Abstract
In this study, 15 early-ripening strawberry cultivars were evaluated on 11 sites in Austria regarding their susceptibility to root and leaf diseases. The main aim was to find cultivars with field resistance to Verticillium dahliae and other soilborne pathogens and to explore the interactions between cultivars and sites. ‘Daroyal’, ‘Clery’, ‘Asia’, ‘Betty’, ‘Queen Elisa’, and ‘Alba’ showed a comparably high vitality on all sites and a low number of plant losses on one site highly infested with V. dahliae. Cultivars susceptible to Verticillium wilt, were also prone to root diseases on non-infested sites. In addition, interactions between cultivars and sites played a significant role.
INTRODUCTION
Root and rhizome diseases (caused by Verticillium sp., Phytophthora sp., Pythium sp., Rhizoctonia sp., Fusarium sp., and root-lesion nematodes) are a main limiting factor in strawberry cultivation worldwide. Generally, soil-borne diseases are difficult to control. Particularly, methods to reduce the pest inoculum in the soil, such as biofumigation, and use of antagonistic microorganisms are still lacking efficiency.
In central Europe, the most important cultivar still is ‘Elsanta’, which is known to be prone to root diseases. To find alternatives to ‘Elsanta’, a field trial with early ripening strawberry cultivars on several farms was established. The main aim of this study was to investigate the susceptibility or resistance of the cultivars to soilborne pathogens in general, to V. dahliae in particular, as well as to leaf diseases and pests. The results of the investigation of vegetative parameters are shown in this article, whereas the results regarding yield parameters of the same cultivars are already published in a paper by CitationWeissinger et al. (2010).
There are breeding efforts for Verticillium-resistant cultivars in some countries since fumigation with methylbromide is forbidden. However, the availability of resistant cultivars is still scarce. Resistance in strawberry is polygenic and works against a broad range of different V. dahliae strains, although a low level of cultivar-strain interaction exists (CitationGordon et al., 2006). Genetic factors or physiological processes controlling resistance are widely unknown (CitationKlosterman et al., 2009), which complicates resistance breeding.
To estimate the infestation risk of Verticillium wilt, the soil can be analyzed prior to planting. Susceptible cultivars should not be grown on infested soils. Due to the diversity of the investigated sites (in terms of farm management, soil characteristics, inoculum of V. dahliae, and climate), another aim of this study was to find out if there are cultivars with a general field resistance, which therefore can be recommended for any site, or if there are a lot of interactions between cultivars and sites.
MATERIALS AND METHODS
In spring 2007, cold stored plants of 15 cultivars () were planted on 11 sites in Austria. Before planting, soil parameters, such as pH, humus content, and amount of microsclerotia of V. dahliae in the soil [according to the method described in CitationHarris et al. (1993)], were analyzed on each site. Climate data were collected by CitationZAMG (2010) (). Inoculum of V. dahliae ranged from 0 to 10 microsclerotia per gram soil. ‘Jedlersdorf’, ‘Kremsmünster’, and ‘Wiesen 1’ were sites with a very high infestation risk for Verticillium wilt; ‘Gschmeier’ and ‘St. Ruprecht’ were sites with a high risk; ‘St. Georgen’, ‘Grafenegg’, and ‘Pöttsching’ were sites with a medium risk. In ‘St. Egyden’, ‘Stammersdorf’, and ‘Wiesen 2’ no microsclerotia were found. Five sites had an alcalic soil, three sites had a pH 6–7, and one site had a pH < 6. All sites were owned by farmers and managed individually. In ‘Jedlersdorf’, ‘Stammersdorf’, and ‘Wiesen 2’, strawberries were produced under organic guidelines.
TABLE 1 Origin and Source of Plants of the Tested Cultivars
TABLE 2 Site Characteristics
After the harvest season in 2008, strawberry plants were cleared in ‘Wiesen 1’ and ‘Wiesen 2’. The reason was severe plant losses, which was not affordable for the farmers. The data from these sites were only used for the comparison of cultivars, not for the comparison of sites since data was collected only in 2007. In the planting year, plant vigor (with a scale from 1–9; 1 = very low, 9 = very high), chlorosis, infestation with leaf mildew (Sphaerotheca macularis), and incidence of tarsonemid mite (Phytonemus pallidus fragarie) (scale 1–9; 1 = no symptoms, 9 = very heavy symptoms) were assessed. In 2008 and 2009, soil cover (estimation of covered surface in %) and plant losses (areas with dead plants or very weak plants, scale 1–9; 1 = no plant losses, 9 = all plants dead) and infestation with leaf spot diseases (leaf scorch caused by Diplocarpon earliana and leaf spot caused by Mycosphaerella fragariae) were assessed in addition to the parameters observed in 2007. Angular leaf spot (Xanthomonas fragariae), which was observed in 2008 on one site, was also assessed with a scale from 1–9. In 2009, chlorosis symptoms were only assessed on the sites with pH > 7 because on the other sites symptoms were unconsiderable. On the site ‘Jedlersdorf’, symptoms of Verticillium wilt were evaluated once a year for every single plant: 1 = plant without symptoms, 2 = weak plant, 3 = very weak plant, 4 = dead plant. The infestation degree was calculated as follows: (number of healthy plants + 2 * number of weak plants + 3 * number of very weak plants + 4 * dead plants)/total number of plants.
