differential hiStoPathological reSPonSe of PePPer

Solanaceae) cultivarS to nacobbuS celatuS

nematoda) PoPulationS

(

reSPueSta hiStoPatológica diferencial de cultivareS de Pimiento

(Solanaceae) a PoblacioneS de nacobbuS celatuS (nematoda)

Verónica A. Cabrera¹* , Marcelo E. Doucet² & Paola Lax²*

Summary

Background and aims: The false-root knot nematode (Nacobbus spp.) comprises

1

. Laboratorio de Morfología

polyphagous species, with pepper (Capsicum annuum) being one of the most

aﬀected crops. Due to the lack of resistant pepper genotypes, we compared the

responses of diﬀerent commercial cultivars to identify possible plant defence

mechanisms against N. celatus.

M&M: Nematodes from Río Cuarto (Córdoba Province) and Lisandro Olmos (Buenos

Aires Province) were inoculated on pepper cultivars: California Wonder (control),

Fyuco INTA, Yatasto, and Fenomeno RZ. Plants were grown under a greenhouse

and galls were analysed by histopathological techniques.

Vegetal. Instituto Multidisciplinario

de Biología Vegetal (CONICET-UNC),

Facultad de Ciencias Exactas, Físicas

y Naturales, Universidad Nacional

de Córdoba, Córdoba, Argentina

2

. Instituto de Diversidad y Ecología

Animal (CONICET-UNC) and Centro

de Zoología Aplicada, Facultad

Results: The roots of the commercial cultivars showed the typical morpho-anatomical

alterations induced by N. celatus: gall formation, hyperplasia reactions, development

of syncytia in the central cylinder and disorganisation of vascular tissues. Syncytial

cells in contact with females of nematodes from Lisandro Olmos showed a defence

reaction by Fyuco INTA, whereas feeding sites in Fenomeno RZ did not denote high

metabolic activity in nematodes of both origins.

de Ciencias Exactas, Físicas

Naturales, Universidad Nacional de

Córdoba, Córdoba, Argentina

y

*veronica.cabrera@unc.edu.ar,

plax@unc.edu.ar

Conclusions: The diﬀerent responses observed between populations and/or hosts

demonstrate the importance of considering nematodes from diﬀerent geographical

origins when testing plant material for tolerance and/or resistance to N. celatus.

Studies of this nature are necessary since they facilitate a more in-depth

understanding of the parasite-plant interaction.

Citar este artículo

CABRERA, V. A., M. E. DOUCET

&

P. LAX. 2024. Differential

histopathological response of

pepper (Solanaceae) cultivars to

Nacobbus celatus (Nematoda)

populations. Bol. Soc. Argent. Bot.

Key wordS

Capsicum annuum, defence mechanism, false root-knot nematode, histology,

syncytium.

5

9: 151-159.

reSumen

DOI: https://doi.

org/10.31055/1851.2372.v59.

n2.44120

Introducción y objetivos: El falso nematodo de la agalla (Nacobbus spp.)

comprende especies polífagas, siendo el pimiento (Capsicum annuum) uno de los

cultivos más afectados. Debido a la falta de genotipos resistentes del pimiento,

comparamos las respuestas de diferentes cultivares comerciales para identiﬁcar

posibles mecanismos de defensa contra N. celatus.

M&M: Nematodos provenientes de Río Cuarto (provincia de Córdoba) y Lisandro

Olmos (provincia de BuenosAires) se inocularon en cultivares de pimiento: California

Wonder, Fyuco INTA, Yatasto y Fenomeno RZ. Las plantas se desarrollaron en

invernadero y las agallas se analizaron mediante técnicas histopatológicas.

Resultados: Las raíces de los cultivares analizados mostraron las alteraciones morfo-

anatómicas típicas inducidas por N. celatus: formación de agallas, reacciones de

hiperplasia, desarrollo de sincitios en el cilindro central y desorganización de los

tejidos vasculares. Las células sincitiales en contacto con hembras de Lisandro

Olmos mostraron una reacción de defensa por parte de Fyuco INTA, mientras que

los sincitios en Fenomeno RZ denotaron baja actividad metabólica en nematodos

de ambas procedencias.

