Can. J. Plant Pathol. (2010), 32(3): 287–297

Special topics/Sujets spéciaux

Minireview/MinisynthèseTCJP Integrated management of silver scurf ( solani)

T.Potato silver scurfJ. management AVIS*, C. MARTINEZ AND R. J. TWEDDELL

Centre de recherche en horticulture, Pavillon de l’Envirotron, Université Laval, Québec, QC G1V 0A6, Canada

(Accepted 15 May 2010)

Abstract: Silver scurf is a surface blemish disease of potato ( tuberosum L.) tubers, caused by Durieu & Mont., which has gained increasing economic importance in recent years. The disease develops initially in the field but fully expands in the warehouse under storage conditions favourable to the spread of the pathogen. Control of the disease, once provided by the fungicide thiabendazole, is now difficult due to the appearance of thiabendazole-resistant strains and the lack of potato cultivars with high levels of resistance to silver scurf. An integrated disease management programme including appropriate cultural methods and storage conditions along with the use at planting and/or at harvest of synthetic chemical fungicides is recommended to reduce the incidence and the severity of silver scurf. Recent studies put forth the possibility that ‘generally recognized as safe’ (GRAS) compounds and microbial antagonists could eventually be integrated into silver scurf management strategies.

Keywords: cultural control, disease management, Helminthosporium solani, postharvest disease

Résumé: La gale argentée est une maladie de la pomme de terre (Solanum tuberosum L.), causée par Helminthosporium solani Durieu et Mont., qui forme des taches à la surface des tubercules et qui a pris de plus en plus d’importance économiquement depuis les dernières années. Au départ, la maladie est contractée au champ, mais c’est en entrepôt qu’elle se développe complètement, lorsque les conditions d’entreposage sont favorables à la prolifération de l’agent pathogène. La lutte contre la maladie, autrefois dépendante du fongicide thiabendazole, est aujourd’hui compromise à cause de l’apparition de souches résistantes au thiabendazole et à l’absence de cultivars hautement résistants à la gale argentée. Un programme de gestion intégrée de la maladie incluant des méthodes culturales, des conditions d’entreposage appropriées, et Downloaded by [Universite Laval] at 06:02 25 March 2013 l’utilisation, au moment des semis ou de la récolte, de fongicides de synthèse, est recommandé pour réduire l’incidence et la sévérité de la gale argentée. Des études récentes suggèrent que des composés généralement considérés comme inoffensifs et des antagonistes microbiens puissent éventuellement être intégrés dans les stratégies de gestion de la gale argentée.

Mots clés: lutte culturale, gestion des maladies, Helminthosporium solani, maladies post-récolte

Introduction reported in most potato growing areas of the Americas (Melhus, 1913; Conners, 1924; Hermila-Sanz, 1976), Silver scurf is a fungal surface blemish disease of potato Europe (Schultz, 1916; Mooi, 1968; Hide et al., 1969b; (Solanum tuberosum L.) tubers, caused by Helminthospo- Ivanyuk & Zezyulina, 1991; Sneig, 1992; Bång, 1993; rium solani Durieu & Mont., which has gained increasing El Immane-Collet et al., 1995; Stachewicz, 1999), the economic importance in recent years. First reported in Middle East and India (Singh, 1972; Zimmerman-Gries & Moscow in 1871 (Harz, 1871), silver scurf has now been

Correspondence to: R. J. Tweddell. E-mail: [email protected] *Present address: Department of Chemistry, Carleton University, 1125 Colonel By Drive, Ottawa , ON K1S 5B6, Canada

ISSN 0706-0661 print/ISSN 1715-2992 online © 2010 The Canadian Phytopathological Society DOI: 10.1080/07060661.2010.508627 T. J. Avis et al. 288

