Review and Critical Analysis of Soilborne Disease Management in the Vegetable Sector

Introduction

Soilborne pathogens cause significant losses in vegetable crops from nursery to harvest.
Vegetables are highly susceptible to diseases due to their dynamic nature, wide variety, continuous innovation, and intensive cultivation.
Italy is an interesting case study due to its intensive vegetable production and diverse phytopathological problems.
The phaseout of methyl bromide on January 1st, 2005, in industrialized countries, particularly those with intensive use like Italy, has made some phytopathological problems difficult to manage.
The re-evaluation of pesticides under European Directive 91/414/EEC dramatically reduced available fumigants.
Dazomet was authorized as a soil fumigant from June 1st, 2011, for 10 years, followed by metham (including -potassium and -sodium) approved from July 1st, 2012.
Both soil fumigants may be authorized for pre-planting application, limited to once every three years on the same field.
Chloropicrin was withdrawn by June 23, 2012, with a grace period until June 23, 2013.
1,3-dichloropropene (1,3-D) authorization was withdrawn in 2008, and a new application was rejected in 2011; however, some Member States granted emergency use authorizations.
The new European regulation, Reg. (EC) No. 1107/2009, will further reduce the crop protection portfolio due to hazard-based cut-off criteria.
Studies indicate a loss of about 50% of registered fungicides and fumigants, with a further 20–64% of remaining fungicide candidates for substitution (Backhaus 2010).
Directive 2009/128/EC on sustainable use of pesticides will strongly affect soilborne disease management, requiring preference for non-chemical methods starting in 2014.
This review concentrates on the situation of vegetable crops where methyl bromide has been replaced by other techniques, including host resistance and grafting, focusing on practical problems encountered in Italy, such as the emergence of new or re-emergence of old diseases.

