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. 2025 Sep 13;10(10):942–947. doi: 10.1080/23802359.2025.2559718

Characterization and phylogenetic analysis of the mitochondrial genomes of four Xanthoparmelia (Vain.) Hale lichen fungi

Jinsiguli Bahenuer 1, Anwar Tumur 1,✉, Muhammad Shahid Iqbal 1
PMCID: PMC12434865  PMID: 40959691

Abstract

In this study, the complete mitochondrial genomes of four Xanthoparmelia species (X. chlorochroa, X. coreana, X. pulvinaris, and X. stenophylla) were sequenced, assembled and annotated. The four mitochondrial genomes are all composed of circular DNA molecules, with a total length ranging from 81,294 bp to 88,296 bp, containing 41–42 genes (14 protein-coding genes (PCGs), 2 rRNA genes, and 25–26 tRNA genes), the GC content is 30%–30.7% and the AT skew is positive. Phylogenetic analysis based on 14 PCGs and rRNA genes revealed that the four Xanthoparmelia species form a well-supported clade within Parmeliaceae.

Keywords: Comparative analysis, mitochondrial genome, phylogenetic analysis, xanthoparmelia

1. Introduction

The genus Xanthoparmelia(Vain.) Hale, belongs to the Kingdom Fungi, Phylum Ascomycota, Class Lecanoromycetes, Order Lecanorales, Family Parmeliaceae. This genus is the most species rich genus in the lichen family Parmeliaceae. Currently, among the known lichen forming fungi, only two genera are hyper diverse (with more than 500 species) (Lücking et al. 2017), and Xanthoparmelia is one of them, with over 800 described species (Lücking et al. 2017). According to Indexfungorum.com, Xanthoparmelia is currently represented by 888 species worldwide (https://www.indexfungorum.org/names/Names.asp?pg=2025). It is widely distributed around the world, with two main centers of diversity: Australia and the Cape region of South Africa (Leavitt et al. 2018). It is mainly distributed on siliceous rocks or soils in arid and semi-arid regions, characterized by dry conditions and abundant sunlight (Autumn et al. 2020). The mitochondrial genome data of Xanthoparmelia are far less abundant than nuclear genome data (https://www. ncbi. nlm.nih.gov/nuccore). Therefore, there are still some gaps in the phylogeny and comparative genomics of Xanthoparmelia. This genus shows rich morphological and ecological diversity in nature. However, evidence based on morphological and chemical characteristics is not sufficient to accurately reflect species diversity or species delimitation and may distort the diversity of lichen - forming fungi. Especially in closely related species with very similar morphologies, the combination of molecular data (single-locus or multi-locus concatenation) can classify species more accurately. This has also been widely applied in the taxonomic and phylogenetic studies of lichen - forming and non - lichen - forming fungi (Leavitt et al. 2018; Kondratyuk et al. 2019; Zhao et al. 2023).

In this study, the complete mitochondrial genomes of four Xanthoparmelia species, Xanthoparmelia chlorochroa (Tuck.) Hale, 1974, Xanthoparmelia coreana (Gyeln.) Hale, 1988, Xanthoparmelia pulvinaris (Gyeln.) Ahti & D. Hawksw, 2008 and Xanthoparmelia stenophylla (Ach.) Ahti & D. Hawksw, 2005, collected from Xinjiang, were sequenced, assembled and annotation. Finally, a phylogenetic tree based on protein - coding genes and rRNA genes was constructed to reveal the role of protein coding genes and rRNA genes in the mitochondrial genomes in determining the phylogenetic relationships of this genus.

2. Materials and methods

2.1. Sample collection and DNA extraction

The specimens of four species of the genus Xanthoparmelia (X. chlorochroa, X. coreana, X. pulvinaris, X. stenophylla) used in this study were collected from Zhaobishan Township, Mulei County, Hui Autonomous Perfecture of Changji; Aktuyuk, Barluk Mountain National Nature Reserve, Tacheng Prefecture; Binghu, Dabancheng District, Urumqi and Yumin Tasite, Barluk Mountain National Nature Reserve, Tacheng Prefecture, Xinjiang, China respectively (Figure 1, see Supplementary Table S1). The four species of the genus Xanthoparmelia were identified through morphological- anatomical methods, color test(CT) and rDNA ITS sequences, PCR amplification with ITS 1 F and ITS 4 as primers (Table S2). Voucher specimens were deposited at the College of Life Science and Technology, Xinjiang University (Contact person: Anwar Tumur; Email: awartumursk@xju.edu.cn), with the voucher numbers 20240731001, 20240626002, 20240704003, 20240625004. Genomic DNA was extracted using a Magbead Tissue DNA Kit (Kangwei Century Biotechnology, Jiangsu, China) according to the manufacturer’s instructions (Figure S1).

