Genome streamlining via complete loss of introns has occurred multiple times in lichenized fungal mitochondria

Pogoda, Cloe S.; Keepers, Kyle G.; Nadiadi, Arif Y; Bailey, Dustin W; Lendemer, James C.; Tripp, Erin A.; Kane, Nolan C.

doi:10.1002/ece3.5056

Cited by 29 publications

(29 citation statements)

References 102 publications

(148 reference statements)

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“…2 and 3), the evolutionary history of the mitochondrial genome appears to be more complex in this group. As has been demonstrated in other studies, mitochondrial genome evolution in fungi is complex 103,104 . Mitochondrial genome evolution in the R. melanophthalma species complex also appears to be affected by dynamic evolutionary processes, with different phylogenetic relationships inferred from different portions of the mitochondrial genome ( Supplementary Fig.…”

Section: Discussionsupporting

confidence: 78%

Genome-scale data reveal the role of hybridization in lichen-forming fungi

Keuler

Garretson

Saunders

et al. 2020

Sci Rep

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Advancements in molecular genetics have revealed that hybridization may be common among plants, animals, and fungi, playing a role in evolutionary dynamics and speciation. While hybridization has been well-documented in pathogenic fungi, the effects of these processes on speciation in fungal lineages with different life histories and ecological niches are largely unexplored. Here we investigated the potential influence of hybridization on the emergence of morphologically and reproductively distinct asexual lichens. We focused on vagrant forms (growing obligately unattached to substrates) within a clade of rock-dwelling, sexually reproducing species in the Rhizoplaca melanophthalma (Lecanoraceae, Ascomycota) species complex. We used phylogenomic data from both mitochondrial and nuclear genomes to infer evolutionary relationships and potential patterns of introgression. We observed multiple instances of discordance between the mitochondrial and nuclear trees, including the clade comprising the asexual vagrant species R. arbuscula, R. haydenii, R. idahoensis, and a closely related rock-dwelling lineage. Despite well-supported phylogenies, we recovered strong evidence of a reticulated evolutionary history using a network approach that incorporates both incomplete lineage sorting and hybridization. these data suggest that the rock-dwelling western north American subalpine endemic R. shushanii is potentially the result of a hybrid speciation event, and introgression may have also played a role in other taxa, including vagrant species R. arbuscula, R. haydenii and R. idahoensis. We discuss the potential roles of hybridization in terms of generating asexuality and novel morphological traits in lichens. furthermore, our results highlight the need for additional study of reticulate phylogenies when investigating species boundaries and evolutionary history, even in cases with wellsupported topologies inferred from genome-scale data. open Scientific RepoRtS | (2020) 10:1497 | https://doi.org/10.1038/s41598-020-58279-x www.nature.com/scientificreports www.nature.com/scientificreports/ nuclear markers, which in turn can influence the genome in both adaptive and maladaptive ways 5,[19][20][21][22] . Adaptive introgression of mitochondrial DNA may play an important role in speciation and phylogeography 23,24 .While hybridization has been well-documented among pathogenic fungi 21,[25][26][27][28][29][30] , the role of hybridization on the process of speciation of fungal lineages with different life histories and ecological functions is not well understood, including among lichen-forming fungi. The role of gene flow and hybridization in lichen-forming fungal evolution has been a long-standing question [31][32][33][34][35] . Species boundaries in fungi, including symbiotic fungi such as lichen formers, have received substantial attention and become more robust with molecular sequence data 36 . However, processes involved in speciation in lichen-forming fungi have received far less attention. With a poor fossil record 37,38 and pote...

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Section: Discussionsupporting

confidence: 78%

Genome-scale data reveal the role of hybridization in lichen-forming fungi

Keuler

Garretson

Saunders

et al. 2020

Sci Rep

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“…Less common in fungi, group II introns usually contain reverse transcriptases. Homing endonucleases and transcriptases are selfish because they pose no obvious value to their host genomes [174,[184][185][186][187].…”

Section: Mitogenome Characteristics Of Fungi and Oomycetesmentioning

confidence: 99%

“…Fungi exhibit remarkable variation in intron content [187], which can also be observed in plant pathogens. The Fusarium proliferatum mitogenome, for example, contains only a single intron [188], which is in contrast to R. solani which contains dozens of introns [179].…”

