Effect of pH soil and irrigation regimes on management of potato scab

ABSTRACT

Potato scab caused by different species of phytopathogenic Streptomyces is considered one of the main bacterial diseases of economic crop importance worldwide. Several studies are being carried out in order to control the disease, but until now, there is no efficient way to do this. Some management strategies have been investigated including application of chemical and biological products and utilization of resistant cultivars of potato but there are few reports about the impact of pH and irrigation regimes on the disease. The present study aimed to evaluate the effects of these last two factors on the incidence and severity of potato scab caused by S. scabiei, S. acidiscabies, Streptomyces sp., S. caviscabies and S. europaeiscabiei in assays at pH 4.0, 4.5, 5.0, 5.5, 6.5 and 7.5; and irrigation regimes of once a week, alternate days and daily in greenhouse conditions. The experimental design for the pH tests was randomized blocks arranged in a 5x2 factorial scheme, with 5 replications and 3x2 for the irrigation regimes with 5 replications. The pH tests showed significant differences between the treatments and pH 4,0 - 4,5 presented lower incidence and severity of the disease for the most species tested but no significant differences were observed between the irrigation regimes. The soil acidification is considered a classic strategy for management of the disease and the results obtained herein corroborated this hypothesis.

Keywords  Streptomyces ; potential of hydrogen; soil moistur; disease control

INTRODUCTION

Potato (Solanum tuberosum) is the third most consumed food in the world after wheat and rice (DEVAUX et al., 2014; HAVERKORT; STRUIK, 2015). The crop can be affected by bacteria, fungi and viruses causing damage to all parts of the plant, with significant losses in production (FIERS et al., 2012).

Potato scab is an important bacterial disease caused by Streptomyces species that affect mainly the tubers causing necrotic lesions with a corky texture that may be from superficial to more extensive levels with different colors and aspects (DELLEMAN et al., 2005; LORIA, 2001). The disease external symptoms modify the appearance of potato tubers reducing their market value in natura or processed and in seed tubers production (LORIA et al., 1997). The severity and occurrence of symptoms may vary according to the environment, cultivar susceptibility, pathogen virulence and amount of inoculum (KEINATH; LORIA, 1991; LORANG et al., 1995; TÓTH et al., 2001). In Brazil, this disease is widespread throughout the country and has become a limiting factor in potato fields. Besides potato, phytopathogenic Streptomyces cause diseases in diverse root crops like radish, turnip, beet, carrot and sweet potato (GOYER; BEAULIEU, 1997; LABEDA; LYONS, 1992).

The description of potato scab occurred over 100 years ago (LORIA et al., 1997), but there is not yet a fully efficient control for the disease. According to DEES; WANNER (2012), the main control strategies of the disease include increased soil moisture during the tuberization period, soil acidification, crop rotation, biological control, healthy seeds, chemical control and use of resistant cultivars. However, these methods are not always reliable since contradictory results are presented in the literature and are not valid for all species associated to the disease (LAZAROVITS, 2010; PETERS et al., 2004; WATERER, 2002; WILSON et al., 2001).

The practices for altering the pH and soil moisture are considered classic measures regarding to potato scab control (LORIA, 2001). Maintenance or reduction of soil pH to values less than 5.2 generally suppress Streptomyces scabiei, causal agent of common scab (LAMBERT; LORIA, 1989a; LAMBERT et al., 2005). However, other pathogenic species such as Streptomyces acidiscabies (LAMBERT; LORIA, 1989b) and Streptomyces turgidiscabies (MIYAJIMA et al., 1998) tolerate soil pH values lower than 5.2. LACEY; WILSON (2001) found good control results for common scab with pH values lower than 5.0, but WIECHEL; CRUMP (2010) concluded that disease control was not related to the pH.

The increase of soil moisture, mainly in the period of tuberization, is considered a strategy to contain the disease since humid soils can provide a high growth rate of antagonists, greater availability of manganese and reduction the oxygen concentrations, conditions that can affect the growth rate of pathogenic Streptomyces (LEWIS, 1970). According to WILSON et al. (2001), non-irrigated soils in the tuberization period showed a higher degree of disease symptoms; however, LARKIN et al. (2011) reported that irrigation caused an increase in the number of potato scab symptoms.