Conclusiones: Las diferencias observadas entre las poblaciones y/o hospedadores

demuestran la importancia de considerar nematodos de diferentes orígenes

geográﬁcos al analizar material vegetal para determinar su tolerancia y/o resistencia

a N. celatus. Estudios de esta naturaleza son necesarios ya que facilitan una

comprensión más profunda de la interacción parásito-planta.

Recibido: 9 Ene 2004

Aceptado: 20 May 2024

Publicado impreso: 30 Jun 2024

Editora: Ana María Gonzalez

PalabraS clave

Capsicum annuum, histología, falso nematodo de la agalla, mecanismo de defensa,

sincitio.

ISSN versión impresa 0373-580X

ISSN versión on-line 1851-2372

151

Bol. Soc. Argent. Bot. 59 (2) 2024

introduction

previously (Lax et al., 2006, 2016; Gómez-

Rodríguez et al., 2019), and, in limited situations,

The genus CapsicumL. belongs to the Solanaceae the histopathology of the interaction was considered

family and currently includes 43 species; it is native (Moyetta et al., 2007).

to temperate, subtropical, and tropical regions of

Argentina is the main pepper producer in South

the Americas, ranging from the southern United America, with some 6,000 ha under cultivation and

States to central Argentina and Brazil, with the an annual production of approximately 153,000

main centre of diversity in the Andes (Barboza et tonnes (FAO, 2022). In the country, nematode

al., 2022). This genus comprises a diverse group N. celatus (ex N. aberrans) is an important pest

of sweet and hot peppers, which are consumed for this crop grown in the ﬁeld and greenhouses.

by a quarter of the global population (Parvez, To identify potential defence mechanisms of

2

017). There are ﬁve domesticated species, among the plant reaction, we analysed and compared

which Capsicum annuum L. stands out for being the response of commercially available cultivars

extensively cultivated worldwide (Barboza et al., [Fyuco INTA, Yatasto, and Fenomeno RZ (resistant

2

022). to Meloidogyne spp.)], for which the histopathology

The genus Nacobbus Thorne & Allen, 1944 of the parasite-host interaction is unknown.

Phylum Nematoda) is native to the American

(

continent and comprises sedentary endoparasitic

species of nematodes with polyphagous habits. material and methodS

Among its wide host range, several species

belonging to the Solanaceae family are highlighted, Nematode populations and plant material

being pepper one of the crops that is severely

Based on its known aggressiveness to pepper, two

aﬀected (Lorenzo et al., 2001; Manzanilla-López Argentine populations of N. celatus were selected

et al., 2002; Tordable et al., 2010; Lax et al., 2016, from the localities of Río Cuarto (abbreviation

2

021). The establishment of the immature female RC, from Córdoba Province) and Lisandro Olmos

on the host root and the development of its feeding (abbreviation LO, from La Plata, Buenos Aires

site (syncytium) induce the formation of galls Province). Seeds from commercially available

(Lax et al., 2022). Because of the great damage cultivars of C. annuum were acquired from the

they cause to agriculture, the Nacobbus species market; commercial names: Fyuco INTA, Yatasto,

are of quarantine importance (EPPO, 2024). These and Fenomeno RZ (35-615). According to the

parasites are known as false root-knot nematodes supplier company, the last cultivar has resistance to

(

abbreviation FRKN) because the root symptoms RKN species: Meloidogyne incognita, M. javanica,

are similar to those produced by the Meloidogyne and M. arenaria. California Wonder was also used

species (root-knot nematodes, abbreviation RKN). as a positive control due to its known susceptibility

There are no pepper cultivars available that to this nematode (Tordable et al., 2007).

show a certain degree of resistance to Nacobbus Pepper seeds were germinated in sterile soil. A

species (Lax et al., 2016; Gómez-Rodríguez et al., completely randomized experimental design was

019). For this reason, it is of great importance to used with eight plants for each cultivar; single four-

