Meloidogyne Species Associated with Weeds in Rio Grande do Sul

Espécies de Meloidogyne Associadas a Plantas Daninhas no Rio Grande do Sul

ABSTRACT:

The frequency of species of root-knot nematodes (Meloidogyne spp.) was evaluated in weeds collected in different fallow farms in the State of Rio Grande do Sul, Brazil. In the samples where the nematode was found, the species of the root-knot nematode was identified by electrophoresis using the isozyme esterase. They were obtained from weeds belonging to 24 weed species from 13 different botanical families: Amaranthaceae, Asteraceae, Commelinaceae, Convovulaceae, Cyperaceae, Euphorbiaceae, Lamiaceae, Malvaceae, Oxalidaceae, Poaceae, Portulacaceae, Solanaceae, Verbenaceae. Meloidogyne javanica Est J3 (Rm: 1.0, 1.25, 1.40) was the most frequent species and occurred in 53.3% of the samples. M. arenaria with phenotype Est. A2 (Rm: 1.20, 1.30) was detected in 15.6% of the samples. M. incognita Est. I2 (Rm: 1.0, 1.1), M. ethiopica Est. E3 (Rm: 0.9, 1.15, 1.30), M. enterolobii Est. M2 (Rm: 0.7, 0.75, 0.9, 0.95) and M. hapla Est. H1 (Rm: 1.17) in 13.3%, 8.9%, 6.7% and 2.2% of the samples, respectively. Therefore, knowledge of the range of host plants to different species of the root-knot nematode can positively contribute to the adoption of management practices that allow the reduction of their populations in the soil.

Keywords:
root-knot nematode; weed plants; isozyme esterase; characterization; hostability

RESUMO:

A frequência de espécies do nematoide-das-galhas (Meloidogyne spp.) foi avaliada em plantas daninhas coletadas em diferentes lavouras em pousio do Estado do Rio Grande do Sul, Brasil. Nas amostras onde o nematoide foi encontrado, a identificação das espécies do nematoide-das-galhas foi feita por eletroforese, utilizando-se a isoenzima esterase. Elas foram obtidas de plantas daninhas pertencentes a 24 espécies de 13 famílias botânicas diferentes, sendo elas: Amaranthaceae, Asteraceae, Commelinaceae, Convovulaceae, Cyperaceae, Euphorbiaceae, Lamiaceae, Malvaceae, Oxalidaceae, Poaceae, Portulacaceae, Solanaceae and Verbenaceae. Meloidogyne javanica Est J3 (Rm: 1.0, 1.25, 1.40) foi a espécie mais frequente e ocorreu em 53,3% das amostras. M. arenaria com fenótipo Est. A2 (Rm: 1.20, 1.30) foi detectada em 15,6% das amostras. Também foram identificadas M. incognita Est. I2 (Rm: 1.0, 1.1), M. ethiopica Est. E3 (Rm: 0.9, 1.15, 1.30), M. enterolobii Est. M2 (Rm: 0.7, 0.75, 0.9, 0.95) and M. hapla Est. H1 (Rm: 1.17) in 13.3%, 8.9%, 6.7% and 2.2% of the samples, respectively. Portanto, o conhecimento da gama de plantas hospedeiras de diferentes espécies do nematoide-das-galhas pode contribuir de forma positiva para adoção de práticas de manejo que possibilitem a redução de suas populações no solo.

Palavras-chave:
nematoide-das-galhas; plantas infestantes; isoenzima esterase; caracterização; hospedabilidade

INTRODUCTION

The presence and interference of phytonematodes in agricultural areas is responsible for causing limitations to cropping systems, yield reduction and loss of quality of the resulting products. Among the major species, root-knot nematodes of the genus Meloidogyne are the most important group worldwide, mainly because of the wide variety of hosts, which may exceed 3,000 species of wild and cultivated plants (Hussey and Janssen, 2002; Moens and Perry, 2009). More than 100 species have been described for this genus. M. arenaria, M. hapla, M. incognita and M. javanica are the ones with the largest presence, accounting for about 95% of all infestations in agricultural areas (Brito et al., 2008).

In Brazil, species of Meloidogyne spp. are widely distributed in the different regions; moreover, they cause very severe damage and are difficult to control; therefore, annual and perennial crops, including soybeans, coffee, tomatoes, grapevines, sugarcane and cucumber, are subject to significant damage (Moens and Perry, 2009; Bellé et al., 2017a; Schmitt et al., 2018). In cropping areas, there is also a concomitant presence of different weed species. Such species may be parasitized by phytonematodes, and they have an important role in maintenance and multiplication of these specimens, especially during between harvests, where they are the predominant hosts in agricultural areas (Bellé et al., 2017b).

