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© 2009 Plant Management Network.
Accepted for publication 3 October 2008. Published 16 January 2009.


Hop Stunt Decline: A Disease or Disorder of Unknown Aetiology in Australian Hop Yards


Sarah J. Pethybridge, Botanical Resources Australia, Agricultural Services Pty. Ltd., Ulverstone, Tasmania, 7315, Australia; Patricia McGee, Australian Food and Grocery Council, Kingston, Australian Capital Territory, 2604, Australia; and Peter Hamilton, Hop Products Australia, Bellerive, Tasmania 7018, Australia


Corresponding author: Sarah J. Pethybridge. Sarah.Pethybridge@gmail.com


Pethybridge, S. J., McGee, P., and Hamilton, P. 2009. Hop stunt decline: A disease or disorder of unknown aetiology in Australian hop yards. Online. Plant Health Progress doi:10.1094/PHP-2009-0116-01-RS.


Abstract

Hop stunt decline was first observed in commercial hop yards in northeastern Tasmania in 1991. Over the next seven years, the incidence of hop stunt decline increased and reductions in cone yield were estimated to be approximately 30%. Symptoms of hop stunt decline include retarded spring growth, reduced burr production in summer, prolific lateral branching, and progressively shorter internodes on the main bine, and lateral branches which give the plant a “pine-tree” appearance. Final height of affected plants was between one-half to two-thirds of normal growth. Despite extensive investigations over 10 years, the cause of this problem has not been elucidated. However, the role of herbicides, soil physical properties, all described viruses and viroids affecting hop, phytoplasmas, deficiencies of molybdenum, manganese, boron and zinc, plant-parasitic nematodes, and soil-borne fungal diseases have been excluded. Planting with resistant (or tolerant) cultivars was successful at alleviating hop stunt decline.


Introduction

Hops (Humulus lupulus L.; Family Cannabinaceae) are grown on approximately 500 hectares in two states of Australia, Victoria and Tasmania, supplying both domestic and export markets. The plant is a climbing, dioecious perennial, grown predominantly for the production of cones (strobiles) that contain glands producing resins, essential oils, and polyphenols used primarily to add bitterness and aroma to beer (11).

Hop stunt decline was first observed in January 1991 at two hop farms in northeastern Tasmania (41°15’S, 147°52’E). The disease/disorder was first noticed when plants failed to reach the top of the trellis (6.5 m) in a large area within the center of a single yard at one farm, and along two narrow strips within a low-lying area of two additional yards at another farm. Yards initially affected by hop stunt decline varied between 14 and 28 years old, and spread within yards was noted. Within five years, hop stunt decline had been reported in several yards at an additional farm 200 km from the location of the original description.

Plants affected by hop stunt decline were slow to initiate growth at the beginning of the season and the development of female flowers (burr) was significantly retarded. Affected plants typically only reached one-half to two-thirds of normal height and internode length was reduced progressively towards the top of the plant on the main bine. Internode length was also progressively reduced on the lateral branches, which were produced prolifically. The reduced internode length towards the terminal end of the main bine and laterals lead to an accumulation of leaf and flower buds and the appearance of a thickened “fluffy tip” (Figs. 1 and 2). Basal growth later in the season was typically profuse on affected plants. Leaves on affected plants were smaller and darker than normal, turn upward, and occasionally appeared distorted, such as having a reduced central lobe (Fig. 3). The leaves sometimes appeared crinkled and had sharp-toothed crenations. Overall, this growth habit gave the affected plants a ‘pine tree’ appearance.


 

Fig. 1. Reduced lateral growth and internode elongation in plants affected by hop stunt decline (right) compared to laterals from healthy plants (left).

 

 

Fig. 2. Progressive shortening of internodes and accumulation into a ‘fluffy tip’ of a lateral branch on a plant affected by hop stunt decline.

 

Fig. 3. Reduced central lobe on a young leaf from a plant affected by hop stunt decline.


In the 1940s, similar symptoms of hop stunt decline were described in commercial yards of ‘Fuggle’ and ‘Goldings’ in the United Kingdom. Here symptoms became apparent over four days in late June, and were described as a “sudden check” to the growth of the main bine when it was approximately one meter from the top of the trellis. The tip of the main bine became stiff and stood away from the string, internodes were shortened, leaves distorted and reduced in size, and stipules were prominent. In some yards, up to 50% of plants were affected. In the majority of cases, bines overcame the problem and growth continued but shortened internodes remained where the growth reduction occurred. However, in some cases, the tip of the affected bines failed to grow further. Although the cause was never identified, adverse weather conditions were implicated as prior to symptom onset there were 14 days of abnormally cool weather followed by very high temperatures (8). In another instance, similar symptoms, described as “fluffy tip,” were reported in two-year-old boron-deficient plants grown in sand culture (3).

