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Biological Control 45 (2008) 380–385

Muscodor albus, a potential biocontrol agent againstplant-parasitic nematodes of economically important

vegetable crops in Washington State, USA

Ekaterini Riga a,*, Lawrence A. Lacey b, Neussa Guerra a

a Washington State University, IAREC and Plant Pathology, 24106 N. Bunn Road, Prosser, WA 99350, USAb USDA-ARS, Yakima Agricultural Research Laboratory, 5230 Konnowac Pass Road, Wapato, WA 98951, USA

Received 8 September 2007; accepted 3 January 2008Available online 12 January 2008

Abstract

The fungus, Muscodor albus, was tested for nematicidal and nematostatic potential against four plant-parasitic nematode species withthree different feeding modes on economically important vegetable crops in the Pacific Northwest. Meloidogyne chitwoodi, Meloidogyne

hapla, Paratrichodorus allius, and Pratylenchus penetrans were exposed for 72 h to volatiles generated by M. albus cultured on rye grain insealed chambers at 24 �C in the laboratory. In addition, the nematodes were inoculated into soil fumigated with M. albus, and incubatedfor 7 days prior to the introduction of host plants under greenhouse conditions. The mean percent mortality of nematodes exposed toM. albus in the chamber was 82.7% for P. allius, 82.1% for P. penetrans, and 95% for M. chitwoodi; mortality in the nontreated controlswas 5.8%, 7%, and 3.9%, respectively. Only 21.6% of M. hapla juveniles died in comparison to 8.9% in controls. However, 69.5% of thetreated juveniles displayed reduced motility and lower response to physical stimulus by probing, in comparison to the control juveniles.This is evidence of nematostasis due to M. albus exposure. The greenhouse study showed that M. albus caused significant reduction to allnematode species in host roots and in rhizosphere soil. The percent mortality caused by M. albus applied at 0.5% and 1.0% w/w incomparison to the controls was as follows: 91% and 100% for P. allius in the soil; 100% for P. penetrans in bean roots and soil; 85%and 95% for M. chitwoodi in potato roots, and 56% and 100% in the soil; 100% for M. hapla both in pepper roots and soil. In this study,M. albus has shown both nematostatic and nematicidal properties.Published by Elsevier Inc.

Keywords: Biological control; Muscodor albus; Meloidogyne chitwoodi; Meloidogyne hapla; Nematicidal; Nematostatic; Paratrichodorus allius; Pratyle-

nchus penetrans; Vegetable crops

1. Introduction

Muscodor albus Worapong, Strobel & Hess is an endo-phytic fungus first isolated from the cinnamon tree, Cinna-

momum zeylanicum Breyne in a rainforest in Honduras(Strobel et al., 2001; Worapong et al., 2001). The funguslacks spores and spore-producing structures and has whit-ish hyphae. An important property of this fungus is its abil-ity to produce a mixture of volatile organic compoundscapable of killing a broad range of plant and human path-

1049-9644/$ - see front matter Published by Elsevier Inc.

doi:10.1016/j.biocontrol.2008.01.002

* Corresponding author. Fax: +1 509 786 9370.E-mail address: riga@wsu.edu (E. Riga).

ogenic fungi and bacteria (Strobel et al., 2001; Woraponget al., 2001). Biofumigation with M. albus has been shownto control smut on grain (Strobel et al., 2001), soil-bornepathogens (Stinson et al., 2003; Mercier and Manker,2005), building molds (Mercier and Jimenez, 2007), a vari-ety of post harvest pathogens of fruit (Mercier and Jime-nez, 2004; Mercier and Smilanick, 2005; Schnabel andMercier, 2006), and potato tuber moth, Phthorimaea oper-

culella (Zeller) (Lacey and Neven, 2006; Lacey et al., 2008).Limited nematicidal activity of this fungus has been dem-onstrated against root-knot nematode, Meloidogyne incog-

nita (Kofoid & White) infecting tomatoes (Grimme et al.,2007). The effect of M. albus on a wide range of plant-par-

E. Riga et al. / Biological Control 45 (2008) 380–385 381

asitic nematodes has not yet been evaluated even thoughplant-parasitic nematodes are of importance to agricultureworldwide. Economic damage has been estimated at US$40 billion annually (Chitwood, 2003), while in WashingtonState, crop losses may be as high as US$ 40 million, assum-ing no application of nematicides (Santo, 1994).

