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Use of limestone and agricultural gypsum in cauliflower crop management and clubroot control in mountain farming

ABSTRACT.

The effects of the dose and application method of limestone - broadcast or in furrow - and of agricultural gypsum on soil fertility, the control of clubroot, and cauliflower development in mountain farming areas were evaluated. Initially, four doses of broadcast limestone (0.0, 1.0, 2.0, and 4.0 Mg ha-1) and two cauliflower cultivars (Sharon and Piracicaba Precoce) were analyzed. A second experiment evaluated limestone (4.0 Mg ha-1) application treatments: broadcast and in furrow, broadcast limestone + gypsum (3.0 + 1.0 Mg ha-1), and broadcast gypsum (1.0 Mg ha-1). Soil fertility was improved, and significant increases were observed in the total and healthy root volume with increasing doses of limestone. With 4.0 Mg ha-1, a 58 and 85% increase in yield was observed in Sharon and Piracicaba, respectively, compared to the control. Treatments with limestone and limestone + gypsum, regardless of the application method, elevated pH (≥ 10%), base saturation (V%) (≥ 37%), and calcium (Ca) contents (≥ 100%), and reduced the levels of aluminum ions (Al3+) (≥ 60%) and clubroot severity (≥ 64%) and favored biomass accumulation (≥ 27%) and yield (≥ 9.2%). The application of limestone in the furrow yielded results similar to the broadcast application.

Keywords:
Brassica oleracea var. botrytis; Plasmodiophora brassicae; liming; slope; application method.

Introduction

The municipality of Nova Friburgo, in the state of Rio de Janeiro, is one of the largest cauliflower (Brassica oleracea var. botrytis) producers in Brazil (IBGE, 2006Instituto Brasileiro de Geografia e Estatística [IBGE]. (2006). Censo agropecuário. Retrieved on Jan. 25, 2018 from 25, 2018 from https://sidra.ibge.gov.br/Tabela/818#resultado
https://sidra.ibge.gov.br/Tabela/818#res...
). Its cultivation in the region is mainly carried out by family farmers in areas with high slopes and acid soils and under intensive management. The local topography and climate, as well as the agricultural practices adopted, make this a model of mountain farming in a tropical region. Additionally, regular and intensive planting of cauliflower for more than 30 years in the region; intensive soil tillage, including plowing and harrowing along the slope; and the use of community machinery and implements have resulted in the widespread dissemination and distribution of clubroot (Bhering, Carmo, Matos, Lima, & Amaral Sobrinho, 2017Bhering, A. S., Carmo, M. G. F., Matos, T. S., Lima, E. S. A., & Amaral Sobrinho, N. M. B. (2017). Soil factors related to the severity of Clubroot in Rio de Janeiro, Brazil. Plant Disease, 101(8), 1345-1353. DOI: 10.1094/PDIS-07-16-1024-SR
https://doi.org/DOI: 10.1094/PDIS-07-16-...
), which has limited the cultivation of the species on some farms. A similar situation has been observed in several other regions of Brazil and the world for Brassica spp. cultivation (Dixon, 2009aDixon, G. R. (2009a). The occurrence and economic impact of Plasmodiophora brassicae and clubroot disease. Journal of Plant Growth Regulation, 28(3), 194-202. DOI: 10.1007/s00344-009-9090-y).

Clubroot is caused by Plasmodiophora brassicae Woronin, a common soil protozoan that is an obligatory parasite specific to Brassicaceae species (Dixon, 2014Dixon, G. E. (2014). Clubroot (Plasmodiophora brassicae Woronin) - an agricultural and biological challenge worldwide. Canadian Journal of Plant Pathology, 36(1), 5-18. DOI: 10.1080/07060661.2013.875487
https://doi.org/DOI: 10.1080/07060661.20...
). In the absence of host plants, P. brassicae survives in the soil for several years in the form of resting spores (Dixon, 2009bDixon, G. R. (2009b). Plasmodiophora brassicae in its environment. Journal of Plant Growth Regulation , 28(3), 212-228. DOI: 10.1007/s00344-009-9098-3
https://doi.org/DOI: 10.1007/s00344-009-...
). The pathogen infects the root system of plants, where it causes the development of galls or tumors from cellular hyperplasia and hypertrophy. Consequently, water and nutrient absorption is reduced, which can lead to underdevelopment, reduced production potential, and even death of the plant (Dixon, 2009aDixon, G. R. (2009a). The occurrence and economic impact of Plasmodiophora brassicae and clubroot disease. Journal of Plant Growth Regulation, 28(3), 194-202. DOI: 10.1007/s00344-009-9090-y). The losses are further increased when a high density of resting spores occur in the soil (> 106 units g-1 of soil) (Narisawa, Shimura, Usuku, Fujuhara, & Hashiba, 2005Narisawa, K., Shimura, M., Usuku, F., Fujuhara, S., & Hashiba, T. (2005). Effects of pathogen density, soil moisture, and soil pH on biological control of clubroot in Chinese cabbage by Heteroconium chaetospira. Plant Disease , 89(3), 285-290. DOI: 10.1094/PD-89-0285
https://doi.org/10.1094/PD-89-0285...
) under favorable environmental conditions. The germination of resting spores, infection, and root colonization are favored by acidic or partially acidic soils (pH(H₂O) < 6.2), humidity, low calcium (Ca) levels, and intermediate temperatures of 20 to 25°C (Dixon, 2009bDixon, G. R. (2009b). Plasmodiophora brassicae in its environment. Journal of Plant Growth Regulation , 28(3), 212-228. DOI: 10.1007/s00344-009-9098-3
https://doi.org/DOI: 10.1007/s00344-009-...
; Donald & Porter, 2009Donald, C., & Porter, I. (2009). Integrated control of clubroot. Journal Plant of Growth Regulation, 28(3), 289-303. DOI: 10.1007/s00344-009-9094-7
https://doi.org/10.1007/s00344-009-9094-...
; Dixon, 2014Dixon, G. E. (2014). Clubroot (Plasmodiophora brassicae Woronin) - an agricultural and biological challenge worldwide. Canadian Journal of Plant Pathology, 36(1), 5-18. DOI: 10.1080/07060661.2013.875487
https://doi.org/DOI: 10.1080/07060661.20...
; Gossen, Deora, Peng, Hwang, & McDonald, 2014Gossen, B. D., Deora, A., Peng, G., Hwang, S. E., & McDonald, M. R. (2014). Effect of environmental parameters on clubroot development and the risk of pathogen spread. Canadian Journal of Plant Pathology , 36(1), 37-48. DOI: 10.1080/07060661.2013.859635
https://doi.org/10.1080/07060661.2013.85...
). The losses caused by the disease can be further increased by aluminum ion (Al3+) phytotoxicity (Bhering et al., 2017Bhering, A. S., Carmo, M. G. F., Matos, T. S., Lima, E. S. A., & Amaral Sobrinho, N. M. B. (2017). Soil factors related to the severity of Clubroot in Rio de Janeiro, Brazil. Plant Disease, 101(8), 1345-1353. DOI: 10.1094/PDIS-07-16-1024-SR
https://doi.org/DOI: 10.1094/PDIS-07-16-...
).