2

evaluate aspects of the parasite-host interaction leaf stage seedlings were transplanted into pots (20

in diﬀerent germplasm, even in cases where the cm long, 4 cm wide) containing sterile soil and

nematode succeeds in multiplying, since this sand (3:1). The roots were placed on this substrate,

may reveal patterns of plant defence against the inoculated with 100 second-stage juveniles/1.5

pathogen. Histology is an eﬃcient resource in ml of water and covered with the substrate. Plants

infection processes, helping to elucidate penetration developed in a greenhouse (temperature 25 ±

and colonisation events, and can reveal structural 2 °C; photoperiod 14 h) and were uprooted 60

host defence mechanisms (Bentes & Matsuoka, days after inoculation. The radical systems were

2

005; Petitot et al., 2017; Lopes et al., 2020). The washed to remove soil particles, ﬁxed in FAA

reaction to FRKN infection of diﬀerent commercial (formalin, glacial acetic acid, ethyl alcohol) for

and/or experimental pepper lines, some carrying 48 h and transferred to 70% ethyl alcohol. From

RKN-resistance genes, has been poorly evaluated the diﬀerent treatments, ﬁrst-order lateral root

152

V. A. Cabrera et al. - Histopathological response of pepper to nematode Nacobbus celatus

galls of the four cultivars and fragments (1 cm) of

Diﬀerences were observed between populations,

healthy roots were randomly selected. They were especially with higher development of LO feeding

dehydrated in an ascending series of ethyl alcohol sites. For that population, the syncytial cells in

and embedded in Histowax. Cross-sections of 8-10 contact with the anterior region of the female

µm thick were made with a rotating microtome showed thickened and ligniﬁed walls in Fyuco

and adhered with distilled water to clean slides. INTA (Fig. 2A). In the same cultivar infected

After 24 h, the inclusion medium was removed by RC, only well-developed but non-functional

with xylol; the slides were stained with the triple syncytia were found (Fig. 2B) and the presence

stain (hematoxylin-safranin-permanent green) and of abundant numbers of juveniles in the cortex

mounted in distyrene, tricresyl phosphate and was also noted (Fig. 2C). In galls induced by the

xylene (DPX) (Conn et al., 1960; Zarlavsky, 2014). RC population on the three commercial cultivars,

Observations and photographs were taken with a the development of hyperplastic tissue with

Carl Zeiss Axiophot microscope equipped with an parenchymatic features in the central cylinder was

AxioCam HRC camera.

prominent (Fig. 2C). In Fenomeno RZ, although

the feeding sites of both populations were highly

developed, the cytological characteristics did not

denote great metabolic activity, since they had

low density in their cytoplasmic content and were

reSultS

Healthy roots of all tested pepper cultivars highly vacuolated (Fig. 2D); the most hypertrophic

exhibited a primary structure, with a normal nuclei were observed in the syncytia related to LO.

arrangement of the dermal, fundamental, and Table 1 summarizes the main diﬀerences observed

vascular tissue systems. In cross-section, the between the nematode populations and/or the tested

epidermis was unistratiﬁed and the cortex presented commercial cultivars.

3

-4 layers of parenchyma, with large cells and

a thin wall. The endodermis and pericycle were

unistratiﬁed, with cells smaller than those in the diScuSSion and concluSionS

cortex. The metaxylem was located in the centre,

and phloem groups alternate with protoxylem poles

Fig. 1A).

Histopathological studies provide the basis for

investigating the molecular mechanisms underlying

(

All commercial cultivars tested, as well as the speciﬁc interactions between diﬀerent pathogen

positive control, showed galls measuring 2-4 mm genotypes and a particular host genotype (Toulet

along their long axis, induced by the two N. celatus et al., 2022). Due to the lack of FRKN-resistant

populations (Fig. 1B), with development of the pepper genotypes, it is important to investigate the

feeding site (syncytium) in the central cylinder (Fig. response of available cultivars for possible sources

1

C). The syncytial cells had diﬀerent shapes, mainly of resistance that can be used as parents for breeding

isodiametric or elongated. They were hypertrophic programmesorpotentialuseasrootstocks.Ingeneral,

measuring up to 55 µm along their major axis), the commercial cultivars and the control showed the

(

with dense or ﬁbrillar cytoplasm containing some root typical morpho-anatomical alterations induced

vacuoles. The walls were cellulosic, thickened by FRKN in diﬀerent susceptible hosts, including

