Genome-Wide Association and Selective Sweep Studies Reveal the Complex Genetic Architecture of DMI Fungicide Resistance in Cercospora beticola

Article

Spanner, Rebecca, Taliadoros, Demetris, Richards, Jonathan, Rivera-Varas, Viviana, Neubauer, Jonathan, Natwick, Mari, Hamilton, Olivia, Vaghefi, Niloofar, Pethybridge, Sarah, Secor, Gary A., Friesen, Timothy L., Stukenbrock, Eva H. and Bolton, Melvin D.. 2021. "Genome-Wide Association and Selective Sweep Studies Reveal the Complex Genetic Architecture of DMI Fungicide Resistance in Cercospora beticola." Genome Biology and Evolution. 13 (9), pp. 1-17. https://doi.org/10.1093/gbe/evab209
Article Title

Genome-Wide Association and Selective Sweep Studies Reveal the Complex Genetic Architecture of DMI Fungicide Resistance in Cercospora beticola

ERA Journal ID122964
Article CategoryArticle
AuthorsSpanner, Rebecca (Author), Taliadoros, Demetris (Author), Richards, Jonathan (Author), Rivera-Varas, Viviana (Author), Neubauer, Jonathan (Author), Natwick, Mari (Author), Hamilton, Olivia (Author), Vaghefi, Niloofar (Author), Pethybridge, Sarah (Author), Secor, Gary A. (Author), Friesen, Timothy L. (Author), Stukenbrock, Eva H. (Author) and Bolton, Melvin D. (Author)
Journal TitleGenome Biology and Evolution
Journal Citation13 (9), pp. 1-17
Article Numberevab209
Number of Pages17
Year2021
PublisherOxford University Press
Place of PublicationUnited Kingdom
ISSN1759-6653
Digital Object Identifier (DOI)https://doi.org/10.1093/gbe/evab209
Web Address (URL)https://academic.oup.com/gbe/article/13/9/evab209/6367780
Abstract

The rapid and widespread evolution of fungicide resistance remains a challenge for crop disease management. The demethylation inhibitor (DMI) class of fungicides is a widely used chemistry for managing disease, but there has been a gradual decline in efficacy in many crop pathosystems. Reliance on DMI fungicides has increased resistance in populations of the plant pathogenic fungus Cercospora beticola worldwide. To better understand the genetic and evolutionary basis for DMI resistance in C. beticola, a genome-wide association study (GWAS) and selective sweep analysis were conducted for the first time in this species. We performed whole-genome resequencing of 190 C. beticola isolates infecting sugar beet (Beta vulgaris ssp. vulgaris). All isolates were phenotyped for sensitivity to the DMI tetraconazole. Intragenic markers on chromosomes 1, 4, and 9 were significantly associated with DMI fungicide resistance, including a polyketide synthase gene and the gene encoding the DMI target CbCYP51. Haplotype analysis of CbCYP51 identified a synonymous mutation (E170) and nonsynonymous mutations (L144F, I387M, and Y464S) associated with DMI resistance. Genome-wide scans of selection showed that several of the GWAS mutations for fungicide resistance resided in regions that have recently undergone a selective sweep. Using radial plate growth on selected media as a fitness proxy, we did not find a trade-off associated with DMI fungicide resistance. Taken together, we show that population genomic data from a crop pathogen can allow the identification of mutations conferring fungicide resistance and inform about their origins in the pathogen population.

