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Revista mexicana de fitopatología

On-line version ISSN 2007-8080Print version ISSN 0185-3309

Rev. mex. fitopatol vol.38 n.2 Texcoco May. 2020  Epub Nov 27, 2020

https://doi.org/10.18781/r.mex.fit.2002-3 

Phytopathological notes

Identification of associated fungi to diseases in Cereus jamacaru and Cereus hildmannianus

Rommel dos Santos Siqueira Gomes1  * 

José Thiago Aires Souza1 

Gabriel Ginane Barreto2 

Luciana Cordeiro do Nascimento3 

1 Program of Graduate in Agronomy, Federal University of Paraíba, Rodovia PB 079-Km 12-Caixa Postal 66 - CEP 58397-000-Areia, Brazil;

2 Bachelor in Biological Sciences, Center of Agrarian Sciences, Federal University of Paraíba, Areia, Brazil;

3 Department of Plant Science and Enviromental Sciences, Federal University of Paraíba, Areia, Brazil.


Abstract.

Although cacti are well adapted to the climatic rigors of the Brazilian semiarid region, they run the risk of being affected by important phytosanitary problems. These problems cause serious damage during their development. Therefore, the correct diagnosis of the etiologic agent is the most important step to enable the recommendation of efficient control strategies. The objective of this study was to identify etiological agents that caused diseases in mandacaru cladodes (Cereus jamacaru) and mandacaru spineless (C. hildmannianus). The cladodes were collected from infected plants in the field in the Sítio Paraíso community, in the municipality of Prata, State of Paraíba, Brazil. They were analyzed at the Phytopathology Laboratory/CCA/UFPB. The fungal structures were observed under optical microscopy, from vegetative and reproductive structures of the fungi grown in PDA (potato-dextrose-agar) medium at 25 ±2 ºC and under a photoperiod of 12 h of light. The genera were observed: Aspergillus niger, Aspergillus sp., Cladosporium sp., Colletotrichum sp., Curvularia sp., Fusarium sp., Rhizopus sp. and Scytalidium lignicola. The fungi Colletotrichum sp. and S. lignicola are considered the first reports of episodes of Cereus jacamaru and C. hildemannianus in State of Paraíba, Brazil.

Key words: Cactaceae; mandacaru; northeast; health; Brazilian semiarid region

Resumen.

Aunque los cactus están bien adaptados a los climas semiáridos brasileños, corren el riesgo de verse afectados por importantes problemas fitosanitarios, causando graves daños a su desarrollo. Por lo tanto, el diagnóstico correcto del agente etiológico es el paso más importante para apoyar la recomendación de estrategias de control eficientes. El objetivo de este estudio fue identificar agentes etiológicos causantes de enfermedades en cladodios de mandacaru (Cereus jamacaru) y mandacaru sin espinas (C. hildmannianus). Los cladodios se recolectaron de plantas infectadas en condiciones de campo en la comunidad de Sítio Paraíso, en el municipio de Prata, Estado de Paraíba, Brasil, y se enviaron para su análisis en el Laboratorio de Fitopatología/CCA/UFPB. Las estructuras fúngicas se observaron bajo el microscopio óptico, a partir de estructuras vegetativas y reproductivas de los hongos cultivados en medio PDA (papa-dextrosa-agar) a 25 ±2 ºC y bajo 12 h de fotoperíodo de luz. Los géneros que se observaron fueron: Aspergillus niger, Aspergillus sp., Cladosporium sp., Colletotrichum sp., Curvularia sp., Fusarium sp., Rhizopus sp. y Scytalidium lignicola. Los hongos Colletotrichum sp. y S. lignicola se consideran los primeros informes en cladodios de Cereus jacamaru y C. hildemannianus en el Estado de Paraíba, Brasil.