Blodgett, 1974), Africa (El Immane-Collet et al., 1995), Causal agent China (Tian et al., 2007) and New Zealand (Welsh, 1996). The causal agent, H. solani, is an anamorphic Initially considered a disease of minor importance, belonging to the family , order , silver scurf is now becoming a disease of high economic phylum (Phylogenetic classification) (Kirk et consequence (Errampalli et al., 2001). This emergence of al., 2008). In artificial medium, the fungus generally silver scurf as a significant disease of potato is due to presents a hyaline to dark brown mycelium with conidio- both increased silver scurf incidence and the changing phores and conidia arising from stromata (Luttrell, 1964; habits of consumers and the industry. Essentially, silver Barnett & Hunter, 1998). The conidiophores are thinner scurf incidence has increased with the development of at the apex than the base and bear black, melanized thiabendazole-resistant strains of H. solani (Hide et al., conidia containing two to eight pseudosepta. The first 1988; Mérida & Loria, 1990, 1994a; Bång, 1993; Kaw- conidium develops terminally at the apex of the conidio- chuk et al., 1994; Holley & Kawchuk, 1996) and the fact phore and subsequent conidia develop basipetally (Lut- that no high level resistance to the pathogen exists among trell, 1964; Hunger & McIntyre, 1979). The conidia form potato cultivars (Mérida et al., 1994; Rodriguez et al., pleurogenously in whorls on the conidiophores (Erram- 1996). Moreover, the increasing consumer demand for palli et al., 2001; Stevenson et al., 2001). With the excep- washed potatoes, their packaging in clear bags, and the tion of tuber-bearing Solanum species (Rodriguez et al., increasing quality of product that consumers insist upon 1995), and an isolated report of S. elaeagnifolium Cav. have led to the rejection of silver scurf affected potato leafspot disease (Sethuraman et al., 1997), potatoes are tubers by the industry (Loria, 1992; Secor, 1994; Holley the only known host of H. solani. There are no reports of & Kawchuk, 1996; Frazier et al., 1998). the fungus infecting alternative hosts including other Silver scurf disease of potato has been the subject of a solanaceous crops (Burke, 1938; Kamara & Hugelet, previous review (Errampalli et al., 2001) in which the 1972; Bains et al., 1996). authors focussed on H. solani biology, the epidemiology of the disease, the detection of the pathogen as well as control measures. Considering the continued increase in Disease cycle and the infection process potato silver scurf importance within the past years, the Infected potato seed tubers constitute the primary source present review will concentrate primarily on the more of inoculum (Burke, 1938; Mooi, 1968; Santerre, 1972; recent developments in silver scurf research including the Hide & Adams, 1980; Secor & Gudmestad, 1999). Once understanding of pathogen biology in the infection pro- planted, the inoculum is transferred to the daughter tubers cess and the management of the disease. although the mechanism of transfer is not well under- stood, particularly considering the non-motility of the spores. Disease symptoms Accounting for a large proportion of silver scurf on Silver scurf is a blemish disease of the tubers that ini- progeny seed tubers, H. solani is considered a tuber- tially manifests itself as a tan to grey discolouration of borne pathogen (Geary & Johnson, 2006). Although once Downloaded by [Universite Laval] at 06:02 25 March 2013 the periderm in irregular patterns (Secor & Gudmestad, thought to be unimportant (Santerre, 1967; Jellis & 1999; Stevenson et al., 2001). The discolouration is Taylor, 1977), studies would indicate that overwintering caused by loss of pigment, through cell desiccation, soil-borne inoculum might be an important component of and suberin deposition (Frazier et al., 1998). In red- the disease cycle (Mérida & Loria, 1994b; Firman & skinned potato cultivars, silver scurf can cause a com- Allen, 1995b; Bains et al., 1996; Rodriguez et al., 1996; plete loss of skin pigmentation (Jellis & Taylor, 1977; Frazier et al., 1998). Mérida and Loria (1994b) showed Secor, 1994). It does not cause yield losses at harvest, that disease-free tubers planted in fields with a known but does cause weight loss of stored potatoes due to history of silver scurf became infected with H. solani. increased water loss, resulting in excess shrinkage and Bains et al. (1996) showed that H. solani-free nuclear flabbiness (Secor & Gudmestad, 1999). Portions of the seed tubers planted in fields where potatoes had never periderm may eventually slough off (Olivier et al., been grown, or were grown one, two, three or four years 1998). Black spots can be visible due to the presence previously produced daughter tubers with silver scurf. New of H. solani conidiophores and conidia on the tuber techniques for quantifying H. solani that rely on DNA surface (Stevenson et al., 2001). The disease does not methods (Olivier & Loria, 1998; Cullen & Errampalli, affect any other part of the potato plant except the 2000) rather than conventional bait (Bains et al., 1996) and tubers (Secor & Gudmestad, 1999). plate count methods (that are not truly appropriate for the Potato silver scurf management 289