KeywordsGWAS, CYP51, azole, synonymous mutation, antifungal, selection
ANZSRC Field of Research 2020310805. Plant pathology
310509. Genomics
300409. Crop and pasture protection (incl. pests, diseases and weeds)
Byline AffiliationsDepartment of Agriculture, United States
Christian-Albrecht University of Kiel, Germany
Louisiana State University, United States
North Dakota State University, United States
Centre for Crop Health
Cornell University, United States
Institution of OriginUniversity of Southern Queensland
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Syme, Robert A., Martin, Anke, Wyatt, Nathan A., Lawrence, Julie A., Muria-Gonzalez, Mariano J., Friesen, Timothy L. and Ellwood, Simon R.. 2018. "Transposable element genomic fissuring in Pyrenophora teres is associated with genome expansion and dynamics of host-pathogen genetic interactions." Frontiers in Genetics. 9, pp. 1-15. https://doi.org/10.3389/fgene.2018.00130
Draft genome sequence of Annulohypoxylon stygium, Aspergillus mulundensis, Berkeleyomyces basicola (syn. Thielaviopsis basicola), Ceratocystis smalleyi, two Cercospora beticola strains, Coleophoma cylindrospora, Fusarium fracticaudum, Phialophora cf. hyalina, and Morchella septimelata
Wingfield, Brenda D., Bills, Gerald F., Dong, Yang, Huang, Wenli, Nel, Wilma J., Swalarsk-Parry, Benedicta S., Vaghefi, Niloofar, Wilken, Markus P., An, Zhiqiang, de Beer, Z. Wilhelm, De Vos, Lieschen, Chen, Li, Duong, Tuan A., Gao, Yun, Hammerbacher, Almuth, Kikkert, Julie R., Li, Yan, Li, Huiying, Li, Kuan, ..., Zhang, Xiaoling. 2018. "Draft genome sequence of Annulohypoxylon stygium, Aspergillus mulundensis, Berkeleyomyces basicola (syn. Thielaviopsis basicola), Ceratocystis smalleyi, two Cercospora beticola strains, Coleophoma cylindrospora, Fusarium fracticaudum, Phialophora cf. hyalina, and Morchella septimelata." IMA Fungus: the global mycological journal. 9 (1), pp. 199-223. https://doi.org/10.5598/imafungus.2018.09.01.13
Summer paddock survey finds fungal and bacterial diseases decreased but not eliminated [GRDC Field Crop Diseases Community of Practice, 1 October 2018 - Online community]
Adorada, Dante, Kelly, Lisa, Vaghefi, Niloofar and Sparks, Adam H,. 2018. "Summer paddock survey finds fungal and bacterial diseases decreased but not eliminated [GRDC Field Crop Diseases Community of Practice, 1 October 2018 - Online community]." GRDC Field Crop Diseases Community of Practice. 1 October 2018, pp. 1-8.
First report of Colletotrichum fioriniae causing anthracnose of elephant garlic (Allium ampeloprasum var. ampeloprasum) in New York, USA
Hay, F., Vaghefi, N., Strickland, D., Hadad, R. and Pethybridge, S.. 2018. "First report of Colletotrichum fioriniae causing anthracnose of elephant garlic (Allium ampeloprasum var. ampeloprasum) in New York, USA." New Disease Reports. 38 (1), pp. 1-1. https://doi.org/10.5197/j.2044-0588.2018.038.001
Re-visiting management options for charcoal rot in sorghum [eXtension AUS Field Crop Diseases, 19 March 2018 - Online community]
Adorada, Dante, Vaghefi, Niloofar and Sparks, Adam. 2018. "Re-visiting management options for charcoal rot in sorghum [eXtension AUS Field Crop Diseases, 19 March 2018 - Online community]." eXtension AUS Field Crop Diseases. 19 March 2018, pp. 1-8.
Cryptic diversity, pathogenicity, and evolutionary species boundaries in Cercospora populations associated with Cercospora leaf spot of Beta vulgaris
Vaghefi, Niloofar, Kikkert, Julie R., Hay, Frank S., Carver, Gavriela D., Koenick, Lori B., Bolton, Melvin D., Hanson, Linda E., Secor, Gary A. and Pethybridge, Sarah J.. 2018. "Cryptic diversity, pathogenicity, and evolutionary species boundaries in Cercospora populations associated with Cercospora leaf spot of Beta vulgaris." Fungal Biology. 122 (4), pp. 264-282. https://doi.org/10.1016/j.funbio.2018.01.008
First report of carrot root rot caused by Rhexocercosporidium carotae in the United States - a disease note
Hay, F. S., Vaghefi, N., Ivy, A. and Pethybridge, S. J.. 2017. "First report of carrot root rot caused by Rhexocercosporidium carotae in the United States - a disease note." Plant Disease: an international journal of applied plant pathology. 101 (1), pp. 248-248. https://doi.org/10.1094/PDIS-05-16-0656-PDN
First report of cercospora blight of asparagus officinalis caused by cercospora asparagi in New York
Hay, F. S., Maloney, E., Vaghefi, N., Shivas, R. G and Pethybridge, S. J. 2017. "First report of cercospora blight of asparagus officinalis caused by cercospora asparagi in New York." Plant Disease: an international journal of applied plant pathology. 101 (11), pp. 1953-1953. https://doi.org/10.1094/PDIS-05-17-0648-PDN
Efficacy of fungicides for the control of Cercospora leaf spot in processing table beet, 2015
Pethybridge, S. J., Vaghefi, N. and Kikkert, J.. 2016. "Efficacy of fungicides for the control of Cercospora leaf spot in processing table beet, 2015." Plant Disease Management Reports. 3 (Report No. 10), pp. 1-1.