Palabras clave: Cactaceae; mandacaru; noroeste; sanidad; semiárido brasileiro

The family Cactaceae is native to the American continent, where it displays high species richness and abundance. The family includes over 1,500 species distributed worldwide, inhabiting different environments from drylands to wet forests. They have evolved to be morphologically and physiologically adapted to extreme climates (Cavalcante et al., 2013). Cacti often used as ornamental plants, but they also grow as wild plants in arid and semiarid regions. Moreover, they can be used as an important part of human nutrition due to the quality and flavor of their fruit, which can be consumed fresh, and the use of young cladodes as vegetables in salads (Shetty et al., 2012).

Mandacaru (Cereus jamacaru) and other native cacti are widely distributed in the Caatinga biome, and their presence is important to the fauna and flora of the ecosystem. Mandacaru is used as a source of water during long droughts. In Brazil, it is also used as a strategic forage resource by producers to meet the nutritional demand of ruminants in the dry season (Silva et al., 2010). Cereus hildmannianus, a spineless type of mandacaru, is used as an ornamental plant, and it is nutritious for animals due to its high protein content of 10.7% (Silva et al., 2017). As a forage alternative, the spineless mandacaru may represent an advance in animal nutrition. The absence of spines facilitates its cultivation as well as the feeding process to livestock (Santos and Souza, 2016).

These cacti are subject to pathogen attacks, particularly fungi, that preferentially affect the apical portion of the cladode. Identified Colletotrichum gloeosporioides, Dichotomophthora cactacearum, Lasiodiplodia theobromae, Phoma sp., Phytophthora sp., Scytalidium lignicola, among others, as pathogens of mandacaru (C. jamacaru) plants in the Brazilian state of Ceará (Freire, 2009). However, few studies have described the damage caused by fungal diseases to plants of the genus Cereus. Such studies could clarify the etiology of the disease and aid in the development of management strategies.

The introduction of new ornamental plants varieties has accelerated, particularly through the use of seeds, cuttings and other propagules without certification. These can carry new pathogens into the country. Thus, the presence of fungi can lead to significant disease-related losses due to the use of contaminated or infected seeds or propagules (Barreto et al., 2011). The objective of this study was to identify causative agents of diseases in cladodes of mandacaru and spineless mandacaru.

Cladodes were collected in the sampling point 07o 44’ 36.8” S and 37o 03’ 16.4” W at the Sítio Paraíso community, located in the municipality of Prata, State of Paraíba, Brazil. The infected cladodes were transported to the Laboratory of Phytopathology, in the Department of Plant and Environmental Sciences, Federal University of Paraíba, located in the city of Areia.

Cladodes that presented symptoms of the disease were washed and air-dried at room temperature (25 ± 2 ºC). Tissue fragments were removed using a sterile scalpel to collect parts of the infected cladode tissue. The fragments were disinfected using 70% ethanol for 30 seconds, followed by 1% sodium hypochlorite for 1 minute, and they were rinsed with sterile deionized water. Five tissue fragments were incubated in potato-dextrose-agar (PDA) medium at 25 ºC, with a photoperiod of 12 h light:12 h dark in a biochemical oxygen demand chamber.

Fungi identification was performed after seven days of incubation based on the physical separation of the fungi promoted by the host tissue, using an optical microscope and stereoscope. The morphological and reproductive structures of the fungi were compared with literature descriptions (Seifert et al., 2011). Lastly, the occurrence of fungi associated with either type of mandacaru was determined.

Healthy plants aged 90 days, grown in the greenhouse in 1.5 dm3 pots filled with sterile soil were used in the pathogenicity test. Isolates from symptomatic plants obtained through indirect isolation as described above were used, totaling five plants per isolate. Plants were inoculated by spraying the cladodes with a conidia suspension at 1x106 colony forming units (CFU) mL-1 of the Colletotrichum sp. and Scytalidium lignicola because it was the fungi that had the highest disease intensity in the evaluated cladodes. Controls were sprayed with sterile deionized water. After spraying using a manual spray bottle to the point of dripping, cladodes were covered with polyethylene bags wetted with sterile deionized water and incubated in a moist chamber for 24 h. The inoculated cladodes were kept under greenhouse conditions until the onset of symptoms.

