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Crop Protection 25 (2006) 440–445

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Characterization of Meloidogyne incognita, M. arenaria and M. haplapopulations from Spain and Uruguay parasitizing pepper

(Capsicum annuum L.)

Lee Robertsona,�, Jose A. Lopez-Pereza, Antonio Belloa, Miguel A. Dıez-Rojoa,Miguel Escuera, Ana Piedra-Buenaa, Caridad Rosb, Casimiro Martıneza

aDpto Agroecologıa, Centro de Ciencias Medioambientales, CSIC. Serrano 115 dpdo, 28006 Madrid, SpainbDpto Proteccion Vegetal, IMIDA, Consejerıa de Agricultura, Agua y Medio Ambiente. Mayor s/n, 30150, La Alberca, Murcia

Received 1 April 2005; received in revised form 12 July 2005; accepted 14 July 2005

Abstract

A total of 136 populations of Meloidogyne arenaria, M. hapla, M. incognita and M. javanica were collected from infected soil from

representative horticultural regions of Spain and Uruguay, and evaluated in a bioassay designed to characterize the virulence on

cultivars of pepper, tomato, cotton, tobacco and watermelon. None of the of M. arenaria race 2 or M. javanica populations

parasitized any of the resistant pepper cultivars used, but all of the M. hapla populations reproduced on resistant peppers. Forty-

three populations were found to parasitize both susceptible and resistant pepper cultivars, of those, 37 populations belonged to M.

incognita (all races), one to M. arenaria (new race 3), and five to M. hapla races A and B. Seventeen of the M. incognita populations

that were virulent on resistant pepper did not parasitize the resistant tomato cv. Nikita containing the Mi gene. The results obtained

have important implications for the design of alternative nematode management strategies using resistant cultivars.

r 2005 Elsevier Ltd. All rights reserved.

1. Introduction

Due to their damaging influence on crop yields on aworld wide scale the root-knot nematodes Meloidogyne

incognita (Kofoid and White, 1919; Chitwoodi, 1949),M. javanica (Treub, 1885; Chitwoodi, 1949), M. arenaria

(Neal, 1889; Chitwoodi, 1949) and M. hapla (Chitwoodi,1949) are economically important pests. Among thepossible non-chemical control strategies, the use ofresistant cultivars is preferred, but in order to besuccessful it is necessary to characterize the virulencerange of the nematode population. Pepper (Capsicum

annuum L.) and tomato (Lycopersicon esculentum L.)cultivars were chosen for this study due to theireconomic importance, and also because there are fewcrops in which nematode resistance is available. The test

e front matter r 2005 Elsevier Ltd. All rights reserved.

opro.2005.07.008

ing author. Tel.:+3491 7452500; fax: +3491 5640800.

ess: lee.r@ccma.csic.es (L. Robertson).

of Hartman and Sasser (1985) for characterizing racesand species of the genus Meloidogyne does not allowcharacterization of virulent populations, as resistantpepper and tomatoes are not included. In this study, weexpanded upon the test plant range of Hartman andSasser (1985) to include nematode-resistant pepper andtomato cultivars. The virulence/avirulence characteris-tics of a range of Meloidogyne populations used in thesehost range tests are presented.

In reviewing the literature related to resistance againstroot-knot nematodes in pepper, Hare (1956, 1957)identified pepper cultivars which were resistant toM. incognita, M. javanica and M. arenaria, and foundthat this resistance was conferred by a single dominantgene designated as the N gene. Hare (1966) backcrossedthe N gene into pepper and obtained the cv. MississippiNemaheart, one of the most widely grown peppercultivars. Hendy et al. (1985a, b) found five differentgenes in C. annuum which conferred resistance to

ARTICLE IN PRESSL. Robertson et al. / Crop Protection 25 (2006) 440–445 441

M. arenaria, M. incognita and M. javanica, the majorgenes being Me1, Me2 and Me3. Di Vito et al. (1993)found pepper cultivars resistant to M. arenaria race 2,M. incognita races 1 and 2, and M. javanica but not toM. hapla, confirming that the resistance is conditionedby a single dominant gene. Fery and Dukes (1996) andFery et al. (1998) suggested that resistance in pepper cv.Carolina Hot and Nemaheart is conditioned by twogenes, one dominant and the other recessive; there mayexist another gene in Carolina Hot that would explainits greater level of resistance. Upon infection withM. incognita races 1 and 3, Carolina Hot andNemaheart exhibited a low root galling level. Feryet al. (1998) and Thies and Fery (2000a, b) obtained thefirst bell pepper cultivars, Charleston Belle and CarolinaWonder, resistant to M. incognita.