Horticultural characteristics and susceptibility of table beet cultivars to Cercospora Leaf Spot in New York
Pethybridge, Sarah J., Vaghefi, Niloofar and Kikkert, Julie R.. 2017. "Horticultural characteristics and susceptibility of table beet cultivars to Cercospora Leaf Spot in New York." Horttechnology. 27 (4), pp. 530-538.
Draft genome sequences of Chrysoporthe austroafricana, Diplodia scrobiculata, Fusarium nygamai, Leptographium lundbergii, Limonomyces culmigenus, Stagonosporopsis tanaceti, and Thielaviopsis punctulata
Wingfield, Brenda D., Ades, Peter K., Al-Naemi, Fatima A., Beirn, Lisa A., Bihon, Wubetu, Crouch, Jo Anne, de Beer, Z. Wilhelm, De Vos, Lieschen, Duong, Tuan A., Fields, Christopher J., Fourie, Gerda, Kanzi, Aquillah M., Malapi-Wight, Martha, Pethybridge, Sarah J., Radwan, Osman, Rendon, Gloria, Slippers, Bernard, Santana, Quentin C., Steenkamp, Emma T., ..., Wingfield, Michael J.. 2015. "Draft genome sequences of Chrysoporthe austroafricana, Diplodia scrobiculata, Fusarium nygamai, Leptographium lundbergii, Limonomyces culmigenus, Stagonosporopsis tanaceti, and Thielaviopsis punctulata." IMA Fungus: the global mycological journal. 6 (1), pp. 233-248. https://doi.org/10.5598/imafungus.2015.06.01.15
Rapid changes in the genetic composition of Stagonosporopsis tanaceti population in Australian pyrethrum fields
Vaghefi, Niloofar, Hay, Frank S., Ades, Peter K., Pethybridge, Sarah Jane, Ford, Rebecca and Taylor, Paul W. J.. 2015. "Rapid changes in the genetic composition of Stagonosporopsis tanaceti population in Australian pyrethrum fields." Phytopathology: International Journal of the American Phytopathological Society. 105 (3), pp. 358-369. https://doi.org/10.1094/PHYTO-08-14-0212-R
Global genotype flow in Cercospora beticola populations confirmed through genotyping-by-sequencing
Vaghefi, Niloofar, Kikkert, Julie R., Bolton, Melvin D., Hanson, Linda E., Secor, Gary A., Nelson, Scot C. and Pethybridge, Sarah J.. 2017. "Global genotype flow in Cercospora beticola populations confirmed through genotyping-by-sequencing." PLoS One. 12 (10). https://doi.org/10.1371/journal.pone.0186488
Abscisic acid activates pathogenesis-related defense gene signaling in lentils
Ford, Rebecca, Tan, David, Vaghefi, Niloofar and Mustafa, Barkat. 2017. "Abscisic acid activates pathogenesis-related defense gene signaling in lentils." Pandey, Girdhar K. (ed.) Mechanism of plant hormone signaling under stress. United States. John Wiley & Sons. pp. 243-270
Genetic structure of Cercospora beticola populations on Beta vulgaris in New York and Hawaii
Vaghefi, Niloofar, Nelson, Scot C., Kikkert, Julie R. and Pethybridge, Sarah J.. 2017. "Genetic structure of Cercospora beticola populations on Beta vulgaris in New York and Hawaii." Scientific Reports. 7. https://doi.org/10.1038/s41598-017-01929-4
De novo genome assembly of Cercospora beticola for microsatellite marker development and validation
Vaghefi, Niloofar, Kikkert, Julie R., Bolton, Melvin D., Hanson, Linda E., Secor, Gary A. and Pethybridge, Sarah J.. 2017. "De novo genome assembly of Cercospora beticola for microsatellite marker development and validation." Fungal Ecology. 26, pp. 125-134. https://doi.org/10.1016/j.funeco.2017.01.006
Management of cercospora leaf spot in conventional and organic table beet production
Pethybridge, Sarah J., Vaghefi, Niloofar and Kikkert, Julie R.. 2017. "Management of cercospora leaf spot in conventional and organic table beet production." Plant Disease: an international journal of applied plant pathology. 101 (9), pp. 1642-1651. https://doi.org/10.1094/PDIS-04-17-0528-RE
