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Revista mexicana de fitopatología

versión On-line ISSN 2007-8080versión impresa ISSN 0185-3309

Rev. mex. fitopatol vol.40 no.2 Texcoco may. 2022  Epub 03-Oct-2022

https://doi.org/10.18781/r.mex.fit.2203-2 

Phytopathological notes

Parasitic behavior of Nacobbus aberrans populations from different geographical origin in tomato plants

Mireya Palacios-Alcántara1 

Nahum Marban-Mendoza1 

Calixto Leopoldo Carrillo-Fonseca1 

Jesús Alberto Acuña-Soto2 

Anselmo de Jesús Cabrera-Hidalgo2  * 

1 Departamento de Parasitología Agrícola, Universidad Autónoma Chapingo, Carretera México-Texcoco km 38.5, Chapingo, Edo. de México, México C.P. 56230.

2TecNM-Instituto Tecnológico Superior de Tlatlauquitepec (ITSTL) Carretera Federal Amozoc-Nautla Km. 122+600, Almoloni, Tlatlauquitepec, Puebla, México C.P. 73907.


Abstract.

The parasitic behavior of eight populations of N. aberrans from different geographical origin on tomato plants cv Miroma was evaluated. Tomato plants 29 days old were transplanted in pots previously inoculated with 0.5 g of galls from each population of nematode. Inoculated plants and control plants were kept for 45 days in a greenhouse. After transplanting (dat), three evaluations of penetration and invasion of juveniles were made at 15, 30 and 45 dat. The results showed that at 15 dat, the populations of Romita, Tetela and Chapingo presented the highest penetration and invasion rates with 58, 50 and 50 juveniles/g of root, respectively. At 30 dat, only the Silao population increased its penetration with 66 juveniles/g root, while the rest of the populations showed a significant decrease in their penetration rates. At the end of the experiment, the number of juveniles had increased, causing root swelling in the plants, mainly in those that were inoculated with the populations of Romita (158 juveniles/g of root) and Tetela (102 juveniles/g of root). In conclusion, there are clear differences in the behavior of the populations of N. aberrans in terms of fertility, penetration capacity and invasion of the root system in tomato plants, depending on their geographical origin.

Key words: False root-knot nematode; parasitic hability; juveniles; penetration and Solanum lycopersicum

Resumen.

Se evaluó el comportamiento parasítico de ocho poblaciones de N. aberrans de diferente origen geográfico en plantas de jitomate cv. Miroma. Plantas de 29 días de edad se colocaron en macetas previamente inoculadas con 0.5 g de raíces agalladas, de cada población del nematodo, y se mantuvieron en invernadero durante 45 días. Plantas sin inocular fueron incluidas con fines de comparación. Se realizaron tres evaluaciones, a intervalos de 15 días después de la inoculación (ddi), para determinar la penetración e invasión de juveniles en las raíces de las plantas de jitomate. A los 15 ddi, las poblaciones de Romita, Tetela y Chapingo presentaron las mayores tasas de penetración e invasión con 58, 50 y 50 juveniles/g de raíz respectivamente; mientras que a los 30 ddi, la presencia de juveniles en las raíces se redujo significativamente, y solo la población de Silao incrementó su penetración con 66 juveniles/g de raíz. A los 45 ddi, hubo un incremento en la cantidad de juveniles e hinchamientos en las raíces, principalmente con las poblaciones de Romita y Tetela con 158 y 102 juveniles/g de raíz, respectivamente. Existen claras diferencias en el comportamiento de las poblaciones de N. aberrans en cuanto a su fecundidad, capacidad de penetración e invasión del sistema radical en plantas de jitomate, en función de su origen geográfico.

Palabras clave: “Falso nematodo del nudo”; habilidad parasítica; juveniles; penetración; Solanum lycopersicum

The tomato (Solanum lycopersicum) is a widely cultivated vegetable around the world, and its production covers a total surface of 5,030,545 ha, and it is produced in 166 countries, where Asia concentrates over 51% of the global production. In the American continent, more than 23,786,872 t of tomato are produced, with the United States, Mexico and Brazil being the largest producers of tomato. In 2019, Mexico reported a production of 4,271,914 t in an area of 87,917 ha, with Chihuahua (330,371 t), Guanajuato (197,126 t) and Zacatecas (153,349 t) being the states with the highest production (FAOSTAT, 2021; SIAP, 2021).

