Abstract
Apple and pear scab are foliar diseases of ornamental and fruiting apple and pear trees. Unmanaged, yield and aesthetic losses can be severe. Overreliance on synthetic fungicides means novel means of disease management are required. Field trials were conducted using apple (Malus cv. Crown Gold) and pear (Pyrus communis ‘Williams Bon Chrétien’) to assess the efficacy of a range of commercially available inducing resistance (IR) agents (harpin protein, potassium phosphite, salicylic acid derivative, and chitosan) as root drenches against both scab diseases. A synthetic fungicide (penconazole) spray program used within the UK for apple and pear scab control was included for comparison. Each IR agent was applied four times, (i) before the visible appearance of scab (April through June, i.e., preventatively) or (ii) after symptoms of scab were visibly observed (June through August, i.e., curatively). Limited efficacy as scab protectants was demonstrated when IR agents were applied curatively. Likewise, limited efficacy was recorded when IR agents were applied once or twice as a preventative measure. However, when IR agents were applied as root drenches greater or equal to three times, efficacy as scab protectants was confirmed (increased leaf chlorophyll content, increased fruit yield, reduced leaf and fruit scab severity). A synthetic fungicide penconazole spray program provided the greatest protection against apple and pear scab in all trials when sprayed preventatively rather than curatively. Results suggest application of at least three root drenches from April through June with an appropriate IR agent provides a useful addition to existing methods of apple and pear scab management under field conditions.
- Fungicides
- Integrated Disease Management
- Orchard Management
- Pathogen Control
- Plant Health Care
- Urban Landscapes
- Venturia inaequalis
- Venturia pirina
INTRODUCTION
Ornamental apple (Malus spp.) and pear (Pyrus spp.) varieties/cultivars are a popular and attractive choice for both public and private urban landscapes throughout Europe. Trees are hardy, adaptable to varied soil conditions, and are available in a wide range of sizes and shapes. Species exist to suit almost any purpose, from small urban gardens, entry courtyards, and parking strips, to public parks and highway plantings. Both Malus and Pyrus species bloom profusely in eye-catching shades of pink, red, and white, accented by purple or bronze leaf colour. Their colouration makes them effective ornamental trees in the spring landscape. Because of these characteristics, many species from both the Malus and Pyrus genus are frequently planted within European urban landscapes (Percival 2018). During the growing season, however, both ornamental and fruiting Malus and Pyrus species are highly susceptible to attack by the foliar pathogens Venturia inaequalis (Cke) Wint. and V. pirina Aderhold, causes of apple and pear scab, respectively (Sabri et al. 1997; Cuthbertson and Murchie 2003; Villalta et al. 2004; Hailey and Percival 2014). Scab symptoms initially appear in the spring as small, olive green lesions on the lower leaf surface. As leaves age, the lesions become darker and more distinct in outline. If heavily infected, the leaf becomes distorted and drops prematurely in the summer. Trees of highly susceptible varieties may be severely defoliated by mid to late summer. Fruit symptoms are similar to those found on leaves. The margins of the spots, however, are more distinct on the fruit. The lesions darken with age and become black and scabby. Badly scabbed fruit becomes deformed and may fall before maturity (Percival and Boyle 2005; Aćimović et al. 2016). Within the United Kingdom, thousands of ornamental apple and pear trees exhibit symptoms of these two pathogens, which untreated over time can result in a slow tree decline and possibly death (Percival 2018). Strategies for scab management are difficult because currently there are no synthetic fungicides with systemic properties that directly affect the pathogen registered for use within most European urban landscapes (Lainsbury 2018). An added difficulty is the occurrence and spread of strains of Venturia with resistance to triazole-based fungicides due to overreliance in the production of “scab free” fruiting apples used for human consumption (Cuthbertson and Murchie 2003; Villalta et al. 2004). Consequently, the development of an effective treatment appears a necessary tool to slow apple and pear decline and to protect valuable trees from infection and death.
