
==== Front
Mitochondrial DNA B Resour
Mitochondrial DNA B Resour
Mitochondrial DNA. Part B, Resources
2380-2359
Taylor & Francis

10.1080/23802359.2024.2403409
2403409
Version of Record
Data Note
Mitogenome Report
Characterization and phylogenetic analysis of the Talaromyces liani (kamyschko) Yilmaz, Frisvad & Samson, 2014 (Eurotiales: trichocomaceae) mitochondrial genome
J. He et al.
He Jing ab*
Qu Huijuan c*
Yu Youqiao b
Huang Jingwei b #
a Panxi Crops Research and Utilization Key Laboratory of Sichuan Province, Xichang University, Xichang, Sichuan, China
b Key Laboratory of Coarse Cereal Processing, Ministry of Agriculture and Rural Affairs, Chengdu University, Chengdu, Sichuan, China
c Biotechnology and Nuclear Technology Research Institute, Sichuan Academy of Agricultural Sciences, Chengdu, China
* These authors contributed equally to this work.

# Present address: 2025# Chengluo Avenue, Longquanyi District, Chengdu City, Sichuan Province, China.

Supplemental data for this article can be accessed online at https://doi.org/10.1080/23802359.2024.2403409.

CONTACT Jingwei Huang huangjingwei@cdu.edu.cn Key Laboratory of Coarse Cereal Processing, Ministry of Agriculture and Rural Affairs, Chengdu University, Chengdu, Sichuan, China
12 9 2024
2024
12 9 2024
9 9 12011206
24 5 2024
8 9 2024
KnowledgeWorks Global Ltd.12 9 2024
published online in a building issue12 9 2024
© 2024 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group.
2024
The Author(s)
https://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. The terms on which this article has been published allow the posting of the Accepted Manuscript in a repository by the author(s) or with their consent.

Abstract

The filamentous fungus Talaromyces liani (Kamyschko) Yilmaz, Frisvad & Samson, 2014, has attracted considerable interest in biotechnology due to its diverse industrial applications and physiological characteristics. However, the mitochondrial genome of T. liani remains uncharacterized. Here, we present the complete mitochondrial genome of T. liani, comprising 38,000 bp with a GC content of 24.61%. This genome includes 15 core protein-coding genes, 4 independent ORFs, 6 intronic ORFs, 26 tRNAs, and 2 rRNA genes. Phylogenetic analysis using Bayesian inference (BI) revealed the evolutionary relationships among 15 fungi from Eurotiales, strongly supporting distinct clades and indicating that T. liani most closely related to T. pinophilus.

Keywords

Mitochondrial genome
fungi
evolution
phylogeny
the Open Project Program of Panxi Crops Research and Utilization Key Laboratory of Sichuan Province SZKF2209 Innovation and Entrepreneurship of Chengdu University Students CDUCX2024317 This study was supported by the Open Project Program of Panxi Crops Research and Utilization Key Laboratory of Sichuan Province (No. SZKF2209) and Innovation and Entrepreneurship of Chengdu University Students (No. CDUCX2024317).
==== Body
pmc1. Introduction

The fungal species Talaromyces liani, belonging to the Eurotiomycetes class and Trichocomaceae family, has attracted considerable attention in biotechnology for its physiological characteristics and diverse industrial uses [1,2]. This fungus is known for its capacity to produce a wide array of bioactive compounds and enzymes, such as antibiotics, antioxidants, and anti-inflammatories, which display potent biological activities [3,4]. In the pharmaceutical industry, T. liani is being actively investigated as a potential source of new antibiotics and anticancer agents [5,6]. Furthermore, its enzymes are under scrutiny for industrial applications, including biofuel production and waste management [7,8]. Given its distinctive metabolic abilities and strong adaptability, T. liani is a valuable microbial resource [9]. Its potential in various sectors, such as medicine, bioenergy, and environmental remediation, suggests that further research and development on this fungal species could yield significant advancements in biotechnology [9].

