Management of Fusarium wilt of strawberry

Crop Protection xxx (2015) 1e6

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Management of Fusarium wilt of strawberry Steven T. Koike a, *, Thomas R. Gordon b a b

University of California Cooperative Extension, 1432 Abbott Street, Salinas, CA 93901, USA Department of Plant Pathology, 1 Shields Avenue, University of California, Davis, CA 95616, USA

a r t i c l e i n f o

a b s t r a c t

Article history: Received 4 September 2014 Received in revised form 30 January 2015 Accepted 4 February 2015 Available online xxx

Fusarium wilt of strawberry was first described in the 1960s in Australia and Japan. Since then the pathogen, Fusarium oxysporum f. sp. fragariae (Fof), has been reported worldwide with the majority of cases being found in the 1990s and 2000s. Many of these recent reports are associated with changes in pre-plant soil fumigation practices. The disease is of significant economic importance because infected plants can collapse and die. Field diagnosis of Fusarium wilt is complicated by the fact that other soilborne diseases exhibit very similar symptoms. Methods for detection of Fof based on molecular criteria have been developed, but none have yet been shown to uniquely identify the strain of F. oxysporum causing Fusarium wilt of strawberry. Management of Fusarium wilt is best achieved through the use of resistant strawberry cultivars. Research indicates that sources of Fof resistance exist in strawberry germplasm, though cultivar reactions may differ depending on the Fof isolate. Pre-plant treatment of infested soil with fumigants remains a useful management tool. In addition, alternative treatments such as steam, solarization, anaerobic soil disinfestation, and the planting of brassicaceae crops are being assessed for their effectiveness in managing the disease. Standard integrated pest management practices of crop rotation with non-hosts, planting of pathogen-free transplants, and sanitation of equipment remain important measures that can reduce the risk of damage from Fusarium wilt. © 2015 Elsevier Ltd. All rights reserved.

Keywords: Fungi Fusarium Fusarium wilt Strawberry Fragaria

1. Introduction to Fusarium wilt Fusarium wilt of strawberry (Fragaria x ananassa) is an important disease of this crop worldwide. Caused by the pathogen Fusarium oxysporum f. sp. fragariae (Fof), the disease was first found in Australia in 1962 (Winks and Williams, 1965) and was then found in Japan in 1969 (Okamoto et al., 1970). Since that time, Fusarium wilt was confirmed on strawberry in Korea in 1982 (Kim et al., 1982), Mexico in the late 1980s-early 1990s (Castro-Franco and Davalos-Gonzalez, 1990; Cejas-Torres et al., 2008), China in 2005 (Huang et al., 2005; Zeng et al., 2006; Zhang et al., 2012; Zhao et al., 2009), the United States in 2006 (California: Koike et al., 2009) and 2011 (South Carolina: Williamson et al., 2012), Spain in 2007 (Arroyo et al., 2009), and Serbia in 2013 (Stankovic et al., 2014). In Mexico, researchers feel that Fusarium wilt is part of a disease syndrome in that the combined infections by Fof and a strawberry virus complex has contributed to the decline of strawberry in that region (Davalos-Gonzalez et al., 2014). For the more recent occurrences, Fusarium wilt outbreaks on strawberry have

* Corresponding author.

E-mail address: stkoike@ucdavis.edu (S.T. Koike).

been associated with changes in pre-plant soil fumigation. In California, for example, virtually all of the initial outbreaks were associated with fields that no longer were flat-fumigated with methyl bromide þ chloropicrin that was shank injected under plastic tarps (Koike et al., 2013). Thus, the pathogen may have been present for an extended period but not detected because fumigation maintained inoculum densities below damaging levels. A preliminary assessment of California isolates of Fof has identified three somatic compatibility groups and diverse sequences in the translation elongation factor, suggesting the population is not derived from a single recent introduction (Gordon, unpublished).

Consistent with the narrow host ranges of almost all formae specialis of F. oxysporum, strawberry is the only known host to Fof (Kodama, 1974).