Figure 1.

Figure 1.

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Morphological images of xanthoparmelia. (A) X. chlorochroa; (B) X. coreana; (C) X. stenophylla; (D) X. pulvinaris. The photos were taken by Jinsiguli Bahenuer.

2.2. Mitochondrial genome sequencing, assembly, and annotation

The whole-genome sequencing of the lichen-forming fungi of the genus Xanthoparmelia was carried out using the second-generation DNB-SEQ sequencing platform (Shenzhen Huitong Biotechnology Co., Ltd.). GetOrganelle v1.7.5 (Jin et al. 2020) was used to extract and de novo assemble the mitochondrial genome from the whole-genome dataset, and NOVOPlasty v4.2 (Dierckxsens et al. 2017) was used to verify the assembled mitochondrial genome of the genus Xanthoparmelia. The complete mitogenomes of Xanthoparmelia were annotated using MITOS (http://mitos.bioinf. uni-leipzig.de/index.py) based on the mitochondrial genetic code 4, and Geseq (Tillich et al. 2017). Based on the previously reported method (Zhang and Zhang 2019), the introns of protein-coding genes in the four mitochondrial genomes were classified into different positional classes (Pcl). Graphical maps of the four Xanthoparmelia mitogenomes were drawn using OGDraw v1.2 (Lohse et al. 2007).

2.3. Mitochondrial genome analysis, and phylogenetic studies

Geneious v2025.0.3 (https://www.geneious.com) was used to statistically analyze the characteristic information of the mitochondrial genome. DNASTAR Lasergene v7.1 (https://www. dnastar.com/software/lasergene/) was used to analyze the base composition of the mitochondrial genome of the genus Xanthoparmelia. According to the following formulas: AT skew = [A − T]/[A + T], GC skew = [G − C]/[G + C], the asymmetric deviation of nucleotide composition was evaluated.

The mitochondrial genomes of 12 species of the family Parmeliaceae with reliable annotations obtained from GenBank were used for phylogenetic comparative analysis (Table S3). Firstly, the common genes were extracted through PhyloSuite v1.2.3 (Zhang et al. 2020), and MAFFT (Katoh et al. 2019) was used to separately align the common protein-coding genes of the mitochondrial genome and the two rRNA genes. Secondly, MACSE (Ranwez et al. 2011) was used to optimize the sequences of the protein-coding genes, followed by sequence trimming with Gblocks (Talavera and Castresana 2007), and RNA sequence trimming with trimAI (Capella-Gutiérrez et al. 2009). Finally, the protein-coding genes and rRNA sequences were concatenated in PhyloSuite. ModelFinder (Kalyaanamoorthy et al. 2017) was used to select the most suitable evolutionary model for the combined gene alignment. Under the Edege-linked partitioning model, IQ-tree V1.6.8 (Nguyen et al. 2015) was used for maximum likelihood (ML) analysis, and the best model for ML analysis was GTR+F + I + G4. MrBayes v.3.2.7 (Ronquist and Huelsenbeck 2003) software was used for Bayesian analysis, and the best model for Bayesian analysis (Bayesian information, BI) was GTR+I + G. 25% of the running results were discarded (burnin = 0.25), and 500,000,000 generations were run. The web-based iTOL tool (https://itol.embl.de/) was used to edit and visualize the BI and ML phylogenetic trees.