Among controversies and a few reports on the role of soil pH and irrigation management, this work aimed to evaluate these two parameters in relation to the incidence and severity of potato scab caused by Streptomyces spp.

MATERIAL AND METHODS

Strains and growth conditions

Type strains of S. acidiscabies IBSBF 2110^T (= DSMZ 41668^T), Streptomyces caviscabies (GOYER et al., 1996) IBSBF 2051^T (= CFBP 4545^T), Streptomyces europaeiscabiei (BOUCHEK-MECHICHE et al., 2000) IBSBF 2023^T (= CFBP 4497^T) and two Brazilian strains, S. scabiei IBSBF 2950 and Streptomyces sp. IBSBF 2959, provided by the Phytobacteria Culture Collection of Instituto Biológico (IBSBF), Campinas, São Paulo, Brazil, were used in this study. Streptomyces strains were cultured in YME medium (4 g yeast extract, 10 g malt extract, 4 g dextrose, 18 g agar, per liter), pH 7.0 at 28 °C for 14 days. Then, the inoculum was scraped, added to 250 mL of sterilized Say 2X Solution (40 g sucrose, 2.4 g asparagine, 1.2 g K2HPO4, 20 g yeast extract, per liter), inoculated in sterilized vermiculite and maintained at 28 °C for 14 days. After bacterial growth, the vermiculite was added to the substrate in the proportion 1:12 in 2 L vessels.

pH and irrigation regimes assays

Potato seed minitubers (S. tuberosum L. ‘Agata’) were kindly provided by Solei Papa Tecnologia Company, Vargem Grande do Sul, São Paulo, Brazil. The assays were carried out in the winter (June to August) of 2018 in a greenhouse in the Laboratório de Bacteriologia Vegetal, Instituto Biológico, Campinas, São Paulo, Brazil. The temperatures in this period presented a minimum of 13.1 °C and a maximum of 26.8 °C. In addition, pH tests were also carried out with S. acidiscabies and S. scabiei species in the summer (December to March) with temperatures of 19.2 to 30.9 °C in order to compare the behavior of the pathogens in different temperatures.

Sterilized substrates (Sphagnum) at pH 4.0; 4.5; 5.5; 6.5, and 7.5, kindly provided from Carolina Soil Industrial Company, Santa Cruz do Sul, Rio Grande do Sul, Brazil, were tested. Before testing, the substrates were analyzed and presented the following characteristics: pH 4.0, N-ammonia 3.1 mg·L^–1 (distillation), P 1.0 mg·L^–1 (ICP-OES/Inductively Coupled Plasma Optical Emission Spectrometry), K 0.2 mg·L^–1 (ICP-OES), Ca 7.8 mg·L^–1 (ICP-OES), Mg 3.4 mg·L^–1 (ICP-OES); pH 4.5, N-ammonia 3.5 mg·L^–1 (distillation), P 0.4 mg·L^–1 (ICP-OES), K 0.01 mg·L^–1 (ICP-OES), Ca 2.3 mg·L^–1 (ICP-OES), Mg 1.1 mg·L^–1 (ICP-OES); pH 5.5, N-ammonia 0.3 mg·L^–1 (distillation), P 0.3 mg·L^–1 (ICP-OES), K < 0.01 mg·L^–1 (ICP-OES), Ca 6.0 mg·L^–1 (ICP-OES), Mg 4.9 mg·L^–1 (ICP-OES); pH 6.5, N- ammonia 0.5 mg·L^–1 (distillation), P 0.2 mg·L^–1 (ICP-OES), K < 0.01 mg·L^–1 (ICP-OES), Ca 8.2 mg·L^–1 (ICP-OES), Mg 7.8 mg·L^–1 (ICP-OES); and pH 7.5, N-ammonia 0.7 mg·L^–1 (distillation), P 0.2 mg·L^–1 (ICP-OES), K 0.4 mg·L^–1 (ICP-OES), Ca 10.9 mg·L^–1 (ICP-OES), Mg 4.7 mg·L^–1 (ICP-OES). During the assays the substrate pH measurements were checked using the Pour Through method (LEBUDE; BILDERBACK, 2009).