The N gene in C. annuum confers resistance toM. arenaria races 1 and 2 and to M. javanica but notto M. hapla. Peppers carrying the Me1 gene are resistantto populations of M. arenaria, M. incognita andM. javanica, and virulent populations of M. arenaria

and M.incognita can parasitize peppers containing theMe3 gene (Castagnone-Sereno et al., 2001). Thedominant gene Me3 confers a thermostable resistanceagainst Meloidogyne in pepper with another gene Me4

linked to Me3 (Djian-Caporalino et al., 2001; Thies andFery, 2002a).

Since 1994, we have been studying the virulence of arange of root-knot nematode populations from thehorticultural regions of Spain and Uruguay, with theaim of identifying resistant pepper cultivars to controlMeloidogyne species and have concluded that it isnecessary to develop an appropriate biotest adaptedfor pepper and tomato crops. At present it is notpossible to separate virulent populations from avirulentpopulations by the use of molecular markers as to dateno DNA polymorphisms linked to virulence have beenfound (Semblat and Castagnone-Sereno, 2001).

The main goal of this study was to identify andcharacterize Meloidogyne populations, which repro-duced on resistant peppers.

2. Materials and methods

Isolation and propagation of nematode populations:Susceptible tomato plants cv. Marmande, with two trueleaves, approximately 20 d after germination, weretransplanted to five pots containing 300 g of sterilesandy soil. One week later, the pots were inoculated witha single egg mass from each of the original fieldpopulations. The characterization of each isolate, usinga bioassay modified from the North Carolina differ-ential host test, was conducted when susceptible tomatoroots exhibited a galling index of Xfive (on a scale of0–10 where 0 ¼ no nematodes, 1–4 ¼ galling of second-

ary roots, and 5–10 ¼ galling of primary lateral and taproots with an index of 5 indicating that 50% of the rootsare galled) to ensure a sufficient level of soil infestation(Bridge and Page, 1980).

The original North Carolina differential host test didnot contain resistant peppers or resistant tomatoes. In amodified bioassay, the three resistant peppers, cvs.Charleston Belle, Carolina Wonder (Fery et al., 1998),and Atlante (Arnedo S.A.) and the resistant tomato cv.Nikita were also included, along with cotton DP 61 andtobacco NC 95. The peanut cultivar Florunner was notincluded, as it only allows the separation of the tworaces in M. arenaria, which can also be separated usingpepper (Hartman and Sasser, 1985). All experimentswere conducted in a growth chamber at 24 1C (71 1C)and 16 h photoperiod with a daily watering regime, forat least 45 d to allow the nematodes to complete their lifecycle. After 45 d, the plant roots were examined for thepresence of galls and scored. Roots containing eggmasses were used as inoculum for the next round ofinfection. The process was repeated three times i.e., onepopulation, five replicas and test plants.

Isolates virulent on pepper were grouped as Meloido-

gyne species. A simple statistical analysis of the data wasperformed calculating the average galling indices andstandard deviation from each differential plant, i.e.,susceptible and resistant peppers, susceptible andresistant tomatoes, cotton DP 61 and tobacco NC 95,and from each pot. Only plants with an index of 0 areconsidered to be resistant. Biotypes which parasitizeboth susceptible and resistant peppers were namedPepper, followed by race number (according to Hart-man and Sasser, 1985) and their ability to reproduce i.e.,complete their life cycle on resistant tomatoes carryingthe Mi gene was indicated.

3. Results

A total of 136 populations were studied, of which, 43populations (one M. arenaria, five M. hapla, and 37M. incognita) successfully reproduced on the resistantpepper cultivars, cvs. Charleston Belle, Carolina Won-der and Atlante, as well as the susceptible tomato cv.Marmande and susceptible peppers cvs. Capino andSonar. The isolates were further characterized using thethree differential hosts, resistant tomato cv. Nikita,cotton DP 61 and tobacco NC 95 (Table 1).

The Pepper 1 biotypes parasitize both susceptible andresistant peppers, and suceptible tomatoes. All peppercultivars studied reached galling indices of 5. Cotton,tobacco, and the resistant tomato cv. Nikita werenot hosts of this biotype. Nineteen percent of theM. incognita populations belonged to this group while afurther 13.5% also parasitized the resistant tomato cv.Nikita i.e., biotype Pepper 1-Mi.

