Towards Uncovering New Insights into Respiratory Inhibitor Fungicide Resistance in Monilinia Fungal Plant Pathogens: Insights from a Mitogenomic Approach
DOI:
https://doi.org/10.24925/turjaf.v13i6.1577-1589.7703Keywords:
Mitochondrial genome variation, Monilinia, Respiratory inhibitor resistance, Sequence kernel association testAbstract
Mitochondrial genomes are key targets in controlling fungal plant pathogens and mediate adaptive responses like fungicide resistance. Respiratory inhibitor fungicides (RIs) are widely used against many fungal pathogens, including Monilinia fructi cola and M. laxa, which are casual agents of brown rot of stone fruits worldwide. Although resistance to RIs has been reported in these species, the genetic basis is not fully elucidated. and is hypothesized to involve mitochondrial genome variations. To explore this, mitogenomic variations was comprehensively analysed to assess the resistance responses of two Monilinia species to three RIs, including two technical grade fungicides (bosclid and azoxystrobin) and, a commercial one (signum). Whole mitogenome data from sixteen isolates of two species with different resistance/susceptibility phenotypes were analysed for certain gene mutations, mitochondrial variants, heteroplasmy, and sequence kernel associations. The results indicated that commonly known mutations and low levels of heteroplasmy do not fully explain resistance. In Monilinia fructicola, the presence of multiple variants appears to contribute to resistance, however, no variant patterns corresponded significantly with resistance phenotype in M. laxa. Providing a broad perspective, this study serves as a valuable model and supports the potential of mitogenome-focused RI resistance research. These insights contribute to a better understanding of specific resistance responses, thereby supporting the development of more effective pathogen control strategies.
References
Abate. D.. Pastore. C.. Gerin. D.. De Miccolis Angelini. R. M.. Rotolo. C.. Pollastro. S.. & Faretra. F. (2018). Characterization of Monilinia spp. Populations on Stone Fruit in South Italy. Plant Dis. 102(9). 1708-1717. https://doi.org/10.1094/pdis-08-17-1314-re
Abrantes. P.. Rosa. A.. Francisco. V.. Sousa. I.. Xavier. J. M.. & Oliveira. S. A. (2016). Mitochondrial genome association study with peripheral arterial disease and venous thromboembolism. Atherosclerosis. 252. 97-105. https://doi.org/10.1016/j.atherosclerosis.2016.07.920
Avila-Adame. C.. & Köller. W. (2003). Characterization of spontaneous mutants of Magnaporthe grisea expressing stable resistance to the Qo-inhibiting fungicide azoxystrobin. Curr Genet. 42(6). 332-338. https://doi.org/10.1007/s00294-002-0356-1
Ballard. J. W.. & Whitlock. M. C. (2004). The incomplete natural history of mitochondria. Mol Ecol. 13(4). 729-744. https://doi.org/10.1046/j.1365-294x.2003.02063.x
Barr. C. M.. Neiman. M.. & Taylor. D. R. (2005). Inheritance and recombination of mitochondrial genomes in plants. fungi and animals. New Phytol. 168(1). 39-50. https://doi.org/10.1111/j.1469-8137.2005.01492.x
Belcour. L.. Begel. O.. & Picard. M. (1991). A site-specific deletion in mitochondrial DNA of Podospora is under the control of nuclear genes. Proceedings of the National Academy of Sciences. 88(9). 3579. https://doi.org/10.1073/pnas.88.9.3579
