1. bookVolume 58 (2021): Issue 2 (June 2021)
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Occurrence of Meloidogyne arenaria in black pepper (Piper nigrum L.) in the extreme south of the State of Bahia, Brazil

Online veröffentlicht: 08 Jun 2021
Seitenbereich: 213 - 216
Eingereicht: 20 May 2020
Akzeptiert: 04 Dec 2020
Zeitschriftendaten
License
Format
Zeitschrift
Erstveröffentlichung
22 Apr 2006
Erscheinungsweise
4 Hefte pro Jahr
Sprachen
Englisch
Introduction

Black pepper (Piper nigrum L.), originally from India, is one of the most consumed spices worldwide, being widely used as a condiment in food preparation and processing (Nair, 2011). It is currently grown on a commercial scale in 26 countries, mainly Indonesia, Malaysia, Brazil, Vietnam, China and Thailand (Ravindran, 2000). Brazil stands out as the world’s third largest producer of black pepper, with cultivation growing 53 % in 2017, as the country has ideal conditions for its development, especially in the states of Espirito Santo, Southern Bahia and Pará, the latter being the largest national producer and responsible for almost 70 % of Brazilian production (IBGE, 2017).

Despite the growing production, pipericulture faces serious phytosanitary problems, mainly due to the occurrence of soil pathogens such as fungi and root-knot nematodes, Meloidogyne spp., Goeldi, pathogens that are diffi cult to manage due to their wide dissemination and host range (Antes et al., 2012; Maleita et al., 2012; Negretti et al., 2014; Bellé et al., 2017; Moreira et al., 2017). In addition, phytonematodes are considered the main elements of predisposition to fusariosis, also known as root rot, a disease caused by the fungus Fusarium solani f. sp. piperis anti, 2015).

Considering the importance that root-knot nematodes represent and the lack of consistent information about the distribution and occurrence of these pathogens in black pepper, this work aimed to characterize, biochemically and morphologically, the gall nematode species associated with black pepper plantations in the most southern region of the State of Bahia, Brazil.

Material and Methods

The study was carried out at Fazenda Conjunto Bom Jardim, located in the municipality of Itabela, in the extreme south of Bahia, Brazil, on a property composed of 10 ha grown with black pepper (latitude 16 ° 44 ‘45’ ‘S and longitude 39 ° 28’ 58 ‘’ W), altitude of 120 m at sea level, with four years of age and 3.70 x 1.65 m spacing. Three areas were selected, each consisting of 1 ha, two of them with cv. Kottanadan Roxa and the other with cv. Bragantina. The samples were collected from 0 to 30 cm deep, in the rhizosphere region, giving preference to the collection of radicellae from weakened plants (Fig. 1).

Fig. 1

(A) Weakened black pepper plants grown in the municipality of Itabela in the extreme south of Bahia; (B) Roots with gall symptoms induced by gall nematodes. Photo: Rafael Assis de Souza.

After zig-zag walking in each area, 10 subsamples were collected that made up 1 composite sample for each area.

The samples were packed in plastic bags, duly identified, and sent to the Laboratory of Nematology at the Research Center for Plant Protection and Animal Health, of the Instituto Biológico, in Campinas, SP, for extraction and identification of phytoparasitic nematodes.

The nematodes were extracted from 10g of roots using the method of Coolen and D´Herde (1972) and the quantification was performed in Peters slide.

The identification of the Meloidogyne species was carried out considering three criteria: i) observation of the anterior region of the males; ii) analysis of female perineal configuration (Hunt & Handoo, 2009) and iii) polyacrylamide gel electrophoresis technique according to Oliveira et al. (2012).

Thirty-five females were used in the isoenzymatic identification (esterase) considering five females per sample, totaling seven samples. Five females were also used for identification by the perineal configuration and five males for observation of the anterior region of the nematode.

Ethical Approval and/or Informed Consent

For this study formal consent is not required.

Results and Discussion

Black pepper plants parasitized by gall nematodes generally become chlorotic, with severe leaf yellowing, defoliation and reduction in chlorophyll content, which affects vegetative development, resulting in significant reduction in yield and even death (Freire & Monteiro, 1978; Ferraz & Lordello, 1989; Mohandas & Ramana, 1991). Some of these symptoms, such as yellowing, defoliation and roots with numerous galls were observed in the plants analyzed in our study.

Studying the anterior region of the males and analyzing the perineal configuration of the females, the presence of Meloidogyne arenaria was confirmed (Figs. 2A and 2B).

Fig. 2

(A) Anterior region of the males and (B) Perineal configuration of the characteristic females of Meloidogyne arenaria.