Plant-parasitic nematodes are a strong limitation in agricultural systems, causing losses in yield of 8.8 to 14.6% every year in several crops around the world, which in economic terms translates to approximately $USD 80-173,000 million (Ahuja and Singh, 2020). N. aberrans is a threat to Mexican and international agriculture, since it has a high reproductive ability, a wide range of hosts, potential for losses in yield and a wide geographic distribution, along with the fact that at least 40 countries have established quarantine measures to prevent its entry. These factors lead N. aberrans to be considered as one of the 10 most important nematodes in phytopathology (Jones et al., 2013) and make it an important pathogen, and difficult to manage, since, under favorable environmental conditions, a female can produce 37-833 eggs (Manzanilla-López et al., 2002).

Some studies confirm that the behavior of this nematode is directly influenced by temperature and humidity (Inserra et al., 1985). A study by Martínez-Fuentes et al. (2010) indicates that the N. aberrans populations in Mexico display variation when parasiting bean plants, and reports that some populations do not affect it, whereas other populations can penetrate it and establish themselves in the roots without being able to reproduce, and those that establish themselves display different degrees of reproduction. The variation in pathogenicity within and among populations is common in plant-parasitic nematodes, and it takes places particularly between populations of different geographic origins and they are the result of genetic selection due to specific environmental factors.

An important aspect in the management of any phytopathological agent is the understanding of aspects related to its biology and interaction with its host. For the case of N. aberrans, there is little information related to its biological cycle, stages of survival in the soil and activation factors, pathogenic ability, influence of environmental factors in the eclosion of eggs and behavior of the juveniles, among others. For this reason, the aim of the present study was to evaluate the pathological behavior of N. aberrans populations from different geographic origins in tomato cv Miroma plants.

Biological material. Edaphic and plant (galled root) samples were collected from different agricultural regions of Puebla (Tetela de Ocampo and Libres), Guanajuato (Silao and Romita), Michoacán (Tanhuato and Yurécuaro), Nayarit (Compostela) and the State of Mexico (Chapingo). They were kept in greenhouses (28 ± 3 °C, with 13 hours of light and ± 40% relative humidity, on average) for the conservation and increase in nematode populations. All populations were previously identified as N. aberrans by sequencing ribosomal genes (Cabrera-Hidalgo et al., 2015).

Parasitism of N. aberrans in tomato plants cv Miroma. Eight N. aberrans populations, named after their place of origin (Tetela de Ocampo-TE (19°48’40” N, 97°48’53” O), Libres-Li (19°28’51” N, 97°39’19” O), Silao-Si (20°56’09” N, 101°26’09” O), Romita-RO (20°52’25” N, 101°32’42.1” O), Tanhuato-Ta (20°18’48.4” N, 102°20’40.3” O), Yurécuaro-Yu (20°18’43.7” N, 102°15’47.9” O), Compostela-Co (21°14’37” N, 104°53’10” O) and Chapingo-Cha (19°29’25” N, 98°52’23” O) were inoculated in tomato cv Miroma plants, placing 0.5 g of small, galled root sections of each nematode population in plastic pots with a substrate mixture composed of tezontle + peat moss (1:1). Eight days after inoculation (dai), a tomato cv Miroma plant, aged 29 days, was transplanted into every pot. The inoculated pots were distributed under a completely randomized design with four repetitions and kept in the greenhouse for 45 days. Non-inoculated plants were included to discard the presence of galling plant-parasitic nematodes in the substrate and anatomically compare the growth and development of roots during the experiment. The plants were irrigated every day with drip irrigation and they were fertilized edaphically with a nutrient solution every eight days (N-P-K: 8-24-0). The experiment was established in two different moments and the results were the average of both repetitions. The number of juveniles in the radical system of the tomato plants was quantified 15, 30 and 45 days after transplanting (dat), by staining the roots with acid fuchsine, following the protocol by Byrd et al. (1983) with some modifications. This procedure helps us observe nematodes, after staining, in a bright red color, in contrast to the roots, which are transparent or translucent. The specimens inside the tomato roots stained with acid fuchsine were counted along and the number of eggs/females under an Olympus® model CX31 compound microscope (Olympus, Tokyo, Japan).

The data obtained in the study underwent an analysis of variance and a means comparison test (LSD, α = 0.05). All analyses were performed using the statistical program SAS (Statistical Analysis System) version 9.3.

Response of the parasitism of N. aberrans in tomato plants. The number of juveniles found inside the roots of the tomato cv Miroma plants displayed significant differences in the three evaluation times (α= 0.05) (Table 1). Fifteen dat, the populations of Romita, Tetela and Chapingo presented the highest rates of penetration and invasion in the tomato roots with a total of 58, 50 and 50 juveniles/g of root, respectively (Table 1). It is possible that the speed at which these populations penetrate and invade the root system of the plant give them a competitive advantage against other organism populations, including other species of nematodes, since this may favor, to a higher or lesser degree, their successful establishment and survival, and guarantee a quick source of food. Reports by Umesh (1994) when investigating the competition between Pratylenchus negletus and Meloidogyne chitwoodi in barley plants claim that the species that first parasites the roots prevented the penetration and development of the other. Fernández and Ortega (1982) explain that this effect could be due to the damage caused in the tissues by the genus that first invades the host.