Tree resistance against foliar and root diseases can be enhanced by exposing them to a range of natural and/or synthetic compounds, such as inorganic potassium and phosphate salts, low molecular weight proteins, and salicylic acid (Bécot et al. 2000; Fobert and Després 2005; Garbelotto et al. 2007; Percival et al. 2009). After exposure to these compounds, a suite of physiological, biochemical, and anatomical changes occur within leaf, wood, and root tissue. Changes include synthesis of low-molecular-weight phenols, terpenoids, and alkaloids that possess antimicrobial, antinutritive, and antidigestive activity, synthesis of protein-based oxidative and hydrolytic enzymes, increased proteinase inhibitors, increased leaf lignification, enhanced resin production, and initiation of wound periderm. Inducement of these changes within plant tissue is termed induced resistance (IR). In essence, IR is a form of disease resistance caused by activation of the host plant’s own genetically programmed defence pathways (Hammerschmidt 2007; Akinsanmi and Drenth 2013; Walters et al. 2013; Aćimović et al. 2016).
IR has been studied in herbaceous plant species and, in recent years, woody plants as a potential eco-friendly concept for enhancing tree resistance to diminish the effects of foliar and root pathogen attack and severity (Walters et al. 2013; Percival 2018). Developments in plant protection technology have led to the formulation and commercialisation of a range of IR agents such as harpin protein (trade name Messenger), benzothiadiazole (trade name Bion), potassium phosphite (trade name Phusion), salicylic acid derivative (trade name Rigel-G), and probanazole (trade name Oryzemate®). These products are registered for commercial plant protection use, although their availability differs between countries (Percival and Haynes 2008). Because of their non-direct chemical mode of action aimed at enhancing the defence mechanisms of treated host plants rather than at directly arresting or killing a disease agent, IR agents offer opportunities for the control of fungal pathogens in ecosystems such as urban landscapes. As effects are mostly on the tree itself, there will be little, if any, consequence on the existing tree fungal communities. IR agents have low toxicity to invertebrates, aquatic organisms, or animals, including humans, an important factor when applying plant protection agents in densely populated urban areas (Fernandez-Escobar et al. 1999; Garbelotto et al. 2007).
Research conducted using IR agents has focused mainly on their potential for disease control of economically important crop plants (wheat, rice, potato) with application primarily by foliar sprays. Few studies exist evaluating IR agents as root drenches against diseases of urban landscape trees. Of those available, root drenches have been shown to offer potential against Phytophthora spp. and bacterial diseases, such as horse chestnut bleeding canker (Pseudomonas syringae pv aesculi)(Garbelotto et al. 2007; Percival and Banks 2014).
This paper aims to build on existing research by generating new and novel data by answering the following questions: (1) Do IR agents offer viable management options for scab protection when applied as root drenches? (2) Is efficacy influenced by number of applications, i.e., how many soil drenches need to be applied to achieve scab protection? (3) What is the influence of preventative versus curative treatments, i.e., do they both offer viable options, or is one superior to the other? (4) To study the influence of IR agents applied as root drenches for scab management, since this has not been investigated.
MATERIALS AND METHODS
Field Site and Experimental Trees
The apple trial site consisted of a 0.75-ha block of apple (Malus cv. Crown Gold) interspersed with individual trees of Malus cv. Red Delicious and Gala as pollinators. The pear trial site consisted of a 0.90-ha block of Pyrus communis ‘Williams Bon Chrétien’ interspersed with individual trees of Pyrus communis Beth and Concorde. Planting distances were based on 2 × 2 m spacing. Trees were planted in 2003 and trained under the central-leader system to an average height of 2.5 m ± 0.25 m with mean trunk diameters of 12 cm ± 1.4 cm at 45 cm above the soil level. The trial sites were located at the University of Reading Shinfield Experimental Site, University of Reading, Berkshire (51°43′ N, −1°08′ W).