Eukaryotes harbor a mitochondrial genome that is essential for governing growth and development, preserving cellular homeostasis, and facilitating responses to environmental cues [10–12]. It has been suggested that the mitochondrial genome serves as a beneficial tool for studying fungal phylogeny [13–16]. The mitochondrial genome characteristics of fungi belonging to the Talaromyces genus have been inadequately elucidated, with only three mitochondrial genomes reported thus far [17–19]. This study presents the first complete mitochondrial genome of T. liani, contributing to a better understanding of the genomic features of this important fungal group.

2. Materials and methods

2.1. Sample collection

A specimen of T. liani was isolated from soil in Chengdu, Sichuan, China (103.67°E, 30.60°N) in 2023. The specimens were identified through morphological analysis and nuclear genome molecular markers (including ITS, elongation factor, and beta-tubulin) according to previous studies [20–22]. The specimens were cataloged at the Culture Collection Center of Chengdu University with voucher number Rmic1. For additional information, please contact Jingwei Huang at huangjingwei@cdu.edu.cn (Figure 1).

Figure 1. The colony morphology (a) and microscopic hyphal morphology (b) of Talaromyces liani. The photo of the species was taken by Jingwei Huang using Camera (Canon EOS 5D mark IV, Canon Inc., Japan) and stereoscope (SZX7, Olympus, Japan).

2.2. Mitochondrial genome assembly and annotation

A fungal DNA extraction kit from Omega Bio-Tek (Norcross, GA, USA) was used for DNA extraction from T. liani, while the NEBNext® Ultra™ II DNA Library Prep Kit (NEB, Beijing, China) was used for sequencing library preparation in accordance with the manufacturer’s instructions. Subsequent whole-genome sequencing was carried out on the Illumina HiSeq 2500 Platform (Illumina, San Diego, CA, USA). To maintain data accuracy, low-quality sequences were filtered out using ngsShoRT [23], and adapter reads were removed with AdapterRemoval v2 [24]. The mitochondrial genome of T. liani was assembled de novo using NOVOPlasty version 4.3.3, employing a k-mer size of 28 [25]. The annotation of the mitochondrial genome was conducted following previously established protocols [26–28], which utilized the MFannot tool (https://megasun.bch.umontreal.ca/apps/mfannot/) [29] and MITOS2 [30]. The NCBI Open Reading Frame Finder enables the anticipation or modification of PCGs or ORFs that surpass 100 amino acids in length [31]. The functions of protein-coding genes (PCGs) or open reading frames (ORFs) were annotated via BLASTP searches against the NCBI nonredundant protein sequence database [32]. The accurate identification of exon and intron boundaries in protein-coding genes was facilitated by the use of exonerate version 2.2 [33]. The presence of tRNA genes in the mitochondrial genome of T. liani was established and validated through the use of tRNAscan-SE v1.3.1 [34]. The PMGmap online web tool, accessible at http://www.1 kmpg.cn/pmgmap, was employed to visualize the structures of intron-containing genes and the graphical representation of the mitochondrial genome [35].

2.3. Phylogenetic analysis

The phylogenetic tree was constructed using previously described methods, commonly employed as an inference technique for mitochondrial genomic phylogeny [36–38]. The alignment of individual mitochondrial genes (excluding intron regions) was carried out using MAFFT v7.037 software [39]. We utilized SequenceMatrix v1.7.8 to merge the aligned mitochondrial genes, resulting in a consolidated mitochondrial dataset [40]. To ascertain potential phylogenetic disparities among various mitochondrial genes, an initial partition homogeneity test was carried out utilizing PAUP v 4.0b10 [41], in line with established literature [42]. PartitionFinder 2.1.1 was employed to determine the optimal partitioning schemes and evolutionary models for the combined mitochondrial dataset [43]. The software MrBayes v3.2.6 was used for the construction of phylogenetic trees via the Bayesian inference method [44]. When conducted BI analysis, two independent runs with four chains (three heated and one cold) each were conducted simultaneously for 2 × 106 generations. Each run was sampled every 1000 generations. We assumed that stationarity had been reached when the estimated sample size (ESS) was greater than 100, and the potential scale reduction factor (PSRF) approached 1.0. The first 25% of samples were discarded as burn-in, and the remaining trees were used to calculate Bayesian posterior probabilities (BPP) in a 50% majority-rule consensus tree.