RESULTS AND DISCUSSION
Vegetative Field Parameters of the Cultivars
In , the results of vegetative field parameters (means of 3 years) are shown. ‘Daroyal’ had the highest plant vigor (7.67) and soil cover (93.06%). ‘Queen Elisa’, ‘Clery’, ‘Gloria’, ‘Marianna’, and ‘Asia’ also showed high values of plant vigor (>6.5). ‘Daroyal’, ‘Clery’, ‘Queen Elisa’, and ‘Antea’ had >80% soil cover, which is of special importance for organic growers who are not allowed to use herbicides. ‘Elianny’ was the cultivar with the lowest plant vigor and ‘Elsanta’, ‘Figaro’, and ‘Galante’ had a very poor soil cover with values around 65%.
TABLE 3 Vegetative Parameters of the Cultivars on 11 Sites (2007–2009)
The number of plant losses was lowest in ‘Daroyal’ and highest in ‘Elsanta’, ‘Figaro’, and ‘Galante’. A relation of the estimation of soil cover and of the extent of plant losses is obvious, so both parameters can be seen as parameters for plant vitality, whereas plant vigor refers more to the growth character of the plants, taking into account the vertical growth.
The reasons for plant losses were various and ascribed to the infestation with soilborne pathogens, mainly V. dahliae, Phytophthora spp., Rhizoctonia spp., Pythium spp., and nematode species, such as Pratylenchus penetrans. Incidence of V. dahliae was proven for most sites as microsclerotia could be found in the soil and V. dahliae was re-isolated from plants of these sites. Nevertheless, a mixture of different pathogens may be responsible for the plant losses. On the site ‘Wiesen 2’, for example, where no microsclerotia of V. dahliae were detected, a severe infestation with root-lesion nematodes occurred.
Regarding chlorosis, ‘Marianna’, ‘Galante’, ‘Elianny’, ‘Gloria’, and ‘Figaro’ were rated >3. In the case of ‘Galante’ and ‘Figaro’, chlorosis was associated with a high number of plant losses indicating a high susceptibility to soilborne diseases. In a late stage of the disease, heavy chlorosis was observed. In the case of ‘Marianna’, it is a clear matter of high susceptibility to iron deficiency as otherwise healthy plants had chlorotic leaves.
Leaf mildew was only observed to a noticeable extent in ‘Elsanta’ and in ‘Elianny’, all other cultivars showed low incidence. Infestation with leaf spot diseases was of minor importance in all cultivars and there were only slight symptoms, in conventional and in organic farms. No great differences between cultivars could be detected. Bacterial angular disease was found on one site in 2008, and especially in the cultivar ‘Sugar Lia’ (5.0). In 2009, no symptoms were observed. Tarsonemid mite infestation was observed in 2007. All cultivars showed leaf wrinkling, but the least was seen in the cultivar ‘Elsanta’ and the most was seen in the cultivar ‘Antea’. Curled leaves due to the tarsonemid mite are often observed in the open field in the planting year, but damage appears to be low in consecutive years.
There are only few detailed results about vegetative parameters of other experiments in Europe regarding these cultivars. Either testing was done only for one year, on one site, or without repetition, or incidence of diseases was very low. In an article by CitationKrüger (2008), ‘Daroyal’ and ‘Asia’ were described as robust and vigorous, whereas ‘Figaro’ had some problems with soilborne diseases. In an experiment in Switzerland on 900 m sea level, ‘Clery’ showed severe symptoms of leaf spot diseases, which led to depressed growth (CitationSuter and Häseli, 2007).
Verticillium wilt on the Site ‘Jedlersdorf’
In ‘Jedlersdorf’, where definite symptoms of Verticillium wilt were determined and runners were removed every year, single plants were assessed. The course of disease over 3 years is illustrated in . In the planting year, ‘Elianny’ had the most severe symptoms. ‘Elsanta’ had vital plants in the first year, but was the most susceptible cultivar in 2008. From 2008 to 2009, the infestation degree of ‘Elsanta’ only increased slightly, whereas in most cultivars, the infestation degree of 2009 was much higher than in 2008. For example, the plants of ‘Queen Elisa’ and ‘Antea’ were healthy until summer 2008, but showed severe symptoms in 2009.
