ࡱ> 5@ bjbj22 XXC444gggX ijt|m&o(ooos"st $RBM4O ~ JtttTg"gGeneral enquiries on this form should be made to: Defra, Science Directorate, Management Support and Finance Team, Telephone No. 020 7238 1612 E-mail: research.competitions@defra.gsi.gov.ukSID 5Research Project Final Report l Note In line with the Freedom of Information Act 2000, Defra aims to place the results of its completed research projects in the public domain wherever possible. The SID 5 (Research Project Final Report) is designed to capture the information on the results and outputs of Defra-funded research in a format that is easily publishable through the Defra website. A SID 5 must be completed for all projects. This form is in Word format and the boxes may be expanded or reduced, as appropriate. l ACCESS TO INFORMATION The information collected on this form will be stored electronically and may be sent to any part of Defra, or to individual researchers or organisations outside Defra for the purposes of reviewing the project. Defra may also disclose the information to any outside organisation acting as an agent authorised by Defra to process final research reports on its behalf. Defra intends to publish this form on its website, unless there are strong reasons not to, which fully comply with exemptions under the Environmental Information Regulations or the Freedom of Information Act 2000. Defra may be required to release information, including personal data and commercial information, on request under the Environmental Information Regulations or the Freedom of Information Act 2000. However, Defra will not permit any unwarranted breach of confidentiality or act in contravention of its obligations under the Data Protection Act 1998. Defra or its appointed agents may use the name, address or other details on your form to contact you in connection with occasional customer research aimed at improving the processes through which Defra works with its contractors. Project identification 1. Defra Project code FORMTEXT PS21172. Project title  FORMTEXT Potential of simple salts to partially substitute for conventional foliar fungicides on crops 3. Contractor organisation(s)  FORMTEXT Harper Adams University College  FORMTEXT        FORMTEXT        FORMTEXT        FORMTEXT        FORMTEXT       54. Total Defra project costs  FORMTEXT 41,425 (agreed fixed price) 5. Project: start date  FORMTEXT 01 April 2007  end date  FORMTEXT 31 March 2008 6. It is Defra s intention to publish this form. Please confirm your agreement to do so. YES  FORMCHECKBOX  NO  FORMCHECKBOX  (a) When preparing SID 5s contractors should bear in mind that Defra intends that they be made public. They should be written in a clear and concise manner and represent a full account of the research project which someone not closely associated with the project can follow. Defra recognises that in a small minority of cases there may be information, such as intellectual property or commercially confidential data, used in or generated by the research project, which should not be disclosed. In these cases, such information should be detailed in a separate annex (not to be published) so that the SID 5 can be placed in the public domain. Where it is impossible to complete the Final Report without including references to any sensitive or confidential data, the information should be included and section (b) completed. NB: only in exceptional circumstances will Defra expect contractors to give a "No" answer. In all cases, reasons for withholding information must be fully in line with exemptions under the Environmental Information Regulations or the Freedom of Information Act 2000. (b) If you have answered NO, please explain why the Final report should not be released into public domain  Executive Summary7. The executive summary must not exceed 2 sides in total of A4 and should be understandable to the intelligent non-scientist. It should cover the main objectives, methods and findings of the research, together with any other significant events and options for new work. Overall Aim: The scoping study aimed to explore the potential of reducing the environmental and food chain burden of chemical fungicides by exploiting research which has shown that the severity of certain fungal pathogens, of both protected and field crops, can be reduced from applications of inorganic salts. Background-Literature Review: The first of three objectives was to conduct a literature search on the topic of fungal disease control by inorganic salts by performing keyword searches on bibliographic databases, such as Web of Science and Google Scholar. A systematic survey of the available scientific literature on a global scale revealed 34 inorganic salts involved in the suppression of 49 fungal diseases across 35 plant species. Proven antifungal activity occurs in each of five groups of inorganic salts: 1) bicarbonates (e.g. NaHCO3), 2) phosphates (e.g. KH2PO4), 3) silicates (e.g. K2SiO3), 4) phosphites (e.g. KH2PO3) and 5) chlorides (e.g. KCl). Only one group, the phosphites, appeared to be target-specific (Phytophthora spp. and downy mildews); the other groups were found to possess a broad spectrum of antifungal activity, mainly against foliar and soilborne fungi, but even against postharvest fungi. Many contradictory reports were found with regard to the mode of action of inorganic salts as antifungal substances. Collection and comparison of data from the most relevant, robust and advanced studies, indicated that the most likely mechanisms involved are: 1) pH elevation and dehydration of fungal spores (HCO3-salts), 2) induction of systemic acquired resistance (PO4-salts), 3) strengthening of cell walls on leaf surfaces resulting from the accumulation of flavonoid phytoalexins (SiO3-salts), 4) strong and rapid stimulation of plant defence mechanisms and direct inhibition of fungal sporulation (PO3-salts) and 5) osmotic regulation (Cl-salts). Powdery mildews of cucurbits (mainly cucumber), grapes, wheat and fruit trees were the most studied diseases (accounted for almost one-third of all crop/pathogen/salt combinations) and most effectively and consistently managed by: 1) foliar applications of inorganic salts or 2) hydroponic nutrient solutions amended with SiO3-salts (cucurbits). The existing evidence for these salts indicates that they are in general less efficacious than conventional fungicides and could not, on their own, replace them. It appears that little work has been published on tank mixtures of salts with fungicides. However, experiments on mangos and grapes have revealed that tank mixtures of phosphates or silicates with half- or full-rate fungicides, respectively, enabled a 50% reduction in the number of fungicide applications needed to control powdery mildew. This suggests that such an integrated approach should be investigated further. The use of alternate programmes (i.e. salts and fungicides applied in rotation) in the management of foliar fungal diseases, for which more publications were found relative to tank mixtures, also enabled a reduction in the frequency of fungicide applications required for effective control. These findings translate to both cost and environmental benefits and merit further investigations in the UK. Commercial Use: The second objective was to conduct a review of the current commercial use of inorganic salts as alternatives to fungicides or as components of integrated disease management strategies. The starting point was Internet searches of those inorganic salt-based products identified from the literature survey as having potential for fungal disease control. Direct contact with companies selling such products for this purpose was also established. Further to general technical information found on products labels, particular attention was given to the following: 1) Identification of criteria and current registration status for inorganic salts used in fungal disease control in the UK and the USA, 2) Evidence for compatibility with organic crop production systems, 3) Fungal pathogen-crop combinations where cost benefit and efficacy have justified commercial application), 4) Evidence of combined use of products containing inorganic salts with conventional fungicides, 5) Comparative efficacy with fungicides and 6) Market size. The key findings of these investigations are as follows: 1) 25 commercial salt-containing products are registered in the USA by the Environmental Protection Agency (EPA) as biopesticides with approved uses for fungal disease control (14 phosphites, 7 bicarbonates, 4 phosphates), 2) Four inorganic salts (CuSO4, KHCO3, NaHCO3 and K2SiO3) will have been approved by the National Organic Program (NOP) of the US Department of Agriculture (USDA) by the end of 2008 for use in organic farming, specifically for fungal disease control, 3) Potassium bicarbonate has been granted a Commodity Substance Approval in the UK by the Pesticide Safety Directorate (PSD) and can be used on all crops (outdoor and protected) as a horticultural fungicide, 4) No commercial products approved for use in fungal disease control were found for chloride salts. 5) The market for phosphites has developed since 2001 in the USA and is now in the region of $4-5 million. Implications for future research: The third objective was to identify the scope for further research in the UK. The main target for further research has been identified as powdery mildew (Sphaerotheca fuliginea) in cucurbits because: 1) there is good evidence for control (maximum efficacy 41-99%) by foliar sprays of several inorganic salts from at least 20 peer-reviewed publications, 2) the industry finds it difficult to control, 3) there are very few approved fungicides (e.g. three in pumpkin, all off-label) and there is evidence for resistance to one (bupirimate), 4) potassium bicarbonate has a UK Commodity Substance Approval for this disease.   Project Report to Defra 8. As a guide this report should be no longer than 20 sides of A4. This report is to provide Defra with details of the outputs of the research project for internal purposes; to meet the terms of the contract; and to allow Defra to publish details of the outputs to meet Environmental Information Regulation or Freedom of Information obligations. This short report to Defra does not preclude contractors from also seeking to publish a full, formal scientific report/paper in an appropriate scientific or other journal/publication. Indeed, Defra actively encourages such publications as part of the contract terms. The report to Defra should include: l the scientific objectives as set out in the contract; l the extent to which the objectives set out in the contract have been met; l details of methods used and the results obtained, including statistical analysis (if appropriate); l a discussion of the results and their reliability; l the main implications of the findings; l possible future work; and l any action resulting from the research (e.g. IP, Knowledge Transfer). Statement of objectives The scientific objectives of this project were: To review the scientific literature on fungal disease control with inorganic salts for both protected and field crops on a global basis. To review the current commercial use of salts for fungal disease control for both protected and field crops on a global basis. To assess the scope for potential use of simple salts on fungal pathogens of major conventional and organic crops in the UK, alone or in combination with conventional fungicides, leading to a recommendation of crops, target pathogens, salts and conventional fungicides (where appropriate) warranting further research and development in collaboration with industry through LINK. The above objectives were fully met. The work was conducted by Dr. Thomas Deliopoulos under the direction of Dr. PS Kettlewell and Dr. MC Hare. The action resulting from this research is described at the end of this report. 