The Columbia root-knot nematode, Meloidogyne chit-

woodi Golden et al., and the northern root-knot nematode,Meloidogyne hapla Chitwood, are among the most eco-nomically important nematodes of potatoes in Washingtonand the Pacific Northwest (PNW) of the United States.Both nematodes have wide host ranges outside of potatoes(O’Bannon et al., 1982; Potter and Olthof, 1993).

The stubby nematode, Paratrichodorus allius (Jensen), isbecoming an important pest in the PNW because it trans-mits the tobacco rattle virus (TRV), the cause of corkyringspot disease of potato (Mojtahedi and Santo, 1999;Mojtahedi et al., 2003). Potato, wheat, corn, alfalfa, mint,and onion are among the various hosts commonly grown inthe PNW and parasitized by P. allius (Mojtahedi andSanto, 1999; Mojtahedi et al., 2002). The root lesion nem-atode, Pratylenchus penetrans Cobb, reduces yield in manycrops such as cereals (Kimpinski et al., 1987), forages(Thies et al., 1995), vegetables (Olthof and Potter, 1973),and potato (Florini and Loria, 1990). In the PNW it hasbeen found on several crops including potato (Inghamet al., 2005). The above plant-parasitic nematode speciesrepresent three different feeding types: M. chitwoodi andM. hapla are sedentary endoparasites, P. penetrans is amigratory endoparasite, and P. allius is an ectoparasite(Lambert and Bekal, 2002).

Organic farming is a fast-growing industry in Washing-ton State and worldwide (http://csanr.wsu.edu/Organic).There is an increasing need to assist organic growers withthe management of diseases and plant pathogens, althoughconventional growers would also benefit from novel andeffective bionematicides. Fumigants like 1,3-dichloropro-pene and/or metham sodium that are used extensively inWashington and the PNW (Santo, 1994) are costly, envi-ronmentally undesirable, and have uncertain availabilityin the future (Lambert and Bekal, 2002). A biologicallygenerated fumigant could provide sustainable means forcontrolling plant-parasitic nematodes without some of therisks associated with chemical fumigants.

The objective of this project was to evaluate the effect ofM. albus on several plant-parasitic nematode species, inorder to provide organic and conventional growers withadditional opportunities for managing nematodes in thefuture.

2. Materials and methods

2.1. Source of plant-parasitic nematodes

The P. allius population was isolated from a field inPasco, Washington in 1990 with high prevalence of corkyringspot disease and maintained on ‘‘Samsun NN” tobacco

(Nicotiana tabacum L.) which is a good host for both TRVand the nematode (Mojtahedi and Santo, 1999). Pratylen-

chus penetrans was isolated from an apple orchard in Matta-wa, Washington in 1996 and maintained on mint (Mentha

piperita L.). Meloidogyne chitwoodi (race 1) was isolatedfrom a potato field in Quincy, Washington in 1977 andmaintained on tomato (Lycopersicum esculatum L.), carrot(Daucus carota L.), and wheat (Triticum aestivum L. cv.Nugaines). Meloidogyne hapla was isolated from an alfalfa(Medicago sativa L.) field in Washington, in 1980 and main-tained on pepper (Capsicum anuum L. cv. California Won-der). All nematodes were maintained in the WashingtonState University-IAREC greenhouse in Prosser.

2.2. Muscodor albus inoculum

A sample of desiccated M. albus strain 620 on auto-claved rye grain was obtained from AgraQuest, Davis, Cal-ifornia and stored at 8 �C until used. This M. albus isolatehas been extensively studied and characterized (Woraponget al., 2001; Strobel et al., 2001). Prior to testing in the lab-oratory, aliquots of 30 g of M. albus formulation wereweighed and placed in separate 0.47 L plastic containersand activated through rehydration by adding 30 ml ofdeionized water to each container. The containers werethen sealed with a lid and set aside at room temperaturefor 24 h. Nontreated controls contained non-inoculatedhydrated rye grain. The biofumigation took place inside achamber at 24 �C during which time the lids of the contain-ers with M. albus were removed and any volatile com-pounds produced were released.