Section: Mitogenome Characteristics Of Fungi and Oomycetesmentioning

confidence: 99%

“…In addition, at the population or even strain level, these fungi can differ in intron content [189,190]. However, the same introns may also be found in evolutionarily distant lineages and their widespread distribution in fungi may be due to the intron-rich progenitor from which extensive intron loss has occurred [187,189]. In addition to intron loss, the infective nature of HEGs is believed to cause the observed variation in the intron content between different lineages.…”

Section: Mitogenome Characteristics Of Fungi and Oomycetesmentioning

confidence: 99%

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Promising Perspectives for Detection, Identification, and Quantification of Plant Pathogenic Fungi and Oomycetes through Targeting Mitochondrial DNA

Kulik

Bilska

Żelechowski

2020

IJMS

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Fungi and oomycetes encompass many pathogens affecting crops worldwide. Their effective control requires screening pathogens across the local and international trade networks along with the monitoring of pathogen inocula in the field. Fundamentals to all of these concerns are their efficient detection, identification, and quantification. The use of molecular markers showed the best promise in the field of plant pathogen diagnostics. However, despite the unquestionable benefits of DNA-based methods, two significant limitations are associated with their use. The first limitation concerns the insufficient level of sensitivity due to the very low and uneven distribution of pathogens in plant material. The second limitation pertains to the inability of widely used diagnostic assays to detect cryptic species. Targeting mtDNA appears to provide a solution to these challenges. Its high copy number in microbial cells makes mtDNA an attractive target for developing highly sensitive assays. In addition, previous studies on different pathogen taxa indicated that mitogenome sequence variation could improve cryptic species delimitation accuracy. This review sheds light on the potential application of mtDNA for pathogen diagnostics. This paper covers a brief description of qPCR and DNA barcoding as two major strategies enabling the diagnostics of plant pathogenic fungi and oomycetes. Both strategies are discussed along with the potential use of mtDNA, including their strengths and weaknesses.

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“…Mitochondrial genes in fungi contain highly variable numbers of group I and II introns that are inserted in protein-coding as well as rRNA genes (4). For instance, Endoconidiophora species seem to contain more than 80 mitochondrial introns (5), which can create gene annotation challenges Coccidioides spp.…”

Section: Introductionmentioning

confidence: 99%

Structural characterization and evolutionary analyses of theCoccidioides immitisandCoccidioides posadasiimitochondrial genomes

Teixeira

Lang

Matute³

et al. 2020

Preprint

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Fungal mitochondrial genomes encode for genes involved in crucial cellular processes, such as oxidative phosphorylation and mitochondrial translation, and these genes have been used as molecular markers for population genetics studies. Coccidioides immitis and C. posadasii are endemic fungal pathogens that cause coccidioidomycosis in arid regions across both American continents. To date, almost one hundred Coccidioides strains have been sequenced. The focus of these studies has been exclusively to infer patterns of variation of nuclear genomes (nucDNA). However, their mitochondrial genomes (mtDNA) have not been studied. In this report, we describe the assembly and annotation of mitochondrial reference genomes for two representative strains of C. posadasii and C. immitis, as well as assess population variation among 77 published genomes. The circular-mapping mtDNA molecules are 68.2 Kb in C. immitis and 75.1 Kb in C. posadasii. We identified the fourteen mitochondrial protein-coding genes common to most fungal mitochondria, including genes encoding the small and large ribosomal RNAs (rns and rnl), the RNA subunit of RNAse P (rnpB), and 26 tRNAs organized in polycistronic transcription units, which are mostly syntenic across different populations and species of Coccidioides. Both Coccidioides species are characterized by a large number of group I and II introns, harboring twice the number of elements as compared to closely related Onygenales. The introns contain complete or truncated ORFs with high similarity to homing endonucleases of the LAGLIDADG and GIY-YIG families. Phylogenetic comparison of the mtDNA and nucDNA genomes shows discordance, possibly due to differences in patterns of inheritance. In summary, this work represents the first complete assessment of mitochondrial genomes among several isolates of both species of Coccidioides, and provides a foundation for future functional work.

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Genome streamlining via complete loss of introns has occurred multiple times in lichenized fungal mitochondria

Cited by 29 publications

References 102 publications

Genome-scale data reveal the role of hybridization in lichen-forming fungi

Genome-scale data reveal the role of hybridization in lichen-forming fungi

Promising Perspectives for Detection, Identification, and Quantification of Plant Pathogenic Fungi and Oomycetes through Targeting Mitochondrial DNA

Structural characterization and evolutionary analyses of theCoccidioides immitisandCoccidioides posadasiimitochondrial genomes

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