1. Objective 1 Review of scientific literature Status: fully achieved Research over the last few decades for alternative substances with fungicidal properties has revealed that a potentially useful component of integrated disease management (IDM) programmes against foliar fungal pathogens can be spray applications of inorganic salts, such as chlorides (Mann et al., 2004), phosphates (Mitchell and Walters, 2004) and bicarbonates (Fallik et al., 1997). Although the component ions in salts can be either inorganic or organic, salts of the latter type, such as benzoates and acetates, are not discussed here as they are synthetic compounds with very little evidence for fungitoxic activity in comparison with inorganic salts and therefore were out of the scope of this review. Information on phytotoxicity from the use of inorganic salts is provided only in a small proportion of published articles and therefore when such data were available full details are given. The review covers inorganic salts tested worldwide for their effects on fungal disease control, including salts of heavy metals/metalloids; exceptions are: (I) heavy metals or metalloids that occur often as environmental pollutants, that is Cd, Pb, Zn, Ni, Sb and Bi (Rengel, 2003) and (II) heavy metals prohibited to be placed on the market and used as plant protection products under the EU Council Directive 79/117/EEC (e.g. mercuric salts) (Anon., 1979). The present study was designed with the aim of assessing the potential for reducing the environmental and food chain burden of conventional crop fungicides by exploiting the findings of the research described above. It also aimed to explore the possibility of using inorganic salts: 1) against fungal pathogens for which there is evidence for resistance to synthetic fungicides and 2) on crop/pathogen combinations for which there are few active substances available. To achieve these targets, the available scientific literature on fungal disease control with simple inorganic salts for both protected and field crops was reviewed on a global basis. Information on the use of inorganic salts in fungal disease management was collected primarily from peer-reviewed papers. Relevant research reports and publications from governmental agencies and levy bodies, such as EPA (Environmental Protection Agency), the European Commission, HDC (Horticultural Development Council) and PSD (Pesticide Safety Directorate) were also included. Initial citation searches were taken from PhD literature surveys previously undertaken at Harper Adams University College (Cook, 1997; Mann, 1999). The majority of original papers, however, were identified from web-search based tools (mainly Web of Science but also Google Scholar) and obtained through the University College library electronic and hard copy journal subscriptions. When full-text papers were unavailable on-site, they were supplied by the British Library. All collected references were categorised into five main groups (see section 4.1) plus an extra group of miscellaneous relevant literature, using Endnote software version 9. Particular emphasis was given to recent papers, published in the course of the last 10 years, due to the tremendous advances in molecular biology and other scientific methods, which have aided in understanding the mode of action of several inorganic salts. Numerous inorganic salts have been evaluated worldwide for their efficacy against fungal pathogens and the majority of published reports describe reductions in disease severity. The most common method of application involves foliar sprays with or without an adjuvant (e.g. oils, sucrose etc.). Some inorganic salts are applied through hydroponic nutrient solutions (root-applied, silicates only), while others are applied to the soil surface or as seed treatments. Their effectiveness has been investigated under a broad range of conditions, including, most commonly, glasshouse and field experiments, but also in vitro and controlled environments. The range of crops on which inorganic salts have been trialled for their suitability to suppress fungal diseases is also wide and includes both field and protected crops. The number of potential target fungal pathogens is also large covering diseases of the foliage, stem, ear, fruit/tubers (pre- and post-harvest), seed and the root. Emphasis is given to plant diseases affecting aerial plant parts, typically managed by foliar applications of conventional fungicides. Soilborne fungal diseases against which salts have shown proven efficacy are also discussed, but to a lesser extent. Powdery mildews are the diseases which control with inorganic salts has been investigated the most (more than 50 citations). These inorganic salts are of low mammalian toxicity and most are widely used as food ingredients (Lindsay, 1985) or fertilisers (Simpson, 1986; Fixen, 1993). The evidence for disease control by these salts indicated that they were mostly less efficacious than conventional fungicides and could not replace them. Nevertheless, if used in mixture with fungicides or as a supplementary measure to an existing fungicide programme, inorganic salts could enable the quantity of conventional active substances or the number of fungicide applications to be reduced, therefore providing a more sustainable method for fungal disease control. It can be concluded that spray applications of inorganic salts can be a very useful component in the integrated management of foliar fungal diseases, particularly powdery mildews, and could lead to environmental and financial benefits. The main body of the Literature Review is presented in Section 4, after the report on Objective 3. 2. Objective 2 Review of commercial use Status: fully achieved The starting point for collecting information on the current commercial use of inorganic salts in crop protection was Internet searches. A database of inorganic salt-based products exhibiting antifungal activity and of corresponding companies found in research papers from the literature survey (Objective 1) was initially created. Names of products and companies were then used as search terms in order to find their websites and obtain some technical (e.g. application rates and methods, spectrum of uses) and other information (e.g. effects on humans and the environment). Additional products not present in peer-reviewed journals were identified online and added to our database; sources were farming magazines, university/research stations trials results, gardener handbooks, technical bulletins and reports/newsletters from levy bodies. This was achieved by performing searches using relevant terms, such as biopesticides, natural/food-grade/environmentally friendly substances or using the names of particular salts (e.g. potassium bicarbonate) or their group (e.g. bicarbonates) or more specifically using the names of particular crop/pathogen/salt combinations. Data availability varied with company; some would provide online the products MSDS and label, while others would describe the basic properties of their product in the form of material fact sheet, advantages of product, press release or technical information. In addition to gathering general technical information for commercial products containing inorganic salts, attention was given to their registration status (Table 1), as this relates to the conditions under which these products can be sold and used. Direct contact with companies selling such products was also established by a variety of methods including email, telephone or personal communication at agricultural events and conferences, e.g. in the Potato 2007 BPC Event, Harrogate and the International Plant Protection Congress 2007, Glasgow. The aim was to obtain some extra information on the current commercial use of inorganic salts mainly not available online. A questionnaire was also prepared and emailed or submitted via online forms to ten companies requesting information on the following topics: 1) Field/glasshouse trials results, 2) Range of crop-pathogen combinations where efficacy and cost benefit have justified commercial application, 3) Application methods and rates, 4) Evidence of combined use of name of product with fungicides, 5) Comparative efficacy with fungicides and 6) An indication of quantities sold. Although most companies responded, only five provided us with some data. The rest could not supply the information requested due to the proprietary nature of the data from a technical and business perspective but some advised us to look up brochures available on their website for technical information. One company, Nufarm Americas, Inc., provided information on the comparative efficacy of their product with synthetic fungicides. By far the best response was received from PQ Corporation (Dr. Judy Thompson), a US company that has formulated three K2SiO3-based products; Sil-MATRIX"!, AgSil and KASIL 6. In addition to answering as many of our queries as possible, the company provided us with 13 attached documents on the beneficial effects of K2SiO3 on crop protection, including revised petition to the National Organic Program (NOP) of the US Department of Agriculture (USDA), publications on the use of silicates against fungal pathogens but also against species of insects and nematodes. As informed by the company, the petition mentioned above for aqueous K2SiO3 has been approved by the National Organic Standards Board (NOSB) and it will be allowed for organic growing by the end of 2008. PQ Corporation also informed us that in the USA, to make any claim of plant disease control (whether or not it is a direct effect on the pathogen), the material must be registered with the EPA as a pesticide. Sil-MATRIX"! ( HYPERLINK "http://www.pqcorp.com/products/SilMATRIX.asp" http://www.pqcorp.com/products/SilMATRIX.asp) is an EPA-registered pesticide and consequently the company can make the pesticide claims. This is the only K2SiO3 product sold for crop protection uses in the USA. Information on application rates is available on the EPA label. It is registered for control of the following diseases: 1. powdery mildew grapes, cucurbits, ornamentals, 2. Botrytis blueberry, 3. root diseases such as Pythium, Fusarium crown and root rot cucurbits, peppers, 4. turf diseases including dollar spot, gray leaf spot, brown patch and powdery mildew. The product is also approved for insecticide and miticide uses. Nufarm Americas, Inc., provided data on the use of Phostrol. The main active substances in Phostrol (53.6%) are mono- and dibasic salts of phosphorous acid. The product is labelled as fungicide with EPA and is included in the list of biopesticides. Target fungi include various Phytophthora and Pythium spp. and it can be used on many food and non-food crops, including turf, ornamentals and trees. The company has conducted two trials to compare the efficacy of Phostrol and Alliete in the control of Phytophthora palmivora, causal agent of brown rot. There were significant decreases (ranging from 35-90%) in disease incidence for both Phostrol- and Aliette-treated fruit 45 and 90 days after treatment, compared with the untreated. In both trials and observation dates, fruit treated with Phostrol had lower incidence of brown rot than Aliette, but the difference was significant only in one trial at the 90-day time period (c. 90% lower disease incidence in the former than the latter). The company also sent us results from research trials on the efficacy of Phostrol (as foliar spray or postharvest treatment) against potato late blight and pink rot, in comparison with various synthetic fungicides (Ag Clor 310, Oxidate, Ranman 400, Ridomil Gold 4EC). Data showed that: a) Phostrol was consistently more effective than the competitive treatments against both diseases and b) late blight control was optimised with three foliar applications of Phostrol at 14 l ha-1. The US market for phosphites was non-existent in 2001 and is worth about $4-5 million today. Currently, the biggest markets in the USA are citrus, potatoes, leafy vegetables and grapes (Scott Reichl, Nufarm Americas, personal communication). Mr Gary Schmunk, marketing manager of Helena Chemical Company informed us that Eco-Mate Armicarb O, which contains 85% KHCO3 active substance, is a registered product approved for use in organic crop production by the USDA NOP. It is approved for use on 89 plant species for the control of 20 foliar fungal diseases including several spots, blights and powdery mildews. In the USA, any substance to be used in organic production has to be certified by the NOP. Petitions are prepared by companies and submitted for consideration to the NOSB in collaboration with a panel of technical advisory reviewers. Each of three reviewers uses scientific data to evaluate the proposed substance against seven criteria: 1. Potential for detrimental interactions with other materials used, 2. Toxicity, mode of action, breakdown products, persistence in the environment, 3. Probability of environmental contamination, 4. Effects on human health, 5. Effects on biological and chemical interactions in the agro-ecosystem, 6. Availability of alternatives and 7. Compatibility with sustainable agriculture. The analysis summary includes the reviewers recommendation to NOSB on: a) whether the substance should be listed as synthetic or non synthetic in the National List of Allowed and Prohibited Substances and b) whether the substance should be allowed or prohibited in