Fifteen soil cores from each apple and pear trial site were taken to a depth of 20 cm and radius of 5 cm based on an 8.0-m “W” pattern as stipulated under UK soil sampling procedures (Tytherleigh 2008). The soil was a sandy loam containing 5.2% organic matter with a pH of 6.6; available P, K, Mg, Na, and Ca were 54.3, 685.2, 195.3, 45.1, and 2300 mg/L, respectively. Weeds were controlled chemically using glyphosate (Roundup, Green-Tech, Sweethills Park, Nun Monkton, York, UK) throughout experiments. No watering or fertilisation was applied during the trial. Historically, trees suffered from apple and pear scab infection on an annual basis. Prior to the trial commencing in 2017, trees were inspected in September 2016, and only those apple and pear trees with > 50% of leaves affected with severe foliar discolouration and subsequent scab infection were included in the trial. A minimal insecticide program based on the residual pyrethroid insecticide deltamethrin (product name Bandu, Headland Agrochemicals Ltd, Saffron Walden, Essex, UK) was applied every 2 months commencing in May 2017 to September 2017. All sprays were applied using a Tom Wanner Spray Rig sprayer at 40 mL deltamethrin (Bandu) per 100 L of water. Trees were sprayed until run-off, generally 0.30 L insecticide per tree.
IR and Fungicide Treatments
IR and fungicide treatments were applied either (i) preventatively (no visible symptoms of apple or pear scab at the time of treatment) at four growth stages identified as key application times for scab control under field conditions (Bevan and Knight 2001), namely: bud break (March 9), green cluster (April 8), 90% petal fall (May 16), early fruitlet (June 9); or (ii) curatively, i.e., 5% to 20% of leaves infected with some yellowing, but little or no defoliation at the time of treatment on June 19, July 10, July 31, and August 18. Preventative and curative penconazole (synthetic fungicide) sprays occurred on the same dates as IR drench applications. During spray treatments, polythene screens 2.5 m high were erected around each tree to prevent dispersal of sprays and possible cross contact with other trees. The base of the tree was covered with a 0.5 m × 0.5 m polythene mulch to prevent potential soil percolation. The treatments, 4 IR agents, 1 fungicide, and 1 water control × 2 treatments (preventative vs. therapeutic), were applied in 6 randomised complete blocks, plus a water control with a single tree as the experimental unit (Table 1). Foliar sprays of penconazole were applied until run-off using a hand sprayer.
Products, active ingredient, concentration, acronym, and supplier of treatments used.
As a root drench, 5 L of each IR agent were applied to the soil surface by pouring into a 50- to 60-mm-wide, 20- to 30-mm-deep trench at the base of each tree. Five litres was selected as this was the mean area under the canopy to represent 1 L/m2 of soil surface area.
Plant Vitality Assessments
Measurements were made towards the cessation of the growing season (24 September 2017). To keep the physiological age of the leaves comparable throughout the experiment, plant vitality measurements were made only on fully expanded, mature green leaf tissue.
Leaf Chlorophyll SPAD Measurements
A Minolta chlorophyll meter SPAD-502 was used at the midpoint of the leaf next to the main leaf vein. In all cases, SPAD measurements were taken from 6 leaves (2 from the top of the crown, 2 in the centre, and 2 at the base) per plant. Calibration was obtained by measurement of absorbance at 663 and 645 nm in a spectrophotometer (PU8800 Pye Unicam) after extraction with 80% v/v aqueous acetone (regression equation = 5.64 + 0.059x; r2 adj = 0.97, P < 0.001) (Lichtenthaler and Wellburn 1983).
Scab Severity
Scab severity of leaves and fruit was assessed visually on September 28 and 29. Leaf scab severity of each tree was rated using a visual indexing technique and ratings on the scale: 0 = no scab observed; 1 = less than 5% of leaves affected and no aesthetic impact; 2 = 5% to 20% of leaves affected with some yellowing, but little or no defoliation; 3 = 21% to 50% of leaves affected with significant defoliation and/or leaf yellowing; 4 = 51% to 80% of leaves affected with severe foliar discolouration; 5 = 81% to 100% of leaves affected with 90% to 100% defoliation. Scab severity on fruit was calculated on the scale: 0 = no visible lesions; 1 = < 10% fruit surface infected; 2 = 10% to 25% fruit surface infected; 3 = 26% to 50% fruit surface infected; 4 = > 50% fruit surface infected. The individual ratings for each tree in each treatment were used as a measure of scab severity for statistical analysis. Leaf scab severity ratings used in this study were based on UK and Ireland market standards for fungicide evaluation of scab control (Butt et al. 1990; Swait and Butt 1990). Fruit scab severity was based on a scale used by Ilhan et al. (2006).