(>5 µm thick) and presented some interruptions, the pepper: gall formation, hyperplasia reactions,

allowing the conﬂuence of the cytoplasm in the development of syncytia in the central cylinder

syncytium. Nuclei and nucleoli were hypertrophic; (Moyetta et al., 2007; Tordable et al., 2007), and

on some occasions, nuclei (1 to 3 per syncytial cell) disorganisation of vascular tissues (Lax et al.,

exhibited amoeboid contours (Fig. 1D). Xylem 2013; Cabrera et al., 2017; Tordable et al., 2018).

cells were observed immersed in the syncytium, The main characteristics of the syncytial cells also

resulting in reduction and fragmentation of the agreed with previous reports for this nematode,

conductive tissue. The phloem, and sometimes also including thickened and interrupted cellulose walls,

the xylem, was displaced towards the periphery due dense and/or vacuolised cytoplasm, as well as

to the presence of the syncytium and the nematode hypertrophic nuclei, and nucleoli (Vovlas et al.,

female (Fig. 1E-F).

2007; Tordable et al., 2010; Cabrera et al., 2017).

153

Bol. Soc. Argent. Bot. 59 (2) 2024

Fig. 1. Histopathological response of pepper, Capsicum annuum, cultivars to the nematode Nacobbus

celatus from Río Cuarto (RC) and Lisandro Olmos (LO) localities. A: Healthy root; California Wonder. B:

Root system with galls, egg masses are marked with arrows; California Wonder-LO. C: Gall cross-section

containing the female nematode and syncytium; Fyuco INTA-LO. D: Detail of the syncytial cells; single

arrows indicate interruptions in cell walls; Fyuco INTA-LO. E: Xylem reduction and fragmentation; Yatasto-

LO. F: Phloem displacement and disorganisation; Yatasto-RC. Abbreviations= c: cortex; e: endodermis; g:

gall; hy: hyperplastic tissue; n: nucleus; ne: nematode female; nu: nucleolus; p: phloem; sy: syncytium; x:

xylem. Scale bars= A: 100 µm; B: 1.5 mm; C: 10 µm; D-F: 100 µm.

154

V. A. Cabrera et al. - Histopathological response of pepper to nematode Nacobbus celatus

Fig. 2. Histopathological response of pepper, Capsicum annuum, cultivars to the nematode Nacobbus celatus

from Río Cuarto (RC) and Lisandro Olmos (LO) localities. A: Syncytial cells with thickened and ligniﬁed

walls (marked with arrow) around the nematode; Fyuco INTA-LO. B: Well-developed but non-functional

syncytium; Fyuco INTA-RC. C: Nematode juveniles in the gall cortex and hyperplastic tissue; Fyuco INTA-

RC. D: Syncytium with low metabolic activity; Fenomeno RZ-RC. Abbreviations= hy: hyperplastic tissue; j:

juveniles; ne: nematode female; sy: syncytium; x: xylem. Scale bars= A-D: 100 µm.

Table 1. Main histopathological characteristics observed in commercial pepper, Capsicum annuum,

cultivars parasitised by two Nacobbus celatus populations.

Nematode population/Pepper cultivar

Histological response

Río Cuarto

Lisandro Olmos

Thickened and ligniﬁed cell walls associated with females

Well developed but non-functional syncytia

Juveniles in the cortex

-

Fyuco INTA

-

Hyperplastic tissue in central cylinder

Syncytia with low metabolic activity

Fyuco INTA, Yatasto, Fenomeno RZ

Fenomeno RZ

-

Fenomeno RZ

155

Bol. Soc. Argent. Bot. 59 (2) 2024

The syncytial feeding sites produced by tomato cultivars marketed, as “nematode resistant”

Nacobbus species closely resemble those induced (without specifying the genus and/or species),

by cyst nematodes (abbreviation CN) and diﬀer cell thickening was also observed in the syncytial

signiﬁcantly from the giant cells induced by RKN and parenchyma cell walls surrounding N. celatus