slow-growing and weakly competitive H. solani) will H. solani, when developing silver scurf management most likely highlight the true influence of soil-borne strategies (Martinez et al., 2004). inoculum of H. solani as these molecular tools have been used successfully in the past to detect and monitor soil fungi in natural environments (Bridge & Spooner, 2001). Disease management The appearance of silver scurf symptoms is generally Cultural practices and storage low at harvest. It is under warehouse conditions that the harvested tubers bearing H. solani inoculum undergo Cultural practices in potato farming are known to affect development and spread of the disease. In particular, the incidence and severity of silver scurf. Disease-free conidia can be transported through the air by the ventilation seed tubers, planting dates and densities, harvest dates, system and serve as a secondary inoculum source, caus- and storage conditions are among the more common fac- ing the infection of a large number of tubers (Mérida & tors impacting H. solani development. Loria, 1994b; Rodriguez et al., 1996). Seeding of these The level of H. solani inoculum present on the seed infected tubers the following potato growing season car- tuber affects the severity of the disease on the progeny. ries the inoculum to the field. The relationship between the amount of silver scurf on The infection process has received little attention in seed tubers and on progeny tubers is, however, unclear. the past and very few studies have described the H. solani Indeed, there have been discrepancies in the reported infection of potato tubers. This lack of information is effect of seed tuber silver scurf level on silver scurf important considering that the elaboration of integrated severity on progeny tubers. A negative (Jouan et al., control strategies for silver scurf requires a high level of 1974; Jellis & Taylor, 1977; Adams & Hide, 1980; understanding of the infection process. An initial study of Lennard, 1980; Read & Hide, 1984) and a positive histopathological events was described by Heiny and (Geary & Johnson, 2006) correlation were observed McIntyre (1983) using light and scanning electron micro- between the amount of silver scurf on the seed tubers and scopy (SEM). They showed with the cultivar ‘Norchip’ the amount on the progeny tubers. Zimmerman-Gries & that the infection cycle was completed within seven to Blodgett (1974) observed no significant differences in nine days, with periderm penetration being observed two the level of silver scurf on progeny tubers produced from days after inoculation. Subsequently, Martinez et al. seed tubers with slight or severe symptoms of the disease. (2004) conducted an exhaustive study of the infection The use of disease-free seed tubers is recommended for process using SEM and transmission electron micros- the limitation of silver scurf severity, as studies have copy. They showed with H. solani strain ulaval-1 and shown that the seed tuber is the main source of infection ‘Dark Red Norland’ that tuber periderm penetration of progeny tubers (Secor & Gudmestad, 1999; Geary & occurred between 6 and 9 h after H. solani inoculation Johnson, 2006) and that even a relatively low level of and that no specialized structures, such as appressoria or silver scurf on the seed tuber can result in heavily hyphal enlargements, were produced by the fungus. This infected daughter tubers (Firman & Allen, 1995b). contrasts with previous work, which had shown that H. Planting and harvesting dates also play a role in

Downloaded by [Universite Laval] at 06:02 25 March 2013 solani produced appressoria during penetration (Heiny & disease incidence and severity. More precisely, the length McIntyre, 1983). Hyphae of H. solani, 9 h after inocula- of exposure of tubers to H. solani (from tuber initiation to tion, were observed in numerous cells of the periderm harvest) has been correlated with silver scurf severity. (mainly) and in the cortex although no massive coloniza- Mérida et al. (1994) demonstrated that later harvest dates tion of host cells was noticeable (Martinez et al., 2004). are more conducive to high disease severity whereas earl- Localization of H. solani demonstrated that hyphae were ier harvest dates were found to decrease the level of sil- mostly intracellular and not surrounded by a sheath. ver scurf. Firman & Allen (1995b) also found that earlier Conidiogenesis was observed four days after inoculation, harvesting reduced the severity of silver scurf when rated completing the infection cycle (Martinez et al., 2004). after storage. They concluded that the interval between Observations described by Heiny and McIntyre (1983) tuber initiation and harvesting is a major determinant in and Martinez et al. (2004) suggest that different H. solani severity both at harvest and during storage. Planting strains might produce distinct infection structures. density is also a factor in silver scurf development. These observations also indicate that the time required Firman & Allen (1995a) demonstrated that silver scurf by H. solani to complete its parasitic cycle varies was more severe when planting densities were higher. according to the strain of the fungus and the potato Crop rotation is equally considered to be an important cultivar. These findings point to the importance of management practice, as it has been known to decrease considering different potato cultivars and strains of silver scurf (Hide & Read, 1991; Secor & Gudmestad, T. J. Avis et al. 290