We observed females with perineal pattern rounded to ovoid, with thin to thick streaks. Low dorsal arch, flattened, with smooth or slightly wavy streaks, slightly bent towards the tail tip on the lateral line; usually forming shoulders on the lateral portion of the arch. The dorsal and ventral striations are usually at an angle on the lateral lines; distinct lateral field, slightly irregular. In males, the labial region was continuous with the rest of the body, smooth, labial disc more or less rounded, slightly elevated above the level of the medial lips. Long distance from the orifice of the dorsal esophageal gland to the base of the stylet.

The analysis of polyacrylamide gel electrophoresis also revealed a characteristic profile of M. arenaria (Fig. 3).

Fig. 3

Phenotype of polyacrylamide gel esterase, characteristic of Meloidogyne arenaria, obtained from females of the nematode of galls extracted from black pepper roots. Mj = M. javanica (standard); 2 to 7 = M. arenaria

The numbers of second stage juveniles (J2) + eggs extracted from black pepper roots are shown in Table 1. Both cultivars showed a high number of M. arenaria demonstrating the susceptibility of these cultivars to this species.

Number of second stage juveniles (J2) and eggs of Meloidogyne arenaria obtained in 10 g of root from black pepper cv. Kottanadan roxa and Bragantina in cultivation areas in the extreme south of the state of Bahia, BA.

Area 1‘Kottanadan Roxa’ Area 2‘Kottanadan Roxa’ Area 3‘Bragantina’
root root root
J2 5600 5300 5000
eggs 5600 4300 3100

The first study that showed the presence of Meloidogyne spp. in black pepper plantations was carried out in 1901 by Zimmerman cited by Winoto (1972).

In Brazil, reports involving the black pepper pathosystem x Meloidogyne spp. are rare and mostly related to M. incognita in the State of Pará (Lordello & Silva, 1974; Ichinohe, 1976; Freire & Monteiro 1978).

In Brazil, the only report of M. arenaria in black pepper is from 1965, made by Dr. Jair C. Carvalho, based on the analysis of soil and roots from Caraguatatuba, SP (Carvalho, 1965). It is important to highlight that before the development of the isoenzyme electrophoresis technique, the identification of Meloidogyne species was performed exclusively by examining the perineal configuration (Chitwood, 1949). It is known, however, that this technique is extremely subjective, and it is of fundamental importance also to characterize these pathogens by biochemical means, through the technique of isoenzyme electrophoresis (Carneiro & Almeida, 2001; Oliveira et al. 2012), and by observation of the region of the males, as performed in the present study. The use of these last two techniques associated with the analysis of the perineal configuration brings certainty regarding the correct diagnosis of Meloidogyne spp. (Cunha et al, 2018).

Considering that the success of any nematode management strategy depends, initially, on the knowledge of the species present in the areas where it is desired to reduce the population of these pathogens, the information obtained in the present work may be useful in the development and adoption of appropriate techniques for the management of parasitic nematodes of black pepper.

The species of gall nematode associated with black pepper cultivation in the extreme south of the State of Bahia is Meloidogyne arenaria. It is the first report of this pathosystem in the State, and therefore expands its geographical scope.

Fig. 1

(A) Weakened black pepper plants grown in the municipality of Itabela in the extreme south of Bahia; (B) Roots with gall symptoms induced by gall nematodes. Photo: Rafael Assis de Souza.
(A) Weakened black pepper plants grown in the municipality of Itabela in the extreme south of Bahia; (B) Roots with gall symptoms induced by gall nematodes. Photo: Rafael Assis de Souza.

Fig. 2

(A) Anterior region of the males and (B) Perineal configuration of the characteristic females of Meloidogyne arenaria.
(A) Anterior region of the males and (B) Perineal configuration of the characteristic females of Meloidogyne arenaria.

Fig. 3

Phenotype of polyacrylamide gel esterase, characteristic of Meloidogyne arenaria, obtained from females of the nematode of galls extracted from black pepper roots. Mj = M. javanica (standard); 2 to 7 = M. arenaria
Phenotype of polyacrylamide gel esterase, characteristic of Meloidogyne arenaria, obtained from females of the nematode of galls extracted from black pepper roots. Mj = M. javanica (standard); 2 to 7 = M. arenaria

Number of second stage juveniles (J2) and eggs of Meloidogyne arenaria obtained in 10 g of root from black pepper cv. Kottanadan roxa and Bragantina in cultivation areas in the extreme south of the state of Bahia, BA.

Area 1‘Kottanadan Roxa’ Area 2‘Kottanadan Roxa’ Area 3‘Bragantina’
root root root
J2 5600 5300 5000
eggs 5600 4300 3100

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