Adaptation to Partial Resistance to Powdery Mildew in the Hop Cultivar Cascade by Podosphaera macularis

The hop cultivar Cascade has been grown in the Pacific Northwestern U.S. and elsewhere with minimal input for management of powdery mildew (Podosphaera macularis) for nearly 15 years due to the putatively quantitative resistance in this cultivar. While partial resistance is generally thought to be more durable than qualitative resistance, in 2012, powdery mildew was reported on Cascade in Washington State. Field surveys conducted during 2013 to 2016 indicated increasing prevalence of powdery mildew on Cascade, as well as an increasing number of fungicide applications applied to this cultivar in Washington State. Nearly all isolates of P. macularis tested were able to infect Cascade in laboratory inoculations. However, the greatest number of colonies, most conidia produced, and the shortest latent period was only observed with isolates derived originally from Cascade, as compared with other isolates derived from other cultivars. Further, the enhanced aggressiveness of these isolates was only manifested on Cascade and not six other susceptible cultivars, further indicating a specific adaptation to Cascade by the isolates. There was no evidence of a known major R-gene in Cascade, as seven isolates of P. macularis with contrasting virulence all infected Cascade. Among 158 isolates obtained from hop yards planted to Cascade, only two (1.3%) were able to infect the cultivar Nugget, which possesses the resistance factor termed R6, indicating that isolates of P. macularis virulent on Nugget are largely distinct from those adapted to Cascade. Further, race characterization indicated Cascade-adapted isolates of P. macularis were able to overcome R-genes Rb, R3, and R5, but not other known R-genes. Therefore, multiple R-genes and other sources of partial resistance are expected to provide resistance to Cascade-adapted strains of the fungus. Given the plasticity of the powdery mildew fungus, breeding strategies for powdery mildew need to consider the potential for adaptation to both qualitative and partial resistance in the host.

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Risk Factors for Bud Perennation of Podosphaera macularis on Hop

Phytopathology ◽

10.1094/phyto-04-18-0127-r ◽

2019 ◽

Vol 109 (1) ◽

pp. 74-83 ◽

Cited By ~ 3

Author(s):

David H. Gent ◽

Walter F. Mahaffee ◽

William W. Turechek ◽

Cynthia M. Ocamb ◽

Megan C. Twomey ◽

...

Keyword(s):

Risk Factors ◽

Powdery Mildew ◽

Early Spring ◽

Winter Temperature ◽

Posterior Density ◽

Powdery Mildew Fungus ◽

Production Region ◽

The Pacific ◽

Highest Posterior Density ◽

Podosphaera Macularis

The hop powdery mildew fungus Podosphaera macularis persists from season to season in the Pacific Northwestern United States through infection of crown buds because only one of the mating types needed to produce the ascigerous stage is presently found in this region. Bud infection and successful overwintering of the fungus leads to the emergence of heavily infected shoots in early spring (termed flag shoots). Historical data of flag shoot occurrence and incidence in Oregon and Washington State during 2000 to 2017 were analyzed to identify their association with the incidence of powdery mildew, growers’ use of fungicides, autumn and winter temperature, and other production factors. During this period, flag shoots were found on 0.05% of plants evaluated in Oregon and 0.57% in Washington. In Oregon, the incidence of powdery mildew on leaves was most severe and the number of fungicide applications made by growers greatest in yards where flag shoots were found in spring. Similarly, the incidence of plants with powdery mildew in Washington was significantly associated with the number of flag shoots present in early spring, although the number of fungicide applications made was independent of flag shoot occurrence. The occurrence of flag shoots was associated with prior occurrence of flag shoots in a yard, the incidence of foliar powdery mildew in the previous year, grower pruning method, and, in Washington, winter temperature. A census of hop yards in the eastern extent of the Oregon production region during 2014 to 2017 found flag shoots in 27 of 489 yards evaluated. In yards without flag shoots, 338 yards (73.2%) were chemically pruning or not pruned, whereas the remaining 124 (26.8%) were mechanically pruned. Of the 27 yards with flag shoots, 22 were either chemically pruned or not pruned and 4 were mechanically pruned in mid-April, well after the initial emergence of flag shoots. The prevalence of yards with flag shoots also was related to thoroughness of pruning in spring (8.1% of yards with incomplete pruning versus 1.9% of yards with thorough pruning). A Bayesian logistic regression model was fit to the data from the intensively assessed yards in Oregon, with binary risk factors for occurrence of a flag shoot in the previous year, occurrence of foliar mildew in the previous year, and thoroughness of pruning in spring. The model indicated that the median and 95% highest posterior density interval of the probability of flag shoot occurrence was 0.0008 (0.0000 to 0.0053) when a yard had no risk factors but risk increased to 0.0065 (0.0000 to 0.0283) to 0.43 (0.175 to 0.709) when one to all three of the risk factors were present. The entirety of this research indicates that P. macularis appears to persist in a subset of chronically affected hop yards, particularly yards where spring pruning is conducted poorly. Targeted management of the disease in a subset of fields most at risk for producing flag shoots could potentially influence powdery mildew development regionwide.