Soil Disinfestation Strategies

Initially, growers replaced methyl bromide with other fumigants, often in mixtures, but this was understood to be temporary.
To reduce the environmental impact of fumigant application, virtually or totally impermeable film (TIF) is used as soil mulching to reduce dosage and emissions (Yates et al. 2002).
Mixtures of chemicals should be part of integrated pest management systems (Duniway 2002), but some combinations are not always applicable.
Metham sodium co-application with 1,3-dichloropropene or chloropicrin is not always effective; the efficacy of 1,3-dichloropropene and chloropicrin in mixture with metham-sodium is strongly reduced in wet soil (Guo et al. 2005).
Methyl isothiocyanate generators, 1,3-dichloropropene, and chloropicrin require soil temperatures above 10°C to be effective, limiting their use in Mediterranean countries to between May and September (Gullino et al. 2007).
Other chemicals initially foreseen as methyl bromide replacements, such as methyl iodide, propargyl bromide, sodium azide, have not reached the market, while dimethyl disulfide is still under development (Gullino et al. 2007).
Host resistance is an effective strategy, with resistant or tolerant varieties available for many vegetable crops, and the industry is investing in this field.
Resistant hybrids with multiple resistance to several pathogens have been available for a long time.
Grafting susceptible crops onto resistant rootstocks is used for crops like tomato, cucumber, and melon (King et al. 2008).
Chellemi (2002) reviewed the contribution of host resistance for managing tomato diseases.
Despite disadvantages like additional cost and physiological disorders, the use of resistant rootstock has increased, mainly for tomato, bell pepper, and melon.
In Italy, 59 million vegetable plants are grafted to reduce susceptibility against pests, root rots and wilts, and to increase yield (Rouphael et al. 2010).
Grafting confers resistance to Meloidogyne incognita in bell pepper (Kokalis-Burelle et al. 2009), to Phytophthora nicotianae (Hamdi et al. 2010), and to P. capsici, Verticillium dahliae, and Rhizoctonia solani (G. Gilardi et al., personal communication).
Commercial tomato rootstocks showed resistance to F. oxysporum f. sp. radicis-lycopersici (FORL), V. dahliae, and F. oxysporum f. sp. lycopersici (FOL race 1) under artificial inoculation conditions.
Resistance or partial resistance to F. oxysporum f. sp. lycopersici (FOL race 2) was confirmed with plants inoculated at 30 days, while it was restricted to ‘Maxifort’ and ‘He-man’ in the case of plants inoculated at the age of 15 days.
Two P. nicotianae strains, PH18 and PH20, isolated from the same host (Solanum lycopersicum × Solanum hirsutum ‘Beaufort’), showed different virulence (Gilardi et al. 2011).
Investments in soilless cultivation systems occurred in many vegetable production areas, but high initial investment costs and problems related to the disinfestation, recycling, and disposal of recirculated solutions are major constraints (Garibaldi and Gullino 2010).
This method is gaining popularity in Italy, particularly for high-value vegetable crops like basil, tomato, lettuce, and other leafy vegetables.
Soilless cultivation avoids soil fumigation but requires proper disinfection of recirculating nutrient solutions, mostly based on slow sand filtration.
New developments of steam application methods, such as subsurface steam injection and surface steam application by means of iron pan and sheet steaming, were tested to reduce costs and extend use on crops grown outdoors (Lu et al. 2010b).
Steam injection and pan steaming are effective techniques for steaming, more effective and feasible than sheet steaming at a soil moisture of 60% field capacity (Lu et al. 2010b).
Soil moisture did not influence pathogen suppression in the upper soil layer with pan steam treatment, but eradication was complete at 80% field capacity.
Steam injection strongly controlled the tested fungi also at 40% and 80% field capacity.
Injection can heat soil at 19 cm depth, whereas the pan distribution system can reach depths between 9 and 13 cm (Lu et al. 2010b).
Pan steaming is suitable for short-cycle intensive crops like lettuce, while deeper steam injection is suitable for long-term crops.
Organic soil amendments for soilborne disease suppression are not widely implemented due to concerns about potential side-effects.
Using Brassica species as green manure is a type of biofumigation, releasing isothiocyanates, thiocyanates, nitriles, or oxazolidinethiones that control multiple soilborne problems (Larkin and Griffin 2007), particularly in less intensive agricultural systems.
Biofumigation is achieved by incorporating fresh plant material (green manure), seed meals, or dried plant material treated to preserve isothiocyanate activity, or by using brassica intercrops.
The effectiveness of organic amendments, including brassica residues, is variable and can enhance disease severity (Lu et al. 2010a).
Negative effects may result from increased pathogen inoculum potential or from the amendments themselves (Manici et al. 2004; Lu et al. 2010a).
Seed meals are more interesting in intensive cropping systems, but their effect on both target and non-target organisms can be a drawback (Mazzola et al. 2012).
Combining amendments with solarization can be effective, generating biotoxic volatile compounds and increasing microbial antagonistic activity (Gamliel 2000), but practical applications are few.
Disadvantages include dependence on environmental conditions, the nature and incidence of pathogens, and high labor costs (Gamliel et al. 2000).
This approach is interesting for organic farming, where incorporating grass combined with plastic mulching proved effective against many soilborne pests and pathogens (Goud et al. 2005).
Lettuce soil amendments were effective against Fusarium oxysporum f. sp. radicis-cucumerinum (Pavlou and Vakalounakis 2005).
Biocontrol agents (BCAs) often fail to control disease in the field when applied alone but work when combined with other control measures (Garibaldi and Gullino 2010).
A limited number of BCAs are included in the list of approved plant protection products under Reg. No 1107/2009.
Coniothyrium minitans and several strains of Trichoderma spp. are currently used by European farmers (Tjamos et al. 2010).
Some substrates and compost have suppressive effects towards selected soilborne pathogens.
Hardwood bark (composted or not) generally improves plant growth, especially in potted plants, due to its physical characteristics and higher levels of antagonists (Noble and Coventry 2005; Termorshuizen et al. 2006).
To improve consistency, BCAs are added to compost amendments, which provide a food base for BCAs of soilborne pathogens.
Mixtures of bacterial and fungal BCAs are more effective than single BCAs in inducing suppression of Rhizoctonia and Pythium (Noble and Coventry 2005; Pugliese et al. 2008, 2011).
A practical problem for applying compost to suppress soilborne diseases is the lack of methodology for predicting disease suppression for an individual pile of compost (Hadar 2011).
When such methods are developed, compost amendments could be used in nurseries as partial substitutes for peat, with advantages in terms of cost, production, and environmental impact (Hadar 2011).

