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In vitro, in vivo and in situ Evaluation of Fungicides Tested Individually or in Combination for the Control of the Fusarium Dry Rot of Potato



M. Daami-Remadi, F. Ayed , H. Jabnoun-Khiareddine , K. Hibar and M. El Mahjoub
 
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ABSTRACT

Several fungicides are tested individually or in dual combination against four Fusarium species causing potato tuber dry rot in Tunisia. Incorporated into the culture media PDA, the tested fungicides significantly inhibited the mycelial growth of all Fusarium species incubated at 25°C for 6 days; a significant interaction was observed between the both fixed factors (p≤0.05). Applied on potato tubers (tuber immersion for 10 min) prior inoculation, all tested fungicides, combined or not, have significantly reduced by more than 50%, comparatively to the untreated controls, the development of dry rot occasioned by Fusarium sp. after 21 days of incubation at 25-27°C. A significant interaction was observed between the treatments and the Fusarium species (p≤0.05). In natural conditions, tuber treatment by the tested fungicides, prior their definitive storage, has reduced dry rot development by about 50%. A synergistic effect was observed in vitro, in vivo and in situ between the mixed fungicides traduced by a better efficacy, in comparison to their individual effects, showing their compatibility and the promotion of the disease control. These combined fungicides could play a role in an integrated pest management against potato tuber-borne pathogens.

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M. Daami-Remadi, F. Ayed , H. Jabnoun-Khiareddine , K. Hibar and M. El Mahjoub , 2006. In vitro, in vivo and in situ Evaluation of Fungicides Tested Individually or in Combination for the Control of the Fusarium Dry Rot of Potato. International Journal of Agricultural Research, 1: 564-572.

DOI: 10.3923/ijar.2006.564.572

URL: https://scialert.net/abstract/?doi=ijar.2006.564.572

Introduction

In Tunisia, potato tuber dry rot is caused by a complex of Fusarium species which incidence and frequency are depending on production zones. F. solani, F. oxysporum and at a lesser frequency F. sambucinum and F. graminearum are the most isolated from local tubers showing dry rot symptoms (Daami-Remadi and El Mahjoub, 1996, 2004, 2006; Daami-Remadi et al., 2006; Priou and El Mahjoub, 1999; Chérif et al., 2001).

Benzimidazoles and conazoles fungicides were used since 1970 (Leach, 1971; Murdock and Wopd, 1972; Tisdale and Lord, 1973). Benzimidazoles such as benomyl, carbendazim, thiophanate-methyl and thiabendazole are used against Fusarium and Phoma exigua, Helminthosparium solani, Rhizoctonia solani (Leach and Nielsen, 1975; Tivoli et al., 1986; Carnegie et al., 1990, 1998; Bang, 1992; Kawchuck et al., 1994; Mérida and Loria, 1994; Errampalli and Johnston, 2001).

Interaction of local Fusarium population with benzimidazoles and prochloraz depends on Fusarium species and tested doses used in vitro. Thiophanate-methyl and prochloraz inhibited dry rot development on tubers inoculated by F. sambucinum, (Daami-Remadi and El Mahjoub, 1996, 1997). Chérif et al. (2001) showed efficacy of thiophanate-methyl and carbendazim on germination, mycelial growth and sporulation of a local F. roseum var. sambucinum isolate.

In Tunisia, several rots affect potato tubers in the field and in unrefrigerated rustic stores consisting of heaping tubers in a shaded and aerated place and covering them with a thick layer of straw, weeds or potato haulms. Tuber losses noted during this traditional storage, are mainly due to dry rot, leak caused by Pythium aphanidermatum and P. ultimum and pink rot occasioned by Phytophthora erythroseptica that threat a strategic crop in Tunisia (Daami-Remadi and El Mahjoub, 1996; Triki et al., 1996, 2001; Triki and Priou, 1997, Priou and El Mahjoub, 1999; Chérif et al., 2001; Daami-Remadi, 2001 a,b).

