Broccoli fertilization with composted poultry litter and its impact on clubroot developmentABSTRACT:
Clubroot, caused by Plasmodiophora brassicae, causes significant yield losses in broccoli production. Although, these losses are strongly influenced by soil chemical and physical properties, the effects of organic fertilization remain unclear. This study evaluated the effects of composted poultry litter (CPL) applied at different times before transplanting on clubroot severity, broccoli development, and soil chemical attributes. Two greenhouse experiments were conducted using the ‘Coliseu’ cultivar. Three CPL application timings (175 g plant-1 applied 14, 7, and 0 days before transplanting; -14, -7, and 0 DAT) were compared with a mineral NPK control, under both inoculated and non-inoculated conditions (6.25 x 103 spores cm-3 soil). In the absence of clubroot, CPL application enhanced the development and yield of broccoli inflorescences, regardless of application timing. However, in the presence of the pathogen, CPL favored disease progression, resulting in reduced healthy root biomass and significant decreases in shoot and inflorescence dry mass, irrespective of timing. Although, CPL improved broccoli growth and yield in pathogen-free soils, this benefit was eliminated in soils infested with P. brassicae due to increased disease severity.
Key words:
Brassica oleracea var. italica;
Plasmodiophora brassicae
; organic compost; application time.
RESUMO:
A hérnia das crucíferas, causada por Plasmodiophora brassicae, acarreta grandes perdas na produção de brócolis. Essas perdas são afetadas pelas características químicas e físicas do solo, mas há informações controversas quanto aos efeitos da adubação orgânica. Neste sentido, este estudo tem como objetivo avaliar o efeito da época de aplicação de cama de aviário compostada por 60 dias (CPL) sobre a intensidade da hérnia das crucíferas, o desenvolvimento do brócolis e atributos químicos do solo associados ao manejo de adubação. Para isso, foi realizado dois ensaios em casa de vegetação, utilizando-se a cultivar Coliseu e três épocas de aplicação de 175 g planta-1 de CPL: aos 14 e 7 dias antes e no dia do transplante das mudas (-14, -7 e 0 DAT), além de um tratamento testemunha com NPK mineral; com inoculação com 6,25 x 103 esporos cm-3 de solo e testemunha não inoculada. Os resultados das avaliações mostram que na ausência de hérnia das crucíferas, a adubação com CPL, independente da data de aplicação, favoreceu o desenvolvimento e produção de inflorescências de brócolis. Porém, na presença do patógeno, a adubação com CPL favoreceu o desenvolvimento da doença, com redução de raízes sadias e perdas no acúmulo de massa seca na parte aérea e nas inflorescências, independentemente da época de aplicação. Portanto, a adubação com CPL favoreceu o desenvolvimento e produção de brócolis americano, mas esse efeito positivo foi anulado em solos contaminados com o P. brassicae por favorecer o desenvolvimento da doença.
Palavras-chave:
Brassica oleracea var. italica;
Plasmodiophora brassicae
; composto orgânico; época de aplicação.
INTRODUCTION
The expansion of broccoli (Brassica oleracea var. italica) cultivation in the Southern and Southeastern regions of Brazil has accelerated in response to increasing market demand. In the Mountain Region of Rio de Janeiro state (RJ), production gains have resulted from both the expansion of cultivated areas and increased yields, as well as the extended growing season enabled by the availability of earlier and heat-tolerant cultivars. This intensification, combined with limitations in crop management, has contributed to greater losses caused by pests and diseases (SANTOS et al., 2023).
Among the diseases favored by intensified brassica cultivation, clubroot, caused by Plasmodiophora brassicae Woronin (DIXON, 2009; BHERING et al., 2017; SANTOS et al., 2022), is particularly important. This obligatory parasite can survive in soil for long periods as resting spores (DIXON, 2009). Infection begins when spores germinate in response to abiotic and biotic changes in the rhizosphere induced by brassica root exudates (WANG et al., 2023). The pathogen penetrates root hairs and epidermal cells; subsequently, colonizing the root cortex and inducing gall formation (LIU et al., 2020). As a result, the number of functional roots declines, reducing water and nutrient uptake, which leads to temporary wilting, stunted growth, and lower yields (BHERING et al., 2017).