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Erysiphe trifolii Causing Powdery Mildew of Lentil (Lens culinaris)

Plant Disease ◽

10.1094/pdis-93-8-0797 ◽

2009 ◽

Vol 93 (8) ◽

pp. 797-803 ◽

Cited By ~ 22

Author(s):

Renuka N. Attanayake ◽

Dean A. Glawe ◽

Frank M. Dugan ◽

Weidong Chen

Keyword(s):

Powdery Mildew ◽

Pacific Northwest ◽

The United States ◽

Morphological Characters ◽

Grain Legumes ◽

Its Sequences ◽

Powdery Mildew Fungus ◽

The Pacific ◽

Soybean Genotypes ◽

Erysiphe Trifolii

The taxonomy of the powdery mildew fungus infecting lentil in the Pacific Northwest (PNW) of the United States was investigated on the basis of morphology and rDNA internal transcribed spacer (ITS) sequences. Anamorphic characters were in close agreement with descriptions of Erysiphe trifolii. However, teleomorphs formed chasmothecial appendages with highly branched apices, whereas E. trifolii has been described as producing flexuous or sometimes loosely branched appendages. Branched appendages have been described in Erysiphe diffusa, a fungus reported from species of Lens, Glycine, and Sophora, raising the possibility that the PNW fungus could be E. diffusa. Examination of morphological characters of an authentic specimen of E. trifolii from Austria determined that it included chasmothecial appendages resembling those seen in PNW specimens. Furthermore, ITS sequences from five powdery mildew samples collected from lentils in PNW greenhouses and fields from 2006 to 2008 were identical to one another, and exhibited higher similarity to sequences of E. trifolii (99%) than to those of any other Erysiphe spp. available in GenBank. Parsimony analysis grouped the lentil powdery mildew into a clade with Erysiphe baeumleri, E. trifolii, and E. trifolii–like Oidium sp., but indicated a more distant relationship to E. diffusa. In greenhouse inoculation studies, the lentil powdery mildew fungus did not infect soybean genotypes known to be susceptible to E. diffusa. The pathogenicity of E. trifolii on lentil was confirmed using modified Koch's postulates. This is the first report of E. trifolii infecting lentil. E. diffusa and E. trifolii have different host ranges, so the discovery of E. trifolii on lentil has implications both for determining species of powdery mildews on cool-season grain legumes, and in disease management.

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Identification of Resistance to Powdery Mildew in Publicly Available Male Hop Germplasm

Plant Health Progress ◽

10.1094/php-05-18-0027-rs ◽

2018 ◽

Vol 19 (3) ◽

pp. 258-264

Author(s):

David H. Gent ◽

Briana J. Claassen ◽

Megan C. Twomey ◽

Sierra N. Wolfenbarger

Keyword(s):