Chemical control of local Pythium sp. and Phytophthora sp. isolates was achieved by several fungicides tested in vitro and in vivo such as hymexazol and metalaxyl-mancozeb (Triki and Priou, 1997, Triki et al., 2001, Daami-Remadi, 2001a). In natural conditions, tubers often showed mixed infections of causal agent rot including leak, dry and pink rots. Furthermore, in vitro screening for local Fusarium sp. resistance to some benzimidazoles showed that F. solani, F. oxysoprum f. sp. tuberosi and F. graminearum isolates are susceptible to these fungicides whereas F. sambucinum isolates are resistant (Daami-Remadi and El Mahjoub, 2006a). These chemicals with a single-site mode of action such as benzimidazoles are more likely to lead to development of resistance (Kawchuck et al., 2002). Programs incorporating fungicides with different modes of action to optimise disease control and minimize the risk of resistance development are used in resistance prevention strategies (Beresford, 1994). Consequently, for reducing tuber losses in storage, an integrated control strategy should be followed against all potato post-harvest pathogens and application of mixtures of fungicides may help to slow down the development of resistance. The main purpose of the present study focused on the evaluation of efficacy of several fungicides, with different target effects against Fusarium or Pythiaceae, tested individually or in combination for the chemical control of the causal agents of potato tuber dry rot in vitro, in vivo and in situ.

Materials and Methods

Pathogens
F. solani, F. graminearum, F. sambucinum and F. oxysporum f. sp. tuberosi are isolated on 2002 from tubers of cv. Spunta showing typical symptoms of dry rot. Fusarium sp. are grown at 25°C on PDA for one week. They are stored at -20°C in 20% glycerol solution for long term preservation.

Potato Cultivars
Tubers cv. Spunta, the most cultivated in Tunisia, are used in this current study. They are obtained, on 2003, from the Technical Centre of Potato of Tunisia. For laboratory experiments, tubers are stored in the darkness at 6°C and brought to room temperature three hours before use. In in situ experiments, tubers are stored traditionally.

Fungicides
Tested fungicides are subscribed in the Tunisian phytosanitary index (Anonymous, 2003) and which active ingredient components are showed to be efficient against Pythiaceae and/or Fusarium sp.. Main tested fungicides characteristics are presented in Table 1.

In vitro Activity of Tested Fungicides Against Fusarium sp.
Fungicides are dissolved in sterile distilled water before their incorporation (1%v/v), following chosen doses (Table 1), in PDA in surfusion. A culture media added with a same quantity of ethanol serves as untreated control (dose 0 mg L-1). After solidification, agar discs (of 6 mm in diameter) colonized by the pathogen are placed in the center of the petri dish.

Table 1: Characteristics and doses of fungicides tested against Fusarium spp. causing potato tuber dry rot

Inhibitory activity of fungicides is evaluated on mycelial growth of tested Fusarium sp. estimated via mean colony diameter formed after 6 days of incubation at 25°C. Tested fungicides are applied in culture media individually or in dual combination searching for compatibility between fungicides and synergistic activity against Fusarium sp.

Statistical analysis (ANOVA) are performed following a completely randomised factorial design where treatments (fungicides and untreated control) and Fusarium sp. are both fixed factors. Means are separated using Fisher’s protected LSD test (p≤0.05).

In vivo Activity of Tested Fungicides Against Fusarium sp.
Efficacy of fungicides previously tested in vitro was estimated via development of dry rot on inoculated and treated tubers.

Tubers (cv. Spunta) are superficially disinfected with a solution of 10% sodium hypochlorite, for 5 min and then rinsed abundantly with sterile distilled water. Container and alveolus plaques used for inoculated tubers incubation, are washed before use, dipped for 24 h in sodium hypochlorite solution then rinsed with sterile distilled water.

Fungicides tested individually or in combination, are suspended in water according to tested doses and tuber treatment was realized by dipping tubers, during 10 min, in a fungicidal suspension prior inoculation. Inoculation technique consists of deposing an agar disc (6 mm diameter) colonized by pathogen at occasioned wounds (6 mm diameter and depth). Tuber incubation is realized at 25-27°C for 21 days at high relative humidity. Every elementary treatment is repeated twenty times (ten tubersxtwo wounds).