Boyle. E. A.. Li. Y. I.. & Pritchard. J. K. (2017). An Expanded View of Complex Traits: From Polygenic to Omnigenic. Cell. 169(7). 1177-1186. https://doi.org/https://doi.org/10.1016/j.cell.2017.05.038
Chen. W.-J.. Delmotte. F.. Cervera Sylvie. R.. Douence. L.. Greif. C.. & Corio-Costet. M.-F. (2007). At Least Two Origins of Fungicide Resistance in Grapevine Downy Mildew Populations. Applied and Environmental Microbiology. 73(16). 5162-5172. https://doi.org/10.1128/AEM.00507-07
Cinget. B.. & Bélanger. R. R. (2020). Discovery of new group I-D introns leads to creation of subtypes and link to an adaptive response of the mitochondrial genome in fungi. RNA Biol. 17(9). 1252-1260. https://doi.org/10.1080/15476286.2020.1763024
Cingolani. P.. Platts. A.. Wang le. L.. Coon. M.. Nguyen. T.. Wang. L.. Land. S. J.. Lu. X.. & Ruden. D. M. (2012). A program for annotating and predicting the effects of single nucleotide polymorphisms. SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly (Austin). 6(2). 80-92. https://doi.org/10.4161/fly.19695
Danecek. P.. Auton. A.. Abecasis. G.. Albers. C. A.. Banks. E.. DePristo. M. A.. Handsaker. R. E.. Lunter. G.. Marth. G. T.. Sherry. S. T.. McVean. G.. & Durbin. R. (2011). The variant call format and VCFtools. Bioinformatics. 27(15). 2156-2158. https://doi.org/10.1093/bioinformatics/btr330
Dierckxsens. N.. Mardulyn. P.. & Smits. G. (2020). Unraveling heteroplasmy patterns with NOVOPlasty. NAR Genom Bioinform. 2(1). lqz011. https://doi.org/10.1093/nargab/lqz011
dos Santos Pereira. D. A. (2020). Evolutionary and population genomics of the wheat pathogen Parastagonospora nodorum.
Durak. M. R.. Arslan. K.. Silan. E.. Yildiz. G.. & Ozkilinc. H. (2021). A novel approach for in vitro fungicide screening and the sensitivity of Monilinia populations from peach orchards in Turkey to respiratory inhibitor fungicides. Crop Protection. 147. 105688. https://doi.org/https://doi.org/10.1016/j.cropro.2021.105688
Eichler. E. E.. Flint. J.. Gibson. G.. Kong. A.. Leal. S. M.. Moore. J. H.. & Nadeau. J. H. (2010). Missing heritability and strategies for finding the underlying causes of complex disease. Nature Reviews Genetics. 11(6). 446-450. https://doi.org/10.1038/nrg2809
Franco. M. E. E.. López. S. M. Y.. Medina. R.. Lucentini. C. G.. Troncozo. M. I.. Pastorino. G. N.. Saparrat. M. C. N.. & Balatti. P. A. (2017). The mitochondrial genome of the plant-pathogenic fungus Stemphylium lycopersici uncovers a dynamic structure due to repetitive and mobile elements. PLoS One. 12(10). e0185545. https://doi.org/10.1371/journal.pone.0185545
Gaare. J. J.. Nido. G. S.. Sztromwasser. P.. Knappskog. P. M.. Dahl. O.. Lund-Johansen. M.. Maple-Grødem. J.. Alves. G.. Tysnes. O. B.. Johansson. S.. Haugarvoll. K.. & Tzoulis. C. (2018). Rare genetic variation in mitochondrial pathways influences the risk for Parkinson's disease. Mov Disord. 33(10). 1591-1600. https://doi.org/10.1002/mds.64
Giorgi. E. E.. Li. Y.. Caberto. C. P.. Beckman. K. B.. Lum-Jones. A.. Haiman. C. A.. Le Marchand. L.. Stram. D. O.. Saxena. R.. & Cheng. I. (2016). No Association between the Mitochondrial Genome and Prostate Cancer Risk: The Multiethnic Cohort. Cancer Epidemiol Biomarkers Prev. 25(6). 1001-1003. https://doi.org/10.1158/1055-9965.Epi-16-0111
Grasso. V.. Sierotzki. H.. Garibaldi. A.. & Gisi. U. (2006). Characterization of the cytochrome b gene fragment of Puccinia species responsible for the binding site of QoI fungicides. Pesticide Biochemistry and Physiology. 84(2). 72-82.