organic crop production. The National List of Allowed and Prohibited Substances is a list of exceptions to the general requirement that all naturally-occurring substances are allowed (unless listed as prohibited) and all synthetics are prohibited (unless they are on the list). Such substances may be synthetic, non-synthetic or non-agricultural (non-organic). Three inorganic salts petitioned for use in organic crop production, CuSO4 and KHCO3 (synthetic) and NaHCO3 (non-synthetic), have been specifically approved by NOSB for use in plant disease control without restrictions. Similar approval has been granted for horticultural oils, which are used as surfactants in foliar applications of inorganic salts. Other inorganic salts that have been approved by NOSB for use in organic crop production (allowed for specific uses or prohibited with exceptions) include: NaSiO3 (synthetic) allowed only as floating agent in postharvest handling, CaCl2 (non-synthetic) prohibited unless used as foliar spray to treat physiological disorders associated with calcium uptake, KCl (non-synthetic) prohibited unless it derives from mined sources and is applied in a manner that minimises chloride accumulation in soil. A revised petition has been recently submitted to NOSB by PQ Corporation (Dr. Judy Thompson, personal communication) for aqueous K2SiO3 to be allowed for use in organic crop production. Further information on the current status of inorganic salts with respect to their use in organic agriculture in the USA (with NOSB recommendations) is available at  HYPERLINK "http://www.ams.usda.gov/NOP/indexIE.htm" http://www.ams.usda.gov/NOP/indexIE.htm. Several inorganic salts were found to be included in the EPA website list of biopesticides (Table 2). Biopesticides are defined by the EPA as naturally occurring substances that control pests and classified in three main groups: a) biochemical pesticides (includes the inorganic salts), b) microbial pesticides and c) plant-incorporated protectants (http://www.epa.gov/pesticides/biopesticides/index.htm). In Europe, biopesticides are regulated under Council Directive 91/414/EEC and are divided into four groups: a) biochemicals (includes inorganic salts), b) semiochemicals, c) microorganisms and viruses, d) macroorganisms. According to this Directive, before an active substance, including inorganic salts, can be approved for plant disease control, it has to be thoroughly evaluated in relation to six specialised areas: a) physical chemical properties, b) methods of analysis, c) mammalian toxicology and worker exposure, d) residues, e) ecotoxicology and f) efficacy ( HYPERLINK "http://www.pesticides.gov.uk/approvals.asp?id=247" http://www.pesticides.gov.uk/approvals.asp?id=247). Similarly, in the USA, the Federal Insecticide, Fungicide and Rodenticide Act (FIFRA) requires that EPA carries out extensive evaluation of the proposed substance to assure that there will be no unreasonable risks of harm to human health and the environment from its use ( HYPERLINK "http://www.epa.gov/pesticides/biopesticides/index.htm" http://www.epa.gov/pesticides/biopesticides/index.htm). According to the EPA, the use of KHCO3 and NaHCO3 as fungicides was not expected to have any adverse effects on humans and the environment and would possibly offer an alternative to the more toxic conventional fungicides. The two compounds were eventually registered in the USA as pesticide ingredients in 1994 (Greenway, 1999). An additional advantage with respect to the use of these substances in plant disease management is that in 1996, the EPA has ruled that both are exempt from pesticide residues legislation. This development illustrates that the use of these materials is in accordance with food safety regulations and would facilitate the formulation of commercial bicarbonate products for use in horticulture (Kuepper et al., 2001). In the UK in 2005, KHCO3 (99.0% w/w) was granted Commodity Substance Approval and can be used on all crops (protected and outdoor) as a horticultural fungicide. It is currently sold in the UK as AgriKarb (food-grade KHCO3) by Farm-Fos Ltd. The maximum approved concentration for KHCO3 is 20 g l-1 and the maximum total dose is 60 kg ha-1 per annum (outdoor crops) ( HYPERLINK "http://www.pesticides.gov.uk/approvals.asp?id=1054" http://www.pesticides.gov.uk/approvals.asp?id=1054). Commodity substances are chemicals with various non-pesticidal uses and a limited number of pesticidal uses. If such substances are to be used as pesticides they must be approved under the Control of Pesticides Regulations (COPR) and are granted approval only for use ( HYPERLINK "http://www.pesticides.gov.uk/approvals.asp?id=57" http://www.pesticides.gov.uk/approvals.asp?id=57). Inorganic salt-containing commercial products with approved uses for fungal disease control are presented in Tables 1 and 2. The use sites, target diseases and application methods of the EPA-registered inorganic salt-containing biopesticides are summarised in Table 3. Table 1. Fungal disease control-approved products containing inorganic salts and their registration status Product Name / Salt active substanceCompany NameRegistration Status*1 A. BicarbonatesArmicarb 100-F (KHCO3)Church & Dwight Co., Inc. (NJ, USA)BIOArmicarb Potassium Bicarbonate, FCC (KHCO3)Church & Dwight Co., Inc. (NJ, USA)BIOArmicarb Sodium Bicarbonate, FCC (NaHCO3)Church & Dwight Co., Inc. (NJ, USA)BIOArmicarb Potassium Bicarbonate, TFF (KHCO3)Church & Dwight Co., Inc. (NJ, USA)BIOGreenCure (KHCO3)H & I Agritech, Inc. (NY, USA)BIOKaligreen (KHCO3)Toagosei Co, Ltd (Tokyo, Japan)BIOBi-Carb Old Fashioned Fungicide (KHCO3)Lawn and Garden Products, Inc. (CA, USA)BIOEco-Mate Armicarb "O" (KHCO3)Helena Chemical Company (TN, USA)NOPOmex K-50 (KHCO3)Omex Agriculture Ltd (Lincoln, UK)PHPAgriKarb (KHCO3)Farm-Fos Ltd (Hereford, UK)CSA B. PhosphatesLexx-A-Phos fungicide (K2HPO4)Foliar Nutrients, Inc. (GA, USA)BIOVital (KH2PO4)Luxembourg-Pamol, Inc. (TN, USA)BIOEkspunge (KH2PO4)Lidochem, Inc. (NJ, USA)BIONutrol LC (KH2PO4)Lidochem, Inc. (NJ, USA)BIO C. SilicatesSil-MATRIX"! (K2SiO3)PQ Corporation (PA, USA)NOP*2 D. Phosphites14 products (H3PO3 and its K, Na, NH4 salts)see Table 2BIOExel LG systemic fungicide (KH2PO3, K2HPO3)Organic Laboratories, Inc. (FL, USA)SYS*1 BIO; Biopesticide = Environmental Protection Agency (EPA)-registered/USA ( HYPERLINK "http://www.epa.gov/pesticides/biopesticides" www.epa.gov/pesticides/biopesticides), CSA; Commodity Substance Approval = Pesticide Safety Directorate (PSD)-approved/UK ( HYPERLINK "http://www.pesticides.gov.uk/approvals.asp?id=57" http://www.pesticides.gov.uk/approvals.asp?id=57), NOP; National Organic Program (NOP), = approved by the US Department of Agriculture (USDA) for organic crop production ( HYPERLINK "http://www.ams.usda.gov/nop" www.ams.usda.gov/nop), PHP; Plant Health Promoter, contains 50% KHCO3, SYS; Systemic fungicide ( HYPERLINK "http://www.organiclabs.com/images/logos/110_MSDS%20Exe%20LGl.doc" www.organiclabs.com/images/logos/110_MSDS%20Exe%20LGl.doc) *2; effective from end of 2008 (Dr. Judy Thompson, PQ Corporation, personal communication) 3. Objective 3 Scope for further research in the UK Status: fully achieved In order to fulfil this objective, three stages of work were involved. The first stage was to use the information from Objective 1 which identified salts with efficacy against fungal diseases. The literature review revealed that several salts belonging to different groups were effective against a particular disease. For example, 16 different salts have shown efficacy against powdery mildew in cucurbits, while grape powdery mildew or wheat leaf rust were found to be suppressed from applications of five and four inorganic salts, respectively. The second stage was to identify intractable disease problems relevant to the UK, based on the following main criteria: 1) limited number of approved fungicides, 2) pathogen resistance to synthetic fungicides, 3) problems with synthetic fungicide residues. The third stage was to examine the weight of published evidence (Objective 1) and commercial evidence (Objective 2) for control by salts of the intractable diseases identified in the second stage. The output of these three stages was a shortlist of candidate crop-pathogen-salt combinations for further research in the UK (Table 4). Table 2. Commercial products containing phosphorous acid and its potassium, sodium and ammonium salts; registered in the USA by the Environmental Protection Agency (EPA) as biopesticides for fungal disease control Product NameCompany Name (State)Approved for use on lettuce vs. downy mildew (Bremia lactucae)Agri-Fos Systemic FungicideLiquid Fertiliser Pty. Ltd (trading as agrichem) (IL)YesArborfosJ. J. Mauget Co. (CA)NoFosphite FungicideJH Biotech, Inc. (CA)YesFungi-PhitePlant Protectants, LLC (CA)YesPhos Pro FungicideGrow More, Inc. (CA)YesPhospho-JetArborjet (MD)NoPhosphorous Acid TechnicalNufarm Americas, Inc. (IL)NoPhostrol Agricultural FungicideNufarm Americas, Inc. (IL)YesPlant Synergists Phosphorous Acid TechnicalL & L Formulators, LLC (WA)NoProphytLuxembourg-Pamol, Inc. (TN)YesResistActagro, LLC (CA)YesRiverdale MagellanNufarm Americas, Inc. (IL)NoVital-SignLuxembourg-Pamol, Inc. (TN)NoWhippet FungicideArbor Systems, LLC (NE)No Table 3. Use sites, target diseases and application methods of inorganic salt-containing biopesticides registered in the USA by the Environmental Protection Agency (EPA) with approved uses for fungal disease control Inorganic salt (No. of products)Use sitesTarget diseasesApplication methodPotassium and sodium bicarbonate (7)Wide range of fungal diseases (including powdery and downy mildew)All food commodities, turf, flowers and ornamentals.Diluted with water and sprayed on foliage using ground equipment.Dipotassium phosphate (1) Broad spectrum: powdery mildew, leaf spot, root rot, downy mildew, etc.Woody ornamentals, turfgrass, non-bearing fruit and nut trees and grapes.Leaf spray or soil drench at a rate of 1-2% v/v.Potassium dihydrogen phosphate (3)Powdery mildewApples, grapes, cucumbers, melons, summer and winter squash, watermelons, mangos, peaches, nectarines, plums, cherries, peppers, tomatoes and roses.As needed (not specified). Applications should be repeated at 7-14- day intervals, depending on infestation intensity.Phosphorous acid and its ammonium, sodium and potassium salts (14) Phytophthora and Pythium spp.Many food and non-food crops, including turf, ornamentals and trees.Before disease onset, then at 2-3 week intervals. As foliar spray, sprinkler irrigation systems, direct addition to soil, root dipping transplant. Table 4. Main target fungal diseases for practical research with inorganic salts in the UK Disease/ crop/fungus Fungicides (BCPC, 2008)Intractable Disease ProblemsSalts (weight of evidence)On-label a.s.Off-label a.s. Powdery mildew / cucurbits / Sphaerotheca fuliginea, Erysiphe cichoracearum 1. bupirimate (pro+out) 2. imazalil (pro) 3. copper ammonium carbonate (out) 1. azoxystrobin (pro+out) 2. bupirimate (pro) 3. Fenarimol (pro+out) 4. myclobutanil (pro+out) 5. sulphur (pro) 1. Resistance to bupirimate & imazalil (Alford, 2000) 2. Mildew tolerant cultivars: chlorosis under low light, lower yields compared with susceptibles (Alford, 2000)  KHCO3, K2HPO4, KH2PO4, K2SiO3, MnCl2 etc. (numerous publications and commercial products, 1 Commodity Substance Approval: KHCO3) Downy mildew / lettuce / Bremia lactucae 1. mancozeb (pro+out) 2. propamocarb HCl (pro+out) 3. fosetyl-Al (pro) 4. thiram (pro) 1. dimethomorph+mancozeb (out) 2. fosetyl-Al (pro+out)1. Can devastate crops in prolonged wet & cool conditions (RHS, 2008) 2. 