2. Fusarium wilt symptoms In fields with no or inadequate fumigation, strawberry plants can show initial symptoms of decline as early as 30 days after transplanting; these plants will stop growing and be stunted when compared to healthy plants. However, often the initial symptoms of Fusarium wilt in strawberry occur after the plants are well established and begin to flower or produce fruit, at which time the older

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leaves wilt, turn gray green in color, and begin to dry up. As disease progresses, virtually all of the foliage will collapse and dry up with the exception of the central, youngest leaves. Plants can eventually collapse and die. When internal tissues of plant crowns are examined, vascular and cortical tissues are dark brown to orange brown. Internal tissues of the main roots may also be discolored and dark brown in color. Environmental and other stresses can cause the disease to develop more rapidly and severely. Such factors may include the following: weather extremes, particularly high temperatures; water stress from insufficient irrigation or prolonged saturation in the root zone; poor soil conditions; pressure from pests such as mites.

3. Diagnosis and confirmation of Fusarium wilt 3.1. Diagnosis via culturing and isolation For any crop, deploying effective controls and implementing integrated pest management (IPM) strategies depend on the accurate diagnosis of the disease. Diagnosis and confirmation of strawberry Fusarium wilt in the field is not possible, however.

Strawberry is subject to at least four major soilborne pathogens that cause similar, if not identical, symptoms (Table 1). Poor growth, stunting, wilting and collapse of foliage, and plant death can be caused by Fof, Macrophomina phaseolina (causal agent of charcoal rot), Verticillium dahliae (causal agent of Verticillium wilt), and Phytophthora cactorum (causal agent of Phytophthora crown and root rot). Phytophthora crown and root rot differs from Fusarium wilt in that generally both younger and older foliage will collapse at the same time and the plant roots will be distinctly soft and rotted; this disease is also commonly associated with overly wet soil conditions. Verticillium wilt looks very similar to Fusarium wilt except the internal crown tissue of Verticillium-infected strawberry plants lacks the very dark orange to brown discoloration caused by Fof. However, charcoal rot of strawberry (Koike, 2008) causes symptoms that are identical to those of Fusarium wilt. Accurate field diagnosis of collapsing plants is therefore not possible to achieve without laboratory tests that mostly are based on the culturing and isolating of the causal agent.

3.2. Diagnosis via molecular methods Rapid and accurate identification of the particular formae specialis that causes Fusarium wilt of strawberry would also be of great

Table 1 Comparison of symptoms caused by four major soilborne pathogens of strawberry.

Field symptoms

Pathogens F. oxysporum Macrophomina Verticillium Phytophthora f. sp. fragariae phaseolina dahliae cactorum

Poor growth and stunting Wilting, initially older leaves only Wilting, all leaves at once Plant collapse and death Discolored internal crown tissue Soft, rotted roots Associated with stress factors Dependent on overly wet soilsa a

yes

yes

yes

yes

yes

yes

yes

no

no

no

no

yes

yes

yes

yes

yes

yes

yes

no

yes

no yes

no yes

no yes

yes no

no

no

no

yes

The life cycle of Phytophthora depends on periods of saturated soil.

use. Such precision could be used to distinguish between Fof and non-pathogenic Fusarium oxysporum recovered from plant material and could also be employed to test field soil so as to gauge the risk of planting strawberry in that particular field. Toward this objective, Suga et al. (2013) developed PCR primers that amplified a diagnostic DNA sequence from Fof but not from other formae speciales of F. oxysporum or non-pathogenic strains of this species.