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Table 1

Location of Meloidogyne populations used in this study, average galling index on differential hosts and resulting biotypes taking into account the

race scheme of Hartman and Sasser (1985) and the reaction of the populations with the Mi resistance gene

Population and localitya Peppersb Tomatoesc Cotton DP 61 Tobacco NC 95 Biotype

S R S R

Meloidogyne arenaria

(1) Alcanadre (LR) 3.672.1 1.770.7 5.671.2 2.872.9 0 6.171.9 Pepper 3-Mi

M. hapla

(1) Lourizan (PO) 2.871.3 2.872.5 6.771.7 3.871.5 0 2.371.2 A

(2) Gomeserracın (SG) 1.871.0 4.371.5 3.771.5 4.071.4 0 2.772.0 B

(3) Armellada de O.(LE) 4.971.7 2.971.9 7.672.7 1.070 0 1.070 B

(4) Moguer (H) 3.871.3 6.371.1 6.570.5 3.573.5 0 2.070 B

(5) Cartaya (H) 4.472.4 4.472.8 6.472.5 4.773.0 0 4.672.3 A/B

M. incognita

(1) Perello, El (V) 6.771.5 3.071.0 8.471.5 0 0 0 Pepper 1

(2) San Pedro del P. (MU) 7.072.6 5.072.8 8.072.1 0 0 0 Pepper 1

(3) Fuensanta La (AB) 7.070.0 4.072.0 7.172.1 0 0 0 Pepper 1

(4) Santa Eulalia (IB) 6.771.4 5.671.7 7.071.2 0 0 0 Pepper 1

(5) Mirador El (MU) 6.072.6 5.773.0 7.172.6 0 0 0 Pepper 1

(6) Mareny de B. (V) 6.072.8 2.573.0 9.570.7 0 0 0 Pepper 1

(7) Can Bernadet (IB) 5.972.3 6.171.9 7.872.7 0 0 0 Pepper 1

(8) Maraney de B.(V) 6.171.8 3.773.0 8.371.6 8.571.8 0 0 Pepper 1-Mi

(9) San Pedro del P. (MU) 8.272.5 2.070.0 7.971.9 2.572.1 0 0 Pepper 1-Mi

(10) Maraney de B. (V) 1.771.2 3.971.7 4.673.0 8.271.8 0 0 Pepper 1-Mi

(11) Fuensanta La (AB) 6.071.4 7.571.9 8.171.4 3.071.4 0 0 Pepper 1-Mi

(12) Perello El (V) 6.071.5 3.372.6 7.971.4 8.272.3 0 0 Pepper 1-Mi

(13) Fuensanta La (AB) 6.071.4 1.370.6 9.070.9 0 0 6.571.3 Pepper 2

(14) Mirador El (MU) 5.973.1 4.273.6 7.872.0 0 0 1.871.6 Pepper 2

(15) Torreblanca (MU) 7.572.2 5.471.9 8.771.5 0 0 1.571.0 Pepper 2

(16) Santa Eulalia (IB) 5.371.5 1.472.2 4.971.7 0 0 2.772.5 Pepper 2

(17) Mirador El (MU) 6.573.8 8.173.8 7.671.4 0 0 1.570.8 Pepper 2

(18) Armenime, Adeje (TF) 5.070.0 1.771.2 9.071.2 1.570.7 0 4.871.8 Pepper 2-Mi

(19) Mirador El (MU) 6.572.0 7.072.3 6.672.4 2.372.3 0 1.571.1 Pepper 2

(20) Mirador El (MU) 8.070.0 8.073.1 8.171.5 1.470. 9 0 1.971.4 Pepper 2

(21) Maraney de B. (V) 5.272.4 4.572.6 6.872.5 0 4.071.4 0 Pepper 3

(22) Maraney de B.(V) 4.272.2 1.871.3 8.071.6 0 5.571.6 0 Pepper 3

(23) Villena (A) 4.371.5 3.572.5 7.672.1 0 3.671.5 0 Pepper 3

(24) Caudete (AB) 7.270.4 5.072.7 7.772.5 0 4.371.5 0 Pepper 3

(25) Armenime, Adeje (TF) 7.071.0 5.372.1 7.873.8 0 4.070.0 0 Pepper 3

(26) San Lucar de B. (CA) 4.571.9 3.371.7 4.570.7 0 4.572.6 0 Pepper 3

(27) Fuensanta La (AB) 8.470.5 7.571.9 9.071.4 5.473.8 6.270.4 0 Pepper 3-Mi

(28) Salto (UR) 5.572.2 2.672.5 8.671.2 7.172.5 6.070.9 0 Pepper 3

(29) Bella Union (UR) 4.272.5 6.372.0 7.971.6 7.472.3 4.972.3 0 Pepper 3

(30) Villena (A) 4.872.6 1.673.0 6.872.6 2.774.6 4.071.7 0 Pepper 3

(31) Tacuarembo (UR) 4.372.6 4.870.5 6.272.5 0 4.772.1 3.371.5 Pepper 4

(32) Villena (A) 5.272.1 4.071.7 6.573.2 0 4.671.6 1.070.0 Pepper 4

(33) Fuensanta La (AB) 5.674.0 6.072.2 8.571.7 1.370.6 4.071.0 2.571.3 Pepper 4-Mi