14% samples of protected lettuce residues > MRLs (PSD, 2003) 3. Insensitive isolates to fosetyl-Al reported in CA, USA (Brown et al., 2004)K2HPO3, KH2PO3 (few publications on other crops, e.g. grape, pumpkin, Speiser et al., 2000; Cushman et al., 2007; numerous commercial products, especially phosphites, Table 2; 1 US patent: 6,911,415 B1)pro = protected only; out = outdoor only; pro+out = protected and outdoor Powdery mildew (Sphaerotheca fuliginea Schlecht. ex Fr. and Erysiphe cichoracearum DC. ex Merat) in cucurbits was identified as the main target for further practical research with inorganic salts in the UK. The survey identified 16 salts (silicates, bicarbonates and phosphates) with potential to suppress powdery mildew in cucurbits (percentage reduction in disease severity compared with untreated controls was 41-99%, calculated from the best treatment of each of 20 peer-reviewed studies; examples shown in Table 5). Powdery mildew fungi have a high potential for fungicide resistance development (e.g. bupirimate and azoxystrobin). In bicarbonates, the multiple mechanisms found to be involved in disease suppression (pH elevation on leaf surface, potassium ion imbalance, dehydration of fungal spores) suggest a lower risk of resistance development relative to synthetic fungicides. Phosphates and silicates appear to have more specific modes of action; induction of systemic acquired resistance and accumulation of flavonoid phytoalexins on infected leaves, respectively. Application of salts is primarily by foliar sprays of 0.5-1% (5-10 g l-1) solution, plus an oil or surfactant adjuvant, beginning before the onset of the disease or at first sign of symptoms and then at 7- to 10-day intervals until harvest. Symptoms of slight phytotoxicity (e.g. leaf scorch) have been reported when rates were increased to 2%. The evidence for powdery mildew control by these salts indicated that they are either equally effective (e.g. KH2PO4 vs. pyrifenox) or less effective (e.g. KHCO3 vs. myclobutanil) than conventional fungicides. There was no evidence that salt-fungicide tank mixtures enhance the efficacy of the fungicide treatment alone against cucurbit powdery mildew. The high efficacy of inorganic salts in suppressing cucurbit powdery mildew (Table 5) coupled with recent advances in the formulation of bicarbonate, phosphate and silicate salts (Table 1) may enable a reduction in the number of fungicide applications needed. The challenge remains to identify the rates of fungicides required for optimum control in combination with inorganic salts (applied separately). Downy mildew (Bremia lactucae) in lettuce has been identified as an additional target for further research because few fungicides are approved for this use and published evidence shows insensitivity to approved products and residue problems. The survey found evidence of suppression of downy mildew by phosphite salts on grapes. Successful strategies for using inorganic salts on these two targets have the potential to be extended to a wide range of other species. Based on the above criteria, major UK crop diseases for which there is a large number of fungicide active substances available were not identified as an immediate target for future research. This was despite the fact that the scoping study revealed evidence for efficacy with foliar applications of inorganic salts, in both scientific papers and commercial products brochures. Three such diseases in the UK are wheat powdery mildew and septoria leaf blotch and potato late blight, for which there are 37, 66 and 20 registered fungicides available (BCPC, 2008). For other diseases, such as greymould in strawberries (Botrytis cinerea), there seems to be no benefit from introducing inorganic salts in spraying control programmes, because there was no convincing evidence in the literature for efficacy by salts and there are several fungicides available. Table 5. Published evidence of significant suppression of powdery mildews in cucurbits (Sphaerotheca fuliginea Schlecht. ex Fr. or Erysiphe cichoracearum DC. ex Merat) following applications of inorganic salts Inorganic salt *1AdjuvantApplication MethodCucurbitMaximum Efficacy *2ReferenceK2SiO3noNutSolcucumber99%Adatia and Besford, 1986Na2SiO3noNutSolcucumber98%Blanger et al., 1995KHCO3 + azoxystrobin/chlorothalonilnoFolSprpumpkin62%Cushman et al., 2007KHCO3noFolSprmuskmelon93%McGrath and Shishkoff, 1999K2HPO4, K3PO4noFolSprcucumber56%Mucharromah and Ku, 1991K2HPO4, KH2PO4, NH4H2PO4 noFolSprcucumber94%Reuveni et al., 1995aK2HPO4, KH2PO4, K3PO4, KNO3, KCLTween-20FolSprcucumber99%Reuveni et al., 1995bK2HPO4, KH2PO4, NaHCO3, KNO3Tween-20FolSprcucumber98%Reuveni et al., 1996MnCl2, K2HPO4, CuSO4noFolSprcucumber97%Reuveni et al., 1997KH2PO4Triton X-100FolSprcucumber91%Reuveni et al., 2000K2SiO3noNutSolcucumber41%Liang et al., 2005NutSol = added to hydroponic nutrient solution; FolSpr = foliar spray; *1 Where more than one salt is involved, all had a significant suppressing effect on the disease; salts in bold were the most effective; *2 Percentages indicate reductions in disease severity relative to the untreated and were calculated from the best treatment in each study 4. Findings of the Literature Review 4.1. Classification by chemical grouping For the purpose of this review, the scientific literature on the efficacy of inorganic salts on fungal disease control was collected and classified into five main groups, which include the following, in order of importance in terms of efficacy and consistency as well as weight of published evidence: 1. Bicarbonate salts, 2. Phosphate salts, 3. Silicate salts, 4. Phosphite salts and 5. Chloride salts. 4.1.1. Bicarbonate salts Potassium bicarbonate (KHCO3) and sodium bicarbonate (baking soda; NaHCO3) are two compounds that have been extensively tested over the course of the last 15 years primarily against powdery mildew (PM) of a wide range of crops including cucurbits (cucumber, pumpkin, courgette, muskmelon and cantaloupe), grape, tomato, pepper and ornamentals. There are also reports of efficacy against other foliar fungal diseases, such as leaf rusts, spots and blights. Both these substances are ubiquitous in nature as they are present in virtually all living organisms but also in non-living environments, such as soil and water (Greenway, 1999). Furthermore, they are often used in the food industry as additives (HDC, 2005), where they replaced another bicarbonate salt, ammonium bicarbonate (NH4HCO3, used as a raising agent) due to concerns for increased acrylamide levels in cereal products from the use of the latter (European Commission, 2003; Taeymans et al., 2005). In comparison with KHCO3 and NaHCO3 they are relatively few reports of fungal disease control by NH4HCO3. Additional information on using baking soda as fungicide (e.g. reports from farming magazines, university research trials, gardener handbooks, technical bulletins, URLs of companies selling formulated products) can be found in Kuepper et al. (2001) and HDC (2005). Some citations refer to HCO3-1 as hydrogen carbonate but the term bicarbonate is used throughout this report. Evidence from the scientific literature showed that bicarbonate salts exhibit their antifungal properties when applied as foliar sprays at concentrations between 5-20 g l-1 (e.g. Ziv and Zitter, 1992; Ilhan et al., 2006). Review of the available published reports, details of which are discussed below, revealed that the efficacy of bicarbonate salts can be increased with the addition of adjuvants, such as oils and surfactants, and if applications are repeated at regular intervals. The application method of bicarbonate salts involves almost exclusively foliar sprays. There has been only one report of soil applied bicarbonates for fungal disease control (van Toor et al., 2004). This involved granule formulations of KHCO3 and NH4CO3 (Armicarb 100 and Armicarb 300 respectively; Church & Dwight Co., Inc., Princeton, NJ, USA) at 300 kg ha-1, which were applied to the soil beneath camellia bushes and suppressed the production of apothecia of Ciborinia camelliae (flower blight) by 86 and 91%, respectively. Arslan et al. (2006) evaluated the efficacy of 14 food additives, amongst which were KHCO3, NaHCO3 and NH4HCO3, against bean rust (Uromyces appendiculatus) and wheat leaf rust (Puccinia triticina). In vitro screenings of these compounds showed that all three bicarbonate salts at various concentrations ranging from 0.47 to 12 g l-1 completely inhibited spore germination and germ tube elongation of the urediniospores of the two fungi. Subsequent pot experiments in controlled environments indicated that spray applications of KHCO3 (6 g l-1), NaHCO3 (10.1 g l-1) and NH4HCO3 (9.4 g l-1) to 10-day-old wheat plants of the highly susceptible cv. Gonen reduced the number of P. triticina pustules on the leaves by 82, 92 and 90%, respectively, relative to controls. In the case of U. appendiculatus the greatest reductions in the number of pustules on the leaves of bean plants (cv. Gina) for each salt were achieved with 3.0 g l-1 KHCO3 (46.6%), 10.1 g l-1 NaHCO3 (84.4%) and 9.4 g l-1 NH4HCO3 (54.3%). The authors did not observe any phytotoxicity symptoms on the leaves of wheat and bean plants in 72% of the recorded cases and only slight phytotoxicity in the rest of their observations from the use of these salts. Yildirim et al. (2002) tested the efficacy of a number of salts, among which was NaHCO3, in the control of Uncinula necator (Schw.) Burr., which causes PM in grapes. In initial glasshouse tests, they found that spray applications of NaHCO3 at concentrations within the range 5-20 g l-1 plus a surfactant (phenol-methyl oxide 90% at 0.3 ml l-1) at the 6-7 leaf stage, 24 h prior to inoculation with the fungus (1.8 mg conidial suspension per plant, equivalent to 17 conidia mm-2), reduced the ability of U. necator colonies to form spores on young and old leaves (4 and 7 days after inoculation, respectively). At both dates, the pathogens ability to sporulate was significantly reduced by NaHCO3 and the estimated efficacies were between 83%-100% (efficacy determined as reduction in leaf infection using a 0-3 scale). Field experiments (Yildirim et al. 2002) showed lower protective effects (approximately 35% mean efficacy from two sites, significant reduction from the control) on the leaves compared with the potted plants and the authors attributed this to the late date that treatments began (June instead of mid-April). Bunch infections however, were drastically and significantly inhibited (mean efficacy: 77%) by NaHCO3 treatment. The sugar content of berries was unaffected and no toxic symptoms or residue problems were recorded on either leaves or bunch in response to NaHCO3 sprays. In greenhouse studies, Ziv and Zitter (1992) reported that three different bicarbonate salts, each applied in combination with SunSpray Ultra-Fine Spray Oil (SS) gave better results in the control of four fungal diseases of cucurbits, than either of the materials used alone. In pumpkin, combined KHCO3-SS or NaHCO3-SS treatments, in which the concentration of salts and oil were 5 g l-1 and 5 ml l-1, respectively, were equally effective in inhibiting the development of PM (Sphaerotheca fuliginea) on leaves, but NH4HCO3 was ineffective. Microscopic observations of the upper leaf surface revealed a limited number of conidia produced 6 days after NaHCO3 treatment (relative to distilled H2O-treated controls) and the complete absence of conidia or conidiophores 10 days after KHCO3 treatment. The salt-oil mixtures were applied on heavily PM-infested plants, 3 weeks after inoculation with the fungus. Conversely, NH4HCO3 (10 g l-1) plus SS (10 ml l-1) was slightly more efficacious than the other two salts in reducing: (a) the total number of lesions per leaf of Ulocladium cucurbitae (leaf spot) in cucumber and of Alternaria cucumerina (leaf blight) in muskmelon, (b) the percentage of leaf area affected by the fungus Didymella bryoniae (gummy stem blight) in muskmelon. Control of the three diseases was significantly better (overall reduction factor: 6.4) when NH4CO3-SS was applied 2 h prior to inoculation with the fungus as compared with post-inoculation sprays (after 24 h). 