The experimental design for pH tests was a randomized block with five replicates, in a 5×2 factorial arrangement. According to FAO (2008), soil with pH 5.2-6.4 is considered suitable for potato planting, so this study used the pH 6.5 as positive control and pots non-inoculated pots as negative control. The substrates were moistened with 100 mL of water/vessel on alternate days.

Irrigation assays, using sterilized substrate based on coconut fiber Golden Mix from Amafibra-Fibras e Substratos Agrícolas da Amazônia Company, Holambra, São Paulo, Brazil, consisted of once a week, alternate days and daily were and the experimental design established in a 3 x 2 factorial arrangement, with 5 replications. Until 45 days of planting, the irrigation was done on alternate days with 100 ml of water/vessel for all treatments, after this period the irrigation regimes were initiated with the beginning of the tuberization phase. Substrate without pathogen was used as control and an individual vessel containing one potato plant represented an experimental unit.

Experiments evaluation and statistical analysis

After senescence plants, the tubers were harvested and the disease incidence was calculated according to the diagrammatic scale of JAMES (1971), which evaluated the percentage of area of the tuber covered by lesions (1, 10, 25, or 50%). For the statistical analysis, scores from 1 to 4 were assigned according to the percentage of symptoms, respectively.

The severity of the disease was evaluated according to the scale of WANNER (2007), with a score 0 = without lesions, 1 = superficial lesions, <10 mm in diameter, 2 = superficial lesions> 10 mm in diameter, 3 = raised lesions <10 mm in diameter, 4 = raised lesions > 10 mm in diameter, 5 = deep lesions.

Statistical analysis was achieved using variance analysis (factorial ANOVA, P = 0.05) and Tukey’s test using SISVAR software version 5.3 for Windows (Statistical Analysis Software, UFLA, Lavras, MG, Brazil). The data were transformed by vx +0.5.

RESULTS AND DISCUSSION

pH assays

During the period of the assays, the pH of the substrates was verified and variations of no more than 0.5 were registered. Significant differences between the five values of pH inoculated with S. acidiscabies, S. scabiei, Streptomyces sp. or S. caviscabies were observed. The highest incidence values of potato scab lesions were observed at pH 6.5 and 7.5 for all species tested. Treatments at pH 4.0 showed disease suppression for all strains evaluated when compared with pH 6.5, considered positive control. At pH 4.5, lower incidence values of potato scab lesions were observed for S. scabiei, Streptomyces sp. and S. caviscabieis. Only S. caviscabieis was suppressed at pH 5.5 and S. acidiscabies showed the highest incidence values in all treatments (notes 2.0-2.5), except at pH 4.0 which showed incidence disease note of 1.0 (Fig. 1).

Figure 1
Incidence score of potato scab on different pH values of the substrates attributed to the symptoms caused by different species of Streptomyces. Means with the same lowercase letters in the same Streptomyces species were not significantly different according to Tukey’s test at p = 0.05.

Streptomyces acidiscabies has been related to soils with pH less than 5.2; tolerating pH 3.8, in vitro tests (LAMBERT; LORIA, 1989a). Our results corroborated this data since this bacterial species was the only one that presented highest incidence value of potato scab lesions at pH 4.0.

The behavior of each strain tested was variable. At pH 4.0, S. scabiei showed similar results to the negative control (note 0.5) and at pH 4.5, this bacterial strain presented no significant differences when compared to S. acidiscabies and Streptomyces sp. (IBSBF 2959), but differences were observed when compared to the other treatments. Soils with pH values lower than 5.2 are generally considered suppressive for potato scab caused by S. scabiei (WAKSMAN, 1921; POWELSON et al., 1993).

LACEY and WILSON (2001) observed that 9 of 10 samples tested did not present disease symptoms in soil below pH 5.0, but in our study S. scabiei was able to cause disease symptoms from pH 4.5.

In tests with Streptomyces sp. (IBSBF 2959) strain, the highest incidence score was observed at pH 7.5 (note 2.5) while at pH 4.5, 5.5, and 6.5, the behavior of this strain was similar to S. scabiei, including at pH 4.0 which showed no differences with the negative control.