Considering the existing limitations for the chemical and genetic control of the disease (Donald & Porter, 2009Donald, C., & Porter, I. (2009). Integrated control of clubroot. Journal Plant of Growth Regulation, 28(3), 289-303. DOI: 10.1007/s00344-009-9094-7
https://doi.org/10.1007/s00344-009-9094-...
; Gossen et al., 2015Gossen, B. D., Strelkov, S. E., Manolii, V. P., Rennie, D. C., Cao, T., Hwang, S. F., ... McDonald, M. R. (2015). Spread of Plasmodiophora brassicae on canola in Canada, 2003-2014: Old pathogen, new home. Canadian Journal of Plant Pathology , 37(4), 403-413. DOI: 10.1080/07060661.2015.1105871
https://doi.org/10.1080/07060661.2015.11...
), management practices are the most important strategy for reducing the losses caused by the disease. Among these, soil acidity correction is the most important, followed by basic strategies for successful crop and disease management (Dixon, 2009bDixon, G. R. (2009b). Plasmodiophora brassicae in its environment. Journal of Plant Growth Regulation , 28(3), 212-228. DOI: 10.1007/s00344-009-9098-3
https://doi.org/DOI: 10.1007/s00344-009-...
; Donald & Porter, 2009Donald, C., & Porter, I. (2009). Integrated control of clubroot. Journal Plant of Growth Regulation, 28(3), 289-303. DOI: 10.1007/s00344-009-9094-7
https://doi.org/10.1007/s00344-009-9094-...
; Gossen et al., 2014Gossen, B. D., Deora, A., Peng, G., Hwang, S. E., & McDonald, M. R. (2014). Effect of environmental parameters on clubroot development and the risk of pathogen spread. Canadian Journal of Plant Pathology , 36(1), 37-48. DOI: 10.1080/07060661.2013.859635
https://doi.org/10.1080/07060661.2013.85...
; Bhering et al., 2017Bhering, A. S., Carmo, M. G. F., Matos, T. S., Lima, E. S. A., & Amaral Sobrinho, N. M. B. (2017). Soil factors related to the severity of Clubroot in Rio de Janeiro, Brazil. Plant Disease, 101(8), 1345-1353. DOI: 10.1094/PDIS-07-16-1024-SR
https://doi.org/DOI: 10.1094/PDIS-07-16-...
; Santos, Amaral Sobrinho, Costa, Diniz, & Carmo, 2017Santos, C. A.; Amaral Sobrinho, N. M. B., Costa, E. S. P., Diniz, C. S., & Carmo, M. G. F. (2017). Liming and biofungicide for the control of clubroot in cauliflower. Pesquisa Agropecuária Tropical, 47(3), 303-311. DOI: 10.1590/1983-40632016v4746936
https://doi.org/DOI: 10.1590/1983-406320...
). Cauliflower is a demanding crop in terms of phytotechnical, phytosanitary, and soil fertility management [pH(H₂O) = 6.0 to 6.8, V = 80%, and Ca + magnesium (Mg) content ≥ 3.0 cmolc dm-3] (May et al., 2007May, A., Tivelli, S., Vargas, P., Samra, A. G., Sacconi, L. V., & Pinheiro, M. Q. (2007). A cultura da couve-flor. Campinas, SP: Instituto Agronômico. ; Guerra, Leal, & Ferreira, 2013Guerra, J. G. M., Leal, M. A. A., & Ferreira, M. B. C. (2013). Recomendações de adubos, corretivos e de manejo da matéria orgânica para as principais culturas do Estado do Rio de janeiro: Brócolos, couve, couve-flor e repolho. In Freire L. R. (Ed.), Manual de calagem e adubação do Estado do Rio de Janeiro (p. 107-128). Seropédica, RJ: Editora Universidade Rural .) as well as the required environmental conditions, especially temperature and humidity. Cauliflower has also been reported as being intolerant to Al3+, despite the lack of studies on this specific topic (May et al., 2007May, A., Tivelli, S., Vargas, P., Samra, A. G., Sacconi, L. V., & Pinheiro, M. Q. (2007). A cultura da couve-flor. Campinas, SP: Instituto Agronômico. ).

Despite the recognized importance of soil acidity correction for cauliflower nutrition and clubroot control, this strategy is often neglected (Bhering et al., 2017Bhering, A. S., Carmo, M. G. F., Matos, T. S., Lima, E. S. A., & Amaral Sobrinho, N. M. B. (2017). Soil factors related to the severity of Clubroot in Rio de Janeiro, Brazil. Plant Disease, 101(8), 1345-1353. DOI: 10.1094/PDIS-07-16-1024-SR
https://doi.org/DOI: 10.1094/PDIS-07-16-...
), possibly due to lack of knowledge or the practical difficulties experienced in steep areas. The broadcast application of limestone, followed by uniform incorporation, favors the reaction of the soil amendment (Sousa, Miranda, & Oliveira, 2007Sousa, D. M. G., Miranda, L. N., & Oliveira, S. A. (2007). Acidez do solo e sua correção. In R. F. Novais, V. H. Alvarez, N. F. Barros, R. L. F. Fontes, R. B. Cantarutti, & J. C. L. Neves (Eds.), Fertilidade do solo (p. 205-274). Viçosa, MG: Sociedade Brasileira de Ciência do Solo.; Campos et al., 2013Campos, D. V. B., Freire, L. R., Zonta, E., Eira, P. A., Duque, F. F., De-Polli, H., ... Anjos, L. H. C. A. (2013). Adubos e corretivos. In L. R. Freire (Ed.), Manual de calagem e adubação do Estado do Rio de Janeiro (p. 107-128). Seropédica, RJ: Editora Universidade Rural.) and, consequently, the management of the disease (Donald & Porter, 2009Donald, C., & Porter, I. (2009). Integrated control of clubroot. Journal Plant of Growth Regulation, 28(3), 289-303. DOI: 10.1007/s00344-009-9094-7
https://doi.org/10.1007/s00344-009-9094-...
). However, in steeper areas, especially in regions with high precipitation, the traditional form of incorporation - by plowing and harrowing - may favor water erosion. That is, alternative forms of application and the incorporation of amendments compatible with the conditions of tropical mountain farming and able to aid in the management of clubroot need to be investigated and validated.

Limestone, which is composed of Ca and/or magnesium carbonate, is the most used amendment for the neutralization of soil acidity, for the reduction of toxic Al3+ contents, and as a source of Ca2+ and/or Mg2+ for plants (Sousa et al., 2007Sousa, D. M. G., Miranda, L. N., & Oliveira, S. A. (2007). Acidez do solo e sua correção. In R. F. Novais, V. H. Alvarez, N. F. Barros, R. L. F. Fontes, R. B. Cantarutti, & J. C. L. Neves (Eds.), Fertilidade do solo (p. 205-274). Viçosa, MG: Sociedade Brasileira de Ciência do Solo., Campos et al., 2013Campos, D. V. B., Freire, L. R., Zonta, E., Eira, P. A., Duque, F. F., De-Polli, H., ... Anjos, L. H. C. A. (2013). Adubos e corretivos. In L. R. Freire (Ed.), Manual de calagem e adubação do Estado do Rio de Janeiro (p. 107-128). Seropédica, RJ: Editora Universidade Rural.). The efficiency of this technique for soil acidity correction and clubroot control, however, depends on characteristics such as the total relative neutralizing power (TRNP) (Campos et al., 2013Campos, D. V. B., Freire, L. R., Zonta, E., Eira, P. A., Duque, F. F., De-Polli, H., ... Anjos, L. H. C. A. (2013). Adubos e corretivos. In L. R. Freire (Ed.), Manual de calagem e adubação do Estado do Rio de Janeiro (p. 107-128). Seropédica, RJ: Editora Universidade Rural.), neutralizing value, particle size and distribution, soil quantity, moisture and texture, and variations in the period between application and planting (Donald & Porter, 2009Donald, C., & Porter, I. (2009). Integrated control of clubroot. Journal Plant of Growth Regulation, 28(3), 289-303. DOI: 10.1007/s00344-009-9094-7
https://doi.org/10.1007/s00344-009-9094-...
).