4.1.2. Phosphate salts Phosphates are salts of phosphoric acid (H3PO4) and are formed when a cation binds to the negatively charged oxygen atoms of the phosphate ions PO43-, HPO42- or H2PO41-. The latter is also found in the literature as orthophosphate but the term phosphate is used here. Perrenoud (1990) collected data from 2440 studies on the effects of fertilisers on various pests and diseases and found that P fertilisation resulted in disease suppression in 65% of the reported cases. The author suggested one or more of the following mechanisms to explain the P-induced improvement of plant health: (a) direct effects on pathogen multiplication, growth and survival, (b) direct effects on the metabolism of the plant and consequently on the pathogens food supply, (c) influence of plant defence responses and function of stomata which subsequently affect the establishment and spread of the pathogen within the plant. In a more recent review, Walters and Bingham (2007) reported that phosphates applied to plants could possibly sequester apoplastic calcium, thus altering the integrity of cell membranes and affecting the activity of enzymes like polygalacturonases. This would result in the release of elicitor-active oligogalacturonides from cell walls. Phosphates can exhibit their antifungal properties through induction of systemic acquired resistance (SAR). The main principles of SAR can be summarised to the following: (a) it offers long-lasting protection to plants (Durrant and Dong, 2004), (b) it is effective against a wide range of pathogens, including fungi (Hammerschmidt, 1999) and (c) it requires the presence of the signal molecule salicylic acid in order to be expressed (Walters et al., 2005). It must be noted that although several authors (e.g. Vallad and Goodman, 2004; Walters et al., 2005) have clearly described that of the two forms of induced resistance, SAR and induced systemic resistance (ISR), only SAR can be triggered by abiotic factors, such as phosphate salts (ISR only develops in response to root colonisation by plant growth-promoting rhizobacteria, PGPR), the term induced systemic resistance is often used in the literature instead of SAR to describe the protection offered to plants by phosphates. The phosphate salts most investigated for their antifungal properties include potassium phosphate (K3PO4), dipotassium hydrogen phosphate (K2HPO4) and potassium dihydrogen phosphate (KH2PO4). Reports of reduced disease incidence following applications of phosphate salts of Na, NH4 and Ca were also found. The majority of published articles on induced resistance by phosphates involve experiments on PM primarily in cucumber but also in other plants, such as grape, mango, nectarine, apple, pepper and rose. Phosphate salts have also demonstrated efficacy against other fungal diseases, such as anthracnose and rusts. As Walters and Bingham (2007) reported, the association between phosphates in plants and development of resistance has attracted increased attention since Gottstein and Ku (1989) demonstrated that dibasic and tribasic phosphate salts induced systemic resistance to anthracnose (Colletotrichum lagenarium) in glasshouse-grown cucumber. They showed that the systemic resistance induced by the phosphates in newly developing leaves was still effective 5 weeks after treatments were administered. Spraying the undersides of the first two true leaves with c. 1-2 ml of K3PO4 (exact volume not specified) at concentrations of 2.1, 10.6 or 21.2 g l-1 resulted in decreasing the number of necrotic lesions on leaves 3 and 4 by 78, 96 or 99%, respectively, compared with untreated controls. The authors ruled out the possibility that a specific component of the pathogen was involved in the induction of systemic resistance and attributed the protective effect to a low level metabolic perturbation inducing stress response in the host. They also emphasised that it is only the inducer leaf which produces the alarm signal responsible for eliciting systemic resistance. The findings of Gottstein and Ku (1989) were confirmed by Mucharromah and Ku (1991) in a glasshouse study which included in addition to anthracnose, three other diseases of cucumber; scab (Cladosporium cucumerinum), gummy stem blight (D. bryoniae) and PM (S. fuliginea). Spraying of the lower surfaces of leaf 1 with 1 ml K2HPO4 at 3.5 or 8.7 g l-1 or K3PO4 at 2.7 or 6.8 g l-1 induced resistance on leaf 2 against all four fungi. This was revealed after challenging leaf 2 a week after leaf 1 treatment with all the test pathogens and rating the plants for disease incidence 5-15 days after challenge inoculation. Percentage protection induced by the phosphates across all four diseases was 53% on average compared with the untreated. Symptoms of chlorotic stippling developed on the inducer leaf 48 h after spraying with the phosphates. However, in those plants where chlorosis on the inducer leaves developed into restricted necrotic lesions were better protected than those that had extensive damage but no necrotic lesions. In another glasshouse experiment, Reuveni et al. (1994) reported that foliar sprays of three phosphate salts (K2HPO4, KH2PO4 or NH4H2PO4 at 17.4, 13.6 or 11.5 g l-1, respectively) on the upper surface of the first fully-expanded leaf of cucumber before inoculation with S. fuliginea, reduced PM severity on leaves 2-5 by up to 94%. Protection lasted for up to 25 days after treatments. Post-inoculation foliar sprays of phosphates also resulted in systemic protection against PM, even 4 days after challenge inoculation with the pathogen. As shown in a similar study conducted by the same authors (Reuveni et al., 1995b), the efficiency of phosphate salts in reducing PM pustules or conidia production from colonies of diseased foliage was enhanced when treatments were combined with Tween-20 (0.1 ml l-1), with protection reaching 99% of the untreated disease severity. Post-inoculation phosphate sprays were more effective than the systemic fungicide pyrifenox (Dorado 480 EC, 0.01% w/v, Ciba-Geigy, Switzerland) in reducing PM infection, but only for approximately 2 weeks after application. Reuveni et al. (1996) found that pyrifenox, K2HPO4 and KH2PO4 were equally effective in controlling cucumber PM and that the phosphate salt solutions were not phytotoxic to the foliage. The authors summarised the characteristics that make phosphates ideal candidates for fungal disease management to the following: 1) quick absorption by the plant, 2) great mobility within tissues and 3) low-cost nutrient value. Further evidence for the beneficial effect of foliar sprays of phosphates in suppressing powdery mildew in cucumber is provided by Reuveni et al. (1997) and Reuveni et al. (2000); the latter authors found that KH2PO4-induced systemic protection against PM in a hydroponics system was associated with up to a 50% increase in the Ca content of cucumber leaves. Calcium ions are known to have a key role in the production of chitinase and salicylic acid, both tightly linked with SAR (Schneider-Mller et al., 1994, Reuveni et al. 2000). In glasshouse trials, K3PO4 used on first leaves of barley cv. Golden Promise (applied at 5 g l-1 plus 0.1 ml l-1 Tween-20 as a paint or spray, respectively) reduced the severity of PM (Blumeria graminis f. sp. hordei Marchal) on the second leaves by 89% compared with untreated plants (Mitchell and Walters, 2004). The most efficacious time interval between treatment of first leaf and challenge inoculation with PM (25 conidia mm-2) was 2 days. Interestingly, a significant decrease in the percentage of mildewed leaf area, relative to the untreated, was apparent even when the conidia were administered to the leaves 12 days after K3PO4 application. Application of the phosphate salt solution as a seed treatment or root drench was less effective than foliage application, reaching maximum protection levels of 39% and 30%, respectively. Phosphate treatment of first leaves resulted in a significant stimulation of the activities of phenylalanine ammonia lyase (PAL) and peroxidase in the second leaves. The activity of these enzymes was enhanced further when K3PO4-treated second leaves were challenged with PM. 4.1.3. Silicate salts Although the information in the literature on the role of Si in plant nutrition and physiology is limited and often controversial, especially in dicotyledons (Fawe et al. 1998), there is increasing evidence for its prophylactic role against fungal diseases, especially powdery mildews and root rots (Blanger et al., 1995). In addition to increased resistance to fungal pathogens as well as insects, numerous other benefits to some plants from Si application are documented in the literature. These include correction of nutrient imbalances (e.g. P-induced Zn deficiency in cucumber; Marschner et al., 1990), alleviation of metal toxicity (e.g. Mn in rice and cowpea, Al in maize; Horiguchi, 1988, Iwasaki et al., 2002 and Wang et al., 2004, respectively), increased salt tolerance (e.g. in wheat; Liang, 1999), enhancement of plant growth (e.g. in rice; Hossain et al., 2002, several other examples cited in Epstein, 1994), lignification of cell walls thereby conferring rigidity and mechanical strength to plant cells (e.g. in cucumber; Fawe et al., 1998) and positive effects on plant reproduction (e.g. in rye brome, Bromus secalinus L.; Gali and Smith, 1992). The use of soluble Si in the form of silicate salts of K, Na or Ca (formed by the reaction of hydrated silicon dioxide, SiO2, with the metal oxides K2O, Na2O or CaO) has become very popular in greenhouse hydroponic systems, where it is amended directly in the nutrient solution to help control PM infections (Blanger et al., 1995). In addition to simple silicate salts, reports of fungal disease control by trisilicate (Na2Si3O7) salts were also found, e.g. against PM in wheat (Leusch and Buchenauer, 1989). The majority of published studies on silicates and PM have focused on greenhouse cucumber. The consistency of the positive effect of added silicates into the irrigation water of hydroponically-grown cucumbers has led scientists to investigate the association between Si treatment and disease severity in a wider range of crops, such as courgette, wheat, rice, pea, peach and strawberry. These studies have demonstrated that in addition to PM, several other fungal diseases exhibit decreased symptoms in response to Si fertilisation. For example, well-documented are rice (neck) blast (Magnaporthe grisea) and brown spot (Cochliobolus miyabeanus) (e.g. Berni and Prabhu, 2003 and Datnoff et al., 1991, respectively). Furthermore, different application methods (foliar and soil applied silicates) have been tested, so as to enable Si accumulation in plant tissues of non-hydroponic crops or of crops that cannot transport Si from roots to leaves through the vascular system (Blanger et al., 1995). These involve foliar sprays of silicates (e.g. in cucumber; Liang et al., 2005) or incorporation of Si-rich materials in the soil medium (e.g. Na2Si3O7 or blast furnace lime in wheat; Leusch and Buchenauer, 1989). There has been a lot of research on the mode of action of silicates in reducing fungal disease severity. However, there is also great controversy among the scientific community as to whether the role of Si in plant disease resistance is associated with passive or active mechanical protection or both. Wagner (1940) was the first to study the mode of action of silicates. He reported increased deposition and polymerisation of H4SiO4 on cucumber leaf epidermal cells, which prevented PM infection. Using scanning electron microscopy and X-ray mapping, Samuels et al. (1993) observed highly silicified trichome bases in Si-treated cucumber fruits compared with untreated ones. However, the surrounding epidermis, fleshy mesocarp and endocarp tissues exhibited no differences in the amount of accumulated Si. A large number of researchers have demonstrated that Si-treated plants accumulate increased amounts of Si and phenolic compounds in leaf cell walls at regions of attempted penetration by the PM fungus (e.g. Menzies et al., 1991a, 1991b; Samuels et al., 1991). Daayf et al. (1997) demonstrated that in addition to members of Solanaceae and Leguminosae, cucumber plants are also capable of producing phytoalexins, a group of water-soluble phenolic derivatives with antifungal properties. In a subsequent study conducted by Fawe et al. (1998), although no differences were found in the amount of phenolic compounds in leaf extracts from Si-treated and Si-untreated, PM-infected cucumber plants, a significantly greater accumulation of a flavonoid phytoalexin compound, flavonol aglycone rhamnetin, was observed on leaves of the Si-treated plants, relative to the Si-untreated. It therefore appears that the suppression of fungal diseases by Si fertilisation is linked with both stimulation of the plants natural defence mechanisms and strengthening of cell walls thus creating a natural barrier to fungus penetration. Menzies et al. (1992) studied the effectiveness of silicon fertilisation against PM in cucumber, muskmelon (Cucumis melo L.) and zucchini squash (Cucurbita pepo L.). Silicon was applied in the form of potassium silicate, K2SiO3 (K6, National Silicates Ltd, Toronto, Canada) directly amended in the nutrient solution (at 0.26 g l-1) or as a foliar spray at various concentrations (0.26, 1.3, 2.62 or 5.24 g l-1). The nutrient solution amendment resulted in a significant reduction in the number of PM colonies developed on the leaves compared with control plants (treated with same nutrient solution but without added K2SiO3). The average percentage reduction in disease severity for the three cucurbit species was 72%, 84% and 61% for cucumber, muskmelon and zucchini squash, respectively. Of the foliar applied K2SiO3, similar results to those of the nutrient solution were obtained with 2.62 or 5.24 g l-1 K2SiO3. The foliar treatments, which were sprayed to run-off to upper surfaces of the second leaf in each plant, were more persistent than the Si-amended nutrient solution, providing significant protection against the fungus even when sprayed 7 days prior to challenge inoculation