Fruit Yield
Yield per tree was determined by weighing all fruit (symptomatic and asymptomatic) on each tree at harvest and dividing by the number of trees per treatment.
Experimental Design and Statistical Analysis
The treatments, 4 IR agents and 1 fungicide × 4 spray times, were applied in 6 randomised complete blocks, plus a water control with a single tree as the experimental unit. Mean scab severity values for all treatments were transformed using the Arcsin (sine−1) transformation. All data were analysed using ANOVA, and the differences between means were determined using Tukey w procedure (P = 0.05) using the Genstat for Windows program. Back transformed pathogen severity values are presented here to ease interpretation of these data. This experimental design was adopted in line with Official Recognition of Efficacy Testing Organisations in the United Kingdom guidelines for product efficacy testing and analysed as a randomised complete block design.
RESULTS
Damaging outbreaks of apple and pear scab were recorded on control trees (preventative and curative treatments) as indicated by leaf and fruit scab severity ratings of ≥ 4.5 and ≥ 2.5 on Malus cv. Crown Gold and ≥ 3.1 and ≥ 2.2 on Pyrus communis ‘Williams Bon Chrétien,’ respectively, at the cessation of the 2017 growing season (Tables 2 and 3). None of the treated or control trees died as a result of scab attack during the course of the study. Likewise, none of the IR agents and fungicide evaluated were phytotoxic to the test trees (data not shown). Limited efficacy as scab protectant compounds was demonstrated when IR products and penconazole were applied curatively, i.e., when scab was visibly observed on foliar tissue prior to treatments. Likewise, limited efficacy was recorded when treatments were applied only twice as preventative treatments (Tables 2 to 7). In virtually all cases, leaf and fruit scab severity, leaf chlorophyll content, and fruit yield of both Malus cv. Crown Gold and Pyrus communis ‘Williams Bon Chrétien’ were statistically comparable with control values (Tables 2 to 7). The effectiveness of each IR agent and penconazole on scab severity of leaves and fruit, leaf chlorophyll content, and fruit yield was confirmed when applied preventatively 3 or more times as a root drench. In all cases, scab severity was lower than controls, and leaf chlorophyll content and fruit yield of Malus cv. Crown Gold and Pyrus communis ‘Williams Bon Chrétien’ were greater than control trees (Tables 2, 4, and 6). There was little difference in the degree of efficacy between each IR agent (Tables 2, 4, and 6). Greater than or equal to 3 root drenches of an IR agent applied preventatively reduced leaf and fruit scab severity by 31% to 50% (Malus cv. Crown Gold) and 16% to 48% (Pyrus communis ‘Williams Bon Chrétien’), and 24% to 56% (Malus cv. Crown Gold) and 27% to 68% (Pyrus communis ‘Williams Bon Chrétien’), respectively (Table 2). Improvements in leaf chlorophyll content ranged from 16% to 56% (Malus cv. Crown Gold) and 9% to 36% (Pyrus communis ‘Williams Bon Chrétien’; Table 4), while improvements in Malus cv. Crown Gold and Pyrus communis ‘Williams Bon Chrétien’ fruit yield ranged from 0% to 19% and 3% to 12%, respectively, compared to water-treated control trees (Table 6). Penconazole was the best treatment with the greatest reductions in apple and pear scab severity on leaves and fruit (Table 2) and the largest increases in leaf chlorophyll content and fruit yield (Tables 4 and 6). The influence of penconazole/IR treatment, number of applications, and interactions between these two factors is shown in Tables 2 to 7 with respect to leaf and fruit scab severity, leaf chlorophyll content, and fruit yield. In most instances, a significant effect and interaction was recorded when IR agents were applied preventatively (Tables 2, 4, and 6). Limited effects and interactions were recorded when IR agents were applied curatively (Tables 3, 5, and 7).