United States ◽

Powdery Mildew ◽

Pacific Northwest ◽

Western United States ◽

R Genes ◽

Sources Of Resistance ◽

Department Of Agriculture ◽

Breeding Programs ◽

The Pacific ◽

The U.S

Powdery mildew (caused by Podosphaera macularis) is one of the most important diseases of hop in the western United States. Strains of the fungus virulent on cultivars possessing the resistance factor termed R6 and the cultivar Cascade have become widespread in the Pacific Northwestern United States, the primary hop producing region in the country, rendering most cultivars grown susceptible to the disease at some level. In an effort to identify potential sources of resistance in extant germplasm, 136 male accessions of hop contained in the U.S. Department of Agriculture collection were screened under controlled conditions. Iterative inoculations with three isolates of P. macularis with varying race identified 23 (16.9%) accessions with apparent resistance to all known races of the pathogen present in the Pacific Northwest. Of the 23 accessions, 12 were resistant when inoculated with three additional isolates obtained from Europe that possess novel virulences. The nature of resistance in these individuals is unclear but does not appear to be based on known R genes. Identification of possible novel sources of resistance to powdery mildew will be useful to hop breeding programs in the western United States and elsewhere.

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Responding to an Introduced Pathogen: Podosphaera macularis (Hop Powdery Mildew) in the Pacific Northwest

Plant Health Progress ◽

10.1094/php-2003-1113-07-rv ◽

2003 ◽

Vol 4 (1) ◽

pp. 21 ◽

Cited By ~ 10

Author(s):

Walter F. Mahaffee ◽

Carla S. Thomas ◽

William W. Turechek ◽

Cynthia M. Ocamb ◽

Mark E. Nelson ◽

...

Keyword(s):

Powdery Mildew ◽

Pacific Northwest ◽

Management Practices ◽

Risk Index ◽

Lessons Learned ◽

Infection Model ◽

The Pacific ◽

Sphaerotheca Macularis ◽

The Cost ◽

Podosphaera Macularis

Powdery mildew of hop (Humulus lupus L.), which is caused by Podosphaera macularis (formerly Sphaerotheca macularis) was found in the Yakima Valley, WA in 1996 and subsequently spread to the growing regions in Oregon and northern and southern Idaho. To rapidly assist growers in reducing the cost associated with the preventive fungicide program, the Gubler/Thomas grape powdery mildew risk infection model was adapted for hops. In addition, field surveys were utilized to identify other management practices that impacted disease development. Weather networks were established and utilized to deliver daily regional maps indicating the risk index. These maps were posted to the web for daily access. Lessons learned from this experience will be useful in addressing future pathogen introductions. Accepted for publication 28 March 2003. Published 13 November 2003.

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Powdery Mildew Outbreaks caused by Podosphaera macularis on Hop Cultivars Possessing the Resistance Gene R6 in the Pacific Northwestern United States

Plant Disease ◽

10.1094/pdis-11-13-1127-pdn ◽

2014 ◽

Vol 98 (6) ◽

pp. 852-852 ◽

Cited By ~ 4

Author(s):

S. N. Wolfenbarger ◽

E. B. Eck ◽

C. M. Ocamb ◽

C. Probst ◽

M. E. Nelson ◽

...

Keyword(s):