Based on the micro-morphological characteristics of the conidia, the following fungi were identified: Aspergillus niger, Aspergillus sp., Cladosporium sp., Colletotrichum sp., Fusarium sp., and Scytalidium lignicola in Cereus jamacaru cladodes and Aspergillus niger, Aspergillus sp., Rhizopus sp., Scytalidium lignicola, Fusarium sp. and Curvularia sp. in material isolated from C. hildmannianus. Similar fungi were identified by Freire (2009) in a study of mandacaru pathogens and by Souza et al. (2017) in a study that identified fungi in giant prickly pear (Opuntia ficus-indica).

Based on the apparent symptoms in the cladodes of both types of mandacaru (C. jamacaru and C. hildemannianus), the identified diseases were anthracnose, caused by Colletotrichum sp., and squamous rot caused by Scytalidium lignicola (Figure 1 and 2).

According to Freire (2009), anthracnose in mandacaru is a sporadic disease that occurs particularly during the wet season. This is when the symptoms were observed in the terminal portions of plants collected in Ceará. The disease caused extended, bluish lesions, which at times displayed concentric lines (Figure 1b).

To date, no study has reported S. lignicola as the causative agent of squamous rot in spineless mandacaru. Thus, this is the first report for the studied pathosystem (Figure 2). According to Souza et al. (2010) and Lopes (2012), the disease is characterized by the appearance of wavy spots that resemble scales, which grow over areas of dry rot, starting at the base of the pads at the point of connection and insertion of areoles. The disease can potentially affect the entire O. ficus-indica cladode. These symptoms are similar to those observed in the spineless mandacaru (Figures 2 a, b, c and d).

Figure 1. Symptoms of anthracnose in the terminal portion of the cladodes (a and b) and on fruits (c) of mandacaru (Cereus jamacaru); micro-morphological features of conidia from Colletotrichum sp. (d). 

Lopes (2012) suggested that squamous root can be attributed to S. lignicola based on the identification of morphological macro and microstructures. This is an anamorphous form of Botryosphaeria spp., which has high genetic variability (Crous et al., 2006) and has been associated with other crops, causing spots in vanilla (Vanilla planifolia) leaves, stems, and fruits (Verzignassi et al., 2007) and black rot in cassava (Manihot esculenta) roots (Silva et al., 2017).

Figure 2 Symptoms of squamous rot in spineless mandacaru plants (Cereus hildmannianus) (a) and gallery openings (b and c) caused by Scytalidium lignicola; and S. lignicola conidia structure (d). 

The rotting of cladodes and roots may be associated with the high incidence of Scytalidium sp. widespread squamous rot leads to decreased productivity, hindering cultivation. This effect potentially intensifies and worsens under high humidity and moderate temperatures conditions (Lopes, 2012; Souza et al., 2017).

According to Souza et al. (2010), among the main phytosanitary problems that affect prickly pear (O. ficus-indica) crops in the semiarid region in Paraíba, several diseases were observed, particularly squamous rot caused by the fungus S. lignicola.

Symptoms typical of anthracnose and squamous rot in cladodes of mandacaru with and without spines were reproduced in this study. Anthracnose symptoms appeared in the upper part of the cladodes as necrotic lesions accompanied by soft rot in the fruits, in both species of Cereus, with and spineless. S. lignicola was observed only in spineless mandacaru plants (C. hildmannianus) as rotting of cladodes and roots and gallery openings on the cladodes. In both diseases, symptoms started up to 10 days after inoculation of pathogens. To confirm the disease etiology, re-isolation was performed from the symptoms, in PDA culture medium and observation of morphological structures under microscopy.

The genera were observed: Aspergillus niger, Aspergillus sp., Cladosporium sp., Colletotrichum sp., Curvularia sp., Fusarium sp., Rhizopus sp. and S. lignicola. The fungi Colletotrichum sp. and S. lignicola are considered the first reports of episodes of C. jacamaru and C. hildemannianus in State of Paraíba, Brazil.

Acknowledgments

The authors would like to thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Capes), the Pró-Reitoria de Pesquisa (PROPESQ) of UFPB.

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Received: February 06, 2020; Accepted: March 19, 2020

* Corresponding author: pratacca@gmail.com.

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