Only two Australian-bred hop cultivars have been documented as susceptible to hop stunt decline, ‘Pride of Ringwood’ and ‘Victoria,’ with the “fluffy tip” symptom being more pronounced in the former. Symptomatic plants have not been found in cultivars ‘Willamette,’ ‘Nugget,’ and ‘Topaz’ planted in affected yards. Extensive investigations to determine the cause of hop stunt decline and identify management strategies to minimize losses have been conducted. Although no conclusive results on the cause of this problem were identified, it is hoped the findings reported herein may be useful if encountered elsewhere. Farms affected by hop stunt decline in Australia have now been abandoned due predominantly to world-wide economic pressures of the hop market between 2003 and 2005 involving over-supply and low prices.


Effect of Hop Stunt Decline on Yield

The effect of hop stunt decline on cone yield and levels of alpha and beta acids was characterized in a replicated field trial containing 10 single-plant plots that were established either by softwood cuttings taken from stunt-affected or healthy plants. The procedures for making and establishing softwood cuttings has been described (13). Plants were spaced at 1.8 m along rows and 2.1 m across rows. All management operations (e.g., fertilizer and herbicide application) were as for a commercial hop yard. Procedures used to conduct comparisons in cone yield and levels of alpha and beta acids have been described (13,14).

In the first year, cones produced on plants affected by hop stunt decline were slightly larger or heavier than on healthy plants. Since cone yield is measured by weight, rather than the number of cones, yield was not significantly affected by hop stunt decline due to compensatory effects of increased individual cone size for fewer cones being produced. This may have resulted from additional light being available to the cones. In subsequent seasons, comparisons between affected and healthy plants suggested significant reductions in cone yield of approximately 30%. Hop stunt decline was not found to significantly affect alpha and beta acid levels.


Role of Soil Physical Properties and Nutrients in Hop Stunt Decline

The structural profile of the soil in affected and healthy areas within and between yards was examined in 2-m pits. No differences in the soil structure of the pits, evidence of waterlogging (mottling in the soil profile reflecting iron oxidation), nor impeding layers were observed. Hop root growth continued to significant depths (1.5 to 1.8 m), and showed no evidence of death throughout the profile.

Soil nutrient testing was also conducted at four farms in healthy and stunt-affected areas from 0 to 10 cm and 10 to 20 cm depths by the State Chemistry Laboratory of Tasmania, using standard protocols. All nutrient and organic matter levels were considered adequate for hop growth, with the exception of a higher pH than the adequate 6.0 to 6.5 range in 75% of samples in both healthy and stunt-affected areas, and high (> 40 mg/kg) levels of soil phosphorus in 90% of samples, also occurring in both healthy and stunt-affected areas. High levels of phosphorus may contribute to reduced uptake of zinc and decrease manganese availability (3). Manganese levels varied between 33 and 71 mg/kg across both healthy and stunt-affected areas, and a small number of plants (< 1%) exhibited foliar symptoms similar to manganese deficiency, across both healthy and stunt-affected areas. Boron levels varied between 17 and 25 mg/kg across both healthy and stunt-affected areas, which are considered marginal to low for hop production (3). The role of poor soil structure and associated problems with waterlogging at depth, changes in nutrient availability, and anaerobic conditions from ethylene producing micro-organisms in hop stunt decline were therefore considered unlikely. This hypothesis was further supported considering that affected plants appeared seemingly simultaneously at geographically separated farms.


Role of Boron Deficiency in Hop Stunt Decline

Askew and Monk (1,2) described boron deficiency symptoms in hop as reduced development of new shoots, crinkling of the leaves, reduced internode length, and early lateral development. In Germany and New Zealand, death of the growing point on the main bine was also observed in boron-deficient hop plants. Symptoms in the United Kingdom were described as rigidity in the young tips of the bines which had smaller leaves, large stipules, and shortened internodes (4,5). The role of boron deficiency in hop stunt decline in Australian hop yards was investigated in field and pot trials. A field trial was established in a stunt-affected 12-year-old yard of cultivar Pride of Ringwood. The experimental design was completely randomised and each treatment with five treatments and a nontreated control with each treatment being replicated four times, and each replicate comprising of six plants (3 plants along each row of 2 rows). Treatments included: three applications of Solubor (20.5% B) applied either to the soil at two rates (4.5 and 2.3 kg/ha), to the foliage at two rates (80 and 150 g/ha), or as a combination to the foliage (150 g/ha) and soil (2.3 kg/ha). These treatments were applied in early spring (September) in each of two years (2001 and 2002). The effect of boron application on the ability of plants to reach the top of the trellis and the incidence of hop stunt decline symptoms between 5 and 10 January 2002 and 2003 (both expressed as percentage of plants affected within each treatment block) was assessed by analysis of variance using Genstat 10 Version 1 (Adept Scientific Ltd., Bethesda, MD). The incidence of stunt-affected hop plants across the entire trial area was 48%. No significant decreases in the incidence of plants reaching the trellis top (P = 0.654) and incidence of hop stunt decline symptoms (P = 0.789) were found from boron supplements over both years.