1999; Stevenson et al., 2001). Although crop rotation temperature possible, given the market requirement with non solanaceous crops was not reported to com- (Stevenson et al., 2001). Ogilvy (1992) showed that stor- pletely eradicate silver scurf even with the use of disease- ing tubers at 4 ºC provided improved silver scurf control free seed tubers in a four year rotation scheme (Bains et relative to fungicide treatments. It is, however, important al., 1996), positive effects of crop rotation have been to take into account the effects of modifying storage con- reported. Peters et al. (2003) demonstrated that a three ditions on the potato tubers themselves and, particularly, year crop rotation of barley (undersown with red clover), the quality and the intended use of the tubers (Plissey, red clover and potato would significantly reduce silver 1993). Reducing the relative humidity for control of scurf when compared with a two year rotation of barley silver scurf can cause reduced quality and increased and potato. When averaged over an eight year period, shrinkage of the tuber (Frazier et al., 1998). Moreover, Carter et al. (2003) showed that two year potato rotations storing tubers at 4 ºC is common practice for seed and with red clover significantly decreased silver scurf when some fresh-market tubers but would not be appropriate compared with a rotation with barley or barley and Italian for tubers destined for French frying or chip processing ryegrass. as the lower storage temperature would cause inferior Proper potato warehouse management is necessary to frying colour (Cunnington et al., 1992). reduce incidence and severity of silver scurf. Ensuring appropriate sanitary conditions such as the removal of Chemical control residues and soil has been known to reduce the severity of silver scurf throughout the storage period by reducing In 1968, thiabendazole was first found to be effective H. solani inoculum in proximity of the tubers (Frazier et against a range of potato pathogens including H. solani al., 1998; Errampalli et al., 2001). Postharvest applica- and, since the mid-1970s, it has been widely used on tion of the fungicide thiabendazole had previously been potatoes (Hide et al., 1969a, 1988). Applied as posthar- employed as an efficient method for the control of silver vest or seed treatments, the fungicide provided effective scurf. However, the development of H. solani strains control of silver scurf until resistant isolates increased in resistant to thiabendazole has basically precluded its use frequency. Resistance of H. solani to thiabendazole was as an effective postharvest chemical. Details on resistant first reported in the UK in 1988 in isolates collected from strains of H. solani and other aspects of chemical control 1977 to 1986 in commercial seed and ware tubers (Hide of silver scurf are provided in the following section. et al., 1988). Thiabendazole resistance in H. solani was Among other benefits on tuber quality, curing of the subsequently documented in the USA (Mérida & Loria, potatoes for two to three weeks is performed to allow 1990) and in Canada (Kawchuk et al., 1994; Holley & suberization/scarring of wounds. Tuber scarring prevents Kawchuk, 1996; Platt, 1997). the penetration of various pathogens through wounds that The loss of efficacy of thiabendazole, resulting mainly occurred during the harvesting process. In the case of sil- from the increase in the frequency of resistant isolates, ver scurf, a longer curing period has been reported to has led to the exploration of alternative fungicides for the decrease silver scurf (Hide et al., 1994a, 1994b). In the control of silver scurf. Different synthetic chemical fun-

Downloaded by [Universite Laval] at 06:02 25 March 2013 particular case of relative humidity, care must be taken gicides were tested against potato silver scurf (Table 1). throughout the entire storage period to avoid condensa- Several, including imazalil, fenpiclonil, fludioxonil, thi- tion of moisture on the tubers as this is known to greatly ophanate-methyl, azoxystrobin, prochloraz, propicona- increase the sporulation of the fungus on the skin surface zole and mancozeb were reported effective when applied (Jouan et al., 1974; Hardy et al., 1997). Appropriate ven- as seed treatments. Among these fungicides, mancozeb, tilation of storage units is thus of particular importance. thiophanate-methyl, fludioxonil and azoxystrobin are However, H. solani conidia can be easily dispersed registered in Canada as seed or in-furrow treatments through the ventilation system (Rodriguez et al., 1996) (CRAAQ, 2009). There have been discrepancies in the and be an important source of secondary infection in the reported efficacy of these four fungicides, which could be warehouse. Decreasing relative humidity from 95 to 85% explained by differences in experimental designs includ- has been shown to reduce silver scurf severity (Frazier ing the mode of application and the concentration of fun- et al., 1998). Furthermore, Secor and Gudmestad (1999) gicide tested, the time of harvest, the level of infestation have shown that lowering the relative humidity to 90% in of the seed tuber, and the presence of resistant isolates. the initial month of storage was sufficient to delay H. Inconsistencies in the reported efficacy of seed treat- solani sporulation. The lowering of storage temperature ments to control silver scurf may also be a result of pre- has also been reported to give increased control of silver existing soil-borne inoculum, soil type, soil microbial scurf. In general, tubers should be stored at the lowest populations (Geary et al., 2007) and environmental Potato silver scurf management 291

