

da Costa R, Hu H, Pilgaard B, Vreeburg S, Schuckel J, Pedersen K . Enzyme Activities at Different Stages of Plant Biomass Decomposition in Three Species of Fungus-Growing Termites. Appl Environ Microbiol. 2017; 84(5). PMC: 5812949. DOI: 10.1128/AEM.01815-17. View

18.

Lohse M, Drechsel O, Kahlau S, Bock R . OrganellarGenomeDRAW--a suite of tools for generating physical maps of plastid and mitochondrial genomes and visualizing expression data sets. Nucleic Acids Res. 2013; 41(Web Server issue):W575-81. PMC: 3692101. DOI: 10.1093/nar/gkt289. View

19.

Boetzer M, Henkel C, Jansen H, Butler D, Pirovano W . Scaffolding pre-assembled contigs using SSPACE. Bioinformatics. 2010; 27(4):578-9. DOI: 10.1093/bioinformatics/btq683. View

20.

Garg R, Aggarwal J, Thakkar B . Genome-wide discovery of G-quadruplex forming sequences and their functional relevance in plants. Sci Rep. 2016; 6:28211. PMC: 4914980. DOI: 10.1038/srep28211. View