3. Results

The average depth of the coverage-depth map was 3701.69× (Supplementary Figure 1). The mitochondrial genome of T. liani spans 38,000 bp with a GC content of 24.61%. Gene structures containing introns are illustrated in Supplementary Figure 2. In T. liani, the mitochondrial genome comprises 36.52% adenine, 14.02% guanine, 38.87% thymine, and 10.59% cytosine. Examination of the T. liani mitochondrial genome revealed 25 open-reading frames encompassing 15 core PCGs (cox1, cox2, cox3, atp6, atp8, atp9, cob, nad1, nad2, nad3, nad4, nad4L, nad5, nad6, and rps3), 4 free-standing ORFs, and 6 intronic ORFs (Figure 2). Notably, the functions of proteins encoded by free-standing ORFs remain unknown. The mitochondrial genome of T. liani harbors 10 introns, categorized as 4 Group IB, 2 Group IA, 2 Group I (derived), 1 Group IC2, and 1 Group ID. Some introns contain intronic ORFs encoding LAGLIDADG homing endonucleases or GIY-YIG homing endonucleases. Additionally, the mitochondrial genome of T. liani contains two ribosomal RNA genes, the small subunit (rns) and the large subunit (rnl), and 26 transfer RNA genes. Phylogenetic analysis indicated that T. liani is phylogenetically closest to T. pinophilus, as shown in Figure 3.

Figure 2. The circular mitochondrial genome map of Talaromyces liani. Different color blocks represent different genes. Genes containing introns are labeled. All genes are on the direct strand.

Figure 3. Bayesian inference (BI) tree generated using 14 concatenated mitochondrial protein-coding genes (atp6, atp8, atp9, cob, cox1, cox2, cox3, nad1, nad2, nad3, nad4, nad4L, nad5, and nad6) from Talaromyces liani and 15 other fungal species. Apiotrichum gracile (MZ439918) was used as the outgroup [28]. The accession numbers of the sequences were as follows: Talaromyces pinophilus (CP017352) [17], Talaromyces marneffei (AY347307) [18], Talaromyces stipitatus (JQ354994) [19], Penicillium digitatum (HQ622809) [45], Penicillium polonicum (KU530219) [46], Penicillium solitum (JN696111) [47], Penicillium roqueforti (KR952335), Aspergillus flavus (KP725058), Aspergillus ustus (KM245566) [48], Aspergillus nidulans (JQ435097), Aspergillus Niger (LC670769), Aspergillus tubingensis (DQ217399) [49], Aspergillus oryzae (JQ354998) [19], and Aspergillus fumigatus (JQ346808) [19].

4. Discussion and conclusion

The phylogenetic relationships between species can be better understood by utilizing the mitochondrial genome [50–54]. The lack of a mitochondrial reference genome for T. liani hinders the utilization of mitochondrial genomes for the classification and exploration of the phylogenetic relationships among Eurotiales fungi [54]. In this study, we sequenced the complete mitochondrial genome of a Talaromyces species, revealing a length of 38,000 bp and a GC content of 24.61%. The genome comprised 15 core protein-coding genes (PCGs), 4 independent ORFs, 6 intronic ORFs, 26 tRNAs, and 2 rRNA genes. The rps3 gene was found to be located in the intron region of the rnl gene, which is a Group IA intron. Notably, the mitochondrial genome of T. liani is the largest among the four Talaromyces species [17–19]. Phylogenetic analysis using the BI method placed T. liani closest to T. pinophilus among 15 fungal species from Eurotiales, with robust support for major clades. This research enhances our understanding of Talaromyces species differentiation, mitochondrial evolution, and diversity within this important fungal group.

Supplementary Material

Supplementary figure 2.docx

Disclosure statement

No potential conflict of interest was reported by the author(s).