Preventative treatment. Comparison of selected inducing resistance (IR) agents applied as root drenches for the control of Venturia inaequalis and V. pirina on leaves of apple (Malus cv. Crown Gold) and pear (Pyrus communis ‘Williams Bon Chrétien’), respectively, as measured by an observed scab severity index.
Curative treatment. Comparison of selected IR agents applied as root drenches for the control of Venturia inaequalis and V. pirina on leaves of apple (Malus cv. Crown Gold) and pear (Pyrus communis ‘Williams Bon Chrétien’), respectively, as measured by an observed scab severity index.
Preventative treatment. Comparison of selected IR agents applied as root drenches for the control of Venturia inaequalis and V. pirina on leaves of apple (Malus cv. Crown Gold) and pear (Pyrus communis ‘Williams Bon Chrétien’), respectively, as measured by leaf chlorophyll content SPAD values.
Curative treatment. Comparison of selected IR agents applied as root drenches for the control of Venturia inaequalis and V. pirina on leaves of apple (Malus cv. Crown Gold) and pear (Pyrus communis ‘Williams Bon Chrétien’), respectively, as measured by leaf chlorophyll content SPAD values.
Preventative treatment. Comparison of selected IR agents applied as root drenches for the control of Venturia inaequalis and V. pirina on mean fruit yield of apple (Malus cv. Crown Gold) and pear (Pyrus communis ‘Williams Bon Chrétien’), respectively.
Curative treatment. Comparison of selected IR agents applied as root drenches for the control of Venturia inaequalis and V. pirina on mean fruit yield of apple (Malus cv. Crown Gold) and pear (Pyrus communis ‘Williams Bon Chrétien’), respectively.
DISCUSSION
The effectiveness of triazole-based fungicide spray programmes against apple and pear scab under field conditions has been confirmed several times, although concerns have been raised regarding build-up of triazole resistance among scab populations (Jørgensen and Thygesen 2006; Deising et al. 2008; Percival et al. 2009; Aćimović et al. 2016). Despite this, penconazole is fully approved for apple and pear scab management under current UK pesticide legislation (Lainsbury 2018). Indeed, penconazole, when applied preventatively, i.e., before the visible presence of scab, proved very effective for apple and pear scab control on Malus cv. Crown Gold and Pyrus communis ‘Williams Bon Chrétien,’ which are classified as very susceptible to apple and pear scab infection, respectively (Butt et al. 1990; Swait and Butt 1990; Percival et al. 2009). Although not as effective as when applied preventatively, there was still an influence of repeat penconazole sprays when applied curatively. Previous research indicates most commercially available IR agents are generally less effective than standard synthetic fungicides for foliar pathogen control (Percival et al. 2009; Walters et al. 2013). Results of this study support these conclusions, with penconazole proving to be the best treatment in terms of reduced apple and pear scab severity on leaves and fruit and greatest increases in leaf chlorophyll content and fruit yield.
The use of IR agents applied curatively has received little attention. Data from this study clearly indicated that the best option to manage scab was provided by preventative treatment, as the levels of scab control attained by curative applications of any of the IR agents tested were limited. Similarly, 2 root drenches with an IR agent when applied preventatively failed to have any significant influence on scab severity, leaf chlorophyll content, and fruit yield. Such results indicate that these alternatives, especially if used under environmental conditions favourable to scab development and with high inoculum pressure, would not prevent losses and therefore cannot be recommended. In support of our findings, previous research has shown that fungicide sprays used for scab management are always most effective when applied before a major infection period, with timing of applications determined by weather-based predictive models based on monitoring of spore maturity and discharge (Stensvand et al. 2005).
The commercially available IR agents salicylic acid derivative, potassium phosphite, harpin protein, and chitosan provided a useful degree of efficacy as scab protectant compounds under field conditions when applied 3 or more times as a preventative measure as manifest by reduced leaf and fruit scab development, the main proxy of scab success or aggressiveness. In terms of practical disease control, the frequency of application is a crucial consideration, and although it might be expected that induced resistance might provide long-lasting protection, thus requiring fewer applications of elicitor, results here show that this is not the case. In support of this, in field experiments examining the efficacy of the inducing agent acibenzolar-S-methyl against bacterial spot on tomato, Huang et al. (2012) found that weekly applications provided considerably better disease control than applications every 2 weeks.