Table 1 Total penetration and juveniles average of N. aberrans in tomato roots cv Miroma at 15, 30 and 45 dat. 

Población Juveniles/gramo de raíz
15 ddt 30 ddt 45 ddt
Total y NSz Total NS Total NS
TETELA 50.00 16.67 AB 18.00 6.00 B 102 34.00 B
TANHUATO 30.00 10.00 AB 0.00 0.00 B 38 12.67 C
LIBRES 36.00 12.00 AB 6.00 2.00 B 24 8.00 C
ROMITA 58.00 19.33 A 1.50 0.50 B 158 52.67 A
YURECUARO 6.00 2.00 B 0.00 0.00 B 6 2.00 C
COMPOSTELA 6.00 2.00 B 6.00 2.00 B 42 14.00 C
SILAO 6.00 2.00 B 66.00 22.00 A 18 6.00 C
CHAPINGO 50.00 16.67 AB 8.00 2.67 B 16 5.33 C
CONTROL 0.00 0.00 B 0.00 0.00 B 0 0.00 C
LSD 16.83 13.28 15.78

y Number of juveniles/g of galls (average of three repetitions). dat= Days after transplanting. LS= Level of Significance. LSD= Least Significant Difference.z Means with the same letter in the same column are not statistically different (α=0.05).

The penetration of the juveniles (J2) occurred mainly in the area of elongation of the root (Figure 1A), where, according to Perry (1997), the cells of the apical meristem prepare for their cellular differentiation. The sites of penetration of the juveniles could be easily identified by the presence of necrotic lesions along the cortical parenchyma (Figure 1A-C, red arrows) as a result of the inter and intracellular migration carried out by the nematode, including the vascular cylinder (Figure 1B) (Souza and Baldwin, 2000).

Figure 1 Invasion and penetration of juveniles of N. aberrans in tomato roots cv Miroma at 15 dat. A) Necrotic lesions caused by intra and intercellular movement of the nematode (red arrows). B-C) Juveniles inside cortical cells of the root. D) J3 with C-shaped body in the cortical parenchyma of the root (red arrow). 

J3 and J4 were found isolated, surrounded by necrotic tissue in the radical cortex (Figure 1D, red arrow) and according Manzanilla-López et al. (2002), this is possible because el J2 can change in the root or in the soil to J3, which is less active and tends to remain rolled up in the root cortex (body in a “C” shape).

Thirty dat, a change in the behavior of the nematode populations was observed, since the presence of juveniles in the roots had, in general terms, reduced significantly (α= 0.05). This may be due to the exhaustion of the juveniles inoculated in the soil by the quick initial penetration (15 dat) of these in the roots of the host or by factors of intra and interspecific competition (predation or parasitism) and adaptation (limiting environmental conditions), since nematodes are a group of highly diverse organisms that display a variety of adaptations to extreme soil and plant environments (McSorley, 2003).

The only population to increase its penetration was the one from Silao, with 66 juveniles/g of root, whereas in the rest of the populations, penetration did not exceed 18 juveniles/g of root (Table 1), possibly as a result of partially or totally overcoming the stage of temporary inactivation conditioned by some type of environmental stress or a factor inherent to the biology of the nematode, since according to Evans and Perry (2009), the diapause that takes place in nematodes is not necessarily the result of adverse environmental conditions, nor does it end with favorable conditions, because this is a critical survival mechanism during colder seasons and in the absence of a susceptible host. They add that the latency of the development seems to take place mainly in the egg stage and in the juvenile stages inside the eggs, although cases of diapause are also known to occur in late juvenile stages or in adults, mostly in a few zooparasite nematodes.

In the examined roots, it was common to find juveniles rolled up or in a “C” shape (Figure 2A-D, red arrows) and bulges and swellings were found with necrotic areas (Figure 2C-D), indicating the presence of the nematode inside them, and the formation of the specialized feeding site (syncytium), since according to Prasad and Webster (1967) and Manzanilla-López et al. (2002), this leads to a series of histological and physiological alterations in the area of the radical system of the host, induced by the presence of immature females, normally fixated in the proximity of the central cylinder (Figure 2C-D).

