Species diversity, mating type assays and aggressiveness patterns of Monilinia pathogens causing brown rot of peach fruit in Turkey

2021

Front. Microbiol.

Monilinia fructicola and Monilinia laxa species are the most destructive and economically devastating fungal plant pathogens causing brown rot disease on stone and pome fruits worldwide. Mitochondrial genomes (mitogenomes) play critical roles influencing the mechanisms and directions of the evolution of fungal pathogens. The pan-mitogenomics approach predicts core and accessory regions of the mitochondrial genomes and explains the gain or loss of variation within and between species. The present study is a fungal pan-mitogenome of M. fructicola (N = 8) and M. laxa (N = 8) species. The completely sequenced and annotated mitogenomes showed high variability in size within and between the species. The mitogenomes of M. laxa were larger, ranging from 178,351 to 179,780bp, than the mitogenomes of M. fructicola, ranging from 158,607 to 167,838bp. However, size variation within the species showed that M. fructicola isolates were more variable in the size range than M. laxa isolates. All the mitogenomes included conserved mitochondrial genes, as well as variable regions including different mobile introns encoding homing endonucleases or maturase, non-coding introns, and repetitive elements. The linear model analysis supported the hypothesis that the mitogenome size expansion is due to presence of variable (accessory) regions. Gene synteny was mostly conserved among all samples, with the exception for order of the rps3 in the mitogenome of one isolate. The mitogenomes presented AT richness; however, A/T and G/C skew varied among the mitochondrial genes. The purifying selection was detected in almost all the protein-coding genes (PCGs) between the species. However, cytochrome b was the only gene showing a positive selection signal among the total samples. Combined datasets of amino acid sequences of 14 core mitochondrial PCGs and rps3 obtained from this study together with published mitochondrial genome sequences from some other species from Heliotales were used to infer a maximum likelihood (ML) phylogenetic tree. ML tree indicated that both Monilinia species highly diverged from each other as well as some other fungal species from the same order. Mitogenomes harbor much information about the evolution of fungal plant pathogens, which could be useful to predict pathogenic life strategies.

Section: Methodsmentioning

confidence: 99%

Pan-Mitogenomics Approach Discovers Diversity and Dynamism in the Prominent Brown Rot Fungal Pathogens

Yildiz

2021

Front. Microbiol.

“…Isolates of M. laxa were obtained from brown-rot-diseased peach fruits in Turkey, and after pure culturing, were stored at – 20 °C on filter papers. Species identification based on both morphological criteria and polymerase chain reaction (PCR) with species-specific primers 3 . The isolate used for mitogenome characterization was obtained from the city Nigde and named Ni-B3-A2.…”

Section: Methodsmentioning

confidence: 99%

“…The pathogen could be found from blossom stage to post-harvesting stage, and results serious losses in both quantity and quality of yield 2 . Recently, brown rot of peaches has been observed in Turkey, and Monilinia species as related to the disease were collected and characterized 3 .…”

Section: Introductionmentioning

confidence: 99%

First characterization of the complete mitochondrial genome of fungal plant-pathogen Monilinia laxa which represents the mobile intron rich structure

Yildiz

2020

Sci Rep

Monilinia laxa is an important fungal plant pathogen causing brown rot on many stone and pome fruits worldwide. Mitochondrial genome (mitogenome) plays a critical role in evolutionary biology of the organisms. This study aimed to characterize the complete mitogenome of M. laxa by using next-generation sequencing and approaches of de novo assembly and annotation. The total length of the mitogenome of M. laxa was 178,357 bp, and its structure was circular. GC content of the mitogenome was 30.1%. Annotation of the mitogenome presented 2 ribosomal RNA (rRNA) genes, 32 transfer RNA genes (tRNA), 1 gene encoding mitochondrial ribosomal protein S3, 14 protein-coding genes and 15 open reading frame encoding hypothetical proteins. Moreover, the group I mobile introns encoding homing endonucleases including LAGLIDADG and GIY-YIG families were found both within coding regions (genic) and intergenic regions of the mitogenome, indicating an enlarged size and a dynamic structure of the mitogenome. Furthermore, a comparative mitogenomic analysis was performed between M. laxa and the three closely related fungal phytopathogen species ( Botryotinia fuckeliana, Sclerotinia sclerotiorum and, S. borealis ). Due to the number and distribution of introns, the large extent of structural rearrangements and diverse mitogenome sizes were detected among the species investigated. Monilinia laxa presented the highest number of homing endonucleases among the fungal species considered in the analyses. This study is the first to report a detailed annotation of the mitogenome of an isolate of M. laxa , providing a solid basis for further investigations of mitogenome variations for the other Monilinia pathogens causing brown rot disease.

“…Suggested recombination was obtained due to the NAD5 region, where the downstream region of the intron in M. fructicola aligns with M. laxa. Even though sexual reproduction is indirectly expected in these populations [5,40,41], no in vivo/vitro study have been carried out to observe inter or intraspecies sexual reproduction yet. However, hybrid species have been detected within the Botrytis genus [42] therefore further study is needed to cover on possible recombination status between different Monilinia species as well as observation of intraspecific sexual reproduction.…”

Section: Discussionmentioning

confidence: 99%

Phylogenetic divergences in brown rot fungal pathogens of Monilinia species from a worldwide collection: inferences based on the nuclear versus mitochondrial genes

Sılan

2022

BMC Ecol Evo

Background Phylogenetic analyses for plant pathogenic fungi explore many questions on diversities, relationships, origins, and divergences of populations from different sources such as species, host, and geography. This information is highly valuable, especially from a large global sampling, to understand the evolutionary paths of the pathogens worldwide. Monilinia fructicola and M. laxa are two important fungal pathogens of stone fruits that cause the widespread disease commonly known as brown rot. Three nuclear genes (Calmodulin, SDHA, TEF1α) and three mitochondrial genes (Cytochrome_b, NAD2, and NAD5) of the two pathogen species from a worldwide collection including five different countries from four different continents were studied in this work. Results Both Maximum Likelihood and Bayesian approaches were applied to the data sets, and in addition, Maximum Parsimony based approaches were used for the regions having indel polymorphisms. Calmodulin, SDHA, NAD2, and NAD5 regions were found phylogenetically informative and utilized for phylogenetics of Monilinia species for the first time. Each gene region presented a set of haplotypes except Cytochrome_b, which was monomorphic. According to this large collection of two Monilinia species around the world, M. fructicola showed more diversity than M. laxa, a result that should be carefully considered, as M. fructicola is known to be a quarantine pathogen. Moreover, the other two mitochondrial genes (NAD2 and NAD5) did not have any substitution type mutations but presented an intron indel polymorphism indicating the contribution of introns as well as mobile introns to the fungal diversity and evolution. Based on the concatenated gene sets, nuclear DNA carries higher mutations and uncovers more phylogenetic clusters in comparison to the mitochondrial DNA-based data for these fungal species. Conclusions This study provides the most comprehensive knowledge on the phylogenetics of both nuclear and mitochondrial genes of two prominent brown rot pathogens, M. fructicola and M. laxa. Based on the regions used in this study, the nuclear genes resolved phylogenetic branching better than the mitochondrial genes and discovered new phylogenetic lineages for these species.