3. Results

3.1. Structural characteristics of the mitochondrial genome

The analysis showed that the complete mitochondrial genomes of the fungi of the four lichen species of the genus Xanthoparmelia namely X. chlorochroa (GenBank accession: PV243434); X. coreana (GenBank accession: PV243431); X. stenophylla (GenBank accession: PV243432); and X. pulvinaris (GenBank accession: PV243433), were all composed of circular DNA molecules, with sizes ranging from 81,294 bp to 88,296 bp. The mitochondrial genome of X. chlorochroa was the largest (88,296 bp), and that of X. coreana was the smallest (81,294 bp) (Figure 2). There were 41–42 genes in the mitochondrial genomes of the four species of the genus Xanthoparmelia, including 14 protein-coding genes (PCGs), 2 ribosomal RNA genes (rRNA), and 25–26 transfer RNA genes (tRNA). Among the 14 PCGs, they included 7 subunits of the electron transport chain complex I (nad1, nad2, nad3, nad4, nad4L, nad5, and nad6), 3 cytochrome c oxidase genes (cox1, cox2, cox3), 2 ATP synthase genes (atp6, atp8), 1 cytochrome b (cob), and 1 ribosomal protein subunit 3 (rps3). The 57 introns detected in the four mitochondrial genomes were classified into 17 Pcls (Table S4). The variation in intron types and numbers among the four species suggests intron gain or loss events. The average GC contents of these four mitochondrial genomes were very close, with the GC content ranging from 30% to 30.7%. Among them, the GC content of X. pulvinaris was the lowest, indicating that the base composition had the most significant AT preference. Evidence from earlier studies indicates a critical role of base composition bias in mitochondrial genome replication and transcription (Satoh et al. 2016). All four mitochondrial genomes showed a negative AT skew, with the skew values ranging from approximately −0.007 to −0.013; the GC contents all showed a positive skew, with the skew values ranging from approximately 0.057 to 0.062 (Table S5). It is possible that the observed strand-specific nucleotide asymmetry in Xanthoparmelia impacts mitochondrial genome replication and transcription.

Figure 2.

Figure 2.

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Maps of the four newly sequenced mitochondrial genomes of the species of the genus Xanthoparmelia. The genes are represented by blocks of different colors, as shown in the legend below the figure. The colored blocks outside each circle indicate that the genes are located on the positive strand, while the colored blocks inside the circle indicate that the genes are located on the reverse strand.

3.2. Phylogenetic analysis

Based on the concatenated sequences of core PCGs and two rRNAs, using Bayesian Inference (BI) and Maximum Likelihood (ML) methods, a phylogenetic tree of four species of the genus Xanthoparmelia was constructed based on the core PCGs and two rRNA genes of 11 species in the family Parmeliaceae from the NCBI database (https://www.ncbi.nlm.nih.gov/genbank/). The phylogenetic results of the family Parmeliaceae based on mitochondrial genes showed that all branches were well-supported (Figure 3).

Figure 3.

Figure 3.

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Phylogeny of four species of the genus xanthoparmelia using maximum likelihood (ML) and Bayesian inference (BI) methods based on 14 core PCGs and two rRNAs, with cladonia stipitata Lendemer & Hodkinson, 2009 as the outgroup. The numbers at the nodes represent the bootstrap values (left) and Bayesian posterior probabilities (right). Gen-Bank accession numbers (https://www.ncbi.nlm.nih.gov/genbank/) of all sequences have displayed in the figure with their corresponding names: Alectoria fallacina motyka, 1960 (MG711470) (Pogoda et al. 2018); bryoria tenuis (E.Dahl) Brodo & D. Hawksw, 1977 (NC_034786) (no published in papers); cladonia stipitata (MG851822.1) (Brigham et al. 2018); hypogymnia vittata (ach.) parrique, 1898 (NC_035730) (no published in papers); imshaugia aleurites (ach.) S.L.F.Mey, 1985 (NC_035550)(no published in papers); parmotrema ultralucens (krog) Hale, 1974(NC_040007) (no published in papers); pseudevernia consocians (vain.) hale & W.L. Culb, 1966 (NC_039163) (no published in papers); usnea ceratina ach, 1810 (KX987159) (Funk et al. 2018); U. mutabilis stirt, 1881 (NC_039633) (Funk et al. 2018); U. pennsylvanica motyka, 1937 (KY321923) (no published in papers); U. subgracilis vain, 1915 (MG720066); U. subfusca stirt, 1881 (MG720812) (Funk et al. 2018); xanthoparmelia coreana (PV243431) (this study); X. chlorochroa (PV243434) (this study); X.pulvinaris (PV243433) (this study); X.stenophylla (PV243432) (this study).

Cladonia stipitata served as the outgroup and was located in the outermost branch. The genus Xanthoparmelia was closely related to the genus Parmotrema A. Massal, forming a large branch. Among the separate branch clusters of the genus Xanthoparmelia, X. pulvinaris and X. stenophylla clustered together with a high support rate (100%) and posterior probability (1.00), indicating that these two species have a closer genetic relationship or may suggest originate from the same ancestor. In addition, the branch of X. coreana was closer to the terminal node, suggesting that it was differentiated earlier within the genus Xanthoparmelia, followed by X. chlorochroa. In the results of this phylogenetic analysis, all species clustered closely with high support rates and posterior probabilities, indicating that mitochondrial protein-coding genes and rRNA genes are excellent materials for phylogenetic studies.