In addition, weeds multiply and ensure the maintenance of phytopathogenic organisms, including nematodes. Weeds pose a serious problem in agricultural production and can affect crops through competition for light, space, water and nutrients, as well as through release of allelopathic substances that interfere with plant growth and development (Santos and Cury, 2011; Gharabadiyan et al., 2012). In addition, the main weeds present in agricultural crops are resistant to herbicides, which increases their potential for damage and may reduce crop yield by more than 80% under high infestation conditions, depending on the occurring species (Carvalho et al., 2011). When weeds occur in areas affected by nematodes, their harmful potential is even higher, as they multiply these parasites and hinder the adoption of efficient control measures (Singh et al., 2010).

Species of the genus Meloidogyne are the group of phytonematodes with the highest frequency of infestation in weed roots (Ferraz et al., 1978). In this context, different weed species have been recognized as hosts of Meloidogyne spp. in different regions of the world and in Brazil (Mônaco et al., 2009; Kaspary et al., 2016; Groth et al., 2017). The problem of weeds as alternative hosts of these nematodes is particularly severe in subtropical and tropical environments, where weeds grow year-round (Kokalis-Burelle and Rosskopf, 2012). This fact leads to an increase of nematode populations in the soil, making it difficult to control them and aggravating the resulting damage in agricultural crops.

In view of the high polyphagic potential of phytonematode species of the genus Meloidogyne, knowledge of their wide range of host weeds is of paramount importance to select proper practices to manage these plant parasites. Thus, the aim of this research was to detect the presence of different species of nematodes of the genus Meloidogyne in different weeds in 15 towns of Rio Grande do Sul state, Brazil.

MATERIAL AND METHODS

Sampling took place in 15 towns of the state of Rio Grande do Sul, in fallow areas, from March to May 2018, in a total of 45 samples. Root samples were collected individually and stored in labeled plastic bags and taken to the Soil Biology Laboratory, Federal University of Santa Maria, for observations, analysis and recording of data. Weeds were identified and classified according to Lorenzi (2013).

Subsequently, 40 milky-white Meloidogyne sp. females were extracted from each weed root sample. Each female was then macerated in a capillary tube with 2-3 mL of extraction buffer for the enzyme esterase (sucrose buffer). Next, the protein extract from each sample underwent horizontal electrophoresis, according to the methodology described by Carneiro and Almeida (2001). The respective species (s) of Meloidogyne sp. were identified by esterase polymorphism (Est) in 7% polyacrylamide gel. As the standard of the enzyme esterase, the protein extract of five females from a pure population of M. javanica (Est J3) was included in the gel (Carneiro and Almeida, 2001). Relative mobility (Rm) values of the polymorphic bands were calculated based on the first band of the standard M. javanica. The enzymatic phenotypes were tagged with a letter and a number, corresponding, respectively, to the name of each species and the number of bands with esterase activity (Esbenshade and Triantaphyllou, 1990). After that, the root samples were processed by the method of Coolen and D ‘Herde (1972) by adding sodium hypochlorite to determine nematode population density per gram of root under an optical microscope.

RESULTS AND DISCUSSION

The study identified 24 weed species from 13 botanical families in the study areas infested with Meloidogyne sp. (Table 1). Weed species present in the different collection sites were only identified when they had root galls, namely: Ageratum conyzoides (goatweed), Alternanthera tenella (sanguinaria), Amaranthus hybridus (red amaranth), Amaranthus spinosus (spiny amaranth), Amaranthus viridis (slender amaranth), Bidens pilosa (hairy beggarticks), Chenopodium album (ÿþlamb’s quarters), Commelina benghalensis (Benghal dayflower), Cyperus rotundus (purple nutsedge), Echinochloa colonum (jungle rice), Eclipta alba (false daisy), Euphorbia heterophylla (fireplant), Galinsoga parviflora (potato weed), Ipomoea grandifolia (morning glory), Ipomoea nil (morning glory), Ipomoea purpurea (morning glory), Leonurus sibiricus (honeyweed), Oxalis corniculata (creeping woodsorrel), Portulaca oleracea (common purslane), Sida rhombifolia (arrowleaf sida), Solanum americanum (American black nightshade), Solanum pseudocapsicum (Jerusalem cherry), Solanum sisymbriifolium (sticky nightshade) and Verbena litoralis (ÿþseashore vervain) (Table 1).