Role of Viruses, Viroids, and Phytoplasmas

Viruses, viroids, and phytoplasmas have been discounted as the cause of hop stunt decline. First, when cuttings were taken from affected plants and planted into yards where hop stunt decline had not been found, mature plants remained asymptomatic. Moreover, 80% of cuttings taken from both affected and healthy hop plants that were re-planted into yards where affected plants had been found became symptomatic. Extensive virus testing of over 500 affected and healthy plants for reported viruses infecting hop, including Hop mosaic virus (HpMV), Hop latent virus (HpLV), Arabis mosaic virus-hop strain (ArMV-H), Strawberry latent ringspot virus (SLRV), Apple mosaic virus (ApMV), Tobacco necrosis virus (TNV), Cucumber mosaic virus (CMV), and American hop latent virus (AHLV) (12,17), found high incidences of those viruses found in Australia (i.e., HpMV, HpLV, and ApMV) (14,15), and absence of the non-endemic viruses. Methodology used for virus testing has been described (15). Testing for Hop latent viroid (HpLVd) demonstrated a ubiquitous distribution within both stunt-affected and healthy areas. Hop stunt viroid (HpSVd) was not found in stunt-affected and healthy plants, and is considered exotic to Australian hop yards (17,19). The role of phytoplasmas in hop stunt decline has also been discounted following testing using universal PCR primers specific to highly conserved 16S rRNA gene sequences (9). The only report of phytoplasma infection in hop is associated with hop shoot proliferation disease in Poland and associated with marked differences in symptomatology (18).


Role of Other Plant Pathogens

No symptoms consistent with known fungal plant pathogens of hop are known to cause disease similar to those observed on plants affected by hop stunt decline. The predominant plant-parasitic nematode associated with hop production world-wide, the hop cyst nematode (Heterodera humuli Filipjev 1934), was found at similar population densities (1800 to 2100 H. humuli second-stage juveniles in early spring) in both stunt-affected and healthy yards and therefore its role in hop stunt decline was discounted (7). Moreover, nematicide application significantly reduced populations of plant-parasitic nematodes but did not significantly reduce the incidence of stunt-affected plants. Other plant-parasitic nematodes found in low numbers in both stunt-affected and healthy areas were Heliocotylenchus dihystera, Paratylenchus spp., Pratylenchus spp., and Meloidogyne spp. (root knot nematode) (7).


Role of Herbicides

The role of the residual herbicide simazine in hop stunt decline was also investigated. Simazine is a selective herbicide absorbed through the roots and is translocated acropetally in the xylem, accumulating in the apical meristem and leaves (21). Simazine is used in Australian hop yards in early spring for weed control. Simazine levels in soil collected to depths of 2 m from healthy areas averaged 0.3 mg/kg (pH 5.5), whilst in affected areas concentrations averaged 0.2 mg/kg (pH 6.7). Little information is available on the critical limits for hop production and results were inconclusive due to the similarities in levels between stunt-affected and healthy areas. No additional triazine chemicals were detected in samples from either area.

As forestry plantations were located in close proximity (< 5 km away from the affected yards), herbicides used commonly in tree production were also assessed for their potential role in hop stunt decline. For example, in the same year that hop stunt decline was first reported, surrounding forestry plantations had been harvested in the previous winter and sprayed with hexazinone, which spreads easily in ground water and aerially (4). However, testing of 125 samples from affected farms and throughout the entire catchment was unable to detect hexazinone in ground water, suggesting this was not related to the onset of hop stunt decline.