Hartmann. F. E.. Vonlanthen. T.. Singh. N. K.. McDonald. M. C.. Milgate. A.. & Croll. D. (2021). The complex genomic basis of rapid convergent adaptation to pesticides across continents in a fungal plant pathogen. Molecular Ecology. 30(21). 5390-5405.
Holb. I. (2019). Brown rot: Causes. detection and control of Monilinia spp. affecting tree fruit. Integrated Management of Diseases and Insect Pests of Tree Fruit; Fountain. XM. Ed. 103-150.
Holb. I. J. (2008). Brown rot blossom blight of pome and stone fruits: symptom. disease cycle. host resistance. and biological control. International Journal of Horticultural Science. 14(3). 15-21. https://doi.org/10.31421/IJHS/14/3/796
Hrustić. J.. Mihajlović. M.. Grahovac. M.. Delibašić. G.. Bulajić. A.. Krstić. B.. & Tanović. B. (2012). Genus Monilinia on pome and stone fruit species. Pesticidi i fitomedicina. 27(4). 283-297.
Hrustić. J.. Mihajlović. M.. Tanović. B.. Delibašić. G.. Stanković. I.. Krstić. B.. & Bulajić. A. (2013). First Report of Brown Rot Caused by Monilinia fructicola on Nectarine in Serbia. Plant Dis. 97(1). 147. https://doi.org/10.1094/pdis-08-12-0718-pdn
Ibrahim. M. A.. Al-Shomrani. B. M.. Simenc. M.. Alharbi. S. N.. Alqahtani. F. H.. Al-Fageeh. M. B.. & Manee. M. M. (2021). Comparative analysis of transposable elements provides insights into genome evolution in the genus Camelus. BMC Genomics. 22(1). 842. https://doi.org/10.1186/s12864-021-08117-9
Joardar. V.. Abrams. N. F.. Hostetler. J.. Paukstelis. P. J.. Pakala. S.. Pakala. S. B.. Zafar. N.. Abolude. O. O.. Payne. G.. Andrianopoulos. A.. Denning. D. W.. & Nierman. W. C. (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. https://doi.org/10.1186/1471-2164-13-698
Kaur. N.. & Mehl. H. (2021). Distribution of G143A mutations conferring fungicide resistance in Virginia populations of Parastagonospora nodorum infecting wheat. Plant Health Progress(ja).
Kim. Y. S.. Dixon. E. W.. Vincelli. P.. & Farman. M. L. (2003). Field Resistance to Strobilurin (Q(o)I) Fungicides in Pyricularia grisea Caused by Mutations in the Mitochondrial Cytochrome b Gene. Phytopathology. 93(7). 891-900. https://doi.org/10.1094/phyto.2003.93.7.891
Kozin. M. S.. Kulakova. O. G.. Kiselev. I. S.. Boyko. A. N.. & Favorova. O. O. (2020). [Variability of the Mitochondrial Genome and Development of the Primary Progressing form of Multiple Sclerosis]. Mol Biol (Mosk). 54(4). 596-602. https://doi.org/10.31857/s0026898420040084
Laaksonen. J.. Mishra. P. P.. Seppälä. I.. Lyytikäinen. L.-P.. Raitoharju. E.. Mononen. N.. Lepistö. M.. Almusa. H.. Ellonen. P.. Hutri-Kähönen. N.. Juonala. M.. Raitakari. O.. Kähönen. M.. Salonen. J. T.. & Lehtimäki. T. (2021). Examining the effect of mitochondrial DNA variants on blood pressure in two Finnish cohorts. Scientific Reports. 11(1). 611. https://doi.org/10.1038/s41598-020-79931-6
Lee. S.. Wu. M. C.. & Lin. X. (2012). Optimal tests for rare variant effects in sequencing association studies. Biostatistics. 13(4). 762-775. https://doi.org/10.1093/biostatistics/kxs014
Lesemann. S. S.. Schimpke. S.. Dunemann. F.. & Deising. H. B. (2006). Mitochondrial heteroplasmy for the cytochrome b gene controls the level of strobilurin resistance in the apple powdery mildew fungus Podosphaera leucotricha (Ell. & Ev.) ES Salmon. Journal of Plant Diseases and Protection. 113(6). 259-266.