Although several studies exist evaluating the effects of salicylic acid, potassium phosphite, harpin protein, and chitosan as plant protection agents, these studies were conducted primarily against diseases of crop plants such as wheat, rice, and potato (Lobato et al. 2010; Sharp 2013; Walters et al. 2013). Few studies have evaluated IR efficacy as (i) root drenches and (ii) against diseases of trees under field conditions. Potassium phosphite has been found to be effective in the control of Oomycetes pathogens such as Phytophthora spp., Pythium spp., and downy mildew (Miller et al. 2006; Garbelotto et al. 2007). In addition, phosphites provide a useful means of suppressing apple fire blight caused by the bacterium Erwinia amylovora. The use of the harpin protein (Messenger) has been shown to reduce disease severity of Botrytis cinerea on leaves and fruit of pepper (Capsicum annuum L. var. cvs. ‘Demre,’ ‘Yalova Charleston,’ and ‘Sari Sivri’)(Akbudak et al. 2006), as well as Phytophthora infestans on tomato (Fontanilla et al. 2005) and citrus scab of potted lemon seedlings (Agostini et al. 2003). Salicylic acid and/or its functional analogs, such as 2,6-dichloroisonicotonic acid and benzo-(1,2,3)-thiadiazole-7-carbothioic acid S-methyl ester, reduced severity of several fungal and bacterial pathogens to include early blight of potato (Alternaria solani), brown rot of cherry (Monilinia fructocosa), crown gall (Agrobacterium tumefaciens), powdery mildew (Erysiphe cichoracearum), fire blight (Erwinia amylovora), as well as several Phytophthora species (Bokshi et al. 2003; Sparla et al. 2004; Yao and Tian 2005; Anand et al. 2008; Vlot et al. 2009; Kumar 2014). In these instances, application of salicylic acid alters the metabolic activities of plants, resulting in the activation of a specific set of pathogenesis related genes, many of which encode for proteins with antimicrobial activity (Asghari and Aghdam 2010). Likewise, several studies exist showing that application of foliar- or soil-applied chitosan results in reduced severity of several economically important plant diseases (Ozbay and Newman 2004; Walker et al. 2004; Sharp 2013). Although the mechanistic bases of each IR agent evaluated in this study were not investigated, results published here are the first to show that applications of potassium phosphite, salicylic acid, harpin protein, and liquid chitosan possess useful scab protectant properties when applied as root drenches under field conditions.
From a commercial aspect, producers, suppliers, and vendors of apples generally adopt a zero tolerance policy towards apple and pear scab on fruit (Butt et al. 1990). Consequently, to reduce scab levels to commercially accepted standards, frequent fungicide sprays are applied. However, where fruit produce is sold under an organic or naturally produced label, tolerance of scab severity levels tend to be less stringent (Bevan and Knight 2001). Likewise, ornamental apples planted for aesthetic reasons within town and city landscapes have lower scab acceptability levels (Percival 2018). In these instances, the reductions in scab severity recorded in this investigation may warrant the use of IR agents as an alternative or complement to conventional synthetic fungicides. From a practical point of view, root drenches are simple and relatively inexpensive to use and allow for the direct delivery of a proportionate quantity of IR agent to the plant. Results here indicate IR root drenches do not appear to induce any negative plant growth side effects, i.e., reductions in leaf chlorophyll content or fruit yield. Applications are discrete with no spray drift, an important consideration when applying plant protection agents to trees located in densely populated urban landscapes.
CONCLUSIONS
In conclusion, results of this study provide evidence that potassium phosphite, salicylic acid derivative, harpin protein, and liquid chitosan possess efficacy against apple and pear scab when applied as root drenches, and so could potentially play a role as an alternative and/or supplementary method of management under field conditions, providing at least 3 or more drenches are applied preventatively during April to June.
Footnotes
Conflicts of Interest:
The author reported no conflicts of interest.
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