(34) Galletas Las, Arona (TF) 4.172.7 5.373.0 7.273.1 2.373.5 2.473.8 7.270.5 Pepper 4-Mi

(35) Fuensanta La (AB) 6.870.5 5.372.7 8.371.7 2.572.1 3.571.2 5.571.3 Pepper 4-Mi

(36) Villena (A) 6.370.6 4.872.6 9.371.2 5.074.2 3.871.3 5.371.5 Pepper 4-Mi

(37) Tacuarembo (UR) 2.070.0 5.073.2 7.772.5 2.671.5 5.070.0 3.072.8 Pepper 4-Mi

a(A) Alicante, (AB) Albacete, (CA) Cadiz, (H) Huelva, (IB) Ibiza, (LE) Leon, (LR) La Rioja, (MU) Murcia, (PO) Pontevedra, (SG) Segovia, (TF)

Tenerife, (UR) Uruguay, (V) Valencia.bSusceptible pepper (S): Capino, Sonar; Resistant pepper (R): Atlante, Carolina Wonder and Charleston Belle.cSusceptible tomato (S): Marmande; Resistant tomato (R): Nikita.

L. Robertson et al. / Crop Protection 25 (2006) 440–445442

The Pepper 2 biotypes parasitized susceptible andresistant peppers, susceptible tomatoes and tobacco.This biotype did not reproduce on cotton or resistanttomato and 13.5% of M. incognita populations studiedbelonged to this group with a further 8.0% of the

populations (designated pepper 2-Mi) reproducing onthe resistant tomato cv. Nikita.

The pepper 3 biotype is characterized as parasitizingboth susceptible and resistant peppers, susceptibletomatoes and cotton. Sixteen percent of M. incognita

ARTICLE IN PRESSL. Robertson et al. / Crop Protection 25 (2006) 440–445 443

populations studied belonged to this group. None of thePepper 3 biotypes reproduced on tobacco or ontomatoes carrying the Mi resistance gene. However,11% of the M. incognita populations contained anMi biotype reproducing on resistant tomato, i.e., Pepper3-Mi.

The Pepper 4 biotype is characterized as parasitizingboth susceptible and resistant peppers, susceptibletomatoes, cotton and tobacco. This group comprised5.5%f the M. incognita populations with a further13.5% of the populations reproducing on the resistanttomato cv. Nikita (Pepper 4-Mi).

The M. arenaria population parasitized susceptibleand resistant peppers, susceptible and resistant toma-toes, and tobacco. These populations did not reproduceon cotton or on peanut cv. Florunner (data not shown)suggesting that it is a new race for this species, i.e.,race 3.

All M. hapla populations reproduced on resistantcultivars of pepper. No differences were found betweenthe cytological races A and B.

There were no obvious correlations between biotypesand geographical origin or crop type.

4. Discussion

The North Carolina differential host test does notallow the characterization of virulence of Meloidogyne

populations because it does not include resistantcultivars of pepper and tomato as differential hosts.Our bioassay however included resistant tomato cv.Nikita which carries the Mi resistance gene, and the

Table 2

Responses of the three Meloidogyne species from this study parasitizing resis

various hosts in a modification of the North Carolina differential host test

Biotype Peppera Tomatob C

S R S R

CA,SO A,CW,CB Marmande Nikita

M. incognita

(1) Pepper 1 + + + � �

(2) Pepper 1-Mi + + + + �

(3) Pepper 2 + + + � �

(4) Pepper 2-Mi + + + + �

(5) Pepper 3 + + + � +

(6) Pepper 3-Mi + + + + +

(7) Pepper 4 + + + � +

(8) Pepper 4-Mi + + + + +

M. arenaria

(1) Pepper 3-Mi + + + + �

M. hapla

(1) Pepper A + + + + �

(2) Pepper B + + + + �

aSusceptible pepper (S): CA ¼ Capino, SO ¼ Sonar; Resistant pepper (R)bSusceptible tomato (S): Marmande; Resistant tomato (R): Nikita.

three resistant pepper cvs. Charleston Belle, CarolinaWonder and Atlante. Much variability in the virulenceof M. incognita was observed even within populationsfrom the same locality.

