Etiology of Halo Blight in Michigan Hopyards
- Douglas S. Higgins1
- Ross J. Hatlen1
- Jan M. Byrne1
- Monique L. Sakalidis1 2
- Timothy D. Miles1 †
- Mary K. Hausbeck1 †
- 1Department of Plant, Soil, and Microbial Sciences, Michigan State University, East Lansing, MI 48824
- 2Department of Forestry, Michigan State University, East Lansing, MI 48824
Abstract
Michigan’s hop acreage ranks fourth nationally, but the state’s growers contend with unique disease challenges resulting from frequent rainfall and high humidity. In August 2018, a Michigan hop grower reported necrosis and blighting of foliage and shattering of cones resulting in yield loss. Irregular-shaped lesions developed on leaves, surrounded by a halo of chlorotic tissue, and cone bracts became brown. Pycnidia were observed in symptomatic tissue. The goal of this study was to identify and characterize the causal agent of symptoms in leaf and cone tissue. In symptomatic leaves, 15 of 19 isolates recovered had 96.4% internal transcribed spacer rDNA (ITSrDNA) homology with Diaporthe nomurai. Bayesian and maximum likelihood analyses were performed on a subset of isolates using ITSrDNA, histone H3, beta-tubulin, and elongation factor 1 alpha. Bootstrap and posterior probabilities supported a unique cluster of Diaporthe sp. 1-MI isolates most closely related to the Diaporthe arecae species complex, Diaporthe hongkongensis, and Diaporthe multigutullata. Diaporthe sp. 1-MI was pathogenic in detached leaf and whole plant assays. Single-spore isolates from pycnidia originating from cones and leaves shared 100% ITSrDNA homology with Diaporthe sp. 1-MI obtained from the lesion margins of leaves collected in 2018. The distribution of Diaporthe sp. 1-MI was widespread among 347 cones collected from 15 Michigan hop yards and accounted for >38% of fungi recovered from cones in three hop yards. Diaporthe sp. 1-MI causing halo and cone blight presents a new disease management challenge for Michigan hop growers.
Literature Cited
- 2020. The identification of a new species, Diaporthe humulicola, a pathogen causing Diaporthe leaf spot on common hop. Plant Dis. 104:2377-2390. https://doi.org/10.1094/PDIS-08-19-1770-RE Link, ISI, Google Scholar
- 2012. Temporal patterns of sporulation potential of Phomopsis viticola on infected grape shoots, canes, and rachises. Plant Dis. 96:1297-1302. https://doi.org/10.1094/PDIS-09-11-0806-RE Link, ISI, Google Scholar
- 2010. Highlights of the Didymellaceae: A polyphasic approach to characterise Phoma and related pleosporalean genera. Stud. Mycol. 65:1-60. https://doi.org/10.3114/sim.2010.65.01 Crossref, ISI, Google Scholar
- 1998. Illustrated genera of imperfect fungi, 4th ed. American Phytopathological Society, St. Paul, MN. Google Scholar
- 2017. Characterization of fungal pathogens (Diaporthe angelicae and D. eres) responsible for umbel browning and stem necrosis on carrot in France. Plant Pathol. 66:239-253. https://doi.org/10.1111/ppa.12570 Crossref, ISI, Google Scholar
- 2016. Investigations on the occurrence of mycotoxins in beer. Food Control 63:135-139. https://doi.org/10.1016/j.foodcont.2015.11.040 Crossref, ISI, Google Scholar
- 2013. Characterization of species of Diaporthe from wood cankers of grape in eastern North American vineyards. Plant Dis. 97:912-920. https://doi.org/10.1094/PDIS-04-12-0357-RE Link, ISI, Google Scholar
- 2005. Fusarium cone tip blight of Humulus lupulus. Acta Hortic. 668:123-128. https://doi.org/10.17660/ActaHortic.2005.668.16 Crossref, Google Scholar
- Boerema, G. H., Gruyter, J. d., Noordeloos, M. E., and Hamers, M. E. C., eds. 2004. Phoma identification manual: Differentiation of specific and infra-specific taxa in culture. CABI Publishing, Cambridge, MA. doi.org/10.1079/9780851997438.0000 Crossref, Google Scholar