with conidia of S. fuliginea. All spray solutions (500 ml) contained a drop of Tween-20 and the pH was adjusted to 5.5 with phosphoric acid. In another study (Menzies et al., 1991b), the effect of Si treatment in reducing PM severity was lost within 24 h after removing the Si from the nutrient solution. These findings led Menzies et al. (1992) to speculate that foliar application of silicate salts may be superior to applications through nutrient solutions. Nevertheless, Liang et al. (2005) demonstrated that foliar-applied K2SiO3 (applied at 1.54 or 3.08 g l-1 as described above by Menzies et al., 1992) failed to reduce the severity of PM in two hydroponically-grown cucumber varieties, Ningfeng No. 3 (susceptible) and Jinchun No. 4 (resistant), regardless of challenge inoculation with the mildew fungus, which took place 1 and 7 days after Si treatment. Foliar Si treatment also did not affect the activities of the pathogenesis-related proteins (PRs) peroxidase, polyphenoloxidase and chitinase. When however, plants were irrigated with Hoaglands nutrient solution (renewed every 2 days) amended with 0.26 g l-1 K2SiO3 at 200 ml pot-1, opposite results were obtained, with significant reductions in both the activity of PRs and PM disease severity (maximum suppression 41%, relative to Si-untreated controls), irrespective of the inoculation with PM conidia. The authors concluded that continuously root-applied Si, incorporated in the nutrient solution, stimulates host defence resistance to PM infection. In a field trial conducted with courgette, six foliar applications of 5 g l-1 sodium silicate, Na2SiO3, in conjunction with mineral oil (Newoil) at 10 ml l-1, had also absolutely no effect on the activity of S. fuliginea. Amending the nutrient solution with silicate salts in hydroponic strawberry has been recently shown to reduce germination of PM conidia by up to 60%, relative to Si-untreated plants, and to inhibit appressoria formation and fungal penetration (Kanto et al., 2007). In the study of Yildirim et al. (2002) with PM and grapes (section 4.1.1), single foliar sprays of 1.22 g l-1 Na2SiO3 or 1.54 g l-1 1% K2SiO3 (Water Glass; Tunctas A.S., Izmir, Turkey) without added surfactant, demonstrated 94% and 80% maximum efficacies, respectively. When the same potted plants received a second Si-spray at 12 days after inoculation with the fungus, significant curative effects were obtained. In particular, it was observed that both test solutions reduced the number of active PM colonies counted on old leaves at pre-application stage by nearly three-quarters at 4 days post-application. Although the efficacy of silicates reduced with time, the number of PM colonies per leaf was consistently significantly lower on Si-treated as compared with untreated plants. An important reason for the popularity of silicon application in modern rice production is associated with protective effects against fungal diseases (Winslow, 1992). The main silicate salts used in rice fertilisation are calcium silicate slag (CaAl2Si2O8), calcium silicate (CaSiO3) and sodium silicate (NaSiO3) (Datnoff et al., 1991; Winslow, 1992; Berni and Prabhu, 2003). The method of application is by pre-plant incorporation before seeding. It is now well-established that soil application of silicate salts in rice fields effectively increases crops resistance to neck blast (M. grisea) and brown spot (C. miyabeanus). A large number of articles have been published in this topic and the recent review of Datnoff and Rodrigues (2005) is an excellent source of information for further reading. Maximum percentages of disease reduction over controls found in our survey were 89% for M. grisea (Berni and Prabhu, 2003) and 75% for C. miyabeanus (Datnoff et al., 1991), on rice panicles and leaves, respectively. The extent of yield increases in response to Si fertilisation varies among studies and there are some contrasting reports of efficacy. Although the review of Savant et al. (1997) stated that rice yield enhancement was typically within the range of 10-30%, careful examination of data from individual studies indicated increases in yield of up to 88% (Datnoff et al., 1991). 4.1.4. Phosphite salts Phosphites are alkali metal salts of phosphorous acid (H3PO3) (McDonald et al., 2001) and therefore should not be confused with phosphates, which derive from phosphoric acid (H3PO4). Phosphite salts contain a metal cation, such as K, Na or NH4, and a phosphite anion, PO33-, HPO32- or H2PO31-. When H3PO3 is mixed with water it forms phosphonic acid. The latter is very acidic and is neutralised with an alkali salt, usually KOH, to form potassium dihydrogen phosphite (KH2PO3) or dipotassium hydrogen phosphite (K2HPO3), which are the active substances in several phosphite fungicides and fertilisers (Landschoot and Cook, 2005). There is no consensus in the literature on how inorganic salts of H3PO3 are referred to. The terms phosphites (preferred one here) and phosphonates are most commonly used, followed by the synonymous terms orthophosphites, hydrogonophosphonates, phosphorous acid compounds or phosphonic acid compounds. Hardy et al. (2001) emphasised that the term phosphites distinguishes inorganic salts of H3PO3 from phosphonates, because the latter contain an organic group bonded to a phosphorus ion found in chemical fungicides. A widely used such product is fosetyl-Al (Aliette; 80% aluminum tris O-ethyl phosphonate, WDG Fungicide, Bayer CropScience Ltd) which is ionised to phosphonate (phosphite) inside the plant. Fosetyl-Al can move systemically from foliage to roots and vice versa and is therefore used in the control of both root and foliar fungal pathogens (Cohen and Coffey, 1986). Since fosetyl-Al falls into synthetic products based on organic (carbon-based) chemistry, it was out of the focus of this review and hence no further information on its use is provided. The relevant advantage of phosphites over phosphates, is that they can have direct toxic effects on certain plant pathogens, a property not found in phosphates. A side-effect of phosphites is the increased risk of phytotoxicity when they are applied at excessive concentrations, above 5 g l-1 or 36 kg ha-1 (Hardy et al., 2001; Barrett et al., 2003). The use of phosphites in agriculture has been investigated mostly with respect to their effects in controlling plant diseases rather than providing direct nutrition to plants. The latter may occur only if phosphites are applied to the soil and come in contact with certain bacteria, which can oxidise phosphite to phosphate (McDonald et al., 2001). However, because this process is very slow and can take up to 4 months to complete, it is of no practical importance (McDonald et al., 2001; Lovatt and Mikkelsen, 2006). There is now ample evidence to support that application of phosphite salts can reduce the susceptibility of plants to diseases caused by pseudo-fungi belonging to the Oomycetes (also known as water moulds; Agrios, 1997). The main candidate pathogens for control by phosphites (selected examples described below) are Phytophthora spp., followed by Plasmopara and Alternaria spp. Landschoot and Cook (2005) reported that phosphites tend to have better efficacy when applied preventatively compared with post-infection applications. Application method varies depending on the crop-pathogen combination. They are most commonly applied as foliar sprays (Cooke and Little, 2001; Johnson et al., 2004; Dorn et al., 2007), but also as root drench (Smillie et al., 1989), trunk injection (Hardy et al., 2001), through drip irrigation (Oren and Yogev, 2002), mixed in hydroponic nutrient solutions (Frster et al., 1998), seed treatments (Abbasi and Lazarovits, 2006), as ultra low-volume mist aerial applications (Hardy et al., 2001) or as dip treatment (Zainuri et al., 2001). As with silicates, the mode of action of phosphites has been the topic of great controversy among researchers. It is now believed that phosphites have a complex mode of action against fungal or pseudo-fungal pathogens involving both direct (inhibition of fungal sporulation or slow growth rate) and indirect effects (strong and rapid stimulation of plant defence mechanisms) (Smillie et al., 1989; Grant et al., 1990; Guest and Bompeix, 1990; Guest and Grant, 1991; Jackson et al., 2000; Hardy et al., 2001; Brunings et al., 2005; Daniel and Guest, 2005). The complexity of the mechanisms involved in the prophylactic effects of phosphites against Oomycetes has limited the development of pathogen resistance to these compounds (Grant et al., 1990; Landschoot and Cook, 2005). In glasshouse-grown potatoes, two foliar sprays of KH2PO3 (Prolabo; > 98% pure H3PO3 partially neutralised to pH 6.4 with aqueous KOH) at 3.5 g l-1 applied twice with a 7-day interval significantly reduced the severity of late blight (Phytophthora infestans) on tubers of the maincrop cvs Bintje, King Edward and Russet Burbank by c. 50%, 33% and 60%, respectively, relative to that in tubers of untreated plants (Cooke and Little, 2001). Tuber susceptibility was assessed by lifting healthy tubers from untreated and KH2PO3-treated pots at the end of the experiment, inoculating them by spraying to run-off with a sporangial/zoospore suspension (104-105 sporangia ml-1), incubating them for 28 days in the dark at 15C and counting the number of infected and uninfected tubers. The level of tuber protection was not affected by the pH of the applied phosphite. In contrast with KH2PO3, foliar application of fosetyl-Al failed to prevent tuber blight development. Foliar applications of KH2PO3 as well as K2HPO3 were also found to reduce the susceptibility of potato tubers to late blight in field experiments over a 4-year period (relative to tubers from mancozeb-treated plots; further details in section 4.1.4) (Cooke and Little, 2001). In tomato plants, Dorn et al. (2007) reported that Robus at 1% (described as a natural compound with H3PO3 as the active substance; GIP, Jechtingen, Germany) completely inhibited sporangial germination and mycelial growth in vitro and demonstrated 74% efficacy, relative with the untreated control, against foliar late blight (P. infestans) in growth chamber trials. Robus had been sprayed to run-off on leaves of 2-week old tomato plants, cv. Marmande. Johnson et al. (2004) investigated the field performance of foliar applications of a product containing various phosphite salts (Phostrol; mono- and dibasic Na, K and NH4 phosphites 53.6%, other ingredients 46.4%, Nufarm Americas, Inc., IL, USA) against potato tuber rot caused by the late blight fungus P. infestans (isolate US-8). The experiments were carried out over a 3-year period on commercial potato fields of five different cultivars (Ranger Russet, Umatilla Russet, White Rose, Russet Norkotah, Russet Burbank) and at various locations across the USA. Natural infections with P. infestans on the foliage were deliberately minimised by appropriate fungicides. The first foliar spraying with Phostrol (at 9.37 kg ha-1) took place a week after initial tuber bulking and it was repeated either once or twice with a 2-week interval. Assessment of artificially-inoculated harvested tubers revealed that Phostrol significantly decreased tuber rot incidence and severity in 23 out of 24 observed cases. The mean decrease in incidence and severity of tuber rot (calculated from all tested locations and cultivars) were 67% and 84%, respectively, with two sprays and 88% and 91%, respectively, when Phostrol was applied three times. In 30% of the cases, Phostrol provided 100% protection against P. infestans. When application of Phostrol (at 7.49 or 9.37 kg ha-1) was initiated 4 weeks after initial tuber bulking, protection against late blight tuber rot was by 39% (incidence) and 35% (severity) lower, relative to that obtained when spraying started 1 week after initial tuber bulking. When the effects of foliar-applied Phostrol (9.37 kg ha-1) were assessed on two other fungal pathogens, Phytophthora erythroseptica (pink rot) and Pythium ultimum (Pythium leak), protective effects were observed only with respect to the former species (maximum reduction in severity over controls: 54%; Johnson et al., 2004). In commercial apple orchards, Reuveni et al. (2003) demonstrated that three foliar applications to run-off (2500 l ha-1) of a phosphite salt (made up of KH2PO3 and K2HPO3, pH 4.5; Fertilisers and Chemicals Ltd, Haifa, Israel), starting from bloom until petal fall, reduced the number of fruits infected with Alternaria alternata, causal agent of moldy-core decay, by 60% compared with untreated trees. In the same study, decay by A. alternata was completely inhibited in laboratory tests with 0.5 g l-1 phosphite. Furthermore, foliar applications of phosphite salts have shown efficacy against downy mildews on grapes (Plasmopara viticola; but phosphite residues found in wine, Speiser et al., 2000) and maize (Peronosclerospora sorghi; Panicker and Gangadharan, 1999). Finally, phosphites have been shown to significantly reduce the incidence of dieback disease (Phytophthora cinnamomi) in native plant species in Australia, e.g. Banskia brownii (Hardy et al., 2001; Barrett et al., 2003) and of Phytophthora root rot and brown rot (Phytophthora citrophthora) in oranges and grapefruits (Oren and Yogev, 2002). 