conditions. For example, different studies reported that only salt capable of inhibiting H. solani once the fun- the application as a seed treatment of mancozeb (Collet- gus had penetrated the periderm (Hervieux et al., Elimane & Jouan, 1993; Le Corre et al., 1993; Gaucher, 2002). Phosphorous acid and salts of phosphorous acid 1998; Tsror & Peretz-Alon, 2004) or fludioxonil (Shetty were also effective in controlling silver scurf. Olsen et et al., 1994; Frazier et al., 1998; Geary et al., 2000; Tsror al. (2009) recently reported that postharvest application & Peretz-Alon, 2004; Geary et al., 2007) provided pro- of phosphorous acid significantly reduced silver scurf tection against potato silver scurf while Hervieux et al. incidence, showing its potential use for the suppression (2001) reported that these same fungicides failed to con- of the disease in storage. This raises the possibility of trol the disease. In the latter report, it was suggested that using selected salts on either seed or warehouse tubers the lack of efficacy of the fungicides was the result of for human consumption. Salts constitute an interesting infection by soil-borne inoculum in progeny tubers, alternative to synthetic chemical fungicides for utiliza- which were not protected by the non-systemic fungicides tion as postharvest chemicals considering that they fludioxonil and mancozeb applied on the seed tubers. generally display a broad spectrum of antimicrobial With regard to thiophanate-methyl, resistance of H. solani activity, low mammalian toxicity, biocompatibility, isolates (Kawchuk et al., 1994; Holley & Kawchuk, 1996; and relatively low cost (Horst et al., 1992; Olivier Frazier et al., 1998) may explain the inconsistency in et al., 1998; Mecteau et al., 2002). Moreover, many reported efficacy of the fungicide (Table 1). salts are generally recognized as safe (GRAS) for In order to improve the control of the disease and to human consumption and are presently used in the food maintain, when possible, the efficacy of thiabendazole processing industry. Plant essential oils are other through preventing the development of resistance, GRAS compounds that have received interest in the application of fungicide mixtures has also been tested as control of silver scurf. S-carvone, menthol, pulegone, seed treatments. Different studies reported that the eugenol, cuminaldehyde, benzaldehyde, cinnamalde- application of a thiabendazole+imazalil mixture afforded hyde are purified compounds from essential oils that higher control of the disease when compared to thiaben- suppressed H. solani in vitro mycelial growth (Gorris dazole applied alone (Hide et al., 1987; Hall & Hide, et al., 1994). Petroleum ether extracts of Stevia rebau- 1992, 1994) and prevented in whole or in part (Hall & diana Bertoni leaves also inhibited the in vitro mycelial Hide, 1994) the development of thiabendazole-resistant growth of H. solani (Ghosh et al., 2008). Multiple isolates. Other combinations of fungicides have also been clove oil applications were also reported to reduce sil- reported to be effective against silver scurf including ver scurf severity and incidence on tubers (Frazier thiophanate-methyl+mancozeb (Frazier et al., 1998; Geary et al., 2004, 2006). Fumigation of tubers with natural et al., 2007), captan+mancozeb, thiabendazole+man- plant volatiles such as garlic (Allium sativum L.) or sage cozeb (Frazier et al., 1998), and fludioxonil+quintozene (Salvia officinalis L.) essential oils was also reported to (Geary et al., 2007). control silver scurf development (Bång, 2007). With the increasing concerns of fungicide resistance As for other alternatives to synthetic chemical fungi- and public awareness of the direct, indirect and cumu- cides, chlorine and chlorine dioxide are effective and