Whereas there were no false negatives, six strains identified as Fof based on the PCR detection method were found to be nonpathogenic to strawberry (Suga et al., 2013). In addition, using the same primers, no amplicon was obtained from a subset of Fof isolates originating in the U.S. (Gordon, unpublished results). In China, Li et al. (2014) used both real-time PCR and a semi-selective medium to detect and quantify F. oxysporum following fumigant treatments. There was a strong correlation between results obtained with these two methods, both of which were predictive of disease incidence in a greenhouse trial. However, it appears that results of both procedures were based on total F. oxysporum and not solely the strain causing Fusarium wilt of strawberry. Thus, further work will be required to produce a robust method for detection of Fof based on PCR. 4. Management of Fusarium wilt The overall strategy for managing this disease depends on preventative measures. No effective therapeutic treatments for diseased plants are available. An IPM approach that incorporates planting resistant cultivars, pre-treating infested fields, rotating with non-hosts, and implementing various cultural practices can minimize damage from Fusarium wilt.

4.1. Fusarium-resistant strawberry cultivars The discovery, development, and planting of Fusarium-resistant strawberry cultivars is the most effective and preferred way to control Fusarium wilt. A number of breeding lines and cultivars have been tested in the various countries where the disease has occurred. Such research thereby demonstrated that sources of Fof resistance and diversity in strawberry germplasm exist. In Mexico a number of advanced selections and two cultivars (Cometa, Buenavista) released in 2003 exhibited resistance to Fof (DavalosGonzalez et al., 2006). Australian studies found cvs. Festival, Aromas, and Camino Real to be resistant, with Festival being the most resistant (Fang et al., 2012a). In California, cvs. Portola and San Andreas were found to be highly resistant when subjected to rootdip inoculations (Gordon, 2012, 2013). Breeders in Asia have been actively developing resistant cultivars for many years and have tested and released a number of them over time: Fukuba, Fogyoku, Yachiyo, Benituyu and Senga Gigana (1974); Hatsukuni (1982); Daehak 1, Line 10-2, Senga Sengana (1982); Asuka Wave (1994); Aisutoro and Hogyoku (2005); Komachi Berry (2007) (Kim et al., 1982; Kodama, 1974; Mori et al., 2005; Takahashi et al., 2007).

Wild clones of Fragaria chiloensis, collected originally from California, also exhibited resistance to Fof and therefore could provide another source of genetic material for resistance breeding (DavalosGonzalez et al., 2006).

Interestingly, there are differing accounts on whether certain commercial cultivars are resistant to Fof. In inoculation tests conducted in Spain, cv. Ventana was proven to be very susceptible (Arroyo et al., 2009) while in California cv. Ventana was resistant in most, but not all, inoculation experiments and is considered to be resistant in commercial plantings (Gordon, 2012, 2013). Cv. Camino Real was very susceptible in a California study (Koike et al., 2009) but was the most resistant cultivar in an Australian investigation (Fang et al., 2012a). Such discrepancies could be accounted for if

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researchers are using different sources and clones of the presumed same cultivar or if post-inoculation conditions are significantly different, since Fusarium wilt can be more severe if temperatures are elevated. Kodama (1974) found that several cultivars varied in their level of resistance depending on the environmental conditions under which the plants were grown. Further, differences in isolate virulence have been reported (Fang and Barbetti, 2014; Horimoto et al., 1988), so cultivar reactions may be contingent on isolates used to inoculate them.

Additional breeding efforts are clearly essential for developing cultivars with more complete and durable resistance to Fof (Paynter et al., 2014). Some researchers are exploring the resistance mechanisms for the strawberry-Fof pathosystem; when the strawberry plant is exposed to Fof, changes in plant protein expression signal possible defense-related mechanisms of resistance. Identifying such pathogen-induced, defense-related proteins could be used to search for new sources of resistance to Fof (Fang et al., 2013).

4.2. Pre-plant chemical controls Successful management of all soilborne pathogens of strawberry was achieved by the long standing practice of flat-fumigating fields with high concentrations of methyl bromide þ chloropicrin that was shank injected under plastic tarps; such a practice was pioneered in California (Johnson et al., 1962), has been practiced worldwide for many years, and will continue to provide suitable control of Fusarium wilt if applied in the traditional manner.