After incubation period, tubers were cut longitudinally via sites of inoculation. Parameters of dry rot induced (maximal width (w) and depth (d)) are noted. The pathogen penetration within tubers is calculated following formula of Lapwood et al. (1984) where:

Penetration (mm) = (w/2+(d -6))/2

Statistical analysis (ANOVA) are performed following a completely randomised factorial design where treatments (fungicides and untreated control) and Fusarium sp. are both fixed factors. Means are separated using Fisher’s protected LSD test (p≤0.05).

In situ Activity of Tested Fungicides Against Fusarium sp.
Fungicides, tested in vitro and in vivo are also assessed for their in situ efficacy against dry rot development on treated tubers in comparison to controls. One month after harvest, tubers are washed with tap water and then treated by immersion during 10 min into fungicide suspension prepared according to doses presented in Table 1. Untreated control tubers are dipped in water. Treated tubers are then air dried in boxes prior their storage. Elementary treatments are placed on new straw which is also used for their separation and covering. Each elementary treatment consists of 50 kg of tubers and is repeated three times.

Tuber inspection is realized every 15 days during a storage period of two months. Every elementary treatment is observed, tuber by tuber and rotten tubers are counted then eliminated for avoiding contamination of the remaining healthy ones. At the end of the essay, the total rotten tuber number, per every elementary treatment, is calculated.

Statistical analysis (ANOVA) are performed following a completely randomised design where treatments (fungicides and untreated control) represent the fixed factor and the number of rotten tubers is the dependant variable. Means are separated using Fisher’s protected LSD test (p≤0.05).

Results

Effects of Fungicides on Mycelial Growth of Fusarium sp.
The effect of some fungicides, incorporated in the culture media individually or in dual combination, are tested for in vitro development of Fusarium sp. Table 2 showed mycelial growth of the tested Fusarium sp. obtained at realized treatments.

Mean colony diameter, formed after 6 days of incubation at 25°C, varied upon tested Fusarium species and treatments revealing existence of a significant interaction (at p≤0.05) between both fixed factors.

All fungicides applied in vitro, individually or in combination, significantly reduced mycelial growth of all tested Fusarium species in comparison to untreated controls. More than 90% of mycelial growth inhibition was reached in F. graminearum, F. oxysporum and F. solani for treatments BE, BA, R+BE, R+BA, TC+SW, FU+SW and FU+VN. However, the interaction between F. sambucinum and the other tested fungicides was different. In fact, for benzimidazoles fungicides such as benomyl (BE) and carbendazim (BA), pathogen growth was reduced by only 26 to 46%, comparatively to untreated control, in comparison to 90% noted for the other three Fusarium species.

These both fungicides showed a synergistic effect with the treatment R (Metalaxyl+mancozeb) where 85 to 90% of F. sambucinum inhibition was obtained.

The treatment VN (thiabendazole+flutriafol) totally inhibited mycelial growth of F. oxysporum and F. solani and at a lesser degree F. sambucinum and F. graminearum. Table 2 revealed, in vitro synergistic effect of the entire combinations of tested fungicides (R+BE, R+BA, TC+SW, TC+VN, FU+SW, FU+VN) against all Fusarium species; an important inhibitory effect was obtained in comparison to fungicides individually applied.

Effects of Fungicides on Fusarium sp. Aggressivity on Tubers
Table 3 showed mean pathogen penetration in tubers cv. Spunta, individually inoculated by Fusarium species, noted after 21 days of incubation at 25-27°C, depending on different treatments. Obtained results revealed existence of a significant interaction (at p≤0.05) between treatments and Fusarium sp. All tested fungicides applied individually or in dual combination have significantly limited dry rot development on inoculated tubers by more than 50%. Maximum inhibition was reached with the treatments R+BA, TC+SW where development of dry rot regressed by more than 90%, in comparison to inoculated and untreated control in the case of F. graminearum.

Synergistic effects of combined fungicides were also obtained in vivo. In fact, mean penetration, noted for each combined treatment, regressed by more than 50% for all treatments. Inhibition reached 90% for mixed fungicides, in comparison to inoculated untreated control and individually treatments. This is the case of combined treatments R+BA, TC+SW, FU+SW, FU+VN and at a lesser degree, R+BE and TC+VN where dry rot inhibition was estimated by 74 and 82% respectively, in comparison to inoculated untreated control.