Structure of Cercospora beticola populations in organic and conventional table beet production in New York and implications for disease management
Vaghefi, N., Kikkert, J. and Pethybridge, S.. 2016. "Structure of Cercospora beticola populations in organic and conventional table beet production in New York and implications for disease management." 76th Annual Meeting of the Northeastern Division: The American Phytopathological Society. Ithaca, United States 19 - 21 Oct 2016 United States. American Phytopathological Society. https://doi.org/10.1094/PHYTO-107-2-S2.5
Phylogenetic and population genetic analyses of Stagonosporopsis tanaceti, the cause of ray blight of pyrethrum in Australia
Vaghefi, N., Hay, F. S., Ades, P. K., Pethybridge, S. J., Ford, R. and Taylor, P. W. J.. 2014. "Phylogenetic and population genetic analyses of Stagonosporopsis tanaceti, the cause of ray blight of pyrethrum in Australia." 10th International Mycological Congress (IMC10 2014). Bangkok, Thailand 03 - 08 Aug 2014
Taxonomic reassessment of the ray blight pathogen of pyrethrum in Australia
Vaghefi, N., Pethybridge, S. J., Ford, R., Nicolas, M. E., Crous, P. W. and Taylor, P. W.. 2012. "Taxonomic reassessment of the ray blight pathogen of pyrethrum in Australia." 2012 American Phytopathological Society Annual Meeting (APS 2012). Rhode Island, United States of America 04 - 08 Aug 2012 United States. American Phytopathological Society.
Incidence and pathogenicity of Didymella americana on table beet in new york
Vaghefi, Niloofar, Kikkert, Julie R. and Pethybridge, Sarah J.. 2016. "Incidence and pathogenicity of Didymella americana on table beet in new york." Plant Health Progress. 17, pp. 270-272. https://doi.org/10.1094/PHP-BR-16-0064
A novel pathogenesis-related protein (LcPR4a) from lentil, and its involvement in defence against Ascochyta lentis
Vaghefi, Niloofar, Mustafa, Barkat M., Dulal, Nabeen, Selby-Pham, Jamie, Taylor, Paul W. J. and Ford, Rebecca. 2013. "A novel pathogenesis-related protein (LcPR4a) from lentil, and its involvement in defence against Ascochyta lentis." Phytopathologia Mediterranea. 52 (1), pp. 192-201.
A new anthracnose disease of pyrethrum caused by Colletotrichum tanaceti sp. nov.
Barimani, M., Pethybridge, S. J., Vaghefi, N., Hay, F. S. and Taylor, P. W. J.. 2013. "A new anthracnose disease of pyrethrum caused by Colletotrichum tanaceti sp. nov." Plant Pathology. 62 (6), pp. 1248-1257. https://doi.org/10.1111/ppa.12054
Stagonosporopsis spp. associated with ray blight disease of Asteraceae
Vaghefi, N., Pethybridge, S. J., Ford, R., Nicolas, M. E., Crous, P. W. and Taylor, P. W. J.. 2012. "Stagonosporopsis spp. associated with ray blight disease of Asteraceae." Australasian Plant Pathology. 41 (6), pp. 675-686. https://doi.org/10.1007/s13313-012-0161-3
Identification of the MAT1 locus in Stagonosporopsis tanaceti, and exploring its potential for sexual reproduction in Australian pyrethrum fields
Vaghefi, Niloofar, Ades, Peter K., Hay, Frank S., Pethybridge, Sarah J., Ford, Rebecca and Taylor, Paul W. J.. 2015. "Identification of the MAT1 locus in Stagonosporopsis tanaceti, and exploring its potential for sexual reproduction in Australian pyrethrum fields." Fungal Biology. 119 (5), pp. 408-419. https://doi.org/10.1016/j.funbio.2014.04.004
Revisiting Stagonosporopsis species associated with chrysanthemum and pyrethrum ray blight
Vaghefi, Niloofar, Pethybridge, Sarah J., Hay, Frank S., Ford, Rebecca, Nicolas, Marc E. and Taylor, Paul W. J.. 2016. "Revisiting Stagonosporopsis species associated with chrysanthemum and pyrethrum ray blight." Australasian Plant Pathology. 45 (6), pp. 561-570. https://doi.org/10.1007/s13313-016-0446-z