4.1.5. Chloride salts Five chloride salts have been tested against plant fungal infections: potassium chloride (KCl), sodium chloride (NaCl), aluminium chloride (AlCl3), calcium chloride (CaCl2) and manganese chloride (MgCl2). Researchers at Harper Adams University College, UK, have been investigating, over the last 20 years, the effects of foliar applied inorganic salts on the severity of wheat and barley fungal diseases. Field application of KCl foliar spray at 20 kg ha-1 (applied as solution through hollow-cone nozzles; 99.5% w/w, BDH Chemicals Ltd, Poole, UK) was found to significantly reduce the severity of glume blotch (Septoria nodorum) by 31% compared with control, on the penultimate leaves at anthesis in winter wheat (Kettlewell et al., 1990). Kettlewell et al. (1992) demonstrated that late-season field foliar KCl treatment on barley at 50 g l-1, 20 kg ha-1 (combined with 34.2 or 342 g l-1 sucrose), significantly suppressed the severity of powdery mildew (Erysiphe graminis) on flag leaves (but not on penultimate leaves), but brown leaf rust (Puccinia hordei) was not affected; diseases were assessed using area keys (Anon., 1976; cited by Kettlewell et al., 1992). The authors also observed significantly increased specific grain weight in response to KCl treatment but yield was not increased. After a series of laboratory, field and glasshouse experiments, Cook (1997) confirmed the significant suppressing effect of KCl spray solution on septoria leaf blotch and powdery mildew diseases in wheat (S. tritici and E. graminis, respectively) at early stem extension and after flag leaf emergence. In addition, he attributed the reduction of the leaf area affected by E. graminis to the observed inhibition of spore germination following foliar KCl application. Mann et al. (2004) concluded that mode of action of KCl (optimum concentration 93 g l-1) is contact rather than systemic and moreover, that it has both protectant and curative effects. Experimental evidence for the mode of action of KCl has been provided by Mann (1999), Kettlewell et al. (2000) and Mann et al. (2004), who demonstrated, using KCl solution and the osmoticum polyethylene glycol as control, that the reduced symptoms of S. tritici and E. graminis on winter wheat (up to 50% reduction in leaf blotch severity) were probably the result of adverse osmotic effects on fungal spore germination caused by the salt. In addition to foliar diseases, the role of NaCl in the suppression of soilborne diseases has also been investigated. Research has been undertaken on Fusarium crown and root rot (Fusarium oxysporum, F. proliferatum) in asparagus (Elmer 1995, 2003), Fusarium wilt (F. oxysporum) in cyclamen (Elmer, 2002) and Rhizoctonia root and crown rot (Rhizoctonia solani) in sugar beet (Elmer, 1997). A significant reduction (51%) in fungal root lesions relative to control was recorded when roots of asparagus were directly exposed to NaCl, but some disease suppression also occurred on distal untreated roots, suggesting a systemic mechanism (Elmer, 2003). The author concluded that multiple mechanisms are probably involved in disease suppression by NaCl, one of which, according to their findings, appeared to be associated with a root-mediated change in rhizobacteria (Elmer, 2003) and increased Mn availability in the roots (Elmer, 1995). 4.2. Compatibility of inorganic salts with fungicides Published studies in which the efficacy of inorganic salts to suppress fungal diseases has been investigated in comparison with that of synthetic fungicides were the minority and represented less than 15% of all citations found. The few available references are focused on PM control in cucurbits, wheat, fruit trees and grapes (bicarbonates, phosphates, chlorides and silicates) and on the control of Oomycetes (late blight, downy mildew in potatoes and lettuce, respectively; phosphites only). Findings from these references are described individually for each group in sections 4.2.1-4.2.5. Even where fungicide treatments were included in experiments, there was great inconsistency among studies with respect to comparative efficacy with inorganic salts and the treatment programmes followed (e.g. separate applications of salt/fungicides, alternate treatments or tank mixtures). For example, the evidence from studies with bicarbonates and conventional fungicides indicated variable results depending on the crop pathogen salt fungicide combination. There have been cases where bicarbonate salts: (a) were not capable of further enhancing the efficacy of conventional fungicides (more details in section 4.2.1) when used in tank mixtures (Cushman et al., 2007; Karabulut et al., 2006), (b) were less efficacious (e.g. KHCO3 myclobutanil (Nova 40W, 0.05% w/v, Rohm and Haas Co., PA, USA); McGrath and Shishkoff, 1999), equally effective (e.g. NaHCO3 tebuconazole 25WP (Folicur, 0.025% w/v, Bayer Turk, Turkey); Ilhan et al., 2006) or more efficient (e.g. KHCO3 or NaHCO3 penconazole (Ophir, 0.02% w/v, Ciba-Geigy, Switzerland); Fallik et al., 1997) than fungicides when applied separately. Inevitably, these factors meant that generalisations on the subject of salt fungicide compatibility based on literature findings were difficult to draw, although some patterns emerged. It appears that little work has been published on tank mixtures of salts with fungicides. Evidence from work on mangos (section 4.2.2) and grapes (section 4.2.3), where tank mixtures of phosphates or silicates with half- or full-rate fungicides, respectively, enabled 50% reduction in the number of fungicide applications needed to control PM, suggests that this integrated approach should be investigated further. The use of alternate programmes in the management of foliar fungal diseases (i.e. salts and fungicides applied in rotation), for which more publications were found relative to tank mixtures, also allowed a reduction in the frequency of fungicide applications required for effective control. These findings translate to both cost and environmental benefits and merit further investigations. 4.2.1. Bicarbonates fungicides Further to its potential to lessen the environmental impact of conventional fungicides, HDC (2005) outlined several other advantages from the use of KHCO3 as fungicide. These, in particular, include the relatively low cost compared with synthetic fungicides and the fact that it can be applied near harvest time. An additional advantage is the lower risk of fungal resistance development compared with synthetic fungicides, due to multiple modes of action in bicarbonate salts (HDC, 2005). Cushman et al. (2007) conducted extensive field research to investigate the comparative effectiveness of low-input (LI) and high-input (HI) management approaches in the control of PM and downy mildew (DM) (Sphaerotheca fuliginea and Pseudoperonospora cubensis, respectively) of pumpkin. Both LI and HI consisted of foliar applications of six fungicide/spray combinations beginning either on the onset of the symptoms (LI) or 20 days after seeding (HI) and then continuing at 7- to 10-day intervals until a week prior to harvest. The fungicides, which were applied in rotation throughout the experiments, were azoxystrobin (1.1 l ha-1 at 5 g l-1) (Quadris; Syngenta Crop Protection, Inc., Greensboro, NC, USA) and chlorothalonil (3.5 l ha-1 at 17 g l-1) (Equus 720; Griffin LLC/DuPont, DE, USA). The other tested products were KHCO3 (4.5 kg ha-1 at 21 g l-1) (Armicarb 100), foliar phosphite (3.5 l ha-1 at 17 g l-1) and foliar nitrogen (4.7 l ha-1 at 22 g l-1) (Ele-Max Foliar Phosphite 0-28-26 and CoRoN 25-0-0, respectively; Helena Chemical Co., TN, USA). Spray treatments consisted of tap water (untreated control), azoxystrobin/chlorothalonil alone or azoxystrobin/chlorothalonil with various combinations of the foliar-applied chemicals mentioned above (none of which was tested alone). At each of the four locations in south-eastern USA, plants were assessed and rated twice (45 and 75 days after planting) for PM and DM incidence on the upper (adaxial) leaf surfaces. On average, across both dates and the three azoxystrobin/chlorothalonil treatments which included Armicarb 100, there was a decrease in PM-diseased foliage from 69.5% in untreated controls to 22.2% and in DM-diseased foliage from 59.5% to 29.3% (for both PM and DM, azoxystrobin/chlorothalonil alone: 33.5%). In terms of pumpkin yield the various fungicide/spray combinations were again superior to the water controls but did not differ significantly between them. The authors concluded that since there was no significant benefit from mixing these fungicides with bicarbonates and phosphites, the azoxystrobin/chlorothalonil rotation could be recommended for situations where no strobilurin resistance has developed. Experiments carried out over a 2-year period on field-grown wheat (cv. Gonen) plants showed that two foliar sprays of NaHCO3 at 10.1 g l-1 with a 2-week interval, reduced leaf rust (P. triticina) infection by a factor of 5.2, compared with water-treated control. The efficacy of NaHCO3 was comparable with that of tebuconazole (Folicur 25 WP, 0.19 kg a.s. ha-1), while combination of NaHCO3 with dose of mancozeb (Dithane M-45 80 WP, 2.8 kg a.s. ha-1) did not further enhance the level of disease control achieved by the NaHCO3 treatment alone (Karabulut et al., 2006). 4.2.2. Phosphates fungicides Post-inoculum phosphate sprays (section 4.1.2) were more effective than the systemic fungicide pyrifenox (Dorado 480 EC, 0.01% w/v, Ciba-Geigy, Switzerland) in reducing PM infection in cucumber, but only for approximately 2 weeks after application (Reuveni et al., 1995b). In another study, Reuveni et al. (1996) found that pyrifenox, K2HPO4 and KH2PO4 were equally effective in controlling cucumber PM and that the phosphate salt solutions were not phytotoxic to the foliage. Field spray applications of K3PO4 solution (section 4.1.2) or tebuconazole 25EW (Folicur, 25% w/v, Bayer CropScience, UK) at the rate of 1 l ha-1 at GS31 and GS35, reduced the PM-infected area on the flag leaf of untreated barley plants by 70% and 86%, respectively, with no significant difference between them (Mitchell and Walters, 2004). Reuveni and Reuveni (1995b) conducted field experiments in grapevines, nectarine and mango trees to investigate the comparative effectiveness of spray applications of K2HPO4, KH2PO4+KOH (both plus 0.25 ml l-1 Triton X-100), commercial systemic fungicides and the alternate KH2PO4+KOH/fungicide treatment in PM (U. necator, Sphaerotheca pannosa, Oidium mangiferae, respectively) control. Phosphates (4.4 g l-1 K2HPO4 and 5.4 g l-1 KH2PO4+KOH) and fungicides were sprayed on the foliage to run-off and at various intervals depending on each crop. The fungicides, which were applied at recommended field rates, included pyrifenox (Dorado 480 EC, 0.01% w/v) in grapes, myclobutanil (Systhane 12 E, 0.05% w/v) in nectarines and penconazole (Ophir, 0.03% w/v) and diniconazole (Marit 12.5% WP, 0.04% w/v, Sumitomo, Japan) in mango. All tested treatments completely inhibited the development of PM on fruit clusters of grapevines. Disease rating on fruits and leaves of nectarine trees revealed that phosphate sprays failed to provide protection against PM, in contrast with myclobutanil, but the converse was true in 3-year field experimentation involving foliar applications of 10 g l-1 KH2PO4 (Reuveni and Reuveni, 1998). The alternate treatment KH2PO4+KOH and myclobutanil, each sprayed three times, caused 79% reduction in disease severity, which was not significantly different from that by myclobutanil alone (91%). Likewise, in inflorescences of mango, the alternate treatment of KH2PO4+KOH and diniconazole elicited a significant inhibitory effect against PM. The two phosphate treatments were also effective and reduced PM incidence by c. 80% on average, while penconazole and diniconazole completely inhibited disease development. Reuveni and Reuveni (1995a) demonstrated that the phosphate-induced defence of field-grown winegrapes against PM was associated with enhanced soluble peroxidase activity on both infected (8-fold increase) and non-infected (3-fold increase) berries. Reuveni et al. (1998a) demonstrated that the tank-mix treatment of 10 g l-1 KH2PO4 with half the recommended dose of diniconazole, i.e. 0.02% w/v, applied twice during blooming with a 14-day interval, was as effective as four weekly applications of full-dose diniconazole (standard treatment) in reducing PM infection on flowers and bloom clusters of field-grown mango trees (mean protection c. 77% compared with untreated). Two foliar sprays of the phosphate solution in tank mixture with full-dose diniconazole (Marit) or kresoxim-methyl (BAS 490F, 0.015% w/v, BASF AG, Germany) provided significantly greater protection (> 95%) against O. mangiferae than the standard fungicide-based treatment. It was also demonstrated that the alternate treatment of KH2PO4 (8.2 g l-1) with diniconazole (0.04%), each applied twice at 7-day intervals, was of similar efficacy to the standard fungicide treatment described above. All phosphate solutions contained 0.25 ml l-1 Triton X-100 non-ionic surfactant. When the phosphate sprays were omitted from the alternate treatment and the sterol inhibitor fungicide was applied alone at 14-day intervals, the level of protection against O. mangiferae decreased significantly from 62% (alternate) to 43% diniconazole. All tested treatments increased yield (kg/tree) significantly compared with untreated controls, but there were no significant differences between them. Phosphate spray solutions were not phytotoxic to plant tissue. Broadly similar results to those described here for mango were obtained in apple trees against PM (Podosphaera leucotricha), where the integration of phosphate fertiliser in the management program enabled a 50% reduction in the number of fungicide applications required to manage the disease (Reuveni et al., 1998b). 