Brewers Association . 2019. State craft beer sales and production statistics, 2018: Michigan. https://www.brewersassociation.org Google Scholar- 1999. A method for designing primer sets for speciation studies in filamentous ascomycetes. Mycologia 91:553-556. https://doi.org/10.1080/00275514.1999.12061051 Crossref, ISI, Google Scholar
- 1973. Diaporthe sarmenticia associated with Humulus lupulus. Herb IMI: 172750a. International Mycological Institute Fungarium, Kew, UK. Google Scholar
- 1965. A mycological English-Latin glossary. Mycological memoirs (No. 1). Hafner Publishing Company, New York, NY. Google Scholar
- 1999. Single spore isolation of fungi. Fungal Divers. 3:29-38. Google Scholar
- 2004. Calonectria species and their Cylindrocladium anamorphs: Species with sphaeropedunculate vesicles. Stud. Mycol. 50:415-430. Google Scholar
- 2015. Fungal planet description sheets: 371-399. Persoonia 35:264-327. https://doi.org/10.3767/003158515X690269 Crossref, ISI, Google Scholar
- 1984. Department of hop research annual report 1983, Wye College. Invicta Press, Ashford, UK. Google Scholar
- 1988. Alternaria alternata infection of hop (Humulus lupulus) cones. Mycol. Res. 90:650-653. Google Scholar
- 2012. jModelTest 2: More models, new heuristics and parallel computing. Nat. Methods 9:772. https://doi.org/10.1038/nmeth.2109 Crossref, ISI, Google Scholar
- 2016. Occurrence and management of hop (Humulus lupulus) powdery mildew (Podosphaera macularis) in Michigan. Phytopathology 106(Suppl.):S4.187. ISI, Google Scholar
- 2016. Phylogeny and morphology reveal two new species of Diaporthe from Betula spp. in China. Phytotaxa 269:90-102. https://doi.org/10.11646/phytotaxa.269.2.2 Crossref, ISI, Google Scholar
- 2018. Diaporthe from walnut tree (Juglans regia) in China, with insight of the Diaporthe eres complex. Mycol. Prog. 17:841-853. https://doi.org/10.1007/s11557-018-1395-4 Crossref, ISI, Google Scholar
- 2002. Morphological and molecular characterization of Phomopsis vaccinii and additional isolates of Phomopsis from blueberry and cranberry in the eastern United States. Mycologia 94:494-504. https://doi.org/10.1080/15572536.2003.11833214 Crossref, ISI, Google Scholar
- 2016. Unravelling Diaporthe species associated with Camellia. Syst. Biodivers. 14:102-117. https://doi.org/10.1080/14772000.2015.1101027 Crossref, ISI, Google Scholar
- 2017. Diaporthe is paraphyletic [published correction appears in IMA Fungus 2017;8:82]. IMA Fungus 8:153-187. https://doi.org/10.5598/imafungus.2017.08.01.11 Crossref, ISI, Google Scholar
- 1993. ITS primers with enhanced specificity for basidiomycetes‐application to the identification of mycorrhizae and rusts. Mol. Ecol. 2:113-118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x Crossref, ISI, Google Scholar
- 2009. Alternaria cone disorder. Page 15 in: Compendium of hop diseases and pests. W. F. Mahaffee, S. J. Pethybridge, and D. H. Gent, eds. American Phytopathological Society, St. Paul, MN. Google Scholar
- 2013. Red crown rot of hop in Oregon caused by Phomopsis tuberivora. Plant Health Prog. 14:52. https://doi.org/10.1094/PHP-2013-0624-01-BR Link, Google Scholar
- 2009. Fungal diseases and pathogens of minor importance. Pages 36-38 in: Compendium of hop diseases and pests. W. F. Mahaffee, S. J. Pethybridge, and D. H. Gent, eds. American Phytopathological Society, St. Paul, MN. Google Scholar
- 2018. USA hops 2017 statistical report. Hop Growers of America. https://www.usahops.org Google Scholar
- 2020. USA hops 2019 statistical report. Hop Growers of America. https://www.usahops.org Google Scholar
- 1995. Development of primer sets designed for use with the PCR to amplify conserved genes from filamentous ascomycetes. Appl. Environ. Microbiol. 61:1323-1330. https://doi.org/10.1128/AEM.61.4.1323-1330.1995 Crossref, ISI, Google Scholar