Development of a multiplex PCR diagnostic assay for the detection of Stagonosporopsis species associated with ray blight of Asteraceae
Vaghefi, Niloofar, Hay, Frank S., Pethybridge, Sarah J., Ford, Rebecca and Taylor, Paul W. J.. 2016. "Development of a multiplex PCR diagnostic assay for the detection of Stagonosporopsis species associated with ray blight of Asteraceae." European Journal of Plant Pathology. 146 (3), pp. 581-595. https://doi.org/10.1007/s10658-016-0944-4
Genotypic diversity and resistance to azoxystrobin of Cercospora beticola on processing table beet in New York
Vaghefi, Niloofar, Hay, Frank S., Kikkert, Julie and Pethybridge, Sarah J.. 2016. "Genotypic diversity and resistance to azoxystrobin of Cercospora beticola on processing table beet in New York." Plant Disease: an international journal of applied plant pathology. 100 (7), pp. 1466-1473. https://doi.org/10.1094/PDIS-09-15-1014-RE
One stop shop: backbone trees for important phytopathogenic genera: I (2014)
Hyde, Kevin D., Nilsson, R. Henrik, Alias, S. Aisyah, Ariyawansa, Hiran A., Blair, Jaime E., Cai, Lei, de Cock, Arthur W. A. M., Dissanayake, Asha J., Glockling, Sally L., Goonasekara, Ishani D., Gorczak, Michal, Hahn, Matthias, Jayawardena, Ruvishika S., van Kan, Jan A. L., Lawrence, Matthew H., Levesque, C. Andre, Li, Xinghong, Liu, Jian-Kui, Maharachchikumbura, Sajeewa S. N., ..., Zhou, Nan. 2014. "One stop shop: backbone trees for important phytopathogenic genera: I (2014)." Fungal Diversity. 67 (1), pp. 21-125. https://doi.org/10.1007/s13225-014-0298-1
Carpogenic germination of sclerotia of Sclerotinia minor and ascosporic infection of pyrethrum flowers
O'Malley, Thomas B., Hay, Frank S., Scott, Jason B., Gent, David H., Shivas, Roger G. and Pethybridge, Sarah J.. 2015. "Carpogenic germination of sclerotia of Sclerotinia minor and ascosporic infection of pyrethrum flowers." Canadian Journal of Plant Pathology. 37 (2), pp. 179-187. https://doi.org/10.1080/07060661.2015.1036122
First report of Didymella americana on baby lima bean (Phaseolus lunatus)
Gorny, Adrienne M., Pethybridge, Sarah J., Kikkert, Julie R. and Shivas, Roger G.. 2016. "First report of Didymella americana on baby lima bean (Phaseolus lunatus)." Canadian Journal of Plant Pathology. 38 (3), pp. 389-394. https://doi.org/10.1080/07060661.2016.1195877
Confirmation of Paracercospora egenula causing leaf spot of eggplant in Hawaii
Vaghefi, Niloofar, Pethybridge, Sarah J., Shivas, Roger G. and Nelson, Scot C.. 2016. "Confirmation of Paracercospora egenula causing leaf spot of eggplant in Hawaii." Australasian Plant Disease Notes. 11 (1), pp. 35-37. https://doi.org/10.1007/s13314-016-0223-4
Genetic relationships among populations of Gibberella zeae from barley, wheat, potato, and sugar beet in the upper midwest of the United States
Burlakoti, R. R., Ali, S., Secor, G. A., Neate, S. M., McMullen, M. P. and Adhikari, T. B.. 2008. "Genetic relationships among populations of Gibberella zeae from barley, wheat, potato, and sugar beet in the upper midwest of the United States." Phytopathology: International Journal of the American Phytopathological Society. 98 (9), pp. 969-976. https://doi.org/10.1094/PHYTO-98-9-0969
Comparative mycotoxin profiles of Gibberella zeae populations from barley, wheat, potatoes, and sugar beets
Burlakoti, Rishi R., Ali, Shaukat, Secor, Gary A., Neate, Stephen M., McMullen, Marcia P. and Adhikari, Tika B.. 2008. "Comparative mycotoxin profiles of Gibberella zeae populations from barley, wheat, potatoes, and sugar beets ." Applied and Environmental Microbiology. 74 (21), pp. 6513-6520. https://doi.org/10.1128/AEM.01580-08