Figure 2 Invasion and penetration of juveniles of N. aberrans in tomato roots cv Miroma at 30 dat. A-D) Juveniles with C-shaped body inside the cortical cells (red arrows). C-D) Juveniles surrounding the vascular cylinder. Notice the swelling associated with the presence of juveniles 

At 45 dat, an increase in the number of juveniles and radical galling was observed in the tomato plants, mainly with the populations of Romita and Tetela, finding 158 and 102 juveniles/gram of root, respectively (Table 1, Figure 3A-B). These populations displayed constant flows of penetration (Figure 4) as a result of a better adaptation to the particular soil and environmental conditions. Initially, it is possible that the eggs found in the fragments of inoculated root in both populations responded favorably to the stimuli for their eclosion and finalization of some internal latency condition (diapause) or to some type of environmental stress (quiescence) such as temperature (Van Gundy, 1985) or the presence of the host or radical leachate (Huang and Pereira, 1994; Sikora and Noel, 1996). On the other hand, this could be due to these populations having found optimal conditions for their development, in such a way that allowed them to quickly complete their biological cycle (egg to egg) in comparison with the rest of the populations, leading to the production of overlapping populations.

Figure 3 Invasion and penetration of juveniles of N. aberrans in tomato roots cv Miroma at 45 dat. A) Clustering of nematodes in the cortical cells and vascular cylinder of tomato roots (red circle). B) Swelling and root necrosis (red arrow). C) Adult male in galls (red arrow). D) Adult females in galls (red arrows). 

Figure 4 Penetration flows of N. aberrans populations at 15, 30 and 45 dat. Bars indicate standard deviation. 

It is possible that the low penetration of the juveniles of the populations from Yurécuaro and Compostela registered in this study are due to problems in the biological adaptation to the prevailing edaphic conditions, which may have affected their orientation, mobility and penetration abilities in the host, and the greater time it remained in the soil may have led it to experience some type of latency, since according to McSorley (2003), the soil surroundings provide nematodes with diverse degrees of protection against dehydration, although they run the risk of increasing the loss in body water as soils become drier, and this seriously affects their parasitic behavior.

Another reason that explains the low penetration of these populations may be that the biological stages (eggs and juveniles) were in a latency phase (diapause or quiescence) during inoculation and that a lack of favorable conditions for their development kept them in this way for longer. It is known that the stimulation of the eclosion of eggs in plant-parasitic nematodes is quite complex. For example, in some species of galling (Meloidogyne sp.) and cyst nematodes (Heterodera sp., Globodera sp.), a portion of the eggs hatching quickly, whereas others hatching slowly in time (Zheng and Ferris, 1991; Huang and Pereira, 1994), and the latter could have occurred in the Yurécuaro and Compostela populations.

All the populations, to a higher or lesser degree, managed to penetrate and invade the root system of the tomato plant, confirming the viability of the eggs and biological stages of the nematode. Differences in the rates of penetration and invasion based on the populational geographic origin of the nematodes were clearly observed, with the populations of Romita and Tetela being the most aggressive and best adapted, displaying several peaks of penetration (Figure 4). When fragments of galled roots are used as a source of inoculants, it is common to find all the biological stages of the nematode inside them, from masses of eggs in gelatinous matrices to mature and immature females, and uncommonly, adult males (Figure 3C), which have a certain degree of protection to edaphic factors (temperature, humidity, predators, parasites, etc.) when inside the roots. Once favorable conditions for their development are presented (whether environmental or the presence of a food source), they successfully infect their host, in comparison to those nematodes that only remain in associations with soil particles (Cristóbal-Alejo et al. 2001). According to McSorley (2003), the nematodes found in the roots of plants enjoy an optimum humidity and protection against desiccation, so long as the host -in this case, the fragments of inoculated galls- remains viable.

On the other hand, in the masses of eggs in the galls that were extracted, 1-2 females were found per gall (Figure 3D), similar to reports by Manzanilla-López et al. (2002). The adult female in the galls had a saccular-shaped midsection of the body, a rounded tail, a short neck and a rounded posterior section; these characteristics coincide with descriptions by Manzanilla-López et al. (2002) for N. aberrans. Several males were found around the egg masses (Figure 3C; data not registered). Manzanilla-López (1997) mentioned that up to 16 males have been found around the galls containing unfertilized females in tomato roots. This occurs because they are attracted by the gelatinous mass; they can be found in the egg mass (1 to 18) or inside the gall, beside the tail of the female.

Based on the results of this study, we can conclude that plant-parasitic nematodes in all biological stages were found (eggs, J2-J4, males, immature and mature females) in the different times evaluated (15, 30 and 45 dat). In addition, the populations of Romita and Tetela displayed the highest parasitic ability over the roots of tomato cv Miroma, presenting continuous flows of penetration and invasion in the plant root systems. Finally, there are clear differences in the behaviors of the populations of N. aberrans in terms of their fertility, ability of penetration and invasion of the radical system in tomato plants, depending on their geographic origin.

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Received: March 13, 2022; Accepted: April 24, 2022

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