Table 1
Meloidogyne populations, number of Meloidogyne per gram of root (NMGR) and esterase (EST) phenotype diagnosed from root samples of different weeds collected in 15 towns of Rio Grande do Sul, Brazil

Town	Scientific name	NMGR	EST	Meloidogyne species
Alpestre	Leonurus sibiricus	560	I2	M. incognita
	Ipomoea nil	318	H1	M. hapla
	Ageratum conyzoides	210	I2	M. incognita
	Echinochloa colonum	138	I2	M. incognita
Cachoeira do Sul	Solanum pseudocapsicum	675	M2	M. enterolobii
	Sida rhombifolia	350	M2	M. enterolobii
	Portulaca oleracea	476	M2	M. enterolobii
Caiçara	Amaranthus spinosus	674	J3	M. javanica
	Ipomoea nil	275	J3	M. javanica
Cruz Alta	Oxalis corniculata	502	J3	M. javanica
	Euphorbia heterophylla	210	J3	M. javanica
	Solanum americanum	980	J3	M. javanica
	Cyperus rotundus	242	J3	M. javanica
Frederico Westphalen	Galinsoga parviflora	518	I2	M. incognita
	Commelina benghalensis	210	J3	M. javanica
	Oxalis corniculata	340	E3	M. ethiopica
Ijuí	Ipomoea grandifolia	196	I2	M. incoginta
	Solanum americanum	374	I2	M. incognita
Novo Barreiro	Ipomoea grandifolia	620	A2	M. arenaria
	Portulaca oleracea	120	A2	M. arenaria
	Amaranthus viridis	540	A2	M. arenaria
	Chenopodium album	380	A2	M. arenaria
Palmeira das Missões	Amaranthus viridis	652	J3	M. javanica
	Amaranthus hybridus	450	J3	M. javanica
	Verbena litoralis	338	J3	M. javanica
Panambi	Eclipta alba	420	J3	M. javanica
	Solanum sisymbriifolium	204	J3	M. javanica
Santa Rosa	Portulaca oleracea	682	J3	M. javanica
	Bidens pilosa	130	J3	M. javanica
	Echinochloa colonum	430	J3	M. javanica
Santo Ângelo	Ipomoea nil	540	J3	M. javanica
	Bidens pilosa	130	J3	M. javanica
Sarandi	Euphorbia heterophylla	450	A2	M. arenaria
	Portulaca oleracea	250	A2	M. arenaria
	Commelina benghalensis	206	A2	M. arenaria
Seberi	Alternanthera tenella	98	J3	M. javanica
	Commelina benghalensis	375	J3	M. javanica
	Sida rhombifolia	690	J3	M. javanica
Tupanciretã	Commelina benghalensis	1250	J3	M. javanica
	Ipomoea purpurea	565	J3	M. javanica
	Sida rhombifolia	670	J3	M. javanica
	Amaranthus hybridus	850	J3	M. javanica
Vicente Dutra	Sida rhombifolia	502	E3	M. ethiopica
	Ipomoea purpurea	374	E3	M. ethiopica
	Oxalis corniculata	632	E3	M. ethiopica

A total of 45 populations of Meloidogyne spp. were collected from the infected weed species, and six different esterase phenotypes were identified, corresponding to M. javanica Est. J3 (Rm: 1.0, 1.25, 1.40), M. arenaria Est. A2 (Rm: 1.20, 1.30), M. incognita Est. I2 (Rm: 1.0, 1.1), M. ethiopica Est. E3 (Rm: 0.9, 1.15, 1.30), M. enterolobii Est. M2 (Rm = 0.7, 0.75, 0.9, 0.95) and M. hapla Est. H1 (Rm: 1.17).

The most common root-knot nematode species was M. javanica, corresponding to 53.3%, identified in A. tenella, A. spinosus, A. viridis, B. pilosa, C. benghalensis, C. rotundus, E. colonum, E. alba, E. heterophylla, I. nil, I. purpurea, O. corniculata, P. oleracea, S. rhombifolia, S. americanum, S. sisymbriifolium and V. litoralis. For this nematode species, the number of second stage juveniles (J2) per gram of root ranged from 130 in B. pilosa to 1,250 in C. benghalensis, in the towns of Santo Ângelo and Tupaciretã, respectively. The species M. arenaria was detected in A. viridis, C. album, C. benghalensis, E. heterophylla, I. grandifolia and P. oleracea, corresponding to 15.6% of the analyzed samples, ranging from 120 to 620 J2 per gram of root. M. incoginta was found in 13.3% of the samples, in I. grandifolia, A. conyzoides, E. colonum, S. americanum, G. parviflora and L. sibiricus; the latter weed had the highest number of nematodes per gram of root: 560 specimens.