Agricultural gypsum (CaSO4.2H2O), in turn, has also been recommended to improve soil chemical conditions for root development (Sousa et al., 2007Sousa, D. M. G., Miranda, L. N., & Oliveira, S. A. (2007). Acidez do solo e sua correção. In R. F. Novais, V. H. Alvarez, N. F. Barros, R. L. F. Fontes, R. B. Cantarutti, & J. C. L. Neves (Eds.), Fertilidade do solo (p. 205-274). Viçosa, MG: Sociedade Brasileira de Ciência do Solo.). As this salt is more water soluble than limestone, under certain conditions, it can mobilize Ca2+ and Al3+ to the subsoil through formation of an ion pair with sulfate (Sousa et al., 2007Sousa, D. M. G., Miranda, L. N., & Oliveira, S. A. (2007). Acidez do solo e sua correção. In R. F. Novais, V. H. Alvarez, N. F. Barros, R. L. F. Fontes, R. B. Cantarutti, & J. C. L. Neves (Eds.), Fertilidade do solo (p. 205-274). Viçosa, MG: Sociedade Brasileira de Ciência do Solo.), where it reduces the toxic effect of Al3+ on the roots and reduces the subsurface Ca2+ deficiency (Lopes & Guilherme, 2007Lopes, A. S., & Guilherme, L. R. G. (2007). Fertilidade do solo e produtividade agrícola. In R. F. Novais, V. H. Alvarez, N. F. Barros, R. L. F. Fontes, R. B. Cantarutti, & J. C. L. Neves (Eds.), Fertilidade do solo (p. 2-64). Viçosa, MG: Sociedade Brasileira de Ciência do solo.). These two effects could favor the growth of roots in deeper soil layers and, consequently, increase the efficiency of water and nutrient use (Sousa et al., 2007Sousa, D. M. G., Miranda, L. N., & Oliveira, S. A. (2007). Acidez do solo e sua correção. In R. F. Novais, V. H. Alvarez, N. F. Barros, R. L. F. Fontes, R. B. Cantarutti, & J. C. L. Neves (Eds.), Fertilidade do solo (p. 205-274). Viçosa, MG: Sociedade Brasileira de Ciência do Solo.) and reduce root losses from the disease and the negative impacts of these losses on production. However, the effect of gypsum on cauliflower and clubroot management likely is more attributable to the supply of Ca2+ than to the pH correction/elevation (Donald & Porter, 2009Donald, C., & Porter, I. (2009). Integrated control of clubroot. Journal Plant of Growth Regulation, 28(3), 289-303. DOI: 10.1007/s00344-009-9094-7
https://doi.org/10.1007/s00344-009-9094-...
).

Therefore, two field experiments were carried out on the cauliflower crop. In the first experiment, the objective was to determine the best limestone dose based on the improvements in the soil conditions, clubroot control, and development of the cauliflower plants. In the second experiment, the objective was to evaluate the efficiency of the application method of limestone - broadcast or in furrow - and the use of agricultural gypsum on soil fertility, disease control, and cauliflower development.

Material and methods

Two experiments were carried out under field conditions in an area of family farms, in the municipality of Nova Friburgo, state of Rio de Janeiro, Brazil (22°19’45”S-22°23’45”S and 42°35’05”W-42°40’10”W). The studied mountain farming areas have been cultivated with cauliflower for more than 30 years and exhibited clubroot occurrence.

Prior to treatment application and soil preparation, composite soil samples (exploratory analysis) were collected from the two study areas for fertility analysis at a depth of 0-20 cm in the first and 0-20 and 20-40 cm in the second. The soil was analyzed according to Donagema, Campos, Calderano, Teixeira, and Viana (2011Donagema, G. K., Campos, D. B., Calderano, S. B., Teixeira, W. G., & Viana, J. M. (2011). Manual de métodos de análise de solo. Rio de Janeiro, RJ: Embrapa Solos.); no physical soil analyses were performed. Weather data for the respective periods were obtained from the Instituto Nacional de Metereologia (INMET, 2017 Instituto Nacional de Meteorologia [INMET]. (2017). Estações automáticas. 2017. Retrieved on Jan. 5, 2017 from 5, 2017 from http://www.inmet.gov.br/portal/index.php?r=estacoes/estacoesAutomaticas
http://www.inmet.gov.br/portal/index.php...
).

First experiment

The first experiment was conducted from September 2014 to March 2015 following the last planting of Brassica spp. in the area one year prior. The soil analysis of the area showed the following values: pH(H₂O) = 5.29, Al = 0.30 cmolc dm-3, hydrogen (H) + Al = 9.65 cmolc dm-3, Ca = 5.45 cmolc dm-3, Mg = 1.20 cmolc dm-3, potassium (K) = 0.34 cmolc dm-3, cation exchange capacity (CEC) = 16.71 cmolc dm-3, C = 2.15%, base saturation (V%) = 42.5%, and phosphorus (P) = 144.5 mg L-1.

Three doses of partially calcined limestone (TRNP 104.5%) (1.0, 2.0, and 4.0 Mg ha-1), the control (no limestone), and two cauliflower cultivars [SharonH (Sakata) and Piracicaba Precoce (TopSeed)] were evaluated. Based on the neutralization curve, the limestone dose required to achieve a pH of 6.5, which been recommended for cauliflower (May et al., 2007May, A., Tivelli, S., Vargas, P., Samra, A. G., Sacconi, L. V., & Pinheiro, M. Q. (2007). A cultura da couve-flor. Campinas, SP: Instituto Agronômico. ) and clubroot management (Dixon, 2009bDixon, G. R. (2009b). Plasmodiophora brassicae in its environment. Journal of Plant Growth Regulation , 28(3), 212-228. DOI: 10.1007/s00344-009-9098-3
https://doi.org/DOI: 10.1007/s00344-009-...
), was determined. To obtain the curve, soil samples from the experimental area (200 g) were incubated with increasing doses of limestone. The pH(H2O) was measured at 48-hour intervals until stabilization was reached 30 days after the start of the incubation. Using the obtained data, the dose was estimated [pH = 5.28 + 0.302 (dose), R2 = 0.96], and the amount of limestone required to reach pH 6.5 was calculated to be 4.0 Mg ha-1. The other doses were obtained by sequentially dividing of this dose.

The respective limestone doses were applied by broadcasting followed by incorporation with a rotary hoe at a depth of 20 cm. After 70 days, the soil samples of the respective plots were collected at 0 - 20 m depth for fertility analysis (Donagema et al., 2011Donagema, G. K., Campos, D. B., Calderano, S. B., Teixeira, W. G., & Viana, J. M. (2011). Manual de métodos de análise de solo. Rio de Janeiro, RJ: Embrapa Solos.) and for counts of the number of P. brassicae spores (Bhering et al., 2017Bhering, A. S., Carmo, M. G. F., Matos, T. S., Lima, E. S. A., & Amaral Sobrinho, N. M. B. (2017). Soil factors related to the severity of Clubroot in Rio de Janeiro, Brazil. Plant Disease, 101(8), 1345-1353. DOI: 10.1094/PDIS-07-16-1024-SR
https://doi.org/DOI: 10.1094/PDIS-07-16-...
). In December, 34-day-old seedlings of the respective cultivars were transplanted into 20 × 20 × 15 cm furrows, spaced 60 × 60 cm apart. The furrows were previously fertilized with ammonium sulfate (35 kg ha-1 of N), single superphosphate (100 kg ha-1 of P2O5), and potassium chloride (40 kg ha-1 of K2O). The amount of nutrients to be applied was defined based on soil fertility analysis and the crop recommendations prescribed in the “Manual de Calagem e Adubação para o Estado do Rio de Janeiro” (Freire et al., 2013Freire, L. R., Campos, D. V. B., Anjos, L. H. C., Zonta, E., Pereira, M.G., Bloise, R. M., ... Eira, P. A. (2013). Análise química de amostras de terra. In L. R. Freire (Ed.), Manual de calagem e adubação do Estado do Rio de Janeiro (p. 107-128). Seropédica, RJ: Editora Universidade Rural .; Guerra et al., 2013Guerra, J. G. M., Leal, M. A. A., & Ferreira, M. B. C. (2013). Recomendações de adubos, corretivos e de manejo da matéria orgânica para as principais culturas do Estado do Rio de janeiro: Brócolos, couve, couve-flor e repolho. In Freire L. R. (Ed.), Manual de calagem e adubação do Estado do Rio de Janeiro (p. 107-128). Seropédica, RJ: Editora Universidade Rural .).

A randomized complete block design was used in a 4 × 2 factorial arrangement, with four replications, totaling 32 plots of 16 m2 and 64 plants.

Then, standard crop management practices for the region, which comprise two weeding rounds, sprinkler irrigation, and three top-dressing fertilizations, were applied. In the first and third fertilizations, at 20 and 60 days after transplanting (DAT), ammonium sulfate (85 kg ha-1 of N) and potassium chloride (75 kg ha-1 of K2O) were applied as top-dressing. In the second fertilization, approximately 120 g of poultry litter were applied at 40 DAT, and the plants were sprayed with boric acid solution (2 g L-1).