Downloaded by [Universite Laval] at 06:02 25 March 2013 lative effects of synthetic chemical fungicides on both economical biocides that have been extensively used as the environment and human health, there is a trend disinfectants. Reports suggest that these relatively safe towards the reduction of use of synthetic chemical fun- and inexpensive compounds, which pose little threat to gicides in agriculture. In this context, different chem- human health or the environment, have shown potential ical compounds including salts, disinfectants and plant for the postharvest control of silver scurf (Secor & essential oils have been tested as alternatives to syn- Gudmestad, 1999; Tweddell et al., 2003). Secor and thetic chemical fungicides for the control of silver Gudmestad (1999) reported that chlorine dioxide, intro- scurf. Several inorganic and organic salts were shown duced through the humidification system during potato to strongly inhibit the in vitro growth and development storage, reduced both the incidence and severity of sil- of H. solani (Olivier et al., 1998; Hervieux et al., 2002; ver scurf. Applied alone or in combination with thi- Avis et al., 2007). Among these salts, aluminium chlo- ophanate-methyl as a pre-planting seed tuber treatment, ride, aluminium lactate, sodium metabisulphite, triso- chlorine dioxide was not effective to control silver scurf dium phosphate, sodium carbonate and potassium on progeny tubers (Errampalli et al., 2006). Tweddell et sorbate (Olivier et al., 1998, 1999; Hervieux et al., al. (2003) showed that exposure of recently infested 2002; Griffiths & Zitter, 2006) were shown to mark- potato tubers to atmospheres containing chlorine com- edly reduce silver scurf severity. Aluminium chloride pounds was very effective in controlling silver scurf. is of particular interest, given that it is presumably the Indeed, it was observed that, over a storage period of T. J. Avis et al. 292

Table 1. Different fungicides tested for control of potato silver scurf.

Fungicide Application Disease reductiona Reference

Azoxystrobin Seed + Geary et al. (2000) Seed − Hervieux et al. (2001) Seed + Tsror & Peretz-Alon (2004) Seed + Geary et al. (2007) Captan Postharvest treatment of seed + Copeland & Logan (1975) Captafol Postharvest treatment of seed + Copeland & Logan (1975) Fenpiclonil Seed − Cooke & Little (1995) Seed + Gaucher (1998) Seed + Leadbeater & Kirk (1992) Seed + Welsh (1996) Fludioxonil Seed + Errampalli et al. (2001) Seed + Frazier et al. (1998) Seed + Geary et al. (2000) Seed − Hervieux et al. (2001) Seed + Shetty et al. (1994) Seed + Tsror & Peretz-Alon (2004) Seed + Geary et al. (2007) Flutolanil Seed + Gaucher (1998) Fuberidazole Postharvest treatment of seed + Copeland & Logan (1975) Imazalil Postharvest treatment of seed + Cayley et al. (1983) Seed + Collet-Elimane & Jouan (1993) Seed − Cooke & Little (1995) Seed + Hall & Hide (1992) Seed − Hervieux et al. (2001) Seed + Hide (1994) Seed + Hide et al. (1987) Seed + Hide et al. (1994a) Seed + Tsror & Peretz-Alon (2002) Seed + Tsror & Peretz-Alon (2004) Iprodione Seed − Hervieux et al. (2001) Seed + Tsror & Peretz-Alon (2004) Mancozeb Seed + Collet-Elimane & Jouan (1993) Seed + Gaucher (1998) Seed − Hervieux et al. (2001) Seed + Le Corre et al. (1993) Seed − Geary et al. (2007)

Downloaded by [Universite Laval] at 06:02 25 March 2013 Seed + Tsror & Peretz-Alon (2004) Pencycuron Seed − Cooke & Little (1995) Prochloraz Seed + Denner et al. (1997) Seed + Hide et al. (1987) Seed + Tsror & Peretz-Alon (2004) Propiconazole Seed + Bisht & Bains (1995) Seed + Hide et al. (1987) Propineb Seed + Tsror & Peretz-Alon (2004) Thiophanate-methyl Seed + Bisht & Bains (1995) Seed − Frazier et al. (1998) Seed + Jouan et al. (1974) Seed − Geary et al. (2007) Thiram Postharvest treatment of seed + Copeland & Logan (1975) Tolylfluanid Seed + Wainwright et al. (1996)

Notes: aFungicide was reported effective (+) or ineffective (–) in controlling potato silver scurf. Potato silver scurf management 293