- 2013. Diaporthe: A genus of endophytic, saprobic and plant pathogenic fungi. Persoonia 31:1-41. https://doi.org/10.3767/003158513X666844 Crossref, ISI, Google Scholar
- 1917. The British species of Phomopsis. Royal Botanic Gardens, Kew, UK. doi.org/10.2307/4113396 Crossref, Google Scholar
- 2003. A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst. Biol. 52:696-704. https://doi.org/10.1080/10635150390235520 Crossref, ISI, Google Scholar
- 1997. Sunflower diseases. Pages 263-379 in: Sunflower technology and production. A. A. Schneiter, ed. American Society of Agronomy, Madison, WI. Crossref, Google Scholar
- 1932. A new species of Phomopsis. Can. J. Res. 6:253-254. https://doi.org/10.1139/cjr32-017 Crossref, Google Scholar
- 2011. Phylogenetic trees made easy: A how-to manual. Oxford University Press, New York, NY. Google Scholar
- 1983. Diaporthe stem canker of sunflower. Plant Dis. 67:911-913. https://doi.org/10.1094/PD-67-911 Crossref, ISI, Google Scholar
- 2019. An emerging pathogen (Diaporthe sp.) of hop (Humulus lupulus) associated with foliar necrosis in commercial production yards in Michigan. Phytopathology 109:S2.111. ISI, Google Scholar
- 2017. Fungicides and cultivars can limit hop downy mildew (Pseudoperonospora humuli) in Michigan. Phytopathology 107:S5-S78. ISI, Google Scholar
- 2018. Effective management strategies for hop downy mildew (Pseudoperonospora humuli) in Michigan. Phytopathology 108:S2.28. Google Scholar
- 2015. Endophytic Diaporthe associated with Citrus: A phylogenetic reassessment with seven new species from China. Fungal Biol. 119:331-347. https://doi.org/10.1016/j.funbio.2015.02.006 Crossref, ISI, Google Scholar
- 2004. Phylogenetic analysis of Phytophthora species based on mitochondrial and nuclear DNA sequences. Fungal Genet. Biol. 41:766-782. https://doi.org/10.1016/j.fgb.2004.03.007 Crossref, ISI, Google Scholar
- 1988. Observations by scanning electron and bright-field microscopy on the mode of penetration of soybean seedlings by Phomopsis phaseoli. Plant Dis. 72:115-118. https://doi.org/10.1094/PD-72-0115 Crossref, ISI, Google Scholar
- 2003. Quantitative models for describing temperature and moisture effects on sporulation of Phomopsis amygdali on peach. Phytopathology 93:1165-1172. https://doi.org/10.1094/PHYTO.2003.93.9.1165 Link, ISI, Google Scholar
- 2001. Neolecta a fungal dinosaur? Evidence from β-tubulin amino acid sequences. Mycologia 93:1151-1163. ISI, Google Scholar
- 2015. Death of endemic Virgilia oroboides trees in South Africa caused by Diaporthe virgiliae sp. nov. Plant Pathol. 64:1149-1156. https://doi.org/10.1111/ppa.12341 Crossref, ISI, Google Scholar
- Mahaffee, W. F., and Engelhard, B. 2009. Gray mold. Pages 24-25 in: Compendium of hop diseases and pests. W. F. Mahaffee, S. J. Pethybridge, and D. H. Gent, eds. American Phytopathological Society, St. Paul, MN. Google Scholar
- Mahaffee, W. F., Pethybridge, S. J., and Gent, D. H., eds. 2009. Compendium of hop diseases and pests. American Phytopathological Society, St. Paul, MN. Google Scholar
- 2015. Phomopsis stem canker: A reemerging threat to sunflower (Helianthus annuus) in the United States. Phytopathology 105:990-997. https://doi.org/10.1094/PHYTO-11-14-0336-FI Link, ISI, Google Scholar
- 2018. Comparison of greenhouse-based inoculation methods to study aggressiveness of Diaporthe helianthi isolates causing Phomopsis stem canker of sunflower (Helianthus annuus). Plant Health Prog. 19:92-96. https://doi.org/10.1094/PHP-10-17-0059-RS Link, ISI, Google Scholar
- 2009. Red crown rot. Pages 31-32 in: Compendium of hop diseases and pests. W. F. Mahaffee, S. J. Pethybridge, and D. H. Gent, eds. American Phytopathological Society, St. Paul, MN. Google Scholar