Author contributions

J H and J-W H planned and designed the research. J-W H collected the materials, J H performed the experiments, and H-J Q and Y-Q Y analyzed the data and review the manuscript. J H and J-W H wrote the manuscript.

Ethics statement

The study did not involve humans or animals. In this study, samples were collected without ethical approval or permission.

Data availability statement

The genome sequence data that support the findings of this study are openly available in the NCBI GenBank at https://www.ncbi.nlm.nih.gov/under accession no. PP626204. The associated BioProject, SRA, and Bio-Sample numbers are PRJNA1098444, SRR28606097 and SAMN40907818, respectively.
==== Refs
References

1 Christiansen JV, Isbrandt T, Petersen C, Sondergaard TE, Nielsen MR, Pedersen TB, Sørensen JL, Larsen TO, Frisvad JC. 2021. Fungal quinones: diversity, producers, and applications of quinones from Aspergillus, Penicillium, Talaromyces, Fusarium, and Arthrinium. Appl Microbiol Biotechnol. 105 (21–22 ):8157–8193. doi:10.1007/s00253-021-11597-0.34625822
2 Méndez-Líter JA, de Eugenio LI, Nieto-Domínguez M, Prieto A, Martínez MJ. 2021. Hemicellulases from Penicillium and Talaromyces for lignocellulosic biomass valorization: a review. Bioresour Technol. 324 :124623. doi:10.1016/j.biortech.2020.124623.33434871
3 Nicoletti R, Bellavita R, Falanga A. 2023. The outstanding chemodiversity of marine-derived talaromyces. Biomolecules. 13 (7 ):1021. doi:10.3390/biom13071021.37509057
4 Nicoletti R, Salvatore MM, Andolfi A. 2018. Secondary metabolites of mangrove-associated strains of talaromyces. Mar Drugs. 16 (1 ):12. doi:10.3390/md16010012.29316607
5 Nicoletti R, Trincone A. 2016. Bioactive Compounds Produced by Strains of Penicillium and Talaromyces of Marine Origin. Mar Drugs. 14 (2 ):37. doi:10.3390/md14020037.26901206
6 Yuan WH, Teng MT, Sun SS, Ma L, Yuan B, Ren Q, Zhang P. 2018. Active metabolites from endolichenic fungus Talaromyces sp. Chem Biodivers. 15 (11 ):e1800371. doi:10.1002/cbdv.201800371.30198640
7 Zhang D, Wang X, Liu B, Li S, Wang Y, Guo T, Sun Y. 2023. New dipyrroloquinones from a plant-derived endophytic fungus Talaromyces sp. Molecules. 28 (23 ):7847. doi:10.3390/molecules28237847.38067576
8 Lan D, Wu B. 2020. Chemistry and bioactivities of secondary metabolites from the genus talaromyces. Chem Biodivers. 17 (8 ):e2000229. doi:10.1002/cbdv.202000229.32432837
9 Morales-Oyervides L, Ruiz-Sánchez JP, Oliveira JC, Sousa-Gallagher MJ, Méndez-Zavala A, Giuffrida D, Dufossé L, Montañez J. 2020. Biotechnological approaches for the production of natural colorants by Talaromyces/Penicillium: a review. Biotechnol Adv. 43 :107601. doi:10.1016/j.biotechadv.2020.107601.32682871
10 Murphy MP. 2009. How mitochondria produce reactive oxygen species. Biochem J. 417 (1 ):1–13. doi:10.1042/BJ20081386.19061483
11 Ernster L, Schatz G. 1981. Mitochondria: a historical review. J Cell Biol. 91 (3 Pt 2 ):227s–255s. doi:10.1083/jcb.91.3.227s.7033239
12 McBride HM, Neuspiel M, Wasiak S. 2006. Mitochondria: more than just a powerhouse. Curr Biol. 16 (14 ):R551–560. doi:10.1016/j.cub.2006.06.054.16860735