Spatial Pattern of Hop Stunt Decline

To develop hypotheses on the cause of hop stunt decline, spatial patterns of affected plants were intensively mapped within two yards on 5 January 2001. In the first yard, the block consisted of 434 plants (20 plants down rows and 22 rows with six missing). The block within the second yard consisted of 500 plants (20 plants down rows and 25 rows). Individual plants within each block were visually assessed for hop stunt decline on the same day. Both yards were planted with the cultivar Pride of Ringwood and plants were spaced 1.8 m along rows and 2.1 m across rows. The spatial pattern of stunted plants was assessed by a modified version of radial correlation analysis (6) and ordinary runs analysis (10). Ordinary runs analysis was used to assess the proportion of infected plants both along and across rows exhibiting significant (P = 0.05) clustering. A run was defined as a succession of one or more healthy or infected plants flanked by a plant of the opposite state in an ordered sequence (10). Rows were combined with adjacent rows and columns with adjacent columns to perform the row and column analyses, respectively, by joining the end plant of the row (column) a, with that of row (column) a + 1 in a serpentine fashion. Ordinary runs analyses were performed using Microsoft Excel. Radial correlation analysis was conducted using the program 2DCORR to estimate the probability of deviation from a random spatial distribution by a Kolmogorov-Smirnov-type one-tail analysis (P < 0.05) based on a cumulative probability density function for the total number of infected-infected plant pairs within a given distance. The resulting distance, r, is an estimate of the length scale (radius) over which disease was correlated (6,16,20). The spatially aggregated distribution within fields of essentially flat topography also suggested that climatic or microclimatic conditions were not the primary cause.


 

Fig. 4. Spatial patterns of hop stunt decline affected plants in two yards (A and B) in Tasmania, Australia.

 

The incidence of stunt-affected plants was 38% and 54% in yards A and B, respectively. Figure 4 (A and B) demonstrates the spatial distribution of hop stunt decline in each of these yards. Ordinary runs analyses of the spatial pattern of stunt-affected hop plants in both yards indicated significant aggregation of affected plants both along and across rows (Table 1). This was supported by results from radial correlation analysis, which detected significant radial correlation in both yards (Table 2).


Table 1. Spatial test for aggregation of hop stunt decline affected plants by ordinary runs analysis in two hop yards in Tasmania, Australia.

Yard Stunted
plants
Total
plants
Expected
runs
Observed runs
(along/across rows)
Z-statistic (along/across rows)*
A 163 434 204.56 153/187 -5.23/-1.75
B 272 500 249.06 168/189 -7.27/-5.37

 * If Z-statistic is less than –1.64 (P = 0.05), the row of affected plants had an aggregated pattern of affected plants.


Table 2. Spatial test for aggregation of hop stunt decline affected plants by radial correlation analysis in two hop yards in Tasmania, Australia.

Yard Theoretical vs calculated difference magnitude* Kolmogorov-Smirnov D value** Radius of spatial correlation (r)
A 1.12 x 10-2 (sig.) 0.9 x 10-2 (sig.) 5
B 2.27 x 10-2 (sig.) 6.38 x 10-3 (sig.) 7

 * Radial spatial correlation is significant if there were more plant pairs (either affected or healthy) than expected within ‘r’ plant separation units in all directions.

** Probability values from the 2DCORR probability matrix for expected observed like pairs of adjacent plants (affected-affected or healthy-healthy plant pairs either down-row or cross-row).


Summary

The cause of hop stunt decline in Australian hop yards remains unknown. During almost ten years of investigations several factors were excluded as contributing factors, including the majority of known pathogens of hop. The finding that cuttings from stunted hop plants taken to healthy gardens remained healthy whilst cuttings from stunted and healthy hop plants re-planted into stunt-affected yards, became stunted, suggests a localized soil effect, as did the aggregated spatial pattern of affected plants. The only management option for hop stunt decline in Australian hop yards was found to be replanting with tolerant cultivars, including ‘Nugget,’ ‘Willamette,’ and ‘Topaz.’ Further investigations should focus on the influence of additional pesticides and/or examine soil dilution effects with affected and healthy field soil, soil fumigation, micro-nutrient deficiencies, such as manganese, and soil microbiology in further detail. We hope this information will be useful if a similar problem is found on hop elsewhere.


Acknowledgments

Research was supported by the Australian Research Council - Strategic Partnerships in Industry and Research Program, Horticulture Australia Limited, and Hop Products Australia (HPA). We also thank others consulted as part of this research including Mr. Darby Munro and Dr. Gradon Johnstone (formerly Department of Primary Industries and Fisheries, Tasmania), Dr. Ian Porter (BioSciences Research Division, Department of Primary Industries Victoria, Australia), Dr. Jerry Uyemoto (United States Department of Agriculture, Agricultural Research Services, Davis, CA), Dr. Leigh Sparrow [Tasmanian Institute of Agricultural Research, University of Tasmania (TIAR-UTAS), Mt. Pleasant, Tasmania], Dr. Frank Hay (TIAR-UTAS, Burnie, Tasmania), Associate Professor Calum Wilson (TIAR-UTAS, New Town, Tasmania), and Ms. Leanne Sherriff and the late Mr. Grey Leggett (both formerly of HPA).


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