50 days, exposure of tubers to available chlorine con- Suppressive soils centration of 20 mg L−1 in moist air resulted in disease In the course of field studies aimed to evaluate fungicides reductions of 84, 97, 97 and 97% after exposure of 1, 2, for the control of potato silver scurf (Geary et al., 2000; 7 and 50 days, respectively. Continuous exposure of − Hervieux et al., 2001), it was observed that experimental tubers to 2 mg L 1 available chlorine was also effective, sites influence disease severity, suggesting that soils resulting in a 73% disease reduction. Finally, hydrogen influence silver scurf development. In order to identify peroxide, which is registered in Canada as a postharvest suppressive soils towards silver scurf and to gain an treatment of tubers (CRAAQ, 2009), has also been understanding into the precise properties that afford soils reported to control silver scurf in stored tubers when their suppressive nature, 45 soils from the province of applied in the storage room by fogging (Afek et al., Québec reported to produce potato tubers with reduced 2001). silver scurf symptoms were assayed for their influence on These studies suggest that postharvest application of disease, by planting artificially infected seed tubers salts (Olivier et al., 1998, 1999; Hervieux et al., 2002), directly in these soils under greenhouse conditions plant essential oils (Gorris et al., 1994; Frazier et al., (Martinez et al., 2002). Results from the study showed 2004, 2006; Bång, 2007), chlorine (Tweddell et al., that soil types greatly influenced the development of sil- 2003), chlorine dioxide (Secor & Gudmestad, 1999) or ver scurf, rated both at harvest and following a three hydrogen peroxide (Afek et al., 2001) could eventually month storage period and that some soils displayed an be integrated into silver scurf control strategies. interesting level of suppressiveness. In order to determine the properties of the soil that most significantly influ- Host resistance enced disease development, 12 physico-chemical proper- ties were measured and correlated with silver scurf One of the major reasons for the increasing economic severity. The results obtained from these trials revealed a importance of silver scurf is the lack of high levels of significant negative correlation between silver scurf resistance in potato cultivars (Mérida et al., 1994; severity and soil NO3 and available Fe contents, indicat- Rodriguez, 1994; Errampalli et al., 2001). Although ing a possible suppressive effect of these two soil compo- there are few published studies on cultivar susceptibility nents. NO3 had previously been negatively correlated to silver scurf, the investigated potato cultivars do, how- with silver scurf disease (Adams et al., 1970) but it is still ever, present differential susceptibility to H. solani. not clear how it may influence severity or which NO3 ‘Superior’ and ‘Chippewa’ gave consistently lower mechanisms may reduce disease development. Since silver scurf symptoms whereas ‘Norland’ had higher NO3 is known to be efficiently used as a nitrogen source severity in a whole tuber assay (Mérida et al., 1994). by H. solani (Singh, 1968), a direct adverse effect on sil- Secor (1994) evaluated 19 potato cultivars and selec- ver scurf is not likely. A probable explanation of NO3 tions but none revealed high resistance to silver scurf. could be its effect on other soil microorganisms (Mar- High levels of silver scurf were reported in ‘Yukon tinez et al., 2002) and, possibly, H. solani antagonists. In Gold’ (Errampalli et al., 1999) as well as ‘Russet Burbank’, the case of Fe, the effect on lowering silver scurf severity Downloaded by [Universite Laval] at 06:02 25 March 2013 ‘Kennebec’, ‘Shepody’ and ‘Superior’ (Errampalli et al., could be either a direct inhibitory effect on H. solani or 2001). through its effect on other soil microorganisms. Breeding programmes that utilize wild Solanum spp. In order to ascertain the effect of soil microorganisms have been attempted in an effort to increase H. solani on silver scurf severity, microbial populations from these resistance in potato. Rodriguez et al. (1995) screened 45 soils were classified and quantified to assess their over 200 tuber-bearing species and found that some effect on silver scurf. While previous work reported a representatives of S. acaule Bitter, S. chacoense Bitter, S. highly significant negative correlation between silver demissum Lindl., S. hondelmannii Hawkes & Hjert., S. scurf and total bacterial count (Adams et al., 1970), this oxycarpum Schiede and S. stoloniferum Schltdl. consist- study did not show any strong correlation between silver ently demonstrated low H. solani-sporulation on the scurf severity and populations of fluorescent pseudomon- tubers. Genes from some of these species have already ads, gram-negative bacteria, actinomycetes, fungi or total been introduced into the background of potato cultivars, microorganisms. However, six bacteria isolated from the although the breeding was not specifically for H. solani suppressive soils were shown to reduce silver scurf by resistance (Murphy et al., 1999). However, there have more than 50% when applied individually on artificially been no reports, to our knowledge, of silver scurf resist- inoculated potato tubers (Martinez et al., 2002). These ant potato cultivars. results suggested that microbial antagonists may be the T. J. Avis et al. 294