Throughout the cycle, until the beginning of the harvest, all dead, underdeveloped, withered, and nonflowering plants were counted, as were the normal plants, which had fully expanded leaves and well-formed inflorescences. From 53 to 86 DAT, the inflorescences were harvested at commercial maturity, i.e., when well developed and with flower buds still attached (May et al., 2007May, A., Tivelli, S., Vargas, P., Samra, A. G., Sacconi, L. V., & Pinheiro, M. Q. (2007). A cultura da couve-flor. Campinas, SP: Instituto Agronômico. ). In each plot, the number of plants with normal or at-commercial-maturity inflorescences (NI) was counted, and ten plants were sampled for analysis. Initially, the shoot was harvested from each plant by cutting it close to the base of the stem. The roots were then harvested with the aid of a spade to maintain maximum integrity and washed in running water.

The leaf (LFW), stem (SFW), inflorescence (IFW), and shoot (ShFW) fresh weights were determined by their sum, and the inflorescence longitudinal diameter (ID) was also calculated. The IFW and NI data per plot were used to estimate the yield (Mg ha-1). Root development (volume and fresh weight) and clubroot severity were also quantified. The clubroot severity was estimated with the aid of a scale composed of seven scores (0%, 8%, 20%, 42%, 68%, 87%, and 95% of roots with galls) (Santos et al., 2017Santos, C. A.; Amaral Sobrinho, N. M. B., Costa, E. S. P., Diniz, C. S., & Carmo, M. G. F. (2017). Liming and biofungicide for the control of clubroot in cauliflower. Pesquisa Agropecuária Tropical, 47(3), 303-311. DOI: 10.1590/1983-40632016v4746936
https://doi.org/DOI: 10.1590/1983-406320...
). The volumes of the healthy roots (HRV) and diseased roots (DRV) were calculated based on the water displacement method, and the total volume (TRV) was calculated by the sum of the HRV and the DRV (Bhering et al., 2017Bhering, A. S., Carmo, M. G. F., Matos, T. S., Lima, E. S. A., & Amaral Sobrinho, N. M. B. (2017). Soil factors related to the severity of Clubroot in Rio de Janeiro, Brazil. Plant Disease, 101(8), 1345-1353. DOI: 10.1094/PDIS-07-16-1024-SR
https://doi.org/DOI: 10.1094/PDIS-07-16-...
). The fresh weights of the healthy roots (HRFW), diseased roots (DRFW), and total roots (TRFW) were also determined. The percentages of the diseased roots were calculated using the root volume and the fresh weight data, and these are expressed as volume (PDRV = DRV.TRV-1.100) and fresh weight (PDRFW = DRFW.TRFW-1.100).

Second experiment

The second experiment was conducted from June to December 2015 following the last planting of Brassica spp. in the area five years prior. The soil analysis of the area showed the following values at a depth of 0 - 20 cm: pH(H₂O) = 4.58, Al = 1.00 cmolc dm-3, H + Al = 9.08 cmolc dm-3, Ca = 1.60 cmolc dm-3, Mg = 1.90 cmolc dm-3, K = 0.82 cmolc dm-3, CEC = 13.47 cmolc dm-3, C = 2.06%, V% = 37.27%, and P = 68.64 mg L-1. The values at a depth of 20 - 40 cm were the following: pH(H₂O) = 4.87, Al = 1.00 cmolc dm-3, H + Al = 10.23 cmolc dm-3, Ca = 1.10 cmolc dm-3, Mg = 2.50 cmolc dm-3, K = 0.73 cmolc dm-3, CEC = 14.63 cmolc dm-3, C = 0.98%, V% = 38.21%, and P = 65.68 mg L-1.

This second experiment was designed based on the results from the first experiment and the difficulty of incorporating large amounts of limestone under the local conditions, i.e., areas with steep slopes. The objective was to test methods of corrective application that are more practical and require less soil movement. We defined 4.0 Mg ha-1 as the maximum amount of product (limestone or limestone + gypsum) to be incorporated. The gypsum was added as a treatment to test its possible effect of improving the chemical conditions in the subsurface soil layer (Sousa et al., 2007Sousa, D. M. G., Miranda, L. N., & Oliveira, S. A. (2007). Acidez do solo e sua correção. In R. F. Novais, V. H. Alvarez, N. F. Barros, R. L. F. Fontes, R. B. Cantarutti, & J. C. L. Neves (Eds.), Fertilidade do solo (p. 205-274). Viçosa, MG: Sociedade Brasileira de Ciência do Solo.) and increasing cauliflower root development that would compensate for root losses due to P. brassicae infection (Bhering et al., 2017Bhering, A. S., Carmo, M. G. F., Matos, T. S., Lima, E. S. A., & Amaral Sobrinho, N. M. B. (2017). Soil factors related to the severity of Clubroot in Rio de Janeiro, Brazil. Plant Disease, 101(8), 1345-1353. DOI: 10.1094/PDIS-07-16-1024-SR
https://doi.org/DOI: 10.1094/PDIS-07-16-...
). The gypsum dose was defined based on the soil characteristics in the subsurface layer (clay, CEC, V% and Al+ 3) and the criteria established by Sousa, Lobato, and Rein (2005Sousa, D. M. G., Lobato, E. & Rein, T. A. (2005). Uso de gesso agrícola nos solos de cerrado (Circular Técnica, 32). Planaltina, DF: Embrapa-Cerrados.).

Five treatments were evaluated, consisting of the combination of two limestone application methods and the use or not of gypsum: 1) limestone applied by broadcast, 4.0 Mg ha-1; 2) limestone applied in furrows, 4.0 Mg ha-1; 3) limestone and gypsum, applied by broadcasting, 3.0 and 1.0 Mg ha-1, respectively; 4) gypsum applied by broadcasting, 1.0 Mg ha-1; and 5) control. Calcined limestone with 104.5% TRNP was used. The limestone and/or gypsum were applied by broadcasting, with the aid of a rotary hoe, at 15-cm depth. In furrows, limestone was applied in a radius of approximately 10 to 15 cm and incorporated to a depth of 15 cm using a hoe.

At 83 days after application of the treatments, composite soil samples were collected, at depths of 0 - 20 cm and 20 - 40 cm, for analysis of the fertility and for a count the number of resting spores of P. brassicae (0 - 20 cm) (Bhering et al., 2017Bhering, A. S., Carmo, M. G. F., Matos, T. S., Lima, E. S. A., & Amaral Sobrinho, N. M. B. (2017). Soil factors related to the severity of Clubroot in Rio de Janeiro, Brazil. Plant Disease, 101(8), 1345-1353. DOI: 10.1094/PDIS-07-16-1024-SR
https://doi.org/DOI: 10.1094/PDIS-07-16-...
). The composite soil samples from each plot were obtained by combining six simple samples. In the in-furrow application treatment, the samples were collected on the edge of the furrows (with a radius of approximately 15 cm).

In September, 90 days after treatment application, 30-day-old seedlings of the BarcelonaH (Seminis) cauliflower cultivar were transplanted spaced 60 × 60 cm apart. At the time of transplanting, the furrows were fertilized as described in the previous experiment.

The standard crop management practices were applied, which consisted of two weeding rounds, sprinkler irrigation and three top-dressing fertilizations at 20, 57, and 85 DAT. At 20 and 85 DAT, fertilization was performed as described in the previous experiment. At 57 DAT, 1.4 Mg ha-1 of organic compound [15% of organic C, 1% of nitrogen (N)] were applied, and the plants were sprayed with boric acid solution (2 g L-1).

A randomized block design with five treatments and four replications was used, totaling 20 plots of 13.5 m2 and 40 plants each. The 12 central plants were used for data collection.

The plants, shoot, and roots were harvested at 100 and 106 DAT, and the evaluations were performed according to the methodology described for the previous experiment. The evaluations determined disease severity (Santos et al., 2017Santos, C. A.; Amaral Sobrinho, N. M. B., Costa, E. S. P., Diniz, C. S., & Carmo, M. G. F. (2017). Liming and biofungicide for the control of clubroot in cauliflower. Pesquisa Agropecuária Tropical, 47(3), 303-311. DOI: 10.1590/1983-40632016v4746936
https://doi.org/DOI: 10.1590/1983-406320...
) and root development by measuring the volume and weight of the healthy and diseased roots [HRV, DRV, TRV, HRFW, DRFW, TRFW, PDRV, PDRFW, and total root dry weight (TRDW)] and IFW and ID. Yield (Mg ha-1) was estimated based on the IFW. In addition, leaf, stem, and inflorescence samples were dried, and the respective dry weights (LDW, SDW, and IDW) and the total plant dry weight (TPDW) were determined by summing the dry weights of the different parts.