Broccoli cultivation requires mild temperatures and fertile soils with pH between 6.5 and 7.0, base saturation of approximately 80%, and adequate water availability throughout the crop cycle (NICK & BORÉM, 2022). These conditions, along with soil microbial activity, can be enhanced by increasing soil organic matter or applying organic amendments (BONANOMI et al., 2018; HOFFLAND et al., 2020). However, the effects of organic fertilization depend on the type, amount, timing, and characteristics of the material applied (BONANOMI et al., 2018). In the Mountain Region of RJ, organic fertilization is commonly performed using high doses of composted poultry litter (CPL), a by-product of poultry production (SANTOS et al., 2022; SANTOS et al., 2023). CPL is typically applied at planting and as topdressing, often in fresh, non-composted form.
Despite reports that organic matter addition may enhance disease suppression (BONANOMI et al., 2018), few studies have examined its effects on clubroot. Interactions among P. brassicae, Brassica spp., and tropical environmental conditions, as well as effective management strategies under these conditions, remain limited. Previous studies conducted in the Mountain Region of RJ have indicated a direct relationship between heavy CPL fertilization and clubroot-related losses in cauliflower (BHERING et al., 2017; SANTOS et al., 2023). These adverse effects have been attributed to soil acidification associated with the application of high doses of non-composted poultry litter, either at planting and/or as topdressing, contradicting recommendations that organic fertilizers be applied two to four weeks before seedling transplanting (BONANOMI et al., 2018; NICK & BORÉM, 2022).
Given the need to better understand potential interactions between CPL fertilization practices and clubroot development in brassicas, this study evaluated the effects of composted poultry litter application timing on broccoli growth, clubroot severity, and soil chemical attributes.
MATERIALS AND METHODS
Two concurrent greenhouse experiments were conducted at the Universidade Federal Rural do Rio de Janeiro (UFRRJ), Seropédica, RJ, Brazil, under different soil and environmental conditions. In both experiments, broccoli plants of the cultivar ‘Coliseu’ (Feltrin) and resting spores of Plasmodiophora brassicae were used. These spores were obtained from galls of infected plants preserved by freezing (SANTOS et al., 2018). The galls were collected from broccoli fields in the Mountain Region of Rio de Janeiro State. The isolates used in this study are registered in the SisGen database under code A76EBFC.
Poultry litter collection and composting
Poultry litter was collected from a broiler chicken farm in Rio de Janeiro state in 2022 and composted afterward following the methodology described by LIMA et al. (2022). Piles approximately 1.0 m high were formed on plastic sheeting, turned weekly, and watered to maintain moisture at approximately 60%. After 60 days of composting, samples were collected, sieved, homogenized, and chemically characterized according to TEIXEIRA et al. (2017). The following properties were determined: pH = 7.50; electrical conductivity (EC) = 12.51 dS m-1; C/N ratio = 8.83; C = 109.50 g kg-1; N = 12.40 g kg-1; Ca = 12.35 g kg-1; Mg = 3.00 g kg-1; P2O5 = 8.65 g kg-1; K2O = 12.70 g kg-1; Fe = 5637.50 mg kg-1; Cu = 80.00 mg kg-1; Zn = 204.50 mg kg-1; Mn = 275.00 mg kg-1.
Greenhouse experiments: evaluation of compost application timing
Two simultaneous experiments were conducted from July to September 2022 in Seropédica, RJ, in two climate-controlled greenhouses (Van der Hoeven®) with distinct soils, designated as Experiment ES (Department of Soils) and Experiment EH (Horticulture Sector). In Experiment ES, temperatures ranged from 27 ± 5 ºC with lower light intensity (217-1190 μmol m-2 s-1 on sunny days and 82-406 μmol m-2 s-1 on cloudy days). The soil presented pH 5.40, 2.06% organic matter, and Ca = 2.99 cmolcdm-3. In Experiment EH, temperatures ranged from 25 ± 5 ºC with higher light intensity (266-1503 μmol m-2 s-1 on sunny days and 174-461 μmol m-2 s-1 on cloudy days). The soil presented pH 5.10, 1.34% organic matter, and Ca = 2.32 cmolc dm-3. Additional soil attributes are provided in Supplementary material 1.