most important component contributing to soil suppres- in an attempt to elucidate the mechanisms behind their siveness and that antagonists may be a privileged avenue inhibitory effects. for biological control of silver scurf. The following Helminthosporium solani was therefore submitted to section highlights the work that has been done with silver direct confrontation assays and to precultured solid scurf biological control and, in particular, the use of media with the potential antagonists to determine their antagonists. inhibitory effect on mycelial growth and conidial germi- nation (Martinez et al., 2006). Results from this study indicated that A. piechaudii, A. autotrophicum, B. cereus, Biological control C. fimi, K. rosea, P. chlororaphis, P. fluorescens, P. put- Biological control is considered an attractive alternative ida and S. griseus were able to inhibit mycelial growth to chemicals for the efficient, reliable, and environmen- and/or conidial germination through the production of tally safe control of plant pathogens. The identification of diffusible metabolites and that antibiosis was likely antagonistic microorganisms against H. solani may there- responsible, at least in part, for their antagonism of H. fore open the way to new avenues of investigation solani. towards achieving biocontrol of potato silver scurf. Pseu- Among commercially available biopesticides, Serenade domonas putida (Trev.) Mig., Xanthomonas campestris ASO (a formulation of Bacillus subtilis) has demon- (Pam.) Dowson, and Nocardia globerula (Gray) Waksman strated suppression of silver scurf. Johnson (2007) & Henrici showed some promise in controlling silver showed that Serenade ASO reduced both the incidence scurf (Elson et al., 1997). Secor and Gudmestad (1999) and the severity of silver scurf under low disease pressure also indicated that a fungus of the genus Cephalosporium and delayed the onset of silver scurf in storage for five Corda was able to reduce the dissemination of silver months. At high disease pressure, only the severity of scurf in storage. This Cephalosporium sp. has now been silver scurf was reduced by Serenade ASO. Other com- renamed W. Gams and has shown mercially available biopesticides, Bio-Save products the ability to significantly reduce sporulation, spore ger- (various formulations of non-pathogenic and antagonistic mination and mycelial growth of H. solani, although it Pseudomonas syringae strains) are presently registered does not reduce silver scurf on previously infected pota- as biopesticides for postharvest control of potato silver toes (Rivera-Varas et al., 2007). Other work indicated scurf in the USA (Stockwell & Stack, 2007). To the best that Trichoderma hamatum (Bonord.) Bainier, T. koningii of our knowledge, Bio-Save products are still being eval- Oudem., T. polysporum (Link) Rifai, T. harzianum Rifai uated in Canada for registration purposes. Recent discover- and T. viride Pers. isolated from potato growing soil and ies may lead to the use of more microbial antagonists as a the rhizosphere of potato plants during sprouting were component of an integrated pest management programme the most inhibitory microorganisms to H. solani growth for the control of H. solani. in vitro (Kurzawinska, 2006). When isolating potential antagonists from suppressive Conclusions soils in the province of Québec, numerous microorganisms

Downloaded by [Universite Laval] at 06:02 25 March 2013 were shown to individually procure an inhibitory effect on The emergence of silver scurf as a significant disease of H. solani in artificially infected tubers (Martinez et al., potato is due to (i) increased silver scurf incidence 2002; Michaud et al., 2002). Among these microorganisms, (development of thiabendazole-resistant strains, no culti- Alcaligenes piechaudii Kiredjian et al., Aquaspirillum vars with a high level of resistance to silver scurf) and (ii) autotrophicum Aragno & Schlegel, Arthrobacter oxydans changes in marketing of potatoes (washed potatoes in Sguros, Frankland & Frankland, B. clear plastic bags). An integrated disease management mycoides Flügge, Cellulomonas fimi (McBeth & Scales) programme including appropriate cultural methods and Bergey et al., Kocuria rosea (Flügge) Stackebrandt et al., storage conditions along with the use at planting and/or at K. varians (Migula) Stackebrandt et al., Pseudomonas chlo- harvest of registered fungicides is recommended to roraphis (Guignard & Sauvageau) Bergey et al., P. fluores- reduce the disease. Recent studies put forth the possibil- cens Migula, P. putida, Rhodococcus erythropolis (Gray & ity that GRAS compounds and microbial antagonists Thornton) Goodfellow & Alderson, R. globerulus Goodfel- could eventually be integrated into silver scurf control low et al., and Waksman & Henrici strategies. Overall, the successful management of the dis- demonstrated the most potential in controlling silver scurf. ease will undoubtedly depend on more research and In an effort to determine their potential as biological control development as well as a concerted effort between scien- agents, these microorganisms were more closely scrutinized tists and the industry to promote and use an integrated Potato silver scurf management 295

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