However, because methyl bromide contributes to ozone depletion, this fumigant is being phased out, is no longer available in many countries, and will eventually be unavailable for pre-plant soil fumigation in strawberry fruit production. A number of pre-plant chemical alternatives to the methyl bromide þ chloropicrin treatment have been investigated and include: chloropicrin alone, chloropicrin þ1, 3-D broadcast (Telone C35) or drip applied (InLine or Pic-Clor 60), and methyl isothiocyanate products (such as Basamid, Dazomet, Kpam, or Vapam). These alternatives do not provide the equivalent level of control when compared to the methyl bromide þ chloropicrin treatment (Koike et al., 2013). For example InLine, which is widely used in several strawberry producing regions in California, showed an intermediate ability to kill propagules of F. oxysporum when tested under controlled laboratory conditions (Klose et al., 2007) and failed to provide seasonlong control in a field study (Koike et al., 2013). The efficacy of these alternative treatments is further reduced by the trend in California and elsewhere to only apply the materials via irrigation drip tape to pre-formed, raised beds. This method of application results in the survival of Fof where the soil is not sufficiently wetted with lethal concentrations of chemical, especially along the edges of the beds and at depths greater than 12 inches away from the drip tapes that delivered the fumigants (Gordon, 2012). Improving the bed application method, such as by increasing the number of drip lines per bed, might result in better distribution of fumigants and more complete treatment of the soil in the beds. Fof inoculum residing in the furrows between beds, however, will not be exposed to these bed-applied treatments. This incomplete treatment of soil allows inoculum levels to increase over successive years to the point that plants in untreated buffer zones develop symptoms soon after transplanting and yield no marketable fruit.

4.3. Pre-plant non-chemical controls A number of non-chemical pre-plant approaches are being evaluated or are in commercial use for dealing with soilborne pathogens such as Fof. In most cases, these approaches require particular soil or environmental conditions to be effective and

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therefore do not work in all situations or are not possible in all production fields. The planting of broccoli or other brassicaceous plants such as mustard, or the importing and incorporating of brassicaceous crop residues, creates a biofumigation effect that suppresses soilborne pathogens (Muramoto et al., 2014; Njoroge et al., 2011; Subbarao et al., 1999). This approach has proven to be effective on various Fusarium pathogens (Relevante and Cumagun, 2013).

Pre-plant steaming of soil is being investigated in California for weed and soilborne pathogen control. Field trials have demonstrated the potential to control Verticillium dahliae by using steam to heat soil (Samtani et al., 2012). Additional California trials utilizing steam will be targeting Macrophomina phaseolina and Fof. Solarization of soil has successfully managed Fusarium wilt in regions having solar radiation that is sufficient to achieve the needed elevated temperatures. In Japan, solarization has been effective in both field and greenhouse settings when combined with plastic mulch covers and solar-heated water (Kodama and Fukui, 1982a; 1982b; Sugimura et al., 2001). Soil solarization may create an induced suppressiveness due to the activity of beneficial, antagonistic soil microorganisms, as suggested by Greenberger et al. (1987). This increase in soil microbial activity may account in part for the suppression of Fof in Japan (Kodama et al., 1980).

Anaerobic soil disinfestation (ASD) (also known as biological soil disinfestation or reductive soil disinfestation) is an alternative preplant, soilborne pathogen control technique that was first developed in Japan and The Netherlands (Momma et al., 2013). ASD involves incorporating an organic carbon source (such as wheat or rice bran, molasses, or ethanol) into the soil, covering the field or beds with plastic tarps, and subsequently irrigating the site so as to maintain field capacity and create anaerobic soil conditions (Momma et al., 2013; Shennan et al., 2014). The method has controlled Fusarium wilt diseases of cucurbits and tomato both experimentally and in commercial practice. ASD has also successfully managed Verticillium wilt in strawberry fields in California (Shennan et al., 2014). Although ASD has been studied extensively, the mechanism by which pathogen activity is suppressed remains unknown. The efficacy of ASD is likely to be affected by a number of factors including field temperatures, consistency and degree of the anaerobic conditions, soil type, nature of the indigenous soil microorganisms, duration of the treatment, and inherent susceptibility of the target plant pathogen. For example, in Japan Fof was controlled by ASD (Ebihara and Uematsu, 2014; Oyamada et al., 2003; Yonemoto et al., 2006) but was not controlled in one field experiment with a fall application of ASD to pre-formed beds in California (Shennan et al., 2014). Under different parameters, ASD applied in the summer to flat ground in California did result in a reduction of Fusarium wilt severity (Muramoto, personal communication). Differences in temperature and other ASD factors may explain such inconsistencies in Fusarium wilt control for strawberry.