13 Li Q, Bao Z, Tang K, Feng H, Tu W, Li L, Han Y, Cao M, Zhao C. 2022. First two mitochondrial genomes for the order Filobasidiales reveal novel gene rearrangements and intron dynamics of Tremellomycetes. IMA Fungus. 13 (1 ):7. doi:10.1186/s43008-022-00094-2.35501936
14 Li Q, Li L, Zhang T, Xiang P, Wu Q, Tu W, Bao Z, Zou L, Chen C. 2022. The first two mitochondrial genomes for the genus Ramaria reveal mitochondrial genome evolution of Ramaria and phylogeny of Basidiomycota. IMA Fungus. 13 (1 ):16. doi:10.1186/s43008-022-00100-7.36100951
15 Li Q, Luo Y, Sha A, Xiao W, Xiong Z, Chen X, He J, Peng L, Zou L. 2023. Analysis of synonymous codon usage patterns in mitochondrial genomes of nine Amanita species. Front Microbiol. 14 :1134228. doi:10.3389/fmicb.2023.1134228.36970689
16 Xu JP, Wang PF. 2015. Mitochondrial inheritance in basidiomycete fungi. Fungal Biol Rev. 29 (3-4 ):209–219. doi:10.1016/j.fbr.2015.02.001.
17 Li CX, Zhao S, Zhang T, Xian L, Liao LS, Liu JL, Feng JX. 2017. Genome sequencing and analysis of Talaromyces pinophilus provide insights into biotechnological applications. Sci Rep. 7 (1 ):490. doi:10.1038/s41598-017-00567-0.28352091
18 Woo PC, Zhen H, Cai JJ, Yu J, Lau SK, Wang J, Teng JL, Wong SS, Tse RH, Chen R, et al. 2003. The mitochondrial genome of the thermal dimorphic fungus Penicillium marneffei is more closely related to those of molds than yeasts. FEBS Lett. 555 (3 ):469–477. doi:10.1016/s0014-5793(03)01307-3.14675758
19 Joardar V, Abrams NF, Hostetler J, Paukstelis PJ, Pakala S, Pakala SB, Zafar N, Abolude OO, Payne G, Andrianopoulos A, et al. 2012. Sequencing of mitochondrial genomes of nine Aspergillus and Penicillium species identifies mobile introns and accessory genes as main sources of genome size variability. BMC Genomics. 13 (1 ):698. doi:10.1186/1471-2164-13-698.23234273
20 Peterson SW, Jurjević Ž. 2019. The Talaromyces pinophilus species complex. Fungal Biol. 123 (10 ):745–762. doi:10.1016/j.funbio.2019.06.007.31542192
21 Sun BD, Chen AJ, Houbraken J, Frisvad JC, Wu WP, Wei HL, Zhou YG, Jiang XZ, Samson RA. 2020. New section and species in Talaromyces. MycoKeys. 68 :75–113. doi:10.3897/mycokeys.68.52092.32733145
22 Wang XC, Zhuang WY. 2022. New species of Talaromyces (Trichocomaceae, Eurotiales) from Southwestern China. J Fungi (Basel). 8 :647. doi:10.3390/jof8070647.
23 Chen C, Khaleel SS, Huang H, Wu CH. 2014. Software for pre-processing Illumina next-generation sequencing short read sequences. Source Code Biol Med. 9 (1 ):8. doi:10.1186/1751-0473-9-8.24955109
24 Schubert M, Lindgreen S, Orlando L. 2016. AdapterRemoval v2: rapid adapter trimming, identification, and read merging. BMC Res Notes. 9 (1 ):88. doi:10.1186/s13104-016-1900-2.26868221
25 Dierckxsens N, Mardulyn P, Smits G. 2017. NOVOPlasty: de novo assembly of organelle genomes from whole genome data. Nucleic Acids Res. 45 (4 ):e18. doi:10.1093/nar/gkw955.28204566
26 Li Q, Ren Y, Xiang D, Shi X, Zhao J, Peng L, Zhao G. 2020. Comparative mitogenome analysis of two ectomycorrhizal fungi (Paxillus) reveals gene rearrangement, intron dynamics, and phylogeny of basidiomycetes. IMA Fungus. 11 (1 ):12. doi:10.1186/s43008-020-00038-8.32670777