Statistical analysis

Data from the first experiment were subjected to analysis of variance (ANOVA) and when significant, linear regression analysis (p < 0.05) as a function of the dose. Data from the second experiment were subjected to ANOVA and, when significant, to Tukey’s test (p < 0.05) for a comparison of the means. SISVAR software was used for the analyses (Ferreira, 2011Ferreira, D. F. (2011). Sisvar: a computer statistical analysis system. Ciência e Agrotecnologia, 35(6), 1039-104. DOI: 10.1590/S1413-70542011000600001
https://doi.org/10.1590/S1413-7054201100...
).

Results and discussion

Effect of limestone doses

Frequent and well-distributed rainfall was recorded in the period between the application of the soil amendment and transplanting (314.6 mm) and during the crop cycle (458.8 mm), with 120 mm falling in the first 10 DAT (INMET, 2017 Instituto Nacional de Meteorologia [INMET]. (2017). Estações automáticas. 2017. Retrieved on Jan. 5, 2017 from 5, 2017 from http://www.inmet.gov.br/portal/index.php?r=estacoes/estacoesAutomaticas
http://www.inmet.gov.br/portal/index.php...
). The average temperature during the crop cycle was 15 to 20°C and was slightly higher (17 to 22°C) during the first 10 DAT (INMET, 2017 Instituto Nacional de Meteorologia [INMET]. (2017). Estações automáticas. 2017. Retrieved on Jan. 5, 2017 from 5, 2017 from http://www.inmet.gov.br/portal/index.php?r=estacoes/estacoesAutomaticas
http://www.inmet.gov.br/portal/index.php...
). These conditions, especially in the first 10 DAT, and the high density of P. brassicae spores-above 108 spores g soil-1-were favorable to clubroot infection and development (Narisawa et al., 2005Narisawa, K., Shimura, M., Usuku, F., Fujuhara, S., & Hashiba, T. (2005). Effects of pathogen density, soil moisture, and soil pH on biological control of clubroot in Chinese cabbage by Heteroconium chaetospira. Plant Disease , 89(3), 285-290. DOI: 10.1094/PD-89-0285
https://doi.org/10.1094/PD-89-0285...
; Gossen et al., 2013Gossen, B. D., Kasinathan, H., Cao, T., Manolii, V. P., Strelkov, S. E., Hwang, S. F., & McDonald, M. R. (2013). Interaction of pH and temperature affect infection and symptom development of Plasmodiophora brassicae in canola. Canadian Journal of Plant Pathology , 35(3), 294-303, 2013. DOI: 10.1080/07060661.2013.804882
https://doi.org/10.1080/07060661.2013.80...
; Gossen et al., 2014Gossen, B. D., Strelkov, S. E., Manolii, V. P., Rennie, D. C., Cao, T., Hwang, S. F., ... McDonald, M. R. (2015). Spread of Plasmodiophora brassicae on canola in Canada, 2003-2014: Old pathogen, new home. Canadian Journal of Plant Pathology , 37(4), 403-413. DOI: 10.1080/07060661.2015.1105871
https://doi.org/10.1080/07060661.2015.11...
). The first symptoms of the disease were observed at approximately 30 DAT-plants withered in the hottest hours of the day and were underdeveloped-in all plots. The diagnosis was confirmed by the observation of root galls.

A significant effect (p < 0.05) of the limestone doses was observed on the Ca, Mg, P, and K contents; on the sum of the bases (SB) and V%; and on the attributes related to soil acidity, namely, the pH, H + Al, and Al3+ content and saturation in the soil. A linear increase was observed for the Ca and Mg contents in the soil with an increasing limestone dose (Ca cmolc dm-3 = 4.08 + 1.22x; R2 = 0.91) and (Mg cmolc dm-3 = -0.10x2 + 0.46x + 0.76; R2 = 0.76). However, even in the control treatment, the Ca + Mg contents were high (4.07 cmolc dm-3) and approached the level recommended for the crop: 3.0 cmolc dm-3 (Guerra et al., 2013Guerra, J. G. M., Leal, M. A. A., & Ferreira, M. B. C. (2013). Recomendações de adubos, corretivos e de manejo da matéria orgânica para as principais culturas do Estado do Rio de janeiro: Brócolos, couve, couve-flor e repolho. In Freire L. R. (Ed.), Manual de calagem e adubação do Estado do Rio de Janeiro (p. 107-128). Seropédica, RJ: Editora Universidade Rural .). With increasing limestone doses, a similar increase occurred in the pH, with a maximum of 6.7 (Figure 1A), and in V%, which reached a maximum value of 68.1% at the dose of 4.0 g. ha-1 (Figure 1B); this value is less than that recommended for the crop, which is 80% (May et al., 2007May, A., Tivelli, S., Vargas, P., Samra, A. G., Sacconi, L. V., & Pinheiro, M. Q. (2007). A cultura da couve-flor. Campinas, SP: Instituto Agronômico. ). Furthermore, a linear reduction of potential acidity (Figure 1C) was also observed. Doses of 2.0 and 4.0 g. ha-1 of limestone resulted in adjustment of the soil pH to values favorable to the cauliflower crop - higher than 6.0 (May et al., 2007May, A., Tivelli, S., Vargas, P., Samra, A. G., Sacconi, L. V., & Pinheiro, M. Q. (2007). A cultura da couve-flor. Campinas, SP: Instituto Agronômico. ) - and unfavorable to clubroot (Figure 1A). The minimum pH recommended in the management of clubroot is 5.7 (Webster & Dixon, 1991Webster, M. A., & Dixon, G. R. (1991). Calcium, pH and inoculum concentration influencing colonization by Plasmodiophora brassicae. Mycological Research, 95(1), 64-73. DOI: 10.1016/S0953-7562(09)81362-2
https://doi.org/10.1016/S0953-7562(09)81...
; Donald & Porter, 2009Donald, C., & Porter, I. (2009). Integrated control of clubroot. Journal Plant of Growth Regulation, 28(3), 289-303. DOI: 10.1007/s00344-009-9094-7
https://doi.org/10.1007/s00344-009-9094-...
; Dixon, 2014Dixon, G. E. (2014). Clubroot (Plasmodiophora brassicae Woronin) - an agricultural and biological challenge worldwide. Canadian Journal of Plant Pathology, 36(1), 5-18. DOI: 10.1080/07060661.2013.875487
https://doi.org/DOI: 10.1080/07060661.20...
; Gossen et al., 2014Gossen, B. D., Deora, A., Peng, G., Hwang, S. E., & McDonald, M. R. (2014). Effect of environmental parameters on clubroot development and the risk of pathogen spread. Canadian Journal of Plant Pathology , 36(1), 37-48. DOI: 10.1080/07060661.2013.859635
https://doi.org/10.1080/07060661.2013.85...
).

The Al3+ content and saturation were significantly reduced from 0.20 cmolc dm-3 to 0.0 cmolc dm-3 and from 5.7% to 0.0%, respectively, with the addition of 1.0 Mg ha-1 of limestone due to the pH values being elevated above 5.5 (Figure 1A), as described by Sousa et al. (2007Sousa, D. M. G., Miranda, L. N., & Oliveira, S. A. (2007). Acidez do solo e sua correção. In R. F. Novais, V. H. Alvarez, N. F. Barros, R. L. F. Fontes, R. B. Cantarutti, & J. C. L. Neves (Eds.), Fertilidade do solo (p. 205-274). Viçosa, MG: Sociedade Brasileira de Ciência do Solo.). The original levels of Al3+ in the experimental area were below 0.3 cmolc dm-3, the amount considered critical for most crops (Freire et al., 2013Freire, L. R., Campos, D. V. B., Anjos, L. H. C., Zonta, E., Pereira, M.G., Bloise, R. M., ... Eira, P. A. (2013). Análise química de amostras de terra. In L. R. Freire (Ed.), Manual de calagem e adubação do Estado do Rio de Janeiro (p. 107-128). Seropédica, RJ: Editora Universidade Rural .), and were neutralized with the addition of the lowest dose of limestone to the soil: 1.0 Mg ha-1. The improvement in the chemical conditions of the soil provided an increase in the availability of P, with a linear increase in assimilable P as a function of the limestone doses (Figure 1D).