Eight-liter pots were used, and the same treatments were applied in both experiments. Each pot received CPL equivalent to 175 g on a dry matter basis (4,860 kg ha-1 and 2.17 g N plant-1), and the material was homogenized using a concrete mixer. The four fertilization treatments consisted of CPL applied at 14 or 7 days before transplanting (-14 and -7 DAT), on the day of transplanting (0 DAT), and a control treatment receiving mineral NPK fertilization (4.82 g urea, 20.72 g single superphosphate, and 9.09 g KCl per pot). The mineral fertilizer was applied on the day of transplanting, with application rates calculated based on the chemical composition of the CPL to equalize the N, P, and K inputs across treatments. To adjust soil P levels for crop requirements, single superphosphate was applied to the CPL treatments at 14.21 g pot-1 in ES and 11.37 g pot-1 in EH (FREIRE et al., 2013). Soil samples from each treatment, collected prior to chemical fertilizer application and transplanting, were analyzed according to TEIXEIRA et al. (2017) (Supplementary material 1).
Thirty-day-old seedlings with three to four true leaves were transplanted into the pots. Immediately after transplanting, half of the pots in each experiment were inoculated with 50 mL of a suspension containing 106 resting spores mL-1, resulting in approximately 6.25 × 10³ resting spores of P. brassicae cm-3 soil (estimated according to MURAKAMI et al., 2001). The inoculum was prepared by macerating 5.0 g of galls in 200 mL of autoclaved distilled water, filtering through muslin cloth, and centrifuging at 2000 rpm for 10 min. The pellet was resuspended and homogenized in autoclaved distilled water, and the spore concentration was determined using counts in a Neubauer chamber under an optical microscope (40× objective).
Both experiments followed a randomized complete block design in a 4 × 2 factorial arrangement (four fertilization types × inoculation with or without the pathogen), with four replicates in ES and six in EH.
Plants were irrigated each day, with equal water volumes applied to all pots. At 30 and 45 days after transplanting (DAT), all plants received top-dressing applications of 5 g plant-1 of a 20-20 NK mineral fertilizer (1 g N and 1 g K2O) and foliar sprays of boric acid (1.0 g L-1) and ammonium molybdate (0.5 g L-1).
At the end of the crop cycle, shoots and roots were harvested and evaluated. Shoot parameters included fresh inflorescence mass (FIM), dry inflorescence mass (DIM), inflorescence diameter (ID), number of leaves (NL), leaf fresh mass (LFM), leaf dry mass (LDM); stem fresh mass (SFM), stem dry mass (SDM), and total shoot dry mass (TSDM), calculated as the sum of DIM, LDM, and SDM (BHERING et al., 2017). Cycle duration (CD) was recorded from transplanting to inflorescence maturity and harvest, and DIM accumulation efficiency was calculated as DIM/CD. Roots were carefully removed, washed, and assessed for disease severity, (SEV) which was estimated using a visual rating scale (0%, 8%, 20%, 42%, 68%, 87%, and 95% of galled roots) (SANTOS et al., 2017). Roots were then separated into galled and healthy fractions, and healthy root volume (HRV) and gall volume (GV) were determined by water displacement in a graduated cylinder. Healthy root fresh mass (HRFM) and gall fresh mass (GFM) were also measured. Total root fresh mass (TRFM) and total root volume (TRV) were calculated as the sums of HRFM + GFM and HRV + GV, respectively (BHERING et al., 2017). Percentages of galled roots were expressed as volume (PGRV) and fresh mass (PGFM).
Data analysis
Data were subjected to analysis of variance followed by Tukey’s test (P < 0.05), after confirming homogeneity of variances (Bartlett’s test) and normality of residuals (Shapiro-Wilk test), using R statistical software (R Core Team, version 4.1).