Lesniak. K. E.. Proffer. T. J.. Beckerman. J. L.. & Sundin. G. W. (2011). Occurrence of QoI Resistance and Detection of the G143A Mutation in Michigan Populations of Venturia inaequalis. Plant Dis. 95(8). 927-934. https://doi.org/10.1094/pdis-12-10-0898
Li. H. (2011). A statistical framework for SNP calling. mutation discovery. association mapping and population genetical parameter estimation from sequencing data. Bioinformatics. 27(21). 2987-2993. https://doi.org/10.1093/bioinformatics/btr509
Li. H.. & Durbin. R. (2009). Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics. 25(14). 1754-1760. https://doi.org/10.1093/bioinformatics/btp324
Li. H.. Handsaker. B.. Wysoker. A.. Fennell. T.. Ruan. J.. Homer. N.. Marth. G.. Abecasis. G.. & Durbin. R. (2009). The Sequence Alignment/Map format and SAMtools. Bioinformatics. 25(16). 2078-2079. https://doi.org/10.1093/bioinformatics/btp352
Li. M.. Schönberg. A.. Schaefer. M.. Schroeder. R.. Nasidze. I.. & Stoneking. M. (2010). Detecting heteroplasmy from high-throughput sequencing of complete human mitochondrial DNA genomes. Am J Hum Genet. 87(2). 237-249. https://doi.org/10.1016/j.ajhg.2010.07.014
Li. Y.. Beckman. K. B.. Caberto. C.. Kazma. R.. Lum-Jones. A.. Haiman. C. A.. Le Marchand. L.. Stram. D. O.. Saxena. R.. & Cheng. I. (2015). Association of Genes. Pathways. and Haplogroups of the Mitochondrial Genome with the Risk of Colorectal Cancer: The Multiethnic Cohort. PLoS One. 10(9). e0136796. https://doi.org/10.1371/journal.pone.0136796
Liu. K.. Xie. N.. & Ma. H. J. (2021). Next-generation sequencing reveals the mitogenomic heteroplasmy in the topmouth culter (Culter alburnus Basilewsky. 1855). Mol Biol Rep. https://doi.org/10.1007/s11033-021-06913-w
Ludwig-Słomczyńska. A. H.. Seweryn. M. T.. Kapusta. P.. Pitera. E.. Handelman. S. K.. Mantaj. U.. Cyganek. K.. Gutaj. P.. Dobrucka. Ł.. Wender-Ożegowska. E.. Małecki. M. T.. & Wołkow. P. P. (2020). Mitochondrial GWAS and association of nuclear - mitochondrial epistasis with BMI in T1DM patients. BMC Med Genomics. 13(1). 97. https://doi.org/10.1186/s12920-020-00752-7
Ma. B.. & Tredway. L. P. (2013). Induced overexpression of cytochrome P450 sterol 14α-demethylase gene (CYP51) correlates with sensitivity to demethylation inhibitors (DMIs) in Sclerotinia homoeocarpa. Pest Manag Sci. 69(12). 1369-1378. https://doi.org/10.1002/ps.3513
Ma. Z.. Felts. D.. & Michailides. T. J. (2003). Resistance to azoxystrobin in Alternaria isolates from pistachio in California. Pesticide Biochemistry and Physiology. 77(2). 66-74. https://doi.org/https://doi.org/10.1016/j.pestbp.2003.08.002
Ma. Z.. Proffer. T. J.. Jacobs. J. L.. & Sundin. G. W. (2006). Overexpression of the 14alpha-demethylase target gene (CYP51) mediates fungicide resistance in Blumeriella jaapii. Applied and Environmental Microbiology. 72(4). 2581-2585. https://doi.org/10.1128/AEM.72.4.2581-2585.2006
Maeda. R.. Kami. D.. Maeda. H.. Shikuma. A.. & Gojo. S. (2020). High throughput single cell analysis of mitochondrial heteroplasmy in mitochondrial diseases. Scientific Reports. 10(1). 10821. https://doi.org/10.1038/s41598-020-67686-z