27 Li Q, Ren Y, Shi X, Peng L, Zhao J, Song Y, Zhao G. 2019. Comparative mitochondrial genome analysis of two ectomycorrhizal fungi (Rhizopogon) reveals dynamic changes of intron and phylogenetic relationships of the subphylum Agaricomycotina. Int J Mol Sci. 20 (20 ):5167. doi:10.3390/ijms20205167.31635252
28 Li Q, Xiao W, Wu P, Zhang T, Xiang P, Wu Q, Zou L, Gui M. 2023. The first two mitochondrial genomes from Apiotrichum reveal mitochondrial evolution and different taxonomic assignment of Trichosporonales. IMA Fungus. 14 (1 ):7. doi:10.1186/s43008-023-00112-x.37004131
29 Valach M, Burger G, Gray MW, Lang BF. 2014. Widespread occurrence of organelle genome-encoded 5S rRNAs including permuted molecules. Nucleic Acids Res. 42 (22 ):13764–13777. doi:10.1093/nar/gku1266.25429974
30 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. doi:10.1016/j.ympev.2012.08.023.22982435
31 N.R. Coordinators. 2017. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 45:D12–D17. doi:10.1093/nar/gkw1071.
32 Bleasby AJ, Wootton JC. 1990. Construction of validated, non-redundant composite protein sequence databases. Protein Eng. 3 (3 ):153–159. doi:10.1093/protein/3.3.153.2330366
33 Slater GS, Birney E. 2005. Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics. 6 (1 ):31. doi:10.1186/1471-2105-6-31.15713233
34 Lowe TM, Chan PP. 2016. tRNAscan-SE On-line: integrating search and context for analysis of transfer RNA genes. Nucleic Acids Res. 44 (W1 ):W54–57. doi:10.1093/nar/gkw413.27174935
35 Zhang X, Chen H, Ni Y, Wu B, Li J, Burzyński A, Liu C. 2024. Plant mitochondrial genome map (PMGmap): a software tool for the comprehensive visualization of coding, noncoding and genome features of plant mitochondrial genomes. Mol Ecol Resour. 24 (5 ):e13952.38523350
36 Li Q, He X, Ren Y, Xiong C, Jin X, Peng L, Huang W. 2020. Comparative mitogenome analysis reveals mitochondrial genome differentiation in ectomycorrhizal and asymbiotic amanita species. Front Microbiol. 11 :1382. doi:10.3389/fmicb.2020.01382.32636830
37 Li Q, Wu P, Li L, Feng H, Tu W, Bao Z, Xiong C, Gui M, Huang W. 2021. The first eleven mitochondrial genomes from the ectomycorrhizal fungal genus (Boletus) reveal intron loss and gene rearrangement. Int J Biol Macromol. 172 :560–572. doi:10.1016/j.ijbiomac.2021.01.087.33476615
38 Li Q, Zhang T, Li L, Bao Z, Tu W, Xiang P, Wu Q, Li P, Cao M, Huang W. 2022. Comparative mitogenomic analysis reveals intraspecific, interspecific variations and genetic diversity of medical fungus Ganoderma. J Fungi (Basel). 8 (8 ):781. doi:10.3390/jof8080781.
39 Katoh K, Rozewicki J, Yamada KD. 2019. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform. 20 (4 ):1160–1166. doi:10.1093/bib/bbx108.28968734
40 Vaidya G, Lohman DL, Meier R. 2011. SequenceMatrix: concatenation software for the fast assembly of multi‐gene datasets with character set and codon information. Cladistics. 27 (2 ):171–180. doi:10.1111/j.1096-0031.2010.00329.x.34875773
41 Swofford D. 2002. PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4.0b10. 4 ed. Sunderland, Massachusetts: Sinauer Associates. doi:10.1111/j.0014-3820.2002.tb00191.x.
42 Xiang XG, Schuiteman A, Li DZ, Huang WC, Chung SW, Li JW, Zhou HL, Jin WT, Lai YJ, Li ZY, et al. 2013. Molecular systematics of Dendrobium (Orchidaceae, Dendrobieae) from mainland Asia based on plastid and nuclear sequences. Mol Phylogenet Evol. 69 (3 ):950–960. doi:10.1016/j.ympev.2013.06.009.23811435