4.4. Biological control applications The search for effective, affordable, and commercially available biocontrol products for managing soilborne pathogens has been earnest. Biocontrol organisms have shown some efficacy against Fof under controlled experimental conditions and include the following: Bacillus subtilis, Bacillus velezensis, non-pathogenic F. oxysporum isolates recovered from strawberry, Trichoderma harzianum (Moon et al., 1995; Nam et al., 2009; Okayama et al., 1991; Tezuka and Makino, 1991; Zhang et al., 2012). However, no commercially viable product has yet been developed for use against Fusarium wilt of strawberry.

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4.5. Crop rotation Continuous planting of strawberry will allow the soil population of Fof and other soilborne pathogens to increase. Therefore, successive plantings of strawberry crops should be avoided. Broccoli may be particularly useful as a rotation crop due to its status as a non-host to Fof and the suppressive effect that broccoli crop residues (see biofumigation above) have on a number of soilborne pathogens (Njoroge et al., 2011; Subbarao et al., 1999). Crop rotation with non-hosts is a proven IPM strategy that is essential for managing any soilborne disease problem, including Fusarium wilt of strawberry (Fang et al., 2011a, 2012b; Horimoto et al., 1988; Okayama et al., 1988). If crop rotation and land availability permits, it is always preferable to avoid planting strawberries in fields known to be infested with Fof. 4.6. Planting Fusarium-free strawberry transplants In contrast to most annual crops, commercial strawberries worldwide are propagated vegetatively. Strawberry transplants are obtained by harvesting daughter plants that develop from stolons leading from the mother plants. Researchers have demonstrated that the systemic Fof pathogen can be transmitted from infected mother plants to developing daughter plants (Mori et al., 1999; Nam et al., 2011). Therefore, successful management of Fusarium wilt of strawberry depends on the production and planting of Fusarium-free transplants.

4.7. Sanitation practices and the cleaning of equipment Because Fof produces chlamydospores, which can survive in soil, it is critical to minimize movement of soil and mud from infested fields into fields that do not have a history of the disease. Washing tractors and farm implements, limiting vehicle access to fields, and other measures could be taken to minimize spread of the pathogen to clean fields. Soil preparation procedures could first be completed in uninfested fields before moving tractors and equipment to known infested fields.

4.8. Avoid planting into buffer zones For production regions that still allow the use of pre-plant soil fumigation, field buffer zones, which by regulation will not be treated with any pre-plant fumigant or chemical, may harbor significant populations of soilborne pathogens such as Fof. For fields known to be infested with Fof, growers would be advised to not plant strawberries in buffer zones so as to reduce the build-up of this pathogen in untreated soil.

4.9. Miscellaneous cultural practices A few growing or cultural practices can possibly reduce Fusarium wilt disease of strawberry. Because stress factors tend to increase severity of Fusarium wilt, growers are advised to reduce stress to the crop as much as possible. Heat and elevated temperatures are particularly important factors for Fusarium wilt of strawberry. Fang et al. (2011b) found that when inoculating the susceptible cv. Camarosa, disease severity was minimal at 17C; however, at 27C disease severity increased significantly and plants rapidly declined and died. While growers cannot control the ambient temperatures, awareness of this dynamic should encourage growers to avoid water and heat stress by appropriately irrigating strawberries during warmer times of the year. Stress on plants can also be reduced by planting into well prepared beds and managing arthropod pests, especially spider mites.