2.3. Chamber assay

The chamber assay used to evaluate the effect of M.

albus on plant-parasitic nematodes has been described byLacey and Neven (2006). Briefly, fiberglass chambers(28.3 L, Labconco vacuum desiccators, model 5530, Kan-sas City, MO) were used for exposing plant-parasitic nem-atodes to volatile compounds of M. albus. Each chamberwas hermetically sealed and equipped with a circulatingfan. Juvenile or adult nematodes (ca. 100/species) wereplaced in individual petri dishes (60 � 15 mm, Falcon,Oxnard, CA) containing 15 ml of sterilized tap water.One container of M. albus culture was placed in each cham-ber. Once inside the chamber, the lids of five petri dishescontaining nematodes were removed and nematodes ineach dish were exposed to volatiles produced by M. albus

for 72 h at 24 �C. Controls contained only rye seeds withwater. Each test consisted of 5 randomized replicate dishesof 100 juveniles or adults for each nematode species andtheir respective controls. Separate chambers were usedfor each nematode species and their respective control.After 72 h, nematode mortality was evaluated using a dis-secting microscope (Leica, DMIL, Wetzlar, Germany). Inaddition to mobile nematodes, nematodes that were immo-bile but responded to probing with a fine needle were con-

382 E. Riga et al. / Biological Control 45 (2008) 380–385

sidered alive. The chamber assay was repeated three timeson three different dates.

2.4. Greenhouse/host plant—pot assay

Twelve separate 2-L plastic containers were each filledwith 2500 g of potting soil. The soil consisted of 84% sand,10% silt, 6% clay, 0.5% organic matter, pH 6.9, and waspreviously fumigated with methyl bromide at 0.3 kg/m3.The pots were inoculated with a concentration of either 2juveniles of P. allius, and P. penetrans, or eggs of M. chit-

woodi and M. hapla per g soil. The same formulation andstrain of M. albus was used in the greenhouse test as inthe chamber. Two concentrations were used in the green-house test, 0.5% and 1.0% w/w M. albus to soil and non-treated controls with 5 replicates for each treatment andcontrol. Muscodor albus was mixed into the soil thor-oughly. The inoculated soil was moistened up to 80% fieldcapacity and kept in hermetically closed plastic containersin the dark for 7 days at 24 �C. Then 500 g of each concen-tration of M. albus treated soil and nontreated controlswere inoculated with each nematode species was allocatedto 0.5-L plastic pots. One appropriate plant host wasimmediately transplanted to each of 15 pots as follows:4-week-old tobacco Nicotiana tabacum L. cv. Samsun-NN was used for P. allius; 2-week-old beans, Phaseolus vul-

garis L. var. Pinto was used for P. penetrans; 4-week-oldpotato, Solanum tuberosum L. cv Russet Burbank was usedfor M. chitwoodi (race 1); and 4-week-old pepper, Capsicum

annum L. cv California Wonder was used for M. hapla.Five control pots without M. albus were used for each nem-atode species. All plants were maintained at 24 �C for 8weeks in a naturally illuminated and ventilated greenhouse.Plants in pots were fertilized every 4 weeks with 10 g/pot(Osmocote 14-14-14, Scotts, Marysville, OH) and wateredevery 1–2 days until the end of the test. The greenhouse testwas repeated three times on three different dates and theplants within a treatment were randomized.

After 8 weeks, all nematode species were extracted fromthe soil using the Baermann pan technique (Townshend,1963). In addition, the host roots of P. penetrans, M. chit-

woodi, and M. hapla, were stained with acid fuchsin for thepresence of nematodes using a technique by Byrd et al.(1983). Nematodes extracted from the soil or stained inthe host plant roots were examined under the dissectingmicroscope and enumerated. Collected data from soil wereexpressed as nematodes per 100 gram soil. Data from rootswere expressed as nematodes per gram dry root which wasobtained from one gram of wet root from each plant, thendried in an oven overnight and the dry weight obtained wasused to estimate nematodes per gram dry root.