The use of soils with acidic pH can cause soil nutritional modification, with less distribution of some nutrients and increase of others. Low pH soils can cause an increase in the manganese levels (WATERER, 2002) and, according to THOMPSON and HUBER (2007), manganese increases the resistance of the tuber tissue to pathogen attack and inhibits the vegetative growth of S. scabiei before infection. New tests should be carried out in order to investigate the role of manganese on pathogenic process of Streptomyces strains.

S. caviscabies strain showed no significant differences in the values of disease incidence when compared to the negative control. The disease symptoms were verified in the pH 6.5 and 7.5, indicating that pH values below 6.5 may be a management strategy for soils contaminated with this bacterial species.

Our data demonstrated that pH of the substrate directly interfered in the development of potato scab symptoms in Brazil, under greenhouse conditions, and that pH values above 5.5 can increase the disease incidence. In contrast, WIECHEL and CRUMP (2010) evaluated the effect of soil pH on the disease symptoms in Australia for three years and concluded that the incidence of potato scab is not directly associated to pH factor. Only complementary studies with inoculations under field conditions to confirm if the symptoms caused by Brazilian strains can be suppressed at low pH values.

The evaluation of disease severity, using the scale of WANNER (2007), showed high averages in all pH values for S. scabiei strain, except at pH 4.0, indicating the high virulence degree of this bacterial species. S. caviscabies strain was described associated with deep scab lesions (GOYER et al., 1996), but surprisingly under Brazilian conditions this species showed low severity values and pH values close to 4.0 were considered the better to suppress the disease (Fig. 2).

Figure 2
Severity score of potato scab on different pH values of the substrates attributed to the symptoms caused by different species of Streptomyces. Means with the same lowercase letters in the same Streptomyces species were not significantly different according to Tukey’s test at p = 0.05.

Irrigation management

In the irrigation assays, no significant differences (P <0.05) were observed for S. acidiscabies, S. scabiei and Streptomyces sp. strains (Figure 3). The soil moisture can help in the development of antagonistic microorganisms that can move in soil through water films, colonizing the lenticels of potato tubers faster competing with Streptomyces (LEWIS, 1970). Since that the substrate used in the tests was sterilized, eliminating the presence of microorganisms, this may have been the reason why the moisture did not interfere in the disease, indicating that the presence of antagonistic microorganisms can be an important factor in the interaction pathogen-host-environment. According to LARKIN et al. (2011), the relationship between soil moisture and potato scab disease remains unclear and that this pathosystem is more complex than previously thought.

Figure 3
Score on the incidence of potato scab from plants grown on substrates inoculated with different irrigation regimes. Means with the same lowercase letters were not significantly different according to Tukey’s test at a = 0.05.

In the S. europaescabiei assays, the highest disease incidence was observed with irrigation regime with alternate days (herein considered control of the treatments), while the decrease of incidence was verified with higher (dayly) or lower (once a week) humidity. JOHANSEN et al. (2014) also evaluated this bacterial species for three years on field and variations in the disease incidence between each year of planting were observed. During the first two years, higher disease incidence with dry soil conditions was detected (once a week regime), however in the third year the higher incidence was observed with irrigation on alternate days as verified in our study. These results indicate how complex the Streptomyces pathosystem can be and, therefore, only more studies on irrigation will can contribute for a better understanding this system.

CONCLUSIONS

The disease symptoms caused by different Streptomyces species at pH 4.0 were not verified, demonstrating that this practice may be an interesting strategy for potato scab management, however the soil acidification must be considered since it may lead to decreased tubers production.

The incidence and severity of disease caused by S. caviscabies were suppressed at pH 4.5 – 6.5, indicating that this range of pH can be used as an alternative practice in fields infected with this bacterial species.

The three irrigation regimes did not interfere in the incidence of potato scab for S. acidiscabies, S. scabiei and Streptomyces sp. strains, except for S. europaescabiei, which presented suppression of disease with higher or lower humidity.

ACKNOWLEDGEMENTS

We would like to thank the Coordination for the Improvement of Higher Education Personnel (CAPES/Brazil, Finance code 001) and Associacão Brasileira da Batata (ABBA) for the supply of infected potato tubers and financial support.