Figure 1
Values of pH(H₂O) (A), base saturation (V%) (B), potential acidity (H + Al) (C), and phosphorus content (D) as a function of the limestone doses-partially calcined limestone with TRNP of 104.5%-70 days after application and incorporation into the soil. Nova Friburgo, Rio Janeiro State, Brazil, 2015. * indicates significance (p < 0.05).

The improvement of soil chemical conditions, namely, the elevation of pH, reduction of potential acidity, increases in V% and P availability (Figure 1A, B, C, and D), and the neutralization of Al3+, favored root development with a linear increase observed in TRFW, TRV, and HRV of the roots (Figure 2A and B). However, a significant interaction (p < 0.05) was observed between the limestone dose and cultivar on the TRFW, with a stronger response from Sharon than from Piracicaba Precoce (Figure 2A), and a simple effect of dose and cultivar (p < 0.05) on the volume, with higher mean volume of total and healthy roots in Sharon (79.84 and 74.37 mL, respectively) compared to Piracicaba Precoce (58.38 and 53.93 mL, respectively). However, no significant effect of dose or cultivar was observed on DRV, HRFW, DRFW, and, consequently, the severity of clubroot according to the scale or percentage of diseased root calculated based on the volume (PVRH) or the fresh weight (PMFRH). That is, the effect of limestone doses on the cauliflower production and on disease management is due to the favorable root development and the greater weight and volume of the healthy roots, which could compensate for the loss of active roots due to infection.

Figure 2
Mean values of total fresh root weight (A), total and healthy root volume (B), shoot and inflorescence fresh weight (C), inflorescence longitudinal diameter (D), number of normal plants (E), and estimated yield (F) of cauliflower as a function of doses of partially calcined limestone with TRNP = 104.5% applied to the soil. Nova Friburgo, Rio Janeiro State, Brazil, 2015. *indicates significance (p < 0.05). 1In Figure 2A, the means of each cultivar followed by the same letter at each dose did not differ significantly from each other by Tukey’s test (p < 0.05). In Figure 2B, C, D, and E, the data represent the means of the two cultivars.

A positive relation between the increase in pH and neutralization of Al3+ with root development, with a consequent reduction of losses from clubroot, was observed by Bhering et al. (2017Bhering, A. S., Carmo, M. G. F., Matos, T. S., Lima, E. S. A., & Amaral Sobrinho, N. M. B. (2017). Soil factors related to the severity of Clubroot in Rio de Janeiro, Brazil. Plant Disease, 101(8), 1345-1353. DOI: 10.1094/PDIS-07-16-1024-SR
https://doi.org/DOI: 10.1094/PDIS-07-16-...
) in a survey conducted in approximately 16 cauliflower production areas in Nova Friburgo, Rio de Janeiro State, Brazil. The positive effect of increasing doses of limestone on cauliflower (Figure 2) may also be characterized by an increase in the percentage of normal and apparently healthy plants (fully expanded leaves and inflorescences) recorded at the beginning of the harvest, regardless of the cultivar. Approximately 32.0% of the plants with normal inflorescences were identified in the control treatment, without liming, and 48.5, 47.4, and 53.1% were identified in the treatments with 1.0, 2.0, and 4.0 g ha-1 of limestone, respectively. Most of the dead or underdeveloped plants had galls and an underdeveloped root system (Figure 2E).

The improvement of soil fertility (Figure 1) and root development (Figure 2A and B) with increasing limestone doses significantly favored shoot development and consequently showed a linear increase in IFW and ID (Figure 2C and D) regardless of the cultivar. The Sharon cultivar was characterized by a significantly (p < 0.05) higher accumulation of LFW, SFW, and IFW (1,270.4, 277.6, and 509.2 g, respectively) compared to Piracicaba Precoce (850.9, 151.3, and 469.46 g). The gain in mass and diameter resulted in a gain in quality, as longitudinal diameter is an important attribute in the commercial classification of cauliflower (May et al., 2007May, A., Tivelli, S., Vargas, P., Samra, A. G., Sacconi, L. V., & Pinheiro, M. Q. (2007). A cultura da couve-flor. Campinas, SP: Instituto Agronômico. ). The increases in inflorescence weight and diameter and in the number of plants with normal inflorescences resulted in a linear and significant increase in yield (Figure 2F), with increases of approximately 10.36 to 16.37 Mg ha-1 in Sharon and of 5.19 to 14.81 Mg ha-1 in Piracicaba at a dose of 4.0 Mg ha-1 of limestone compared to the control. These values represent a gain of approximately 58.01 and 85.35% in the cultivars, respectively.

Effect of the application of limestone and the addition of gypsum

A significant effect (p < 0.05) of the treatment was observed on the pH(H₂O), Ca2+, K+ , and Al3+, the potential acidity (H + Al), SB, aluminum saturation (m), and V% at a soil depth of 0 - 20 cm and on the pH(H₂O), Ca2+, Al3+, SB, CEC, aluminum saturation (m), and V% at a depth of 20 - 40 cm (Table 1).

The three treatments with limestone, applied in the furrow, by broadcasting, and by broadcasting combined with gypsum, significantly increased pH(H₂O) from 5.02 to 5.47, 5.66, and 5.40, respectively, in the 0 - 20 cm layer. The dose applied, however, was not enough to reach the ideal pH recommended for cauliflower, which is 6.0 to 6.8 (May et al., 2007May, A., Tivelli, S., Vargas, P., Samra, A. G., Sacconi, L. V., & Pinheiro, M. Q. (2007). A cultura da couve-flor. Campinas, SP: Instituto Agronômico. ) (Table 1). The lower efficiency of the limestone treatment in this trial compared to the first, even using the same dose, was probably due to the lower initial pH value and the meteorological conditions. During the period from the application of limestone in June to the collection of soil samples in September, dry and cold days predominated. In this experiment, only 90 mm of rainfall were recorded during the limestone reaction period, but in the previous experiment, approximately 315 mm of rainfall were recorded from the application of limestone in September until the collection of the soil samples in December. Compared to the control, a significant increase occurred in the V%, from 22.39 to 39.82, 46.80, and 40.69%, and a significant reduction occurred in the Al3+ content from 0.92 cmolc dm-3 of soil to 0.32, 0.12, and 0.36 cmolc dm-3 in the treatments with limestone applied in the furrow, by broadcasting, and by broadcasting combined with gypsum, respectively. The values obtained were below the recommended values for the crop: V = 80% (May et al., 2007; Guerra et al., 2013Guerra, J. G. M., Leal, M. A. A., & Ferreira, M. B. C. (2013). Recomendações de adubos, corretivos e de manejo da matéria orgânica para as principais culturas do Estado do Rio de janeiro: Brócolos, couve, couve-flor e repolho. In Freire L. R. (Ed.), Manual de calagem e adubação do Estado do Rio de Janeiro (p. 107-128). Seropédica, RJ: Editora Universidade Rural .) and Al3+ content < 0.30 cmolc dm-3 (Freire et al., 2013Freire, L. R., Campos, D. V. B., Anjos, L. H. C., Zonta, E., Pereira, M.G., Bloise, R. M., ... Eira, P. A. (2013). Análise química de amostras de terra. In L. R. Freire (Ed.), Manual de calagem e adubação do Estado do Rio de Janeiro (p. 107-128). Seropédica, RJ: Editora Universidade Rural .).

Despite being elevated with the addition of limestone, the pH(H₂O) remained below 5.15 In the 20 - 40 cm layer, with a significant difference only observed between the broadcast limestone application and gypsum treatments. At this depth, the Al3+ content decreased from 1.02 to 0.63, 0.53, and 0.66 in the treatments with limestone applied in the furrow, by broadcasting, and by broadcasting in combination with gypsum, respectively, compared to the control (Table 1). However, these levels remained very high for the crop (Freire et al., 2013Freire, L. R., Campos, D. V. B., Anjos, L. H. C., Zonta, E., Pereira, M.G., Bloise, R. M., ... Eira, P. A. (2013). Análise química de amostras de terra. In L. R. Freire (Ed.), Manual de calagem e adubação do Estado do Rio de Janeiro (p. 107-128). Seropédica, RJ: Editora Universidade Rural .). Gypsum application did not significantly reduce the Al3+ content compared to the control in the soil layers at both depths, and only the broadcast limestone treatment significantly reduced the potential acidity (H + Al) in the 0 - 20-cm layer and the Al3+ content in the 20 - 40-cm layer (Table 1). Although the three limestone treatments significantly increased the Ca2+ content and SB, the original contents aligned with the recommended range for the crop (Guerra et al., 2013Guerra, J. G. M., Leal, M. A. A., & Ferreira, M. B. C. (2013). Recomendações de adubos, corretivos e de manejo da matéria orgânica para as principais culturas do Estado do Rio de janeiro: Brócolos, couve, couve-flor e repolho. In Freire L. R. (Ed.), Manual de calagem e adubação do Estado do Rio de Janeiro (p. 107-128). Seropédica, RJ: Editora Universidade Rural .).