Emerging Problems and Solutions

Several different formae speciales of F. oxysporum have been reported on vegetables in recent years.
Fusarium wilts have been observed recently in Italy on lettuce (Lactuca sativa), wild (Diplotaxis spp.) and cultivated (Eruca sativa) rocket, lamb’s lettuce (Valerianella olitoria), cichory (Cichorium intybus), and endive (Cichorium endivia) (Matheron and Gullino 2012).
These diseases are emerging as major production problems in Lumbardy and represent a potential threat to vegetable production.
Being seed-transmitted, they spread easily.
Many widely grown lettuce varieties are susceptible to Fusarium wilt.
Using resistant cultivars and seed dressing are among the best strategies for limiting Fusarium wilt of lettuce (Matheron and Gullino 2012).
Disease resistance is not always perfect and can be overcome by the appearance of new races of the pathogen.
Phytophthora capsici and P. nicotianae are recurrent problems, with P. nicotianae becoming important on tomato.
Rhizoctonia solani was recently detected in Italy on Diplotaxis tenuifolia and Valerianella olitoria.
Crown and root rot of strawberry, incited by Macrophomina phaseolina, has been recently reported in several production areas, related to the difficulties in replacing methyl bromide on strawberry (Avilés et al. 2008; Koike 2008; Zveibil and Freeman 2005).
In grafted plants, resistance may be broken down under high disease pressure, with new races of pathogens evolving on rootstocks.
Other limitations are related to the evolution of new strains of pathogens, while pathogens generally considered minor can become major pathogens on the rootstocks in the absence of soil fumigation.
Recently, new diseases were recorded in Italy on grafted plants.
Verticillium wilt incited by Verticillium dahliae was consistently observed on eggplant grafted on Solanum torvum, while Colletotrichum coccodes attacks were observed on grafted tomato plants after repeated cropping cycles of tomato.
The combination of grafting on resistant rootstock and soil fumigation with dimethyl disulfide or metham-sodium was effective (Garibaldi et al. 2008).
Phytophthora nicotianae and P. capsici can affect tomato (Erwin and Ribeiro 1996).
Rootstocks belonging to interspecific hybrids of Solanum lycopersicum x S. hirsutum (cvs. Beaufort, He-Man) and to S. lycopersicum (cv. Energy) were infected by P. nicotianae.
Pathogenic variation among the isolates of P. nicotianae requires further studies to evaluate the possibility of existence of different physiological races within this species (Garibaldi and Gullino 2010), while P. capsici is a pathogen showing a high degree of variability and variation among isolates (Foster and Hausbeck 2010).
Increased symptoms of basal rots caused by Rhizoctonia solani (anastomosys group AG4) were repeatedly observed on tomato grafted onto S. lycopersicum x S. hirsutum under greenhouse conditions.
Phytophthora capsici, P. nicotianae, and C. coccodes showed a broad host range among solanaceous and cucurbitaceous crops, limiting the success of crop rotation.
Colletotrichum coccodes has been recently reported on pepper grafted onto ‘Rocal’ (G. Garibaldi et al., personal communication).
Another emerging and destructive disease present worldwide is vine decline of cantaloupe and other cucurbits, caused by Monosporascus cannonballus (Cohen et al. 2000).
The pathogen has been reported in Italy on watermelon, melon, and cucumber.
Disease problems of soilless cultivation systems can be solved by adopting proper disinfection methods for the recirculating solution.
In Italy and Northern Europe, slow sand filtration has proven effective for water disinfestation.
Indigenous microflora and introduced microbial antagonists in the recirculating solution reduced disease incidence in soilless systems (Garibaldi et al. 2003; Postma 2004).
Closed recirculating soilless systems are interesting for exploiting biological control through microbial optimization (Postma et al. 2006).
Slow sand filtration combined with the application of different antagonistic strains belonging to Fusarium spp. and Trichoderma spp. proved effective against Phytophthora cryptogea of gerbera (Garibaldi et al. 2003).
Suppressiveness of re-used substrates adopted in soilless cultivation represents a very interesting feature (Clematis et al. 2009).
The selection and application of bacterial strains isolated from soilless systems proved effective against Fusarium wilt and Fusarium crown and root rot of tomato and rocket (Liu et al. 2010; Srinivasan et al. 2009), while strains of Trichoderma spp. isolated from soilless systems controlled Pythium ultimum on cucumber.

Conclusions

The search for effective, economically and environmentally sound methods for soil and substrate disinfestation remains a continuous and challenging task.
European Regulation No 1107/2009 and Directive No 2009/128/EC require all professional users to implement the general principles of IPM by 2014.
Research efforts associated with the phaseout of methyl bromide generated new knowledge about the biology, ecology, and management of soilborne pathogens (Gullino et al. 2007; Katan 2000) and led to more attention towards crop and soil health (Katan and Vanachter 2010).
Regulatory pressure will stimulate the development of sustainable practices to control soilborne pests and diseases.
Sustainable cropping systems require broad multidisciplinary cooperation (Chellemi 2010).
Dependence on a single method of control is vulnerable to changes in regulatory policies, input costs, or the emergence of new pathogens (Chellemi 2010; Katan 1999).
Researchers and extension services should validate new proposed strategies under different situations.
Future research should address the need for decision-making tools to determine populations and economic thresholds of pathogens.
A high priority should be placed on the production and use of pathogen-free propagation material (Garibaldi and Gullino 2010).
More research on etiology, monitoring, modeling, and breeding for resistance is also needed.
Understanding changes in the biotic and abiotic components of the soil or substrate caused by any treatment may enable full exploitation of its control potential (Garibaldi and Gullino 2010).
The methyl bromide phaseout made it clear that dependence on a single method should be avoided and that traditional methods such as crop rotation, use of organic amendments, and grafting should be reintroduced (Katan 1999, 2000).
Extension services and growers are applying several strategies in combination, shifting more and more to the adoption of non-chemical methods and checking their long-term effectiveness.

Numerical References

European Regulation No 1107/2009
European Directive No 2009/128/EC
European Directive 91/414/EEC
Reg. (EC) No. 1107/2009
Directive 79/117/EEC
Directive 91/414/EEC