• Peer Review History: Double-blind Peer Review.
• AVAILABILITY OF DATA AND MATERIAL
  The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.
• FUNDING
  Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
  https://doi.org/10.13039/501100002322
  Finance code 001
  Part of this study was funded by Associação Brasileira da Batata (ABBA).
• ETHICAL APPROVAL
  Not applicable.

REFERENCES

• BOUCHEK-MECHICHE, K.; GARDAN, L.; NORMAND, P.; JOUAN, B. DNA relatedness among strains of Streptomyces pathogenic to potato in France: description of three new species, S. europaeiscabiei sp. nov. and S. stelliscabiei sp. nov. associated with common scab, and S. reticuliscabiei sp. nov. associated with netted scab. International Journal of Systematic and Evolutionary Microbiology, London, v.50, n.1, p.91-99, 2000. https://doi.org/10.1099/00207713-50-1-91
  » https://doi.org/10.1099/00207713-50-1-91
• DEES, M.W.; WANNER, L.A. In search of better management of potato common scab. Potato Research, Wageningen, v.55, n.3-4, p.249-268, 2012. https://doi.org/10.1007/s11540-012-9206-9
  » https://doi.org/10.1007/s11540-012-9206-9
• DELLEMAN, J.; MULDER, A.; TURKENSTEEN, L.J. Potato diseases: Diseases, pests and defects. Haia: Aardappelwereld & NIVAP, 2005.
• DEVAUX, A.; KROMANN, P.; ORTIZ, O. Potatoes for sustainable global food security. Potato Research, Wageningen, v.57, n.3-4, p.185-199, 2014. https://doi.org/10.1007/s11540-014-9265-1
  » https://doi.org/10.1007/s11540-014-9265-1
• FAO - Food and Agriculture Organization of the United Nations. Why potato? Rome: FAO, 2008. Available from: http://www.fao.org/potato-2008/en/aboutiyp/index.html Access on: 2 July 2020.
  » http://www.fao.org/potato-2008/en/aboutiyp/index.html
• FIERS, M.; EDEL-HERMANN, V.; CHATOT, C.; HINGRAT, Y.L.; ALABOUVETTE, C.; STEINBERG, C. Potato soil-borne diseases A review. Agronomy for Sustainable Development, Reims, v.32, n.1, p.93-132, 2012. https://doi.org/10.1007/s13593-011-0035-z
  » https://doi.org/10.1007/s13593-011-0035-z
• GOYER, C.; FAUCHER, E.; BEAULIEU, C. Streptomyces caviscabies sp. nov., from deep-pitted lesions in potatoes in Québec, Canada. International Journal of Systematic and Evolutionary Microbiology, London, v.46, n.3, p.635-639, 1996. https://doi.org/10.1099/00207713-46-3-635
  » https://doi.org/10.1099/00207713-46-3-635
• GOYER, C.; BEAULIEU, C. Host range of streptomycete strains causing common scab. Plant Disease, Moscow, v.81, n.8, p.901-904, 1997. https://doi.org/10.1094/PDIS.1997.81.8.901
  » https://doi.org/10.1094/PDIS.1997.81.8.901
• HAVERKORT, A.J.; STRUIK, P.C. Yield levels of potato crops: Recent achievements and future prospects. Field Crops Research, Jinan, v.182, p.76-85, 2015. https://doi.org/10.1016/j.fcr.2015.06.002
  » https://doi.org/10.1016/j.fcr.2015.06.002
• JAMES, W.C. An illustrated series of assessment keys for plant diseases, their preparation and usage. Canadian Plant Disease Survey, Saskatoon, v.51, n.2, p.39-65, 1971.
• JOHANSEN, T.J.; DEES, M.W.; HERMANSEN, A. High soil moisture reduces common scab caused by Streptomyces turgidiscabies and Streptomyces europaeiscabiei in potato. Acta Agriculturae Scandinavica, Section B — Soil & Plant Science, v.65, n.3, p.193-198, 2015. https://doi.org/10.1080/09064710.2014.988641