Table 2: Effect of some fungicides incorporated into culture media PDA, individually or in dual combination, on mycelial growth of four Fusarium species as measured by the mean colony diameter (cm) noted after 6 days of incubation at 25°C
R: metalaxyl-mancozeb, BE: benomyl, BA: carbendazim, TC: chlorothalonil-propamocarb, FU: cymoxanil-mancozeb, SW: fludioxonil-cyprodinil, VN: thiabendazole–flutriafol, F.gram.: F. graminearum, F. samb.: F. sambucinum, F. oxysp.: F. oxysporum f. sp. tuberosi, LSD (Treatments x Fusarium sp.) = 0.18 cm (p≤0.05)

Table 3: Effect of some fungicides applied, individually or in dual combination, on dry rot development occasioned by Fusarium species as measured by the mean pathogen penetration (mm) into inoculated tubers noted after 21 days of incubation at 25-27°C
R: metalaxyl-mancozeb, BE: benomyl, BA: carbendazim, TC: chlorothalonil-propamocarb, FU: cymoxanil-mancozeb, SW: fludioxonil-cyprodinil, VN: thiabendazole–flutriafol, F.gram.: F. graminearum, F. samb.: F. sambucinum, F. oxysp.: F. oxysporum f. sp. tuberosi, LSD (Treatments x Fusarium sp.) = 2.8 mm (p≤0.05)

Table 4: Effect of tuber (cv. Spunta) treatment by fungicides, applied individually or in combination on dry rot development observed after two months of a traditional storage
R: metalaxyl-mancozeb, BE: benomyl, BA: carbendazim, TC: chlorothalonil-propamocarb, FU: cymoxanil-mancozeb, SW: fludioxonil-cyprodinil, VN: thiabendazole-flutriafol

Effects of Fungicides on Dry Rot Development in Natural Conditions of a Traditional Storage
The effect of fungicides, applied individually or in dual combination, was evaluated on potato tubers cv. Spunta, not previously inoculated.

Analysis of variance revealed that the number of rotten tubers, observed on different lots of 150 kg after two months of a traditional storage, did not significantly vary upon applied treatments. However, Table 4 showed that most tested tuber treatments, applied prior final storage, inhibited development of dry rot in store by more than 50% comparatively to untreated controls.

Synergistic effects are observed for different fungicide combinations and dry rot development during traditional storage regressed by 45 to 59%, in comparison untreated control.

Discussion

Potato tuber dry rot is a post harvest disease with an increasingly importance in Tunisia. The complex of Fusarium species involved in disease development, its aggressivity on tubers and potato plants also as wilting agents (Daami-Remadi and El Mahjoub, 2004) and its survival in fields justified necessity of a tuber treatment in addition to respect of prophylactic methods.

The majority of benzimidazoles fungicides, tested in the current study against Fusarium sp. (responsible of tuber dry rot in Tunisia) showed an interaction with the fusarial complex. In fact, F. oxysporum f. sp. tuberosi, F. solani and F. graminearum are susceptible and are inhibited by more than 90% whereas F. sambucinum seems to react differently. Our results dealing with efficacy of benzimidazoles against development of local Fusarium sp. join other findings (Leach and Nielsen, 1975; Carnegie and Cameron, 1992; Kawchuk et al., 1994; Theron and Millard, 1996; Daami-Remadi and El Mahjoub, 1997; Chérif et al., 2001; Ali et al., 2005). The present study showed interspecific difference within the tunisian potato Fusarium complex as estimated by their susceptibility to these fungicides. This result joins our previous findings in a comparative study of local F. solani var. coeruleum isolates and F. sambucinum, F. graminearum and F. culmorum isolated from imported rotten tubers (Daami-Remadi and El Mahjoub, 1997).This Fungicides x Fusarium sp. interaction was also observed by Carnegie et al. (1998) who found that, in the case of Fusarium solani var. coeruleum, fenpiclonil and combined thiabendazole-imazalil are more active than imazalil alone.