Manolio. T. A.. Collins. F. S.. Cox. N. J.. Goldstein. D. B.. Hindorff. L. A.. Hunter. D. J.. McCarthy. M. I.. Ramos. E. M.. Cardon. L. R.. Chakravarti. A.. Cho. J. H.. Guttmacher. A. E.. Kong. A.. Kruglyak. L.. Mardis. E.. Rotimi. C. N.. Slatkin. M.. Valle. D.. Whittemore. A. S.. Boehnke. M.. Clark. A. G.. Eichler. E. E.. Gibson. G.. Haines. J. L.. Mackay. T. F.. McCarroll. S. A.. & Visscher. P. M. (2009). Finding the missing heritability of complex diseases. Nature. 461(7265). 747-753. https://doi.org/10.1038/nature08494
Marquis. J.. Lefebvre. G.. Kourmpetis. Y. A. I.. Kassam. M.. Ronga. F.. De Marchi. U.. Wiederkehr. A.. & Descombes. P. (2017). MitoRS. a method for high throughput. sensitive. and accurate detection of mitochondrial DNA heteroplasmy. BMC Genomics. 18(1). 326. https://doi.org/10.1186/s12864-017-3695-5
McKenna. A.. Hanna. M.. Banks. E.. Sivachenko. A.. Cibulskis. K.. Kernytsky. A.. Garimella. K.. Altshuler. D.. Gabriel. S.. Daly. M.. & DePristo. M. A. (2010). The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20(9). 1297-1303. https://doi.org/10.1101/gr.107524.110
Miessner. S.. & Stammler. G. (2010). Monilinia laxa. M. fructigena and M. fructicola: Risk estimation of resistance to QoI fungicides and identification of species with cytochrome b gene sequences. Journal of Plant Diseases and Protection. 117(4). 162-167.
Mohd-Assaad. N.. McDonald. B. A.. & Croll. D. (2016). Multilocus resistance evolution to azole fungicides in fungal plant pathogen populations. Mol Ecol. 25(24). 6124-6142. https://doi.org/10.1111/mec.13916
Monteiro-Vitorello. C. B.. Bell. J. A.. Fulbright. D. W.. & Bertrand. H. (1995). A cytoplasmically transmissible hypovirulence phenotype associated with mitochondrial DNA mutations in the chestnut blight fungus Cryphonectria parasitica. Proc Natl Acad Sci U S A. 92(13). 5935-5939. https://doi.org/10.1073/pnas.92.13.5935
Mosquera. S.. Chen. L. H.. Aegerter. B.. Miyao. E.. Salvucci. A.. Chang. T. C.. Epstein. L.. & Stergiopoulos. I. (2019). Cloning of the Cytochrome b Gene From the Tomato Powdery Mildew Fungus Leveillula taurica Reveals High Levels of Allelic Variation and Heteroplasmy for the G143A Mutation. Front Microbiol. 10. 663. https://doi.org/10.3389/fmicb.2019.00663
Ozkilinc. H.. Yildiz. G.. Silan. E.. Arslan. K.. Guven. H.. Altinok. H. H.. Altindag. R.. & Durak. M. R. (2020). Species diversity. mating type assays and aggressiveness patterns of Monilinia pathogens causing brown rot of peach fruit in Turkey. European Journal of Plant Pathology. 157(4). 799-814. https://doi.org/10.1007/s10658-020-02040-7
Peters. R. D.. Drake. K. A.. Gudmestad. N. C.. Pasche. J. S.. & Shinners-Carnelley. T. (2008). First Report of Reduced Sensitivity to a QoI Fungicide in Isolates of Alternaria solani Causing Early Blight of Potato in Canada. Plant Dis. 92(12). 1707. https://doi.org/10.1094/pdis-92-12-1707b