  » https://doi.org/10.1080/09064710.2014.988641
• KEINATH, A.P.; LORIA, R. Effects of inoculum density and cultivar resistance on common scab of potato and population dynamics of Streptomyces scabies American Journal of Potato Research, San Luis Valley, v.68, n.8, p.515-524, 1991. https://doi.org/10.1007/BF02853768
  » https://doi.org/10.1007/BF02853768
• LABEDA, D.P.; LYONS, A.J. DNA relatedness among strains of the sweet potato pathogen Streptomyces ipomoea (Person and Martin 1940) Waksman and Henrici 1948. Applied and Environmental Microbiology, Michigan, v.58, n.2, p.532-535, 1992. https://doi.org/10.1128/aem.58.2.532-535.1992
  » https://doi.org/10.1128/aem.58.2.532-535.1992
• LACEY, M.J.; WILSON, C.R. Relationship of Common Scab Incidence of Potatoes Grown in Tasmanian Ferrosol Soils with pH, Exchangeable Cations and other Chemical Properties of those Soils. Journal of Phytopathology, Germany, v.149, n.11-12, p.679-683, 2001. https://doi.org/10.1046/j.1439-0434.2001.00693.x
  » https://doi.org/10.1046/j.1439-0434.2001.00693.x
• LAMBERT, D.H.; LORIA, R. Streptomyces acidiscabies sp. nov. International Journal of Systematic Bacteriology, London, v.39, n.4, p.393-396, 1989a. https://doi.org/10.1099/00207713-39-4-393
  » https://doi.org/10.1099/00207713-39-4-393
• LAMBERT, D.H.; LORIA, R. Streptomyces scabies sp. nov., nom. rev. International Journal of Systematic Bacteriology, London, v.39, n.4, p.387-392, 1989b. https://doi.org/10.1099/00207713-39-4-387
  » https://doi.org/10.1099/00207713-39-4-387
• LAMBERT, D.H.; POWELSON, M.L.; STEVENSON, W.R. Nutritional interactions influencing diseases of potato. American Journal of Potato Research, San Luis Valley, v.82, n.4, p.309-319, 2005. https://doi.org/10.1007/BF02871961
  » https://doi.org/10.1007/BF02871961
• LARKIN, R.P.; HONEYCUTT, C.W.; GRIFFIN, T.S.; OLANYA, O.M.; HALLORAN, J.M.; HE, Z. Effects of different potato cropping system approaches and water management on soilborne diseases and soil microbial communities. Phytopathology, Lake Alfred, v.101, n.1, p.58-67, 2011. https://doi.org/10.1094/PHYTO-04-10-0100
  » https://doi.org/10.1094/PHYTO-04-10-0100
• LAZAROVITS, G. Managing soilborne disease of potatoes using ecologically based approaches. American Journal of Potato Research, San Luis Valley, v.87, n.5, p.401-411, 2010. https://doi.org/10.1007/s12230-010-9157-0
  » https://doi.org/10.1007/s12230-010-9157-0
• LEBUDE, A.V.; BILDERBACK, T.E. The pour-through extraction procedure: A nutrient management tool for nursery crops. Raleigh: North Carolina Cooperative Extension, 2009.
• LEWIS, B.G. Effects of water potential on the infection of potato tubers by Streptomyces scabies in soil. Annals of Applied Biology, Wellesbourne, v.66, n.1, p.83-88, 1970. https://doi.org/10.1111/j.1744-7348.1970.tb04605.x
  » https://doi.org/10.1111/j.1744-7348.1970.tb04605.x
• LORANG, J.M.; LIU, D.; ANDERSON, N.A.; Schottel, J.L. Identification of Potato Scab Inducing and Suppressive Species of Streptomyces Phytopathology, Lake Alfred, v.85, n.3, p.261-268, 1995. https://doi.org/10.1094/Phyto-85-261
  » https://doi.org/10.1094/Phyto-85-261
• LORIA, R. Diseases caused by bacteria. In: STEVENSON, W.R.; LORIA, R.; FRANC, G.D.; WEINGARTNER, D.P. (eds.). Compendium of potato diseases St Paul: APS, 2001.