Forty-four virulent populations of Meloidogyne werefound reproducing on resistant cultivars of pepper, oneof them being M. arenaria, five were M. hapla and 37were M. incognita (Table 1). This confirms previouswork by Dukes and Fery (1997) and Castagnone-Sereno(1999), who reviewed the limitations of using resistantpeppers and tomatoes to manage Meloidogyne becauseof the risk of the appearance of virulent populations.

The fact that none of the M. javanica populationsparasitized any of the pepper cultivars tested (includingthe suceptible cultivars) is agronomically important.Our results thus contrast with previous reports ofM. javanica parasitizing pepper (Santos et al., 1987;Stephan, 1988; Rammah and Hirschmann, 1990; Ah-mad et al., 1998; Khan et al., 2003; Mekete et al., 2003).We note that Hartman and Sasser (1985) found only 7%of 311 M. javanica populations studied were found toparasitize pepper, and all those belonged to M. javanica

race 2. Carneiro et al. (2003) described a new race 4which reproduces on both pepper and peanut. All of theM. hapla populations studied were virulent on pepper,confirming the results of Di vito et al. (1993) and Thiesand Fery (2000a, b, 2002a, b), indicating that cultivars ofpepper carrying the N resistance gene are parasitized byM. hapla.

The tomato cultivars carrying the Mi resistance genewere resistant to four of the M. incognita biotypesvirulent on pepper (Table 2) confirming the results ofCastagnone-Sereno et al. (1996), who demonstrated that

tant pepper, indicating biotype, host race and ability to reproduce on

otton DP 61 Tobacco NC 95 Watermelon CH.Grey Race

� + 1

� + 1

+ + 2

+ + 2

� + 3

� + 3

+ + 4

+ + 4

+ + 3

+ � A

+ � B

: A ¼ Atlante, CW ¼ Carolina Wonder and CB ¼ Charleston Belle.

ARTICLE IN PRESSL. Robertson et al. / Crop Protection 25 (2006) 440–445444

tomatoes carrying the Mi resistance gene resistant to M.

incognita do not reproduce on peppers carrying the Me1

and Me3 resistance genes, whilst virulent populations onpepper carrying the Me3 resistance gene reproduceneither on tomatoes carrying the Mi resistance gene norpeppers with the Me1 resistance gene. This may indicatea specialization of a virulent biotype to the resistantgenes of pepper and tomato, suggesting that a gene forgene relationship may exist between these cultivars ofresistant peppers and tomato and the nematode biotype,but this needs a more extensive study.

From an agricultural perspective, the obsolete butonce widely planted cotton cultivar DP 61 was notparasitized by M. incognita populations that werevirulent on pepper (race 1 and 2), and on tobaccocultivar NC 95 (race 1 and 3), with cotton resistant tothe M. arenaria and M hapla populations (Hartman andSasser, 1985). On the other hand, the virulent popula-tions of M. incognita and M. arenaria parasitize watermelon cv. Charleston Grey. These populations did notreproduce on Tagetes patula, and although a low level ofgalling was observed, nematodes did not produce eggmasses even after prolonged periods in cultivation.

The results obtained are important for the planningand the design of new models of integrated production,allowing available resistance to be utilized to regulatepopulations and retard the development of virulence infield populations (Lacasa et al., 2002; Thies and Fery,2002a; Thies et al., 2004). This methodology, will allowus to characterize Meloidogyne populations from afunctional viewpoint, more in line with the localrequirements for each crop.

Acknowledgments

We would like to thank Dr. Antoon Ploeg for hiscomments on the manuscript. Thanks also go to Dr.Lacasa, IMIDA (Murcia, Spain) and Dr Fery, USDA(Charleston, USA) for supplying the pepper seeds andcollaboration. Thanks to the members of the Depart-ment of Agroecologıa Mar Lopez for their technicalsupport. This work formed part of the project INIA:‘‘Optimization and development of alternatives tomethyl bromide: Critical use. Biofumigation’’, and theproject AGL2002-04040-C05-01 AGR-FOR of theSpanish Ministry of Science and Technology: ‘‘Soilimprovement by the use of crop waste amendments. Soilmetabolism and their biofumigation effect’’. AnaPiedra-Buena was supported by a Spanish Agency ofInternational Co-operation (AECI) scholarship.

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