FIGURE 1 Infestation degree of V. dahliae (site ‘Jedlersdorf’, 2007–2009).
Taking the means of all 3 years, ‘Galante’ was significantly more infested than ‘Antea’, ‘Queen Elisa’, ‘Alba’, ‘Asia’, and ‘Daroyal’. ‘Daroyal’ as the most resistant cultivar differed significantly from ‘Figaro’, ‘Elianny’, and ‘Galante’.
The high resistance to Verticillium wilt of ‘Daroyal’ is in contrast to the study of CitationDressler et al. (2010), where cultivars were artificially inoculated with a mixture of seven isolates of V. dahliae originated from various regions of Germany and Poland. ‘Daroyal’ was classified as a highly susceptible cultivar, whereas ‘Asia’ and ‘Elianny’ were classified as medium susceptible cultivars. This phenomenon is also referred to in a paper by CitationOlbricht and Hanke (2008), where they report that there are cultivars susceptible to Verticillium after inoculation in the greenhouse, but showing a high field resistance under natural conditions. From experimental stations in Germany and Switzerland, ‘Daroyal’ is described as a robust cultivar with high plant vigor, but there are no results concerning Verticillium wilt since the sites in the experiments were not infested. CitationWeissinger et al. (2009) showed in a previous study that, when ‘Daroyal’ was grown on six sites with medium to very high infestation risk, ‘Daroyal’ was less susceptible than all other tested cultivars with the exception of ‘Salsa’. In that trial, ‘Elsanta’ was significantly more infested than ‘Clery’, ‘Alba’, ‘Queen Elisa’, and ‘Daroyal’, whereupon ‘Clery’ again was significantly more infested than ‘Daroyal’.
The onset of the disease (if in the 1st, 2nd, or 3rd year of production), is economically very important for the producer. For the cultivars ‘Queen Elisa’ and ‘Antea’, a 2-year cultivation can be recommended for sites with a high Verticillium risk, whereas it was documented that yield in the 3rd year was reduced due to wilting, also leading to a high amount of gummy fruits. In both harvest years, yield of ‘Galante’, ‘Elianny’, and ‘Figaro’ was very low on the site ‘Jedlersdorf’. The yield of ‘Elsanta’ was higher than the yield of ‘Daroyal’ in 2008, but was clearly lower in 2009 (CitationWeissinger et al., 2010). The susceptibility of ‘Figaro’ is confirmed in a cultivar trial conducted in Poland (CitationMasny and Zurawicz, 2009).
The different onset of the wilt may be due to different grades of both resistance and tolerance. One point is how fast the pathogen enters the xylem and leads to systemic infection, the other to which extent the plant can keep its vitality despite the presence of a pathogen, that means, if tolerance mechanisms are effective. According to a study by CitationShaw et al. (2010), 60% of the genetic variation for visual symptom expression can be explained by differences in the extent of petiole colonization. The rest of 40% of the genetic variation may be ascribed to a plant's capacity to tolerate the presence of the pathogen. CitationShaw et al. (2010) proposed to use quantitative polymerase chain reaction (PCR) to assess the frequency of colonization of V. dahliae in the selection process.
The rapid symptom development in ‘Elsanta’ is confirmed by a work of CitationTahmatsidou et al. (2002). Susceptible, medium resistant, and resistant cultivars were grouped according to the speed of symptom development. Another study divided genotypes according to the inoculum level at which plants develop symptoms (CitationShaw et al., 1997).
Relation between Infestation Risk of Verticillium wilt and Incidence of Plant Losses
The parameter plant losses did not correlate with the number of microsclerotia of V. dahliae (). The highest degree of plant losses was yet found on the site ‘Jedlersdorf’ with ten microsclerotia/g soil, but there was also a high number of plant losses in ‘Pöttsching’, ‘St. Egyden’, and ‘Stammersdorf’ despite a very low or medium infestation risk of Verticillium wilt. This indicates an infestation with other soil pathogens on these sites. On the site ‘Kremsmünster’, a site with a very high infestation risk, a mean degree of 1.90 was assessed. This relatively low degree can be explained by the more humid climate that may delay the pathogenesis, by a higher suppressive potential of the soil and, therefore, less wilting symptoms, or by the occurrence of less pathogenic or apathogenic subtypes of V. dahliae [as described in CitationSchubert et al. (2008)] on this site.