4. Discussion

The mitochondrial genomes of fungi are among the mitochondrial genomes with the greatest length variation and the most complex structures in eukaryotes (Salavirta et al. 2014; Medina et al. 2020). Studies have found that factors such as the size and variation of the fungal mitochondrial genome are mainly related to the intergenic regions and intron regions (Zhang et al. 2015; Fonseca et al. 2021). In this study, the mitochondrial genome of X. chlorochroa was the largest (88,296 bp), and that of X. coreana was the smallest (81,294 bp). The largest mitochondrial genome contained 15 introns, with a length of 24,149 bp, accounting for 28.5% of the entire mitochondrial genome. In contrast, the smallest mitochondrial genome contained 11 introns, with a length of 16,056 bp, accounting for 19.75% of the entire mitochondrial genome. The intron region was the shortest, being 16,056 (19.75%), and the intergenic region was the longest, being 47,361 (58.26%). Therefore, the expansion of the intergenic region may be a factor promoting the expansion of the size of the mitochondrial genome of the genus Xanthoparmelia.

Changes in the size and complexity of nuclear and organelle genomes are typical signs of mutualistic symbiotic relationships (Song et al. 2022). These phenomena occur especially through the loss of protein-coding genes (Andersson and Andersson 1999; Nikoh et al. 2014). The mitochondrial genome of the genus Xanthoparmelia obtained in this study contains 14 protein-coding genes, which is different from most fungal mitochondrial genomes in that it lacks the atp9 gene. This may be because symbiosis between co-evolved taxonomic groups is usually marked by genome reduction as a means to reduce redundancy or intergenomic conflicts. The research results also confirm the early findings (Pogoda et al. 2018). The loss of the key energy-related gene atp9 by the members of the family Parmeliaceae provides genomic evidence for the specificity of this symbiotic relationship (Pogoda et al. 2018). This study provides new resources for further research on the evolution of lichen mitochondrial genomes and the co-evolution with specific symbiotic partners.

In this study, a completely identical and well-supported phylogenetic tree was obtained based on the 14 shared PCGs and 2 rRNA genes. This study provides important insights into potential reliable molecular markers that can be used to reconstruct the phylogenetic tree of fungi, promotes the understanding of the phylogeny and evolution of fungi, and provides a new perspective for future research in genetics, systematics, genomics, and evolution.

Supplementary Material

Table S.xlsx
TMDN_A_2559718_SM3437.xlsx (17KB, xlsx)

Acknowledgments

We are thanks to Dolathan Toksun and Yong Hai Ying (graduate students of Xinjiang University, P.R China) for their help with the field work. Prof. David H.S Richardson (Saint Mary’s University, Canada) for the editorial help and valuable comments.

Funding Statement

This work was supported by the National Nature Science Foundation of China [Grant No.32160046].

Ethic declarations

This research did not involve studies on humans or animals. The sample collection for this study was conducted in accordance with the guidelines of the national guidelines.

Author’s contributions

CRediT: Jinsiguli Bahenuer: Investigation, Methodology, Writing- original draft; Anwar Tumur: Formal analysis, Project administration, Supervision, Writing – review & editing; Muhammad Shahid Iqbal: Formal analysis, Writing – review & editing.

Data availability statement

The genome sequence data that support the findings of this study are openly available in the GenBank of NCBI at (https://www.ncbi.nlm.nih.gov) under the accession number are PV243434、PV243431、PV243432 and PV243433. The associated BioProject, Bio-Sample, and SRA numbers are PRJNA1262737, SAMN48510631, SRR33579995 for X. chlorochroa; PRJNA1263169, SAMN48514701, SRR33609190 for X.coreana; PRJNA1263171, SAMN48514716, SRR33612616 for X. stenophylla and PRJNA1263173, SAMN48514735, SRR33613162 for X.pulvinaris.

Disclosure statement

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

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Table S.xlsx
TMDN_A_2559718_SM3437.xlsx (17KB, xlsx)

Data Availability Statement

The genome sequence data that support the findings of this study are openly available in the GenBank of NCBI at (https://www.ncbi.nlm.nih.gov) under the accession number are PV243434、PV243431、PV243432 and PV243433. The associated BioProject, Bio-Sample, and SRA numbers are PRJNA1262737, SAMN48510631, SRR33579995 for X. chlorochroa; PRJNA1263169, SAMN48514701, SRR33609190 for X.coreana; PRJNA1263171, SAMN48514716, SRR33612616 for X. stenophylla and PRJNA1263173, SAMN48514735, SRR33613162 for X.pulvinaris.

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