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    First characterization of the complete mitochondrial genome of fungal plant-pathogen Monilinia laxa which represents the mobile intron rich structure
    (Nature Portfolio, 2020) Yildiz, Gozde; Ozkilinc, Hilal
    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.
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    Molecular phylogenetic species in Alternaria pathogens infecting pistachio and wild relatives
    (Springer Heidelberg, 2018) Ozkilinc, Hilal; Sevinc, Unal
    Many important pathogens of crops worldwide are members of section Alternaria within the genus Alternaria. Representative species in this section such as Alternaria alternata, Alternaria tenuissima, and Alternaria arborescens show high variability, intermediate characters and plasticity in morphological features, which makes species identification difficult. The aim of this study was to characterize Alternaria species associated with pistachio and wild relatives in Turkey using molecular phylogenetics. One hundred isolates of Alternaria spp. from pistachio and wild relatives from Turkey were investigated. In addition, standard morphological reference isolates and Alternaria blight pathogens of pistachio from USA were included. Sequence data from major allergen a1, ATPase, endopolygalacturanase, and anonymous regions OPA1.3 and SCAR2 were obtained. Gene trees were estimated based on maximum parsimony, maximum-likelihood, and bayesian inference methods. Species tree estimation was performed based on Yule speciation and strict molecular clock assumption. Among the collection of Alternaria spp. from Turkey, only one A. arborescens isolate and three isolates which were morphologically A. alternata/A. arborescens intermediate types, but, phylogenetically close to A. arborescens were discovered. While A. alternata and A. tenuissima formed one phylogenetic species, A. alternata/tenuissima were phylogenetically distinct from A. arborescens. Furthermore, a TaqI restriction site in the endopolygalacturanase gene was explored as a novel diagnosis for identification of A. alternata/tenuissima and A. arborescens. All these molecular phylogenetic approaches allow to distinguish morphologically similar Alternaria pathogens and molecular phylogenies of Alternaria pathogens from pistachio and wild relatives in Turkey are described for the first time.
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    Pathogenicity, Morpho-Species and Mating Types of Alternaria spp. causing Alternaria blight in Pistacia spp. in Turkey
    (Springer, 2017) Ozkilinc, Hilal; Sarpkaya, Kamil; Kurt, Sener; Can, Canan; Polatbilek, Hatice; Yasar, Aysegul; Sevinc, Unal
    Alternaria genus includes many plant pathogens on numerous hosts, causing leaf spots, rots and blights. Alternaria blight has been observed as one of the important fungal diseases of pistachio (Pistacia vera L.) as well as its wild relatives (P. terebinthus, P. lentiscus, P. khinjuk, P. atlantica, P. mutica) in Turkey. Alternaria species were sampled from Pistacia spp. hosts from different geographic regions in Turkey during field trips in late spring to early fall of 2013. Alternaria blight symptoms were observed mainly on fruits and rarely on leaves. Four hundred and twenty two of the isolates were morphologically defined as A. alternata, A. tenuissima, A. arborescens and also intermediate morpho-species between A. alternata/A. arborescens. Pathogenicity of the isolates was confirmed with host inoculations on detached fruits. Mating types of 270 isolates of Alternaria spp. from the collection were identified using a PCR-based mating type assay that amplifies either a MAT1-1 or a MAT1-2 fragment from the mating locus. Although a strongly clonal population structure was expected due to the putative asexual reproduction of these fungi, both idiomorphs were detected at equal frequencies at several different spatial scales. The distribution of mating types within each geographic region, within host species as well as in overall collection was not significantly different from 1:1. Amplified fragments of partial idiomorph sequences were obtained for representative isolates. Parsimony trees were depicted based on sequence data of mating type genes for these representative isolates as well as some other Alternaria species obtained by Genebank. Several point mutations presented a few clusters which are supported by high bootsrapped values. The Alternaria blight disease agents both from cultivated and wild hosts were pathogenic on pistachio which may cause difficulties to control the disease because of extensity of pathogen sources. Besides, equal mating type distribution of the pathogen at both geographic and host species levels suggests a potential for sexual reproduction of Alternaria spp. in Turkey.