- 2011. Identification of differentially expressed genes in a resistant versus a susceptible blueberry cultivar after infection by Colletotrichum acutatum. Mol. Plant Pathol. 12:463-477. https://doi.org/10.1111/j.1364-3703.2010.00687.x Crossref, ISI, Google Scholar
- 2010. Creating the CIPRES science gateway for inference of large phylogenetic trees. Pages1-8 in: Gateway Computing Environments Workshop (GCE), New Orleans, LA. IEEE, Washington, DC. https://doi.org/10.1109/GCE.2010.5676129 Google Scholar
- 2007. The M-Coffee web server: A meta-method for computing multiple sequence alignments by combining alternative alignment methods. Nucleic Acids Res. 35:W645-W648. https://doi.org/10.1093/nar/gkm333 Crossref, ISI, Google Scholar
- 1997. Two divergent intragenomic rDNA ITS2 types within a monophyletic lineage of the fungus Fusarium are nonorthologous. Mol. Phylo. Evol. 7:103-116. https://doi.org/10.1006/mpev.1996.0376 Crossref, ISI, Google Scholar
- 1977. Epidemiology and chemical control of Phomopsis canker of highbush blueberry. Phytopathology 67:484. ISI, Google Scholar
- 2001a. First report of Fusarium crookwellense causing tip blight on cones of hop. Plant Dis. 85:1208. https://doi.org/10.1094/PDIS.2001.85.11.1208A Link, ISI, Google Scholar
- 2001b. First report of infection of hop cones by Alternaria alternata in Australia. Plant Dis. 85:804. https://doi.org/10.1094/PDIS.2001.85.7.804B Link, Google Scholar
- 2006. An overview of fungal community diversity in diseased hop plantations. FEMS Microbiol. Ecol. 56:321-329. https://doi.org/10.1111/j.1574-6941.2006.00102.x Crossref, ISI, Google Scholar
- 1975. Septoria leaf disease of hops (Humulus lupulus) in Kashmir. Indian Phytopathol. 27:247-248. Google Scholar
- 2008. First report of Phoma exigua as a pathogen of hop in Slovenia. Plant Pathol. 57:381. https://doi.org/10.1111/j.1365-3059.2007.01672.x Crossref, ISI, Google Scholar
- 2009. Occurrence of Cercospora cantuariensis on hop in Austria and Slovenia. Plant Pathol. 58:400. https://doi.org/10.1111/j.1365-3059.2008.01962.x Crossref, ISI, Google Scholar
- 2017. Fungal identification using molecular tools: A primer for the natural products research community. J. Nat. Prod. 80:756-770. https://doi.org/10.1021/acs.jnatprod.6b01085 Crossref, ISI, Google Scholar
- 1997. ImageJ. National Institutes of Health, Bethesda, MD. https://imagej.nih.gov/ij/ Google Scholar
- 1994. Nuclear ribosomal internal transcribed spacer phylogeny and host diversity in the coelomycete Phomopsis. Can. J. Bot. 72:1666-1674. https://doi.org/10.1139/b94-204 Crossref, ISI, Google Scholar
- 2012. MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61:539-542. https://doi.org/10.1093/sysbio/sys029 Crossref, ISI, Google Scholar
- 1981. Downy mildew of the hop. Pages 395-419 in: The downy mildews. D. M. Spencer, ed. Academic Press, New York, NY. Google Scholar
- 1878. Fungi veneti novi vel critici vel mycologiae venetae addendi. [Translated with Cash 1965] Michelia 1:361-445. Google Scholar
- 1989. Molecular cloning: A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. Google Scholar
- 2010. Primers for mating-type diagnosis in Diaporthe and Phomopsis: Their use in teleomorph induction in vitro and biological species definition. Fungal Biol. 114:255-270. https://doi.org/10.1016/j.funbio.2010.01.007 Crossref, ISI, Google Scholar
- 2010. How to describe a new fungal species. IMA Fungus 1:109-116. https://doi.org/10.5598/imafungus.2010.01.02.02 Crossref, ISI, Google Scholar
- 1998. Histological observations of latent infection and tissue colonization by Diaporthe toxica in resistant and susceptible narrow-leafed lupins. Can. J. Bot. 76:1305-1316. Google Scholar
- 2010. Quantification of the Alternaria mycotoxin tenuazonic acid in beer. Food Chem. 120:902-906. https://doi.org/10.1016/j.foodchem.2009.10.070 Crossref, ISI, Google Scholar