FIGURE 2 Relation between infestation risk of Verticillium wilt and degree of plant losses.
Cultivar-Site Interactions
The incidence of plant losses of cultivars, differentiated by sites, are illustrated in : (a) cultivars with a mean degree <2 over all sites; (b) cultivars with a mean degree of 2–3 over all sites; (c) cultivars with a mean degree >3 over all sites.
FIGURE 3 (A) Interactions in plant losses between cultivars and sites (June 2009): Cultivars with a mean degree <2 over all sites (cultivar with the lowest grade left, in ascending order). (B) Interactions in plant losses between cultivars and sites (June 2009): Cultivars with a mean degree of 2–3 over all sites (cultivar with the lowest grade left, in ascending order). (C) Interactions in plant losses between cultivars and sites (June 2009): Cultivars with a mean degree >3 over all sites (cultivar with the lowest grade left, in ascending order).
Every cultivar had its own pattern, so site-cultivar interactions played a significant role. ‘Clery’, ‘Betty’, ‘Queen Elisa’, ‘Gloria’, ‘Antea’, ‘Vale’, ‘Elianny’, ‘Marianna’, and ‘Galante’ had the highest degree of plant losses in ‘Jedlersdorf’. ‘Daroyal’ and ‘Elsanta’ showed the most plant losses in ‘Stammersdorf’, while ‘Asia’, ‘Alba’, and ‘Sugar Lia’ showed the most plant losses in ‘Pöttsching’. ‘Alba’, ‘Vale’, ‘Marianna’, and ‘Sugar Lia’ were totally vital on the site ‘Stammersdorf’. ‘Elianny’ had severe problems in ‘Jedlerdorf’, whereas at the other sites, ‘Elianny’ proved to be quite tolerant. ‘Elsanta’ was the only cultivar with symptoms on all sites. In the cultivar ‘Daroyal’, there were only some plant losses in ‘Jedlersdorf’ and ‘Stammersdorf’. ‘Clery’ also showed plant losses on these two sites, furthermore in ‘Gschmeier’. The cultivars ‘Asia’, ‘Betty’, ‘Queen Elisa’, and ‘Alba’ had plant losses on most assessed sites, but never with a degree >4.
CONCLUSIONS
The cultivars ‘Daroyal’, ‘Asia’, ‘Betty’, ‘Queen Elisa’, and ‘Alba’ can be recommended for Verticillium-infested soils. ‘Clery’ might have some problems on sites with a higher infestation risk (what was also seen in a previous trial 2005–2007), but also proves to be quite tolerant to soilborne diseases in general. To include other aspects, such as yield, ‘Asia’, ‘Queen Elisa’, and ‘Alba’ showed high yield potential under organic farming conditions (about 7 kg/m2 in 2 harvest years) whereas the yield of ‘Daroyal’ and ‘Betty’ was significantly lower (4–5 kg/m2). Summarizing important cultivar characteristics, ‘Alba’, ‘Asia’, ‘Queen Elisa’, ‘Clery’, and ‘Daroyal’ are the most interesting cultivars from this trial and can be recommended to substitute ‘Elsanta’ on sites where problems with soilborne diseases may occur. It does not make sense to generally dissuade from a single cultivar, because each cultivar reacts very differently at distinct site conditions and may have good performance on sites with low pathogen pressure. Nevertheless, there is a trend that cultivars, which are susceptible to Verticillium wilt, are also more prone to plant losses in general.
When testing the resistance of cultivars with artificial inoculation, results should be taken with consideration, so that field-resistant cultivars, such as ‘Daroyal’, which may be classified as susceptible during the breeding process, will not be eliminated from further testing. Reasons for the high field resistance, compared with resistance in artificial systems, can be that factors occurring in natural soils (symbiosis with beneficial microorganisms, lower or higher disease thresholds, or different species and strains of pathogens, not tested in the laboratory) are included.
The goal should be to find cultivars with a broad field resistance to several pathogens and diseases and not only breeding for specific resistances, because in most soils several pathogen species and strains are present. This could be achieved if further knowledge about the mechanisms of field resistant cultivars, such as ‘Daroyal’, would be explored. Else, the build-up and preservation of disease-suppressive soils should be paid more attention to. Because there is a lack of reliable and consistent indicators for such soils and, therefore, no clear recommendations for cultural practices, a holistic research approach has to be followed combining disciplines of soil and plant science, which may lead to indicators and in succession to a better knowledge how the disease-suppressive potential of soils can be enhanced (CitationJanvier et al., 2007).
ACKNOWLEDGMENTS
The authors wish to acknowledge the Austrian Ministry of Agriculture for funding this research and thank all growers for providing parts of their fields.
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