United States ◽

Powdery Mildew ◽

Resistance Genes ◽

Washington State ◽

Cultural Control ◽

Control Measures ◽

Crop Damage ◽

Resistant Cultivars ◽

Virulent Strains ◽

The Pacific

Resistant cultivars of hop (Humulus lupulus) have been grown, with the aim of helping to manage powdery mildew in the Pacific Northwest since the first report of the disease in the field in 1997 (4). A major objective of many breeding programs is development of resistance to powdery mildew, and this has generally been achieved by single resistance genes (qualitative resistance). One such gene, R6 (3), has been utilized extensively in new cultivars and has prevented epidemics of the disease in those cultivars across the Pacific Northwestern United States for approximately 15 years. In 2011, a grower in Washington State reported outbreaks of powdery mildew on cv. Apollo, which is thought to possess powdery mildew resistance derived from R6. Fungicides and cultural control measures were applied, and the grower reported no substantial crop damage from the disease. During the winter of 2012, the same grower planted rhizomes of cv. Apollo in a greenhouse in the Yakima Valley of Washington State and later found the plants to be affected by powdery mildew. Affected leaves from plants of cvs. Apollo, Newport, and Nugget (all reported [3] or assumed to possess R6 based on pedigree) grown in the same greenhouse were later provided to the authors. Conidia obtained from each affected plants were transferred to plants of the highly susceptible cv. Symphony, which is not known to contain any resistance genes. After 10 to 14 days of incubation, resultant conidia from each cultivar above (total of three isolates) were transferred to greenhouse grown plants of cvs. Nugget and Symphony and incubated at 18°C. Within 7 days, all three isolates produced powdery mildew colonies characteristic of P. macularis (2) on both cultivars. Cleistothecia did not develop in any colonies. In addition, Nugget and Symphony plants were inoculated with a field population of P. macularis originating from cultivars lacking R6 in Oregon. These inoculations on Nugget did not develop powdery mildew whereas Symphony plants did. Non-inoculated controls remained free of powdery mildew. Results were identical in two additional experiments. The sequence of the mating type idiomorph, MAT1-1, was obtained to confirm identity of the pathogen as P. macularis as described previously (1). The sequences were identical among the three isolates obtained from the greenhouse in Washington and isolates of P. macularis obtained previously from Oregon and Washington. MAT1-2 idiomorph was not detected in the isolates collected. While R6-virulent strains have been detected previously in race characterization experiments, these strains have not caused widespread epidemics of powdery mildew. The increasing prevalence of virulent strains of P. macularis and outbreaks of powdery mildew on formerly resistant cultivars necessitates changes in breeding strategies and disease management efforts to minimize damage resulting from the disease. The distribution of virulent strains of the pathogen and susceptibility of formerly resistance cultivars to powdery mildew are currently under investigation. References: (1) B. Asalfet et al. Phytopathology 103:717, 2013. (2) R. Bélanger et al. The Powdery Mildews: a Comprehensive Treatise. APS Press, St. Paul, MN, 2002. (3) P. Darby. Brew Hist. 121:94, 2005. (4) C. Ocamb et al. Plant Dis. 83:1072, 1999.

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First Report of Powdery Mildew of Myosotis sylvatica (Wood Forget-me-not) Caused by Golovinomyces cynoglossi (Erysiphe cynoglossi) in Washington State

Plant Health Progress ◽

10.1094/php-2004-1124-01-hn ◽

2004 ◽

Vol 5 (1) ◽

pp. 18

Author(s):

Dean A. Glawe

Keyword(s):

Powdery Mildew ◽

Pacific Northwest ◽

Washington State ◽

Causal Organism ◽

First Report ◽

The Pacific ◽

Western Washington ◽

Symptoms And Signs

Wood forget-me-not cultivars are popular ornamentals in the Pacific Northwest. In western Washington, this species frequently displays symptoms and signs of powdery mildew after anthesis. This report records the disease from King, Pierce, Snohomish, and Skagit counties and describes and illustrates symptoms of the disease as well as taxonomically important features of the causal organism. Accepted for publication 29 October 2004. Published 24 November 2004.

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First Report of Powdery Mildew of Eschscholzia californica (California Poppy) caused by Erysiphe cruciferarum in North America

Plant Health Progress ◽

10.1094/php-2006-1213-01-br ◽

2006 ◽

Vol 7 (1) ◽

pp. 45 ◽

Cited By ~ 1

Author(s):

Dean A. Glawe

Keyword(s):

North America ◽

Powdery Mildew ◽

Pacific Northwest ◽

Ongoing Study ◽

Annual Species ◽

Powdery Mildew Fungus ◽

First Report ◽

California Poppy ◽

The Pacific ◽

Erysiphe Cruciferarum

California poppy is an annual species grown widely in the Pacific Northwest. Once established, populations are self-seeding and require little care. During an ongoing study of Erysiphales, a powdery mildew fungus was collected repeatedly on this species in Seattle, WA. The fungus was determined to be Erysiphe cruciferarum Opiz ex Junell, a species not reported previously on this host in North America. This report documents the occurrence of the disease and provides information on the morphology and identification of the causal agent. Accepted for publication 8 November 2006. Published 13 December 2006.