In this study, M. ethiopica (8.9%) was found in I. purpurea, O. corniculata and S. rhombifolia. M. hapla was detected in only one sample of I. nil (2.2%) in the town of Alpeste, where 318 J2 per gram of root were found. M. enterolobii was also found in 6.7% of the samples of P. oleracea, S. rhombifolia and S. pseudocapsicum collected in the town of Cachoeira do Sul, with 476, 350 and 675 specimens per gram of root, respectively (Table 1).

The presence of populations of Meloidogyne sp. in different weed species is indicative of the high level of polyphagia in this group of parasites, and corroborates previous studies that have reported their presence in several plant species (Hussey and Janssen, 2002; Moens and Perry, 2009). Thus, during weed management in agricultural areas, it is not feasible to prioritize the control of one weed species over another when it comes to reducing the phytonematode population. In this context, in the town of Cruz Alta, the species M. javanica was found parasitizing weeds of four different taxonomic families (Table 1): O. corniculata O. corniculata (Oxalidaceae), E. heterophylla (Euphorbiaceae), S. americanum (Solanaceae) and C. rotundus (Cyperaceae), indicating nonspecific parasite capacity and the need to control all weeds in areas with Meloidogyne (Table 1).

The high frequency of M. javanica infesting weeds, i.e., in more than 50% of the evaluated samples, shows its highest incidence in the different towns sampled. This high incidence has also been reported in a survey of 226 weeds, 49 of which were parasitized by M. javanica (Rich et al., 2009). Soybean is the main agricultural crop of the sampled municipalities, which may explain the higher incidence of this species. M. javanica, since it is most often found parasitizing this crop (Kirsch et al., 2016). Thus, weeds that are often present and problematic in soybean, because of competition for environmental resources, are also frequently parasitized by these nematodes, as is the case with Amaranthus sp., Ipomoea sp., Bidens pilosa, C. benghalensis and S. rhombifolia (Table 1).

Nematodes of the species M. arenaria were detected in 15.6% of the weed samples, especially in Sarandi and Novo Barreiro, which are neighboring towns; this is indicative that they are distributed in the region. The species A. viridis and E. heterophylla showed the largest number of M. areanaria specimens: 540 and 450 specimens per gram of root, respectively (Table 1). Corroborating the findings of this research, this species of nematodes has already been reported parasitizing several weeds, e.g., P. oleracea, Aeschynomene americana and A. viridis (Kokalis-Burelle and Rosskopf, 2012; Kaspary et al., 2016).

The species M. incoginta was found in 13.3% of the samples, in I. grandifolia, A. conyzoides, E. colonum, G. parviflora, L. sibiricus and S. americanum (Table 1). This result is different from the usually high proliferation of this species in weeds as well as its ability to parasitize more than 25 native weeds from Rio Grande do Sul (Bellé et al., 2017b). However, this low occurrence may result from the absence of weeds preferentially infested by M. incoginta, as a result of good management of invasive species. There was also a weak presence of other nematode species: 8.9%, 2.2% and 6.7% for M. ethiopica, M. hapla and M. enterolobii, respectively. These species were the least frequent in the cropping systems adopted in the sampled areas.

Infestation of common weeds by root-knot nematodes in various crops increases the harmful potential of such weeds. Other factors include the ability to compete for environmental resources, release allelochemicals and reduce the quality of the end product and the potential of these parasites to multiply. Therefore, it is difficult to adopt efficient control measures (Singh et al., 2010). For this reason, it is essential to adopt management practices that allow proper control of these weeds in order to reduce the population of this pathogen (Singh et al., 2013; Bellé et al., 2017a). Thus, integrated management strategies should be adopted for management of Meloidogyne sp., considering weeds as a source of inoculum for these parasites. Thus, chemical or cultural weed control, crop choice decisionsÿþ and intercropping of cultivated species in infested areas are of paramount importance for successful management of root-knot nematodes.

Therefore, weed control is a very important practice for management of nematodes, during the crop cycle and between harvests, in order to control the host and prevent the reproduction of this parasite, thus reducing damage caused to commercial crops (Singh et al., 2014; Bellé et al., 2017b). Furthermore, broader knowledge of the range of alternative hosts of Meloidogyne sp., especially in weeds, can aid the adoption of more effective pathogen management measures and enhances crop results.