4.2.3. Silicates fungicides Calcium silicate (CaSiO3) at 0.6 g l-1, reduced the in vitro growth of the peach canker fungus Leucostoma persoonii by 73% relative to control, but it was less efficacious than captan (Captan 50 WP, 1.2 mg a.s. ml-1), iprodione (Rovral 50 WP, 1.2 mg a.s. ml-1) and thiophanate-methyl (Topsin-M 85WDG, 0.38 mg a.s. ml-1) which completely inhibited fungal growth (Biggs et al., 1994). Yildirim et al. (2002) tested the efficacy of various salt fungicide sprays on the control of PM in grapes in vineyard trials in two locations in Turkey, one with low and the other with high risk of infection with U. necator. The treatment programme which consisted of four foliar applications of Na2SiO3 (1.22 g l-1) tank-mixed with sulphur WP (0.4%; Sufrol 80 WP, Ozdil San. Tic., Izmir, Turkey) was equally effective in reducing PM severity on leaves and bunches as four applications of the alternate programme penconazole (100 g l-1 EC 0.025; Topas, Novartis, Basel, Switzerland) suphur WP (applied separately twice each). Efficacy from both programmes was higher on bunches than leaves and was within the range of 72-82% compared with control. When KH2PO4 (2.72 g l-1 plus phenol-methyl oxide 90% at 0.3 ml l-1) was used instead of Na2SiO3 similar results were obtained. The test chemicals were applied at 12-day intervals, starting at fruit set stage. When the efficacy of Na2SiO3 alone was compared with that of penconazole in pot trials, no significant differences were observed between the two, with both compounds significantly suppressing (by 94% and 96%, respectively, compared with control) PM infection on leaves. The obtained data indicated that silicates as well as phosphates were very effective in reducing the susceptibility of grapevines to PM infection and that tank mixtures of these compounds with sulphur could eliminate the need to apply conventional synthetic fungicides, such as penconazole, for PM control in vineyards. 4.2.4. Phosphites fungicides In the study of Cooke and Little (2001) (section 4.1.4), single foliar sprays of KH2PO3 or K2HPO3 at 4 kg ha-1 in the field, proved significantly superior to mancozeb at 1.275 kg ha-1 (Dithane Dry Flowable; 750 g kg-1 WG, Rohm and Haas) in reducing the susceptibility of tubers to late blight (P. infestans) development. Of tubers from mancozeb-treated plots (applied at 10-day intervals from mid-June til end of season), 80% developed blight symptoms, whereas with KH2PO3 or K2HPO3 the percentages of infected tubers were c. 30% and 20%, respectively. In two further field trials involving mancozeb and KH2PO3 only, the latter tested at various timings (1-6 sprays) and application rates (2-4 kg ha-1), tuber infection was overall lower from plants lifted from KH2PO3-treated plots as compared with those from mancozeb-treated plots. The level of reduction in disease severity depended on lifting date, cultivar, timing and rate of applications and it was not significant in all cases. The spraying programme of six KH2PO3 applications at 2 kg ha-1 applied at 10-14-day intervals resulted in the least tuber infection (c. 30%), significantly lower than that on tubers from mancozeb-treated plants (mean of 90%). A mid- or late-season KH2PO3 spray at 4 kg ha-1 was approximately 40% more effective than mancozeb against P. infestans. The authors suggested that the 6 2 kg ha-1 treatment regime, despite exhibiting the best results, may be not economic. In the last field trial, the efficacy of KH2PO3 in two alternate programmes with mancozeb was investigated in comparison with three fungicide only treatment regimes: A) mancozeb 12 sprays at 7-day intervals, B) mancozeb 8 (10-14-day), C) (metalaxyl + mancozeb (150 + 1.350 kg ha-1; Fubol 75 WP, Novartis) 3 (10-day) + fluazinam (0.15 kg ha-1; Shirlan, Zeneca) 7 (7-day). The alternate treatments were: D) mancozeb 8 (10-14-day) + 4 kg ha-1 KH2PO3 1 (mid-season), E) mancozeb 6 (10-14-day) + 2 kg ha-1 KH2PO3 6 (14-day). No significant differences were observed in late blight development on inoculated-tubers from the fungicide treatments A, B and C (mean infection c. 80%). However, with KH2PO3 included in the treatment regime, susceptibility of tubers to infection was more than halved (Treatment D) or almost eliminated (Treatment E, c. 95% greater efficacy compared with conventional fungicides). The results indicated that a spray programme in which phosphites are integrated with reduced numbers of applications of a systemic or non-systemic fungicide could be used effectively for foliar and tuber blight control in potatoes and suppress the overwinter survival of P. infestans in tubers. 4.2.5. Chlorides fungicides In comparison with equivalent applications of soil-applied KCl fertiliser (93 g l-1, BDH Laboratory Supplies, Poole, UK), foliar sprays gave consistently better results regarding the control of E. graminis and S. tritici in wheat (Cook, 1997), but they proved significantly less efficacious than the conventional fungicides epoxiconazole (Opus 125 g l-1 a.s., 1 l ha-1; BASF, Cheadle, UK) and chlorothalonil (500 g l-1 a.s., 2 l ha-1; Bravo 500, BASF) in reducing the levels of infection by S. tritici (Mann et al., 2004). The average reduction in disease severity relative to the untreated as observed on the flag leaf and leaves 2, 3 and 4 was 11% by KCl, 60% by epoxinazole and 23% by chlorothalonil. The tank mixture of dose of epoxiconazole with KCl resulted in 38% mean reduction in disease severity. Furthermore, the increase in yield following foliar application of KCl was marginal (3% mean increase in seven field experiments, P > 0.05). It therefore appears unlikely that straight KCl sprays would produce cost-effective disease control but this might be possible if salts are mixed with reduced rates of fungicides (Kettlewell, 2007). Acknowledgments In addition to people already mentioned in this report we would like to thank the following individuals for useful discussions and contribution of data: Dr. Jim Monaghan (Harper Adams University College), Dr. David Norman (Vegetable Consultancy Services), Dr. Kristian Orlovius (Potash Ltd), John Haywood (BioAgro Western), Ian Elliot (Omex), Tom Nellist (Farm-Fos Ltd), Dr. Clive Edwards (Home Grown Cereals Authority), Ross Newham (Horticultural Development Council) and Tommy Wada (Arysta LifeScience Corp.). References Abbasi P, Lazarovits G. 2006. Effect of soil application of AG3 phosphonate on the severity of clubroot of bok choy and cabbage caused by Plasmodiophora brassicae. Plant Disease 90, 1517-1522. Adatia MH, Besford RT. 1986. 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h5>^JhOhO6^JhOhUj6^JhhUj5:^JhOhUj6]^JhUjhUj^Jhr,hr,6^J@|3bco9GvP'v:P'v:P'v:P'v:P'v:P'v:P'v:P'v:P'v:P'v:P'v:P'v:P'v:P'v:P'v:P'v:P'v:P'v:P'v:P'v:P'v:P'v:P'v:$<^`a$gdu8$<^`a$gd6O$<^`a$gdu8mo+9kj,.t"X}mw9GhB[hUj^JmHsHhB[hUj6^JmHsHhUjhUj]^Jh**hUj6]^JhUjhUjH*^JUhOhUj6^JhOhUj6]^Jhz"hUj6^Jhr,hr,6^JhhUj5:^JhUjhUj^J4 Role of salicylic acid and intracellular Ca2+ in the induction of chitinase activity in carrot suspension culture. Physiological and Molecular Plant Pathology 45, 101-109. Simpson K. 1986. Fertilizers and Manures. Longman Group Limited, NY, USA. 254 pp. Smillie R. Grant BR, Guest D. 1989. The mode of action of phosphite: Evidence for both direct and indirect modes of action on three Phytophthora spp. in plants. Phytopathology 79, 921-926. Speiser B, Berner A, Haseli A, Tamm L. 2000. Control of downy mildew of grapevine with potassium phosphonate: Effectivity and phosphonate residues in wine. Biological Agriculture & Horticulture 17, 305-312. Taeymans D, Andersson A, Ashby P, Blank I, Gonde P, van Eijck P, Faivre V, Lalljie SPD, Lingnert H, Lindblom M, Matissek R, Muller D, Stadler RH, Studer A, Silvani D, Tallmadge D, Thompson G, Whitmore T, Wood J, Zyzak D. 2005. Acrylamide: Update on selected research activities conducted by the European food and drink industry. Journal of AOAC International 88, 234-241. Vallad GE, Goodmanb RM. 2004. Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Science 44, 1920-1934. van Toor RF, Jaspers MV, Stewart A. 2004. Bicarbonate salts and calcium cyanamide suppress apothecial production by Ciborinia camelliae. New Zealand Plant Protection 57, 142-145. Wagner F. 1940. Die bedeutung der kieselsare fr das wachstum einiger kulturpflanzen, ihrem nhrstoffhaushalt und ihrer anflligkeit gegen echte mehltaupilze. Phytopathologische Zeitschrift 12, 427-479. Walters DR, Bingham IJ. 2007. Influence of nutrition on disease development caused by fungal pathogens: Implications for plant disease control. Annals of Applied Biology 151, 307-324. Walters D, Walsh D, Newton A, Lyon G. 2005. Induced resistance for plant disease control: Maximising the efficiency of resistance elicitors. Phytopathology 95, 1368-1373. Wang Y, Stass A, Horst WJ. 2004. Apoplastic binding of aluminum is involved in silicon-induced amelioration of aluminum toxicity in maize. Plant Physiology 136, 3762-3770. Winslow MD. 1992. Silicon, disease resistance, and yield of rice genotypes under upland cultural conditions. Crop Science 32, 1208-1213. Yildirim I, Onogur E, Irshad M. 2002. Investigations on the efficacy of some natural chemicals against powdery mildew [Uncinula necator (Schw.) Burr.] of grape. Journal of Phytopathology 150, 697-702. Zainuri DC Joyce, Wearing AH, Coates L, Terry L. 2001. Effects of phosphonate and salicylic acid treatments on anthracnose disease development and ripening of Kensington Pride mango fruit. Australian Journal of Experimental Agriculture 41, 805-813. Ziv O, Zitter TA. 1992. Effects of bicarbonates and film-forming polymers on cucurbit foliar diseases. Plant Disease 76, 513-517. Action resulting from this research A review paper with findings from this research is being prepared for submission to the journal Crop Protection. Selected findings from this research will be presented in a platform presentation entitled: Inorganic Salts for Suppressing Powdery Mildew in Cucurbits A Worldwide Survey (by Thomas Deliopoulos, Peter S. Kettlewell and Martin C. Hare) in the 60th International Symposium on Crop Protection in Ghent, Belgium, 20th May 2008. An extended abstract of the oral presentation mentioned above will be published in a special issue of the Journal Communications in Agricultural and Applied Biological Sciences in December 2008. A research seminar will be given to Staff and Research Students at Harper Adams University College, 15th May 2008, summarising the results of the scoping study and focusing on the compatibility of inorganic salts as fungicides with sustainable agriculture.  References to published material9. This section should be used to record links (hypertext links where possible) or references to other published material generated by, or relating to this project.      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