(Eves-van den Akker et al., 2014). In CN, the ﬂow females, diﬀering from a susceptible cultivar tested

of solutes from the xylem vessels is a limiting factor (Cabrera et al., 2017). In infections with other plant-

for feeding site eﬃciency; for that reason, contact parasitic nematode species, secondary thickening

and connection with the xylem vessels are crucial of the cell walls surrounding the parasite and egg

for their development. The developing syncytia masses has also been reported as a defence reaction

are initially isolated and rely on transport proteins of the plant (Rosso et al., 2004; Hernández-López

for nutrients but then simplasmically connect to et al., 2006; Lomelí-Rosario et al., 2009).

the nutrient-dense phloem (Levin et al., 2020). In

Another difference between populations

FRKN, the initial syncytial cell undergoes local wall observed at Fyuco INTA was the detection of

dissolution, and its protoplast fuses with those of the abundant juveniles in the gall cortex and large, non-

neighbouring cells, which are then incorporated into functional syncytia in plants parasitised by RC. The

the syncytium (Eves-van den Akker et al., 2014). presence of non-functional syncytia may indicate

An unusually high frequency of plasmodesmata a faster invasion and multiplication of individuals

between syncytial cells and neighbouring phloem from the population on this host; the juveniles

elements was also reported in the Nacobbus genus found in the gall cortex would correspond to a

(Jones & Payne, 1977). Our results conﬁrm that new re-infection in the roots from the egg masses.

the feeding sites induced by N. celatus maintain This could be explained by the fact that the RC

close contact mainly with the xylem but also with population has a higher degree of aggressiveness,

the phloem. In addition, it was observed that they being able to evade or suppress the Fyuco INTA

incorporate xylem vessels, such as reported in other defence response observed at the histopathological

Solanaceae species parasitised by FRKN, as the level in LO. It would be interesting to conduct

tomato (Solanum lycopersicum L.) and the potato further studies to understand the molecular and

(S. tuberosum L.) (Tordable et al., 2010, 2018). cellular mechanisms involved in host-specific

This could support parasite development and/ resistance against diﬀerent N. celatus populations

or contribute to maintaining high turgor pressure on the same host.

within the syncytia (Levin et al., 2020).

Moyetta et al. (2007) evaluated the

Although all tested peppers were eﬃcient hosts histopathology of commercial and experimental

for both N. celatus populations, histopathological pepper cultivars with resistance genes against

studies in some cases revealed diﬀerences either RKN infected by N. celatus. However, no morpho-

between the populations or between cultivars. anatomical evidence indicating any degree of

Fyuco INTA infected with RC showed syncytial tolerance or resistance was found. According to the

cells with cellulose walls surrounding the supplier, Fenomeno RZ carries resistance to RKN.

nematodes. However, this cultivar parasitised In rice, Oryza glaberrima Steud., lines resistant to

by LO showed thickened and ligniﬁed syncytial M. graminicola (Petitot et al., 2017) and cowpea,

cell walls associated with the anterior region Vigna unguiculata (L.) Walp., carrying the Rk

of the females, evidencing a defensive reaction gene with resistance to RKN (Das et al., 2008),

by the plant. Ligniﬁcation and suberisation are highly vacuolated feeding sites (giant cells) with

host responses that stop and prevent infection of low cytoplasmic density were observed, indicating

plant tissues (Lomelí-Rosario et al., 2009). The low metabolic activity compared to feeding sites

defence response detected by histopathology for of susceptible cultivars. The same characteristics

LO is reﬂected in the lower multiplication rate were observed in Fenomeno RZ, which could be

(Reproduction Factor: abbreviation RF) previously attributed to its resistance to RKN. Despite this, it

observed, compared to the control (RF Fyuco was still able to provide the necessary nutrients for

INTA LO= 20.4; RF California Wonder= 37.9) and the development of N. celatus, as high RF values

the RC population (RF Fyuco INTA LO= 20.4; have previously been observed for both populations

RF Fyuco INTA RC= 41.5) (Lax et al., 2016). In multiplied on this cultivar (Lax et al., 2016).

156

V. A. Cabrera et al. - Histopathological response of pepper to nematode Nacobbus celatus

In the present work, the variability in the response

of the same population to diﬀerent pepper cultivars

and histopathological diﬀerences between populations

of FRKN were demonstrated. This highlights the

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