2.5. Meloidogyne hapla motility test and greenhouse

infectivity assay

After 72 h exposure to M. albus volatiles, M. hapla

juveniles were transferred to sterilized tap water and

examined microscopically for motility by probing witha fine needle (Cayrol et al., 1989). Nematodes thatshowed slower motility than the controls based on num-ber of sinusoidal waves per minute were immobile butsubsequently responded to probing with a fine needle,were considered alive but showing signs of partial paral-ysis. None of the control nematodes showed signs ofparalysis. Nematodes that demonstrated reduced move-ment were handpicked using an eyelash attached in theend of a metal probe, and then transferred to pots con-taining 100 g of potting soil and 4 week-old pepper. Theplants were maintained for 8 weeks under the samegrowing conditions as described above for seedlings ingreenhouse assays, and the nematodes were also pro-cessed as above. Five pots were used for the treated nem-atodes and five for the nontreated controls on each testdate. This experiment was repeated three times on threedifferent dates and the treatments were in a completelyrandomized design.

2.6. Statistical analysis

ANOVA, P < 0.05 was used to determine the effect ofM. albus on plant-parasitic nematode mortality in thechamber and in the greenhouse assays with significant dif-ferences determined at P < 0.05. The analysis showed nosignificant differences between the three different tests forany of the nematode species. Therefore, data from the trip-licate tests were combined. The treatment means were sep-arated using Fisher’s LSD at P = 0.05. ANOVA wasperformed using SYSTAT.

3. Results

3.1. Chamber assay

Results of this study showed that M. albus volatile com-pounds have significant nematicidal properties against thefour plant-parasitic nematodes species, P. allius, P. pene-

trans, M. chitwoodi, and M. hapla, and nematostatic prop-erties against M. hapla.

In the chamber assay, the mortality observed in P. allius

was higher than that of the controls (F1,28 = 25,8;P < 0.00002) (Fig. 1). The chamber assay of P. penetrans

resulted in higher mortality for treated nematodes in com-parison to the controls (F1,28 = 192; P < 0.00004) (Fig. 1).Similarly, exposure of M. chitwoodi to M. albus resultedin higher mortality in comparison to the nontreated con-trols (F1,28 = 121; P < 0.00002) (Fig. 1). Only 21.6 + 1.9%mortality of M. hapla was observed in the chamber assays.However, 69.5 + 6.8% of M. hapla juveniles showedreduced motility, 8.9 + 1.0% juveniles were alive and activeand only 2.1 + 0.5% of the control juveniles were dead(F2,44 = 71; P < 0.00008) (Fig. 2). Muscodor albus treatedjuveniles produced approximately 50% fewer sinusoidalwaves per minute in comparison to the nontreated juveniles(data not shown).

0

20

40

60

80

100

120

Paratrichodorus allius Pratylenchus penetrans Meloidogyne chitwoodi

M. albus treatment

Untreatedcontrol

Nematode species

% m

orta

lity

Fig. 1. Mean percent mortality of Paratrichodorus allius, Pratylenchus

penetrans, and Meloidogyne chitwoodi juveniles or adults after 72 hexposure to Muscodor albus volatiles in hermetically sealed chambers(bars represent standard error of the mean).

0

20

40

60

80

100

120

Control M. albusTreatments

% d

ead,

aliv

e an

d pa

raly

zed

nem

atod

es deadalive

paralyzed

Fig. 2. The effect of exposing Meloidogyne hopla juveniles for 72 h toMuscodor albus volatiles in hermetically sealed chambers (bars representstandard error of the mean).

E. Riga et al. / Biological Control 45 (2008) 380–385 383

3.2. Greenhouse/host plant—pot assay

In the greenhouse assays, significantly higher mortalitywas observed in the 0.5% and 1.0% w/w M. albus treatedP. allius in comparison to nematodes in the nontreated

Table 1The effect of exposing the plant-parasitic nematodes, Paratrichodorus allius, P

albus produced volatiles in the presence of host plants in pots in a greenhouse

# Nematodes/100 g soil

Nematode species 0.5% M. albus 1.0% M. albus Con

P. allius 1.3 ± 0.3 0 15.0P. penetrans 0 0 10M. chitwoodi 70 ± 10 0 160M. hapla 0 0 107

Data show the mean number of live nematodes ± SEM.All means from 0.5% and 1.0% M. albus treatments are significantly different

a Data from roots are not reported from the ectoparasitic nematode, P. alli

control (F2,44 = 92.9; P < 0.00004) (Table 1). Pratylenchus

penetrans was not found inside bean roots or in the soilaround the bean roots treated with 0.5% or 1.0% M. albus

in comparison