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    Phylogenetic divergences in brown rot fungal pathogens of Monilinia species from a worldwide collection: inferences based on the nuclear versus mitochondrial genes
    (BMC, 2022) Silan, Ece; Ozkilinc, Hilal
    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, TEF1 alpha) 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.
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    Screening fungicide resistance of Alternaria pathogens causing alternaria blight of pistachio in Turkey
    (Centenary University, 2017) Ozkilinc, Hilal; Kurt, Sener
    Alternaria blight is one of the important diseases of pistachio and wild relatives, and its management in pistachio orchards mainly relies on fungicide applications. But, it is observed the disease cannot be declined or controlled by fungicide treatment that might be due to development of fungicide resistance in Alternaria pathogens. On the other hand, wild Pistacia species and some pistachio trees which cultural practices are not applied are not exposed to fungicide treatments in nature. Isolates from orchards and wild systems may show difference in their sensitivities to fungicides. In this study, twenty-two isolates of Alternaria species from different hosts of Pistacia species were investigated in vitro for their sensitivity to different fungicides having different mode of action. Fungicide sensitivity were evaluated based on mycelial growth and spore germination of the isolates by using effective concentrations. The least effective fungicide was azoxystrobin and the most effective one was boscalid + pyraclostrobin among the fungicides tested in this study. Partial gene sequencing of succinate dehydrogenase genes presented boscalid sensitivity of the isolates according to the specific mutations related with boscalid resistance. This study is the first initiation to observe sensitivity of Alternaria pathogens from pistachio and wild relatives against to the most commonly used commercial fungicides in Turkey. © 2017, Centenary University. All rights reserved.
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    The most recent status of genetic structure of Didymella rabiei (Ascochyta rabiei) populations in Turkey and the first genotype profile of the pathogen from the wild ancestor, Cicer reticulatum
    (Springer, 2019) Ozkilinc, Hilal; Can, Canan
    Chickpea is an important legume crop cultivated in many locations of Turkey and wild relatives of chickpea naturally grow in the Southeastern Anatolia Region of Turkey. Ascochyta blight caused by Didymella rabiei is one of the most important limiting factors for chickpea production. In this study, we aimed to investigate the genetic structures of D. rabiei samples from wild and domesticated chickpea hosts from different geographical regions. For this purpose, D. rabiei was collected from different geographic regions of Turkey between March and June in 2014 and 2015. Besides, some isolates were obtained from the wild chickpea species, C. pinnatifidum and C. reticulatum. Total, one hundred and two isolates of D. rabiei were genotyped using six sequence tagged microsatellite (STMS) markers. According to the results of molecular variance, the pathogen isolates from different geographic regions showed a significant genetic variation, but, most of which were confined within the populations. The total genetic diversity was estimated to be 0.612 for D. rabiei isolates from chickpea over the country. For the first time, D. rabiei from C. reticulatum, which is the wild ancestor of domesticated chickpea was found in the world and the isolates from C. reticulatum were represented with a single genotype. Isolates from C. pinnatifidum were genetically closer to the isolates from Southeastern Anatolia Region. All the isolates were grouped as one genetic population according to the Bayesian algorithm and presented a mixed distribution based on the principal coordinate analysis (PCoA) of genetic distances. All the results represented and updated the information about the genetic structure of D. rabiei populations across the country by announcing new information about the isolates from wild relatives. In addition, STMS markers were utilized to test whether allele sizes of microstallite loci change during asexual reproduction in infection period within the host. Thus, the changes in pathogen genotype was traced from seed to seedling. To do tracing, chickpea seeds were treated with two different D. rabiei isolates with known STMS multilocus genotypes. Then, pathogen re- isolations were performed from the plants grown from the infected seeds and these re-isolates were genotyped with the same STMS markers. Allele sizes of re-isolates were different from the parental ones for some of the loci which indicated that microsatellite alleles may have changed during multiple cycles of asexual reproduction through host infection.