Table 1
Effects of limestone, the application method, and agricultural gypsum on soil fertility at depths of 0 - 20 cm and 20 - 40 cm, evaluated at 90 days after treatment application. Nova Friburgo, Rio Janeiro State, Brazil, 2015.

Applying gypsum alone promoted a slight increase in the Ca2+ content and in V% at a depth of 20 - 40 cm, but the mean values did not differ significantly from the mean values of the control. The application of limestone combined with gypsum significantly increased the CEC in the subsurface layer (20 - 40 cm) (Table 1), probably due to the dissolution of the gypsum and the mobilization of the Ca2+ to the lower soil layers (Sousa et al., 2007Sousa, D. M. G., Miranda, L. N., & Oliveira, S. A. (2007). Acidez do solo e sua correção. In R. F. Novais, V. H. Alvarez, N. F. Barros, R. L. F. Fontes, R. B. Cantarutti, & J. C. L. Neves (Eds.), Fertilidade do solo (p. 205-274). Viçosa, MG: Sociedade Brasileira de Ciência do Solo.). In general, the treatments did not affect the organic matter (OM) and the Mg, P, and K contents, except in the treatments with broadcast limestone, applied alone or in combination with gypsum. Compared to the control, these treatments promoted a reduction in the K content in the 0 - 20-cm layer (Table 1).

Although the treatments did not raise the soil pH to levels considered adequate for the management of clubroot (pHH₂O > 6.2) and crop production (pHH₂O 6.0 to 6.8), they promoted a reduction in the severity of the disease, which was estimated based on the scale and PDRFW and increased the accumulation of TPDW and yield. However, they did not affect the volume and the fresh weight of the healthy, total, and diseased roots or PDRV. The severity of the disease, estimated with aid of the scale, was lower in all treatments compared to the control, being significantly lower in the treatment with broadcast limestone combined with gypsum (0.65%) compared to the control (9.49%). This result is due to the significant reduction in the percentage of diseased root fresh weight observed in the treatments with limestone by broadcasting, by broadcasting combined with gypsum, and with gypsum (Table 2).

Table 2
Effect of limestone and its application method and of the use of gypsum on the severity of clubroot, percentage of diseased root weight fresh (PDRFW), total plant dry weight (TPDW), inflorescence fresh weight (IFW), and estimated yield in Barcelona cauliflower plant cultivars, in an experiment conducted from September to December 2015. Nova Friburgo, Rio Janeiro State, Brazil.

In general, although the conditions were favorable to the disease, with intermediate temperatures of 15°C to 20°C, high precipitation (rainfall > 400 mm), and acidic soil (pHH₂O < 5.7), the clubroot severity was low compared to that recorded in the previous experiment and to reports by Bhering et al. (2017Bhering, A. S., Carmo, M. G. F., Matos, T. S., Lima, E. S. A., & Amaral Sobrinho, N. M. B. (2017). Soil factors related to the severity of Clubroot in Rio de Janeiro, Brazil. Plant Disease, 101(8), 1345-1353. DOI: 10.1094/PDIS-07-16-1024-SR
https://doi.org/DOI: 10.1094/PDIS-07-16-...
) and Santos et al. (2017Santos, C. A.; Amaral Sobrinho, N. M. B., Costa, E. S. P., Diniz, C. S., & Carmo, M. G. F. (2017). Liming and biofungicide for the control of clubroot in cauliflower. Pesquisa Agropecuária Tropical, 47(3), 303-311. DOI: 10.1590/1983-40632016v4746936
https://doi.org/DOI: 10.1590/1983-406320...
). This low severity may have made a comparison of the effects of the treatments on the disease control difficult. The low intensity of the disease is probably due to the lower spore density of P. brassicae in the soil (1.90 × 107 to 2.33 × 107 g-1 soil units) compared to the first experiment (above 108 soil g-1), its low viability due to a long period (more than 5 years) without the cultivation of Brassica spp. in the area, and adverse weather conditions, i.e., the long dry period in the initial phase of the crop cycle. This spore density is considered intermediate (Narisawa et al., 2005Narisawa, K., Shimura, M., Usuku, F., Fujuhara, S., & Hashiba, T. (2005). Effects of pathogen density, soil moisture, and soil pH on biological control of clubroot in Chinese cabbage by Heteroconium chaetospira. Plant Disease , 89(3), 285-290. DOI: 10.1094/PD-89-0285
https://doi.org/10.1094/PD-89-0285...
; Ruaro, Lima Neto, & Motta, 2010Ruaro, L., Lima Neto, V.C., & Motta, A.C.V. (2010). Efeito do pH do solo em diferentes níveis de inóculo no controle de Plasmodiophora brassicae. Summa Phytopathologica, 36(1), 16-20. DOI: 10.1590/S0100-54052010000100002
https://doi.org/10.1590/S0100-5405201000...
) and is related to an intermediate to high probability of the occurrence of clubroot in Chinese cabbage (Brassica rapa var. pekinensis). However, the viability of resting spores of P. brassicae decrease over time without cultivation of Brassica spp., and a minimum interval of 2 years between cultivation of host species is recommended as an important strategy for disease management (Peng et al., 2015Peng, G., Pageau, D., Strelkov, S. E., Gossen, B. D., Hwang, S. F., & Lahlali, R. (2015). A> 2-year crop rotation reduces resting spores of Plasmodiophora brassicae in soil and the impact of clubroot on canola. European Journal of Agronomy, 70, 78-84. DOI: 10.1016/j.eja.2015.07.007
https://doi.org/10.1016/j.eja.2015.07.00...
). The last cultivation of Brassica spp. in the study area occurred approximately five years prior, while the duration was only one year in the first experiment.

In general, however, the mild improvement of the soil chemical conditions, such as the increases in the pH(H₂O), Ca2+, and V%; the decrease in the Al3+ and H + Al (Table 1); and the reduction in the disease severity provided a significant increase in the accumulation of TPDW and IFW and, consequently, the yield (Table 2). The higher accumulation of TPDW, IFW, and yield were obtained in the treatments with limestone applied in the furrow and by broadcasting but were not significantly different from treatments with limestone combined with gypsum and only gypsum (Table 2). These last two treatments, which contained gypsum, did not differ significantly from the control (Table 2). No significant effect was observed for the treatments on the dry weight of the different organs of the plant, only on their sum.

Despite the higher yield in the treatments with limestone applied in the furrow and by broadcasting, 12.24 and 11.86 Mg ha-1, respectively, this result was lower than the highest yield observed in the first experiment (16.37 Mg ha-1). Additionally, the yield was lower than that reported by Morais Junior, Cardoso, Leão, and Peixoto (2012Morais Junior, P. O., Cardoso, A. F., Leão, E. F., & Peixoto, N. (2012). Desempenho de cultivares de couve-flor de verão em Ipameri. Ciência Rural, 42(11), 1923-1928. DOI: 10.1590/S0103-84782012005000085
https://doi.org/10.1590/S0103-8478201200...
) (26 to 34 Mg ha-1) and by Santos et al. (2017Santos, C. A.; Amaral Sobrinho, N. M. B., Costa, E. S. P., Diniz, C. S., & Carmo, M. G. F. (2017). Liming and biofungicide for the control of clubroot in cauliflower. Pesquisa Agropecuária Tropical, 47(3), 303-311. DOI: 10.1590/1983-40632016v4746936
https://doi.org/DOI: 10.1590/1983-406320...
) (11.57 to 16.99 Mg ha-1) and higher than that reported by Torres et al. (2015Torres, J. L. R., Araújo, A. S., Barreto, A. C., Silva Neto, O. F., Silva, V. R., & Vieira, D. M. S. (2015). Desenvolvimento e produtividade de couve-flor e repolho influenciados por tipos de cobertura do solo. Horticultura Brasileira, 33(4), 510-514. DOI: 10.1590/S0102-053620150000400017
https://doi.org/10.1590/S0102-0536201500...
) (5.3 to 8.2 Mg ha-1), all in summer crops and with different cultivars. This low yield is probably due to the adverse climatic conditions along the crop cycle: high but poorly distributed rainfall, totaling 404 mm; with 260 mm concentrated in the last 30 days and accompanied by a rising temperature that peaked at 32°C (INMET, 2017 Instituto Nacional de Meteorologia [INMET]. (2017). Estações automáticas. 2017. Retrieved on Jan. 5, 2017 from 5, 2017 from http://www.inmet.gov.br/portal/index.php?r=estacoes/estacoesAutomaticas
http://www.inmet.gov.br/portal/index.php...
); and with inadequate soil fertility conditions, as discussed above. These conditions affected the commercial quality of the inflorescences, contributing to lower diameter and fresh weight and consequently to a low yield. The period of high rainfall also affected the harvesting and evaluation processes and probably the accuracy of the evaluation of the effect of the treatments on the development of the plants.