RESULTS AND DISCUSSION
In both experimental soils, the initial Al3+ content, which can be toxic to plants, was close to or below the critical threshold for broccoli cultivation (< 0.3 cmolcdm-3). Other chemical attributes were below the recommended levels but remained higher in the soil of Experiment ES than in Experiment EH, with pH values of 5.40 and 5.10, base saturation (V%) of 70 and 60%, and organic matter (OM) contents of 2.06 and 1.34 g dm-3, respectively. These values are consistent with those typically reported in brassica cultivation areas (BHERING et al., 2017). In both soils, CPL application increased pH, V%, cation exchange capacity (CEC), OM, total carbon (C), and the macronutrients N, P, K, Ca, Mg, and S, with greater improvements observed in the soil of Experiment ES. The largest increases because of CPL application were, in order, for K and P, whereas N, Ca, and Mg showed smaller increases. Among the micronutrients, the largest increase was observed for Zn, in addition to the input of B. K and P concentrations were within the range recommended for the crop (FREIRE et al., 2013). Although, numerical variation in K, N, P, and pH was observed among CPL application timings, P and K levels remained within the same fertility class recommended by FREIRE et al. (2013).
Significant differences were observed between the two experiments in plant responses to pathogen inoculation and fertilization treatments. In both experiments, inoculation withP. brassicae significantly affected plant development (P ≤ 0.05), influencing both root and shoot growth. Clubroot incidence reached 100% in both experiments, but disease severity (SEV) and the percentage of galled roots by mass (PGRM) and volume (PGRV) were greater in Experiment ES (SEV = 95%; PGRM = 95-99%; PGRV = 93-99%) (Supplementary material 2) than in Experiment EH (SEV = 57-95%; PGRM = 54-98%; PGRV = 53-99%) (Supplementary material 3). These differences are likely associated with soil fertility and environmental conditions. Experiment ES had higher pH and OM levels than EH, and greenhouse conditions differed across experiments, with higher temperatures and lower light intensity recorded in ES. Moderate temperatures favor broccoli growth (NICK & BORÉM, 2022), whereas higher temperatures promote pathogen development (DIXON, 2009). However, information on the influence of light intensity on clubroot development remains limited. Soil acidity is widely recognized as a key factor associated with clubroot incidence (DIXON, 2009; SANTOS et al., 2023). In the present study, disease severity was greater in Experiment ES (pH 5.4-6.0) than in EH (pH 5.1-5.7). These pH values may be unfavorable for optimal crop growth (NICK & BORÉM, 2022) while also remaining insufficiently high to suppress spore germination and root infection (STRUCK et al., 2022). Thus, differences in temperature, light intensity, and soil chemical conditions between the two experiments likely influenced plant growth, pathogen activity, and disease progression.
A significant inoculation × fertilization interaction was detected for clubroot severity and root development, and consequently, overall plant growth, only in Experiment EH, where disease severity was lower. In this experiment, inoculated plants fertilized with CPL showed significant reductions in healthy root fresh mass (HRFM) and healthy root volume (HRV) compared with non-inoculated plants, whereas no significant differences were observed under mineral NPK fertilization (Supplementary material 3, Figure 1A). Under clubroot infection, plants fertilized with CPL, regardless of application timing, exhibited greater disease severity (SEV > 90%) and markedly reduced healthy root development (HRFM < 10.0 g; HRV < 9.50 mL) compared with plants fertilized with mineral NPK (SEV = 57%; HRFM = 31.6 g; HRV = 30.5 mL). Correspondingly, the proportion of galled roots by mass and volume was substantially higher under CPL (PGRM and PGRV > 94.0%) than under mineral NPK fertilization (≈53.0%) (Supplementary material 3). These results support the findings and hypotheses of BHERING et al. (2017), which suggested that CPL fertilization may favor clubroot development. However, in the absence of disease, CPL fertilization significantly increased healthy root mass and volume (Figure 1A; Supplementary material 3) as well as shoot growth and broccoli yield (Figure 1) compared with mineral NPK fertilization. This beneficial effect may be associated with increased Ca and Mg availability, higher soil pH and V%, greater micronutrient supply, higher OM content, and improved soil physical conditioning (SANTOS et al., 2023).