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Temperature Influences on Powdery Mildew Susceptibility and Development in the Hop Cultivar Cascade

Plant Disease ◽

10.1094/pdis-10-21-2133-re ◽

2022 ◽

Author(s):

David H. Gent ◽

Briana Claassen ◽

Michele S. Wiseman ◽

Sierra N Wolfenbarger

Keyword(s):

Powdery Mildew ◽

Partial Resistance ◽

Disease Risk ◽

Rapid Onset ◽

Risk Assessments ◽

Temperature Regimes ◽

Moderate Disease ◽

Ontogenic Resistance ◽

Specific Temperature ◽

Podosphaera Macularis

The hop cultivar Cascade possesses partial resistance to powdery mildew (Podosphaera macularis) that can be overcome by recently emerged, virulent isolates of the fungus. Given that hop is a long-lived perennial and that brewers still demand Cascade, there is a need to better understand factors that influence the development of powdery mildew on this cultivar. Growth chamber experiments were conducted to quantify the effect of constant, transient, and fluctuating temperature on Cascade before, concurrent to, and after inoculation as contrasted with another powdery mildew susceptible cultivar, Symphony. Exposure of plants to supraoptimal temperature (26 and 32°C) prior to inoculation led to more rapid onset of ontogenic resistance in intermediately aged leaves in Cascade as compared to Symphony. Cascade was overall less susceptible to powdery mildew when exposed to constant temperature ranging from 18 to 32°C directly after inoculation. However, cultivar also interacted with temperature such that proportionately fewer and smaller colonies developed on Cascade than Symphony at supraoptimal yet permissive temperatures for disease. When plants were inoculated and then exposed to high temperature, colonies became progressively more tolerant to temperatures of 26 to 30°C with increasing time from inoculation to exposure, as moderated by cultivar, the specific temperature, and their interaction. Subjecting plants to simulated diurnal temperature regimes at the time of inoculation or 24 h later indicated Cascade and Symphony responded proportionately similar on days predicted to be marginally unfavorable or marginally favorable for powdery mildew, although Cascade was quantitatively less susceptible than Symphony. In sum, this research indicates that Cascade is overall less susceptible to powdery mildew than Symphony, and supraoptimal temperature before, concurrent to, or after infection may interact differentially to moderate disease risk in Cascade. Therefore, cultivar-specific risk assessments for powdery mildew appear warranted.

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Hop Powdery Mildew Control Through Alteration of Spring Pruning Practices

Plant Disease ◽

10.1094/pdis-10-15-1127-re ◽

2016 ◽

Vol 100 (8) ◽

pp. 1599-1605 ◽

Cited By ~ 8

Author(s):

Claudia Probst ◽

Mark E. Nelson ◽

Gary G. Grove ◽

Megan C. Twomey ◽

David H. Gent

Keyword(s):

Powdery Mildew ◽

Pacific Northwest ◽

Low Cost ◽

Specific Effect ◽

Disease Development ◽

Quality Factors ◽

Early Season ◽

Yield And Quality ◽

The Pacific ◽

Podosphaera Macularis

Podosphaera macularis, the causal agent of hop powdery mildew, is a recurrent threat to hops in the Pacific Northwest because of the potential to reduce cone yield and quality. Early-season pruning is a common practice in hop production for horticultural reasons. Studies were conducted over a 3-year period in a commercial hop yard to quantify the effect of pruning method and timing on disease development, yield, and cone quality factors. A 4-week delay in pruning reduced the incidence of leaves with powdery mildew from 46 to 10% and cones from 9 to 1%, with the specific effect being season dependent. Pruning using chemical desiccants rather than by mechanical means had similar effects on disease levels on leaves. On cones, though, chemical pruning had a small but significant reduction in the incidence of powdery mildew compared with mechanical pruning. Cone yield, levels of bittering-acids, and color were not negatively affected in any individual year or cumulatively over three seasons when pruning treatments were applied repeatedly to the same plots during the study period. Delayed pruning may offer a low-cost means of reducing both the incidence of powdery mildew and early-season fungicide inputs in certain cultivars.

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