REFERENCES

• Bellé, C. Kaspary TE, Groth MZ, Cocco KLT. Meloidogyne ethiopica parasitizing melon fields in Rio Grande do Sul State, Brazil. J Plant Dis Prot. 2017a;124:393-7.
• Bellé C, Kulczynski SM, Kaspary TE, Kuhn PR. Plantas daninhas como hospedeiras alternativas para Meloidogyne incognita Nematropica. 2017b;47:26-33.
• Brito JA, Kaur R, Çetintaº R, Stanley JD. Identification and isozyme characterization of Meloidogyne spp. infecting horticultural and agronomic crops, and weed plants in Florida. Nematology. 2008;10(5):757-66.
• Carneiro RMD, Almeida MRA. Técnica de eletroforese usada no estudo de enzimas dos nematóides de galhas para identificação de espécie. Nematol Bras. 2001;25:35-44.
• Carvalho LB, Bianco S, Galati VC, Martins TAL, Sousa EM, Calha I, Moreira I, et al. Determination of Merremia cissoides leaf area based on linear measures of the leaflets. Acta Sci Agron. 2011;33:473-6.
• Coolen WA, D’herde CJ. A method for the quantitative extraction of nematodes from plant tissue. Ghent: State Nematology and Entomology Research Station; 1972. 77p.
• Esbenshade PR, Triantaphyllou AC. Isoenzyme phenotypes for the identification of Meloidogyne species. J Nematol. 1990;22:10-15.
• Ferraz LCCB, Pitelli RA, Furlan V. Nematóides associados a plantas daninhas na região de Jaboticabal, SP - primeiro relato. Planta Daninha. 1978;1:5-11.
• Gharabadiyan F, Jamali S, Yazdi AA, Hadizadeh MH, Eskandari Al. Weed hosts of root-knot nematodes in tomato fields. J Plant Protec Res. 2012;52(2):230-4.
• Groth MZ, Bellé C, Cocco KLT, Kaspary TE, Casarotto G, Cutti L. et al. First report of Meloidogyne enterolobii infecting the weed jerusalem cherry (Solanum pseudocapsicum) in Brazil. Plant Disease. 2017;101(3):510.
• Hussey RS, Janssen GJW. Root-knot nematodes: Meloidogyne species. In: Starr JL, Cook R, Bridge J, editors. Plant resistance to parasitic nematodes. Wallingford: CAB International, 2002. p.43-70.
• Kaspary TE, Bellé C, Groth MZ, Cocco KLT, Cutti L, Casarotto G. Amaranthus viridis is a weed host of Meloidogyne arenaria in Rio Grande do Sul State, Brazil. Plant Dis. 2016;101(4):635.
• Kirsch VG, Kulczynski SM, Gomes CB, Bisognin AC, Gabriel M, Bellé C, et al. Caracterização de espécies de Meloidogyne e de Helicotylenchus associadas à soja no Rio Grande do Sul. Nematropica. 2016;46(2):197-208.
• Kokalis-Burelle N, Rosskopf EN. Susceptibility of several common subtropical weeds to Meloidogyne arenaria, M. incognita, and M. javanica J Nematol. 2012;44:142-7.
• Lorenzi H. Plantas daninhas do Brasil. 4ª.ed. Nova Odessa: Instituto Plantarum; 2013.
• Moens M, Perry R. Migratory plant endoparasitic nematodes: A group rich in contrasts and divergence. Ann Rev Phytopathol. 2009;37:313-32.
• Mônaco APA, Carneiro RG, Kranz WM, Gomes JC, Scherer A, Santiago DC. Reação de espécies de plantas daninhas a Meloidogyne incognita Raças 1 e 3, a M. javanica e a M. paranaensis Nematol Bras. 2009;33(3):235-42.
• Rich JR, Brito JA, Kaur R, Ferrell JA. Weed species as hosts of Meloidogyne: A review. Nematropica. 2009;39(2):157-85.
• Santos JB, Cury JP. Black jack: a special weed in tropical soils. Planta Daninha. 2011;29:1159-71.
• Schmitt J, Bellé C, Jacques RJS, Cares JE, Antoniolli ZI. Detection of Meloidogyne arenaria in cucumber in Rio Grande do Sul state, Brazil. Austr Plant Dis Notes. 2018:13:8.
• Singh SK, Paini DR, Ash GJ, Hodda M. Prioritising plant-parasitic nematode species biosecurity risks using self organising maps. Biol Invas. 2014;16(7):1515-30.
• Singh SK, Ash GJ, Banks NC. Plant parasitic nematodes as invasive species: characteristics, uncertainty and biosecurity implications. Ann Appl Biol. 2013;163(3):323-50.
• Singh SK, Khurma UR, Lockhart PJ. Weed hosts of root-knot nematodes and their distribution in fiji. Weed Technol. 2010;24(3):607-61.

Publication Dates

• Publication in this collection
  30 Sept 2019
• Date of issue
  2019

History

• Received
  18 Sept 2018
• Accepted
  31 Oct 2018