There are indications that in the case of strawberries affected with Verticillium wilt, large pieces of strawberry crowns likely harbor high numbers of V. dahliae microsclerotia. Removing or shredding and drying Verticillium-infected crowns prior to disking the field may reduce inoculum levels in the soil. Therefore, a similar strategy might also reduce inoculum of Fof. Any practice that results in more complete decomposition of plant residue should also make fumigation more effective.

The literature on Fusarium wilt management for many crops gives differing accounts of the value of adding organic soil amendments, such as composts, composted animal manures, and “green manures” from cover crops, for managing this disease; in some cases these inputs look promising as disease control strategies but in many instances these inputs do not provide consistent and repeatable results. Likewise, studies conducted with potted strawberry show some potential for manipulating Fof through the addition of organic amendments (Fang et al., 2012b); however, using such inputs in the field has not yet proven to be a practical strategy for effectively and consistently managing Fusarium wilt. In a similar way, manipulating the soil pH has shown some positive effects in lowering Fusarium wilt severity in strawberry (Fang et al., 2012b) and other crops (Jones and Woltz, 1970); consistent experimental results, however, are lacking (Gordon, 2012) and commercial growers have not adopted pH manipulations as a management practice.

4.10. Disease management summary In summary, if available, resistant strawberry cultivars would be the first and preferred means of managing Fusarium wilt. If such cultivars are not available, pre-plant chemical treatment of the soil can significantly reduce soil inoculum levels if efficacious materials are used with appropriate application methods. Non-chemical preplant treatments such as steam, solarization, and anaerobic soil disinfestation show potential in reducing soil inoculum levels but all have limitations. If possible, growers should practice crop rotation by not over-planting strawberry in infested locations and by planting strawberry in fields not known to be infested. Pathogen exclusion steps such as planting only Fusarium-free transplants and avoiding the spread of the pathogen on contaminated field equipment are essential measures.

5. Other Fusarium diseases of strawberry In addition to Fusarium wilt, other Fusarium diseases have been reported on strawberry. A minor strawberry fruit disease is caused

by Fusarium sambucinum and is called fruit blotch (Hunter and Jordan, 1974). This disease causes small (1e2 mm) purple to red lesions on unripe fruit. This disease is infrequently found and control measures are apparently not needed. A crown and root rot caused by Fusarium solani has been reported in Spain (Pastrana et al., 2014). Symptoms of this disease are very similar to those caused by Fof and consist of stunted plants, wilting and drying of older foliage, orange to brown discoloration of internal crown cortical and vascular tissues, and eventually plant collapse and death (Pastrana et al., 2014). In Italy and Mexico a disease known as black root rot, also named strawberry dry wilt (secadera) in Mexico, causes significant crop loss and involves an F. oxysporum pathogen.

However, reports indicate that this disease is associated with an apparent complex of organisms that includes the following: F. oxysporum, F. solani, Alternaria sp., Colletotrichum sp., Cylindrocarpon sp., Phytophthora sp., Pythium aphanidermatum, Rhizoctonia sp., Verticillium sp. (Ceja-Torres et al., 2014, 2008; Manici et al., 2005; Narro-Sanchez et al., 2006). The role of F. oxysporum in this complex, and the relationship of the black root rot or secadera

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F. oxysporum to Fof, both remain unclear. The overall etiology of strawberry dry wilt in Mexico remains unconfirmed. Management programs for these soilborne diseases have not been formally established. Traditional IPM strategies of planting tolerant or resistant cultivars, applying effective pre-plant soil treatments, rotating with non-host crops, planting in fields that do not have a history of these problems, and preparing well draining beds should minimize these problems.

Acknowledgments We thank the California Strawberry Commission for supporting our research on this disease.

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Please cite this article in press as: Koike, S.T., Gordon, T.R., Management of Fusarium wilt of strawberry, Crop Protection (2015), http://dx.doi.org/ 10.1016/j.cropro.2015.02.003