Purcell. S.. Neale. B.. Todd-Brown. K.. Thomas. L.. Ferreira. M. A.. Bender. D.. Maller. J.. Sklar. P.. de Bakker. P. I.. Daly. M. J.. & Sham. P. C. (2007). PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 81(3). 559-575. https://doi.org/10.1086/519795
Rozen. S.. & Skaletsky. H. (2000). Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol. 132. 365-386. https://doi.org/10.1385/1-59259-192-2:365
Samuel. S.. Papayiannis. L. C.. Leroch. M.. Veloukas. T.. Hahn. M.. & Karaoglanidis. G. S. (2011). Evaluation of the incidence of the G143A mutation and cytb intron presence in the cytochrome bc-1 gene conferring QoI resistance in Botrytis cinerea populations from several hosts. Pest Manag Sci. 67(8). 1029-1036. https://doi.org/10.1002/ps.2226
Sierotzki. H. (2015). Respiration inhibitors: complex III. In Fungicide resistance in plant pathogens (pp. 119-143). Springer.
Sierotzki. H.. Frey. R.. Wullschleger. J.. Palermo. S.. Karlin. S.. Godwin. J.. & Gisi. U. (2007). Cytochrome b gene sequence and structure of Pyrenophora teres and P. tritici-repentis and implications for QoI resistance. Pest Manag Sci. 63(3). 225-233. https://doi.org/10.1002/ps.1330
Stammler. G.. Wolf. A.. Glaettli. A.. & Klappach. K. (2015). Respiration inhibitors: complex II. In Fungicide resistance in plant pathogens (pp. 105-117). Springer.
Stewart. J. B.. & Chinnery. P. F. (2015). The dynamics of mitochondrial DNA heteroplasmy: implications for human health and disease. Nat Rev Genet. 16(9). 530-542. https://doi.org/10.1038/nrg3966
Torriani. S. F.. Goodwin. S. B.. Kema. G. H.. Pangilinan. J. L.. & McDonald. B. A. (2008). Intraspecific comparison and annotation of two complete mitochondrial genome sequences from the plant pathogenic fungus Mycosphaerella graminicola. Fungal Genet Biol. 45(5). 628-637. https://doi.org/10.1016/j.fgb.2007.12.005
Vega. B.. & Dewdney. M. M. (2014). QoI-resistance stability in relation to pathogenic and saprophytic fitness components of Alternaria alternata from citrus. Plant disease. 98(10). 1371-1378.
Vielba-Fernández. A.. Polonio. Á.. Ruiz-Jiménez. L.. de Vicente. A.. Pérez-García. A.. & Fernández-Ortuño. D. (2020). Fungicide Resistance in Powdery Mildew Fungi. Microorganisms. 8(9). 1431. https://doi.org/10.3390/microorganisms8091431
Villani. S. M.. & Cox. K. D. (2014). Heteroplasmy of the cytochrome b gene in Venturia inaequalis and its involvement in quantitative and practical resistance to trifloxystrobin. Phytopathology. 104(9). 945-953. https://doi.org/10.1094/phyto-06-13-0158-r
Wallace. D. C. (1992). Mitochondrial genetics: a paradigm for aging and degenerative diseases? Science. 256(5057). 628-632. https://doi.org/10.1126/science.1533953
Willetts. H. J.. Byrde. R. J. W.. Fielding. A. H.. & Wong. A. L. (1977). The taxonomy of the brown rot fungi (Monilinia spp.) related to their extracellular cell wall-degrading enzymes. Microbiology. 103(1). 77-83.
Wu. B.. & Pankow. J. S. (2016). Sequence kernel association test of multiple continuous phenotypes. Genetic epidemiology. 40(2). 91-100.