43 Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B. 2017. PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol Biol Evol. 34 (3 ):772–773. doi:10.1093/molbev/msw260.28013191
44 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. doi:10.1093/sysbio/sys029.22357727
45 Sun X, Li H, Yu D. 2011. Complete mitochondrial genome sequence of the phytopathogenic fungus Penicillium digitatum and comparative analysis of closely related species. FEMS Microbiol Lett. 323 (1 ):29–34. doi:10.1111/j.1574-6968.2011.02358.x.22092677
46 Kang X, Liu C, Liu D, Zeng L, Shi Q, Qian K, Xie B. 2016. The complete mitochondrial genome of huperzine A-producing endophytic fungus Penicillium polonicum. Mitochondrial DNA B Resour. 1 (1 ):202–203. doi:10.1080/23802359.2016.1155086.33644344
47 Eldarov MA, Mardanov AV, Beletsky AV, Dzhavakhiya VV, Ravin NV, Skryabin KG. 2012. Complete mitochondrial genome of compactin-producing fungus Penicillium solitum and comparative analysis of Trichocomaceae mitochondrial genomes. FEMS Microbiol Lett. 329 (1 ):9–17. doi:10.1111/j.1574-6968.2012.02497.x.22239643
48 Ruan Z, Dai F, Fang X, Chen H, Yu D. 2016. The complete mitochondrial genome of a rare human pathogen, Aspergillus ustus. Mitochond DNA A DNA Mapp Seq Anal. 27 (6 ):3876–3877. doi:10.3109/19401736.2014.987241.
49 Juhász A, Engi H, Pfeiffer I, Kucsera J, Vágvölgyi C, Hamari Z. 2007. Interpretation of mtDNA RFLP variability among Aspergillus tubingensis isolates. Antonie Van Leeuwenhoek. 91 (3 ):209–216. doi:10.1007/s10482-006-9110-x.17043909
50 Gao W, Chen X, He J, Sha A, Luo Y, Xiao W, Xiong Z, Li Q. 2024. Intraspecific and interspecific variations in the synonymous codon usage in mitochondrial genomes of 8 pleurotus strains. BMC Genomics. 25 (1 ):456. doi:10.1186/s12864-024-10374-3.
51 Zhang Y, Yang G, Fang M, Deng C, Zhang KQ, Yu Z, Xu J. 2020. Comparative analyses of mitochondrial genomes provide evolutionary insights into nematode-trapping fungi. Front Microbiol. 11 :617. doi:10.3389/fmicb.2020.00617.32351475
52 Zhang YJ, Fan XP, Li JN, Zhang S. 2023. Mitochondrial genome of Cordyceps blackwelliae: organization, transcription, and evolutionary insights into Cordyceps. IMA Fungus. 14 (1 ):13. doi:10.1186/s43008-023-00118-5.37415259
53 Ren LY, Zhang S, Zhang YJ. 2021. Comparative mitogenomics of fungal species in Stachybotryaceae provides evolutionary insights into hypocreales. Int J Mol Sci. 22 (24 ):13341. doi:10.3390/ijms222413341.34948138
54 Zhang S, Wang S, Fang Z, Lang BF, Zhang YJ. 2022. Characterization of the mitogenome of Gongronella sp. w5 reveals substantial variation in Mucoromycota. Appl Microbiol Biotechnol. 106 (7 ):2587–2601. doi:10.1007/s00253-022-11880-8.35318523
55 Caramalho R, Madl L, Rosam K, Rambach G, Speth C, Pallua J, Larentis T, Araujo R, Alastruey-Izquierdo A, Lass-Flörl C, et al. 2019. Evaluation of a novel mitochondrial Pan-Mucorales marker for the detection, identification, quantification, and growth stage determination of mucormycetes. J Fungi (Basel). 5 (4 ):98. doi:10.3390/jof5040098.31614610