• LORIA, R.; BUKHALID, R.A.; FRY, B.A.; KING, R.R. Plant pathogenicity in the genus Streptomyces Plant Disease, Moscow, v.81, n.8, p.836-846, 1997. https://doi.org/10.1094/PDIS.1997.81.8.836
  » https://doi.org/10.1094/PDIS.1997.81.8.836
• MIYAJIMA, K.; TANAKA, F.; TAKEUCHI, T.; KUNINAGA, S. Streptomyces turgidiscabies sp. nov. International Journal of Systematic Bacteriology, London, v.48, n.2, p.495-502, 1998. https://doi.org/10.1099/00207713-48-2-495
  » https://doi.org/10.1099/00207713-48-2-495
• PETERS, R.D.; STURZ, A.V.; CARTER, M.R.; SANDERSON, J.B. Influence of crop rotation and conservation tillage practices on the severity of soil-borne potato diseases in temperate humid agriculture. Canadian Journal of Soil Science, Ottawa, v.84, n.4, p.397-402. https://doi.org/10.4141/S03-060
  » https://doi.org/10.4141/S03-060
• POWELSON, M.L.; JOHNSON, K.B.; ROWE, R.C. Management of diseases caused by soilborne pathogens. In: ROWE, R.C. (ed.). Potato Health Management Saint Paul: APS Press, 1993. p.149-158.
• THOMPSON, I.A.; HUBER, D.M. Manganese and Plant Disease. In: DATNOFF, L.E.; ELMER, W.H.; HUBER, D.M. (eds.). Mineral Nutrition and Plant Disease St. Paul: APS, 2007. chap.10.
• TÓTH, L.; MAEDA, M.; TANAKA, F.; KOBAYASHI, K. Isolation and identification of pathogenic strains of Streptomyces acidiscabies from netted scab lesions of potato tubers in Hokkaido (Japan). Acta Microbiologica et Immunologica Hungarica, Budapest, v.48, n.3-4, p.575-585, 2001. https://doi.org/10.1556/AMicr.48.2001.3-4.21
  » https://doi.org/10.1556/AMicr.48.2001.3-4.21
• WAKSMAN, S.A. The influence of soil reaction upon the growth of Actinomycetes causing potato scab. Soil Science, Baltimore, v.14, n.1, p.61-80, 1921. https://doi.org/10.1097/00010694-192207000-00007
  » https://doi.org/10.1097/00010694-192207000-00007
• WANNER, L.A. A New Strain of Streptomyces Causing Common Scab in Potato. Plant Disease, Moscow, v.91, n.4, p.352-359, 2007. https://doi.org/10.1094/PDIS-91-4-0352
  » https://doi.org/10.1094/PDIS-91-4-0352
• WATERER, D. Impact of high soil pH on potato yields and grade losses to common scab. Canadian Journal of Plant Science, Ottawa, v.82, n.3, p.583-586, 2002. https://doi.org/10.4141/P01-046
  » https://doi.org/10.4141/P01-046
• WIECHEL, T.J.; CRUMP, N.S. Soil nutrition and common scab disease of potato in Australia. In: WORLD CONGRESS OF SOIL SCIENCE, SOIL SOLUTION FOR A CHANGING WORLD, 19., 2010, Brisbane. Proceedings […] Brisbane: International Union of Soil Sciences, 2010. Available from: https://ocp.com.au/wp-content/uploads/2016/11/DPI-Knoxfield-Potato-Field-Trial-ph-plus.pdf Access on: 20 July 2020.
  » https://ocp.com.au/wp-content/uploads/2016/11/DPI-Knoxfield-Potato-Field-Trial-ph-plus.pdf
• WILSON, C.R.; PEMBERTON, B.M.; RANSOM, L.M. The effect of irrigation strategies during tuber initiation on marketable yield and development of common scab disease of potato in Russet Burbank in Tasmania. Potato Research, Wageningen, v.44, n.3, p.243-251, 2001. https://doi.org/10.1007/BF02357902
  » https://doi.org/10.1007/BF02357902

Edited by

• Associate Editor: Silvia Galleti

Publication Dates

• Publication in this collection
  17 Dec 2021
• Date of issue
  2021

History

• Received
  19 Oct 2020
• Accepted
  31 Oct 2021