Because cauliflower has a low tolerance to Al3+ (May et al., 2007May, A., Tivelli, S., Vargas, P., Samra, A. G., Sacconi, L. V., & Pinheiro, M. Q. (2007). A cultura da couve-flor. Campinas, SP: Instituto Agronômico. ), the high levels of Al3+ in the soil (Table 1) and the consequent chemical impedance to root development (Sousa et al., 2007Sousa, D. M. G., Miranda, L. N., & Oliveira, S. A. (2007). Acidez do solo e sua correção. In R. F. Novais, V. H. Alvarez, N. F. Barros, R. L. F. Fontes, R. B. Cantarutti, & J. C. L. Neves (Eds.), Fertilidade do solo (p. 205-274). Viçosa, MG: Sociedade Brasileira de Ciência do Solo.) also negatively affected the plant development and production. Although no specific studies exist on the effect of the different soil levels of Al3+ on the cauliflower plants, this toxic element negatively affects cauliflower production and potentiates the damages caused by clubroot due to the reduction of the active root system (Bhering et al., 2017Bhering, A. S., Carmo, M. G. F., Matos, T. S., Lima, E. S. A., & Amaral Sobrinho, N. M. B. (2017). Soil factors related to the severity of Clubroot in Rio de Janeiro, Brazil. Plant Disease, 101(8), 1345-1353. DOI: 10.1094/PDIS-07-16-1024-SR
https://doi.org/DOI: 10.1094/PDIS-07-16-...
). In the present experiment, only the treatment with limestone applied by broadcasting satisfactorily reduced the Al3+ contents in the soil surface layer to values below 0.3 cmolc dm-3 (0.12 cmolc dm-3), identified as the critical or high threshold value (Freire et al., 2013Freire, L. R., Campos, D. V. B., Anjos, L. H. C., Zonta, E., Pereira, M.G., Bloise, R. M., ... Eira, P. A. (2013). Análise química de amostras de terra. In L. R. Freire (Ed.), Manual de calagem e adubação do Estado do Rio de Janeiro (p. 107-128). Seropédica, RJ: Editora Universidade Rural .) although treatment with limestone in the furrow yielded a value (0.32 cmolc dm-3) close to that of the threshold. In the 0 - 40 cm layer, the contents of the Al3+ were greater than 0.53 cmolc dm-3, that is, very high (Table 1).

Under the experimental conditions adopted in this study, although the pH value was below that recommended for the crop (May et al., 2007May, A., Tivelli, S., Vargas, P., Samra, A. G., Sacconi, L. V., & Pinheiro, M. Q. (2007). A cultura da couve-flor. Campinas, SP: Instituto Agronômico. ), the application of limestone, even when incorporated only in the planting furrow, led to a reduction in the soil acidity and improvement of its fertility and allowed gains, such as a reduction in the clubroot severity and greater biomass accumulation of the plant and the inflorescences.

In the conditions of the region under study, with a predominance of acidic soils, high levels of toxic Al3+, and the wide distribution of P. brassicae, liming is an essential practice for improved crop performance, since the crop requires high soil fertility (May et al., 2007May, A., Tivelli, S., Vargas, P., Samra, A. G., Sacconi, L. V., & Pinheiro, M. Q. (2007). A cultura da couve-flor. Campinas, SP: Instituto Agronômico. ), as well as for the reduction of losses from clubroot, favored by acid soils (Donald & Porter, 2009Donald, C., & Porter, I. (2009). Integrated control of clubroot. Journal Plant of Growth Regulation, 28(3), 289-303. DOI: 10.1007/s00344-009-9094-7
https://doi.org/10.1007/s00344-009-9094-...
; Dixon, 2009bDixon, G. R. (2009b). Plasmodiophora brassicae in its environment. Journal of Plant Growth Regulation , 28(3), 212-228. DOI: 10.1007/s00344-009-9098-3
https://doi.org/DOI: 10.1007/s00344-009-...
; Gossen et al., 2014Gossen, B. D., Deora, A., Peng, G., Hwang, S. E., & McDonald, M. R. (2014). Effect of environmental parameters on clubroot development and the risk of pathogen spread. Canadian Journal of Plant Pathology , 36(1), 37-48. DOI: 10.1080/07060661.2013.859635
https://doi.org/10.1080/07060661.2013.85...
). However, this is a neglected practice due to the lack of information and difficulties imposed by the climate and terrain as well as the high rainfall and steep slopes (greater than 21%) and altitude (above 1300 m). Under these conditions, the application of limestone using the traditionally recommended method, broadcasting followed by incorporation with disc harrow or rotary hoe, is prohibitive, either due to operational difficulty or because it worsens erosion problems. Due to the operational ease, most of the time, the soil preparation and the planting furrows follow the direction of the slope. The methods of acidity correction most compatible with this terrain, climate, and management characteristics need to be tested. In this way, the application in furrows and adequate incorporation can represent a viable alternative. However, adjustments such as the use of amendments with greater reactivity in the soil, such as quicklime or hydrated lime (Sousa et al., 2007Sousa, D. M. G., Miranda, L. N., & Oliveira, S. A. (2007). Acidez do solo e sua correção. In R. F. Novais, V. H. Alvarez, N. F. Barros, R. L. F. Fontes, R. B. Cantarutti, & J. C. L. Neves (Eds.), Fertilidade do solo (p. 205-274). Viçosa, MG: Sociedade Brasileira de Ciência do Solo.), and better dose and uniformity in the incorporation in the furrows should be considered. In addition, the reaction period of the amendments to the soil is important to obtain satisfactory results (Sousa et al., 2007Sousa, D. M. G., Miranda, L. N., & Oliveira, S. A. (2007). Acidez do solo e sua correção. In R. F. Novais, V. H. Alvarez, N. F. Barros, R. L. F. Fontes, R. B. Cantarutti, & J. C. L. Neves (Eds.), Fertilidade do solo (p. 205-274). Viçosa, MG: Sociedade Brasileira de Ciência do Solo.).

Conclusion

Under the experimental conditions, liming, particularly a dose of 4.0 Mg ha-1, provided improvements in the soil chemical conditions for the crop and reduced the occurrence of clubroot.

Correction of the soil acidity favors cauliflower plant and root growth and reduces root loss due to P. brassicae infection.

Different cultivars may respond differently to soil acidity correction.

Both cultivars responded positively to the application of limestone, but Sharon proved to be more productive and more tolerant of acidity.

The application of limestone, whether by broadcasting or in furrow, provides better soil chemical conditions as well as higher yield and biomass accumulation in the plants.

The application of limestone in the furrow, followed by incorporation with a hoe, can be recommended for the cauliflower crop in steep areas that do not support soil tillage.

Acknowledgements

The authors are grateful to the Universidade Federal Rural do Rio de Janeiro (Federal Rural University of Rio de Janeiro; UFRRJ), the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Capes), the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), and the Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ) for funding and supporting this study

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Publication Dates

  • Publication in this collection
    11 May 2020
  • Date of issue
    2020

History

  • Received
    20 Apr 2018
  • Accepted
    02 Oct 2018
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