Wu. M. C.. Lee. S.. Cai. T.. Li. Y.. Boehnke. M.. & Lin. X. (2011). Rare-variant association testing for sequencing data with the sequence kernel association test. Am J Hum Genet. 89(1). 82-93. https://doi.org/10.1016/j.ajhg.2011.05.029
Xu. L.. Yang. K.. Fan. Q.. Zhao. D.. Pang. C.. & Ren. S. (2021). Whole mitochondrial genome analysis in Chinese patients with keratoconus. Mol Vis. 27. 270-282.
Yamamoto. K.. Sakaue. S.. Matsuda. K.. Murakami. Y.. Kamatani. Y.. Ozono. K.. Momozawa. Y.. & Okada. Y. (2020). Genetic and phenotypic landscape of the mitochondrial genome in the Japanese population. Commun Biol. 3(1). 104. https://doi.org/10.1038/s42003-020-0812-9
Yang. J.. Benyamin. B.. McEvoy. B. P.. Gordon. S.. Henders. A. K.. Nyholt. D. R.. Madden. P. A.. Heath. A. C.. Martin. N. G.. Montgomery. G. W.. Goddard. M. E.. & Visscher. P. M. (2010). Common SNPs explain a large proportion of the heritability for human height. Nature Genetics. 42(7). 565-569. https://doi.org/10.1038/ng.608
Yang. J.. Manolio. T. A.. Pasquale. L. R.. Boerwinkle. E.. Caporaso. N.. Cunningham. J. M.. de Andrade. M.. Feenstra. B.. Feingold. E.. Hayes. M. G.. Hill. W. G.. Landi. M. T.. Alonso. A.. Lettre. G.. Lin. P.. Ling. H.. Lowe. W.. Mathias. R. A.. Melbye. M.. Pugh. E.. Cornelis. M. C.. Weir. B. S.. Goddard. M. E.. & Visscher. P. M. (2011). Genome partitioning of genetic variation for complex traits using common SNPs. Nat Genet. 43(6). 519-525. https://doi.org/10.1038/ng.823
Yang. X.. & Griffiths. A. J. (1993). Male transmission of linear plasmids and mitochondrial DNA in the fungus Neurospora. Genetics. 134(4). 1055-1062. https://doi.org/10.1093/genetics/134.4.1055
Ye. K.. Lu. J.. Ma. F.. Keinan. A.. & Gu. Z. (2014). Extensive pathogenicity of mitochondrial heteroplasmy in healthy human individuals. Proc Natl Acad Sci U S A. 111(29). 10654-10659. https://doi.org/10.1073/pnas.1403521111
Yildiz. G.. & Ozkilinc. H. (2020). First characterization of the complete mitochondrial genome of fungal plant-pathogen Monilinia laxa which represents the mobile intron rich structure. Scientific Reports. 10(1). 13644. https://doi.org/10.1038/s41598-020-70611-z
Yildiz. G.. & Ozkilinc. H. (2021). Pan-Mitogenomics Approach Discovers Diversity and Dynamism in the Prominent Brown Rot Fungal Pathogens. Front Microbiol. 12. 647989. https://doi.org/10.3389/fmicb.2021.647989
Zhang. Y.. Wang. S.. Li. H.. Liu. C.. Mi. F.. Wang. R.. Mo. M.. & Xu. J. (2021). Evidence for Persistent Heteroplasmy and Ancient Recombination in the Mitochondrial Genomes of the Edible Yellow Chanterelles From Southwestern China and Europe. Front Microbiol. 12. 699598. https://doi.org/10.3389/fmicb.2021.699598
Zheng. D.. & Köller. W. (1997). Characterization of the mitochondrial cytochrome b gene from Venturia inaequalis. Current genetics. 32(5). 361-366.
Zheng. D.. Olaya. G.. & Köller. W. (2000). Characterization of laboratory mutants of Venturia inaequalis resistant to the strobilurin-related fungicide kresoxim-methyl. Curr Genet. 38(3). 148-155. https://doi.org/10.1007/s002940000147
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