Chérif et al. (2001) found that iprodione, metalaxyl-mancozeb and procymidone were efficient against development of one tested F. sambucinum isolate. Metalaxyl-mancozeb, tested against our Fusarium sp. isolates, significantly reduced their mycelial growth comparatively to untreated controls. Its interaction varied from 25% for F. graminearum to 64% for F. sambucinum; an intermediate result was obtained in the case of F. oxysporum f. sp. tuberosi and F. solani. Its activity against Fusarium sp. is mainly due to mancozeb because metalaxyl in known to be active against Oomycota fungi and it is used against Pythiaceae infecting potato such as Pythium sp. and Phytophthora sp. (Inglis et al., 1999; Powelson and Inglis, 1999; Taylor et al., 2002, 2004; Peters et al., 2001, 2003; Wong and Wilcox, 2001). This same fungicide composed of metalaxyl-mancozeb also showed inhibitory activity against tunisian isolates of Pythium sp. and Phytophthora erythroseptica (Triki and Priou, 1997; Daami-Remadi, 2001b). Large activity of metalaxyl-mancozeb constitutes an alternative for the control of the entire fungal complex of tubers in storage.

This present study showed that several combined treatments such as R+BE (metalaxyl-mancozebe+benomyl), R+BA (metalaxyl-mancozebe+carbendazim), TC+SW (Chlorothalonil-Propamocarbe+Fludioxonil-Cyprodinil), TC+VN (Chlorothalonil-Propamocarbe+Thiabendazole-Flutriafol), FU+SW (Cymoxanil-Mancozeb+Fludioxonil-Cyprodinil), FU+VN (Cymoxanil-Mancozeb+Thiabendazole-Flutriafol) inhibited the mycelial growth of all tested Fusarium species including F. sambucinum which was found to be resistant to three tested benzimidazoles (Daami-Remadi and El Mahjoub, 2006a). The inhibition obtained with mixed fungicides is more important than that achieved with fungicides tested individually. This finding showed presence of a synergistic effect between them, when combined, without affecting their inhibitory activity. These same combined treatments showed efficacy against in vitro development of Pythium sp. and Phytophthora erythroseptica (unpublished data). Powelson and Inglis (1999) showed that dimethomorph+mancozeb, cymoxanil+mancozeb and propamocarb hydrochloride+chlorothalonil, when applied to the seed piece prior inoculation with Phytophthora infestans, significantly increased sprout emergence compared to the inoculated water control.

The majority of fungicide combinations also limited in vivo development of dry rot on artificially inoculated tubers in laboratory experiments and also in natural conditions of a traditional storage. These different combinations could play a role in an integrated control strategy against all tuber fungal agents. Furthermore, although in situ experiments are realized relatively late, about one month after harvest, results noted even at this late application are acceptable. In fact, used tubers are sorted out and washed prior treatment, the fungicide suspensions are renewed after several tuber dipping and the choice of an aired local for tuber storage are the main components participating in optimisation of efficacy of tested fungicide treatments.

Finally, as in Tunisia all potato cultivars are susceptible with variable degrees to Fusarium sp. (Daami-Remadi and El Mahjoub, 1996; Ayed et al., 2006a) and the cultivar Spunta, the almost exclusively used, is also susceptible to the potato post-harvest pathogens (Priou et al., 1997). Furthermore, major traditionally stored tubers are used for late autumn culture, treatment prior storage is indispensable for avoiding emergence and wilt problems. Certain tested fungicides also have an effect in promoting plant development in the field when seeds are treated with fungicides prior plantation (Ayed et al., 2006b).

The present study proposed different individually or combined treatments, tested in their majority for the first time in Tunisia, for chemical control of Fusarium dry rot, reducing incidence of this post-harvest disease and optimising its control. A large range of fungicides, belonging to different chemical families are tested and synergistic effects are obtained with combined treatments in vitro, in vivo and in situ. These chemicals could play an important role in tuber protection in stores and could avoid soil infestation when seeds are previously treated.

Acknowledgments

Authors thank the Technical Potato Centre of Tunisia (CTPT) and the Interprofessional Groupment of Vegetables (GIL) for their financial contribution. Many thanks for Aymen Youssef for his excellent technical assistance.

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