- 2002. Alternaria themes and variations (305-309) Lewia/Alternaria revisited. Mycotaxon 83:127-145. ISI, Google Scholar
- 1984. Ascochyta leaf spots on fig and hop. New records for India. Indian J. Mycol. Plant Pathol. 14:100. Google Scholar
- 2010. Sustainable hop production in the Great Lakes region [E3083]. Michigan State University, MSU Extension, East Lansing, MI. Google Scholar
- 2014. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312-1313. https://doi.org/10.1093/bioinformatics/btu033 Crossref, ISI, Google Scholar
- 2000. Phoma glomerata as a mycoparasite of powdery mildew. Appl. Environ. Microbiol. 66:425-427. https://doi.org/10.1128/AEM.66.1.425-427.2000 Crossref, ISI, Google Scholar
- 2013. Molecular phylogenetic analysis reveals six new species of Diaporthe from Australia. Fungal Divers. 61:251-260. https://doi.org/10.1007/s13225-013-0242-9 Crossref, ISI, Google Scholar
- 2003. Alternaria spp.: From general saprophyte to specific parasite. Mol. Plant Pathol. 4:225-236. https://doi.org/10.1046/j.1364-3703.2003.00173.x Crossref, ISI, Google Scholar
- 2015. Green and brown bridges between weeds and crops reveal novel Diaporthe species in Australia. Persoonia 35:39-49. https://doi.org/10.3767/003158515X687506 Crossref, ISI, Google Scholar
- 2016. Black wilt of hop (Humulus lupulus) caused by Diplodia seriata in New York State. Plant Dis. 100:861. https://doi.org/10.1094/PDIS-10-15-1140-PDN Link, ISI, Google Scholar
- 2015. Development of partial ontogenic resistance to powdery mildew in hop cones and its management implications. PLoS One 10:e0120987. https://doi.org/10.1371/journal.pone.0120987 Crossref, ISI, Google Scholar
- 2014. Insights into the genus Diaporthe: Phylogenetic species delimitation in the D. eres species complex. Fungal Divers. 67:203-229. https://doi.org/10.1007/s13225-014-0297-2 Crossref, ISI, Google Scholar
- 2015. The Diaporthe sojae species complex: Phylogenetic re-assessment of pathogens associated with soybean, cucurbits and other field crops. Fungal Biol. 119:383-407. https://doi.org/10.1016/j.funbio.2014.10.009 Crossref, ISI, Google Scholar
- 2012. A multi-locus phylogenetic evaluation of Diaporthe (Phomopsis). Fungal Divers. 56:157-171. https://doi.org/10.1007/s13225-012-0190-9 Crossref, ISI, Google Scholar
- 1990. Species concepts in some larger genera of the Coelomycetes. Stud. Mycol. 32:3-19. Google Scholar
- 2006. M-Coffee: Combining multiple sequence alignment methods with T-Coffee. Nucleic Acids Res. 34:1692-1699. https://doi.org/10.1093/nar/gkl091 Crossref, ISI, Google Scholar
- 1990. Phomopsis (coelomycetes) species on Compositae and Umbelliferae: A critical evaluation of characters with keys. Linz. Biol. Beitr. 22:161-173. Google Scholar
- 1926. A biologic and phylogenetic study of the stromatic Sphaeriales. Am. J. Bot. 13:575-645. https://doi.org/10.1002/j.1537-2197.1926.tb05903.x Crossref, Google Scholar
- 1933. The genus Diaporthe Nitschke and its segregates. University of Michigan Press, Ann Arbor, MI. Google Scholar
- 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. Pages 315-322 in: PCR protocols: A guide to methods and applications. Vol. 18. M. A. Innis, D. H. Gelfand, J. J. Sninsky, and T. J. White, eds. Academic Press, San Diego, CA. https://doi.org/10.1016/B978-0-12-372180-8.50042-1 Google Scholar
- 1991. Formation of subcuticular coralloid hyphae by Phomopsis leptostromiformis upon latent infection of narrow-leafed lupins. Plant Dis. 75:1023-1026. https://doi.org/10.1094/PD-75-1023 Crossref, ISI, Google Scholar
- 2013. Alternaria redefined. Stud. Mycol. 75:171-212. https://doi.org/10.3114/sim0015 Crossref, ISI, Google Scholar
- 2009. A new species of Alternaria on Humulus scandens from China. Mycotaxon 108:49-52. https://doi.org/10.5248/108.49 Crossref, ISI, Google Scholar