Effects of the interaction between fertilization treatments and pathogen inoculation on broccoli growth and yield variables. Composted poultry litter was applied 14 or 7 days before transplanting or at transplanting (-14, -7, and 0 DAT) and compared with mineral NPK fertilization under inoculated (6.25 × 103 resting spores of Plasmodiophora brassicae cm-3 soil) and non-inoculated conditions. The evaluated variables were healthy root volume (mL), shoot dry mass (g), leaf dry mass (g), inflorescence dry mass (g), inflorescence fresh mass (g), inflorescence diameter (cm), crop cycle duration (days), and dry mass accumulation rate (DM/Day ratio) (g day-1), in broccoli (cv. ‘Coliseu’) grown in a greenhouse at the Horticulture Sector (EH), Universidade Federal Rural do Rio de Janeiro (UFRRJ) Brazil, in 2022. *Means followed by the same letter (uppercase for application timing and lowercase for inoculation) do not differ according to Tukey’s test (P < 0.05).
The greater clubroot severity observed under CPL fertilization, compared with mineral NPK, significantly reduced healthy root development, which subsequently impaired shoot dry mass (SDM), leaf dry mass (LDM) (Figure 1B and Figure 1C) and inflorescence production, including fresh mass (FIM), dry mass (DIM), and diameter (ID) (Figure 1D, 1E and 1F). Conversely, under mineral NPK fertilization, clubroot infection did not significantly affect healthy root development (HRFM and HRV), shoot growth (TSDM and LDM), or inflorescence traits (DIM, FIM, and ID) (Figure 1A, 1B, 1C, 1D, 1E and 1F). The timing of CPL application in inoculated plants did not influence disease severity (SEV, PGRM, and PGRV) or healthy root development (HRV), with statistically similar values observed across the three application timings (Supplementary material 3; Figure 1A). Likewise, in non-inoculated control plants, CPL application timing had no significant effect on root development (HRV and HRFM), shoot growth (TSDM and LDM), or inflorescence traits (DIM, FIM, and ID) (Supplementary material 3; Figure 1). However, CPL fertilization promoted earlier harvests and improved inflorescence production efficiency, expressed as DIM accumulation rate (g day-1), compared with mineral NPK fertilization; although, this effect was observed only in non-inoculated control plants (Figure 1G and Figure 1H).
The high clubroot severity observed in Experiment ES limited a detailed assessment of fertilization effects on disease suppression. In this experiment, HRFM in inoculated plants declined from 53.9 g to 6.1 g compared with the control, impairing water and nutrient uptake and consequently restricting overall plant development. Reductions of 16.9% in NL, 28.7% and 29.9% in LFM and LDM, respectively, and 36.4% in TSDM were recorded. In addition, inflorescence production declined markedly, with decreases of 51.3% and 53.3% in FIM and DIM; respectively, relative to non-inoculated plants (Supplementary material 2). Under these conditions; although, fertilization did not influence clubroot severity or root development, differences emerged in variables related to crop cycle duration and dry mass accumulation (Figure 2A-2D). Mineral NPK fertilization prolonged the crop cycle and increased LDM accumulation relative to CPL application (Figure 2A and Figure 2B). Conversely, CPL applied at transplanting (0 DAT) and particularly seven days before transplanting (-7 DAT) resulted in greater dry mass accumulation and larger inflorescence diameter (DIM and ID) (Figure 2C and 2D).
Effects of fertilization with poultry litter composted for 60 days on broccoli growth and yield variables. Composted poultry litter was applied 14 or 7 days before transplanting or at transplanting (-14, -7, and 0 DAT, respectively) and compared with a mineral NPK fertilizer control. The evaluated variables were crop cycle duration (days), leaf dry mass (g), inflorescence dry mass (g), inflorescence diameter (cm), inflorescence fresh mass (g), and dry mass accumulation rate (DM/Day ratio) (g day-1) in broccoli (cv. ‘Coliseu’). The experiment was conducted under greenhouse conditions in the Department of Soils, Universidade Federal Rural do Rio de Janeiro (UFRRJ), Brazil, in 2022. *Means followed by the same letter do not differ significantly according to Tukey’s test (P < 0.05). Values represent means averaged across inoculated and non-inoculated treatments of Plasmodiophora brassicae.
Although, fertilization did not significantly affect FIM (Figure 1E) and; therefore, did not alter average yield (as observed for DIM and ID), improvements in inflorescence quality were evident. These improvements were reflected in larger ID (Figure 1D) and greater efficiency of inflorescence dry mass accumulation (g day-1) (Figure 1F) in the 0 and -7 DAT treatments. These results suggested that CPL fertilization enhances broccoli growth and inflorescence production, with optimal application occurring close to transplanting, and no additional benefit from application two weeks earlier.
These findings confirm the severe impact of clubroot on the development of broccoli aerial organs, which is directly associated with reductions in healthy root systems, as previously reported by BHERING et al. (2017) and SANTOS et al. (2023). These results further demonstrated that, in the absence of P. brassicae, CPL fertilization significantly improves broccoli development and yield compared with mineral NPK fertilization alone, likely due to increased availability of Ca and Mg, higher soil pH and V%, and improved micronutrient supply (SANTOS et al., 2023). However, this beneficial effect was not observed in P. brassicae-infected plants. Regardless of CPL application timing, the results support the hypothesis proposed by BHERING et al. (2017) of a direct positive relationship between CPL fertilization and clubroot intensity. This effect may be associated with increased soil water retention (HOFFLAND et al., 2020), which favors both plant growth (NICK & BORÉM, 2022) and the primary infection phase of the pathogen (STRUCK et al., 2022). Furthermore, changes in soil microbial communities induced by CPL application may influence pathogen development, particularly during resting spore germination and primary zoospore release. Previous studies have shown that CPL applications can reduce soil bacterial diversity (SANT’ANNA et al., 2024), which may affect the germination of resting spores before host penetration. The germination of P. brassicae resting spores, previously attributed mainly to root exudates, is now known to be strongly influenced by the soil bacterial community (WANG et al., 2023).
When considering healthy, non-inoculated plants, CPL application consistently promoted greater inflorescence production in both experiments, reflected in a shorter crop cycle and higher daily DIM accumulation rates (Figures 1G and 1H; Figure 2A and 2F). Importantly, no significant differences were observed among CPL application timings, indicating that the interval between CPL application and transplanting did not influence plant performance under pathogen-free conditions. Under the high disease severity observed in Experiment ES, FIM and ID values obtained with CPL treatments were statistically similar to those recorded with mineral NPK fertilization (161 g and 13 cm, and 116 g and 13 cm, respectively). However, under the lower disease severity in Experiment EH, CPL treatments produced significantly larger inflorescences, with average FIM and ID values of 201 g and 13 cm, respectively, compared with 72.33 g and 8 cm under mineral NPK. Although these values remain below the optimal ranges of 300 to 500 g and 12 to 15 cm reported by NICK & BORÉM (2022), they fall within commercially acceptable standards. These results were obtained using a super-early cultivar with a 60-day cycle, grown under adverse regional climatic conditions and pot cultivation, which likely limited maximum yield potential.
CONCLUSION
Fertilization with poultry litter composted for 60 days modifies soil chemical properties and promotes broccoli development, resulting in increased inflorescence yield. However, its application, regardless of timing (14 or 7 days prior or on the day of transplanting), may increase clubroot (Plasmodiophora brassicae) severity, thereby reducing plant growth and yield. In pathogen-free soils, CPL can be applied 7 days before or at transplanting without compromising plant development or inflorescence yield.
SUPLEMENTARY MATERIAL
<https://drive.google.com/drive/folders/1WthZSnk0JjW6M-bmOT8pgxLm9GdeR3Ov>.
Supplementary PDF
ACKNOWLEDGMENTS
The authors would like to thank the Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Finance Code 001 for their financial support.
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Edited by
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ASSOCIATE EDITOR:
Leandro Souza da Silva (0000-0002-1636-6643)
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SCIENTIFIC EDITOR:
Alberto Cargnelutti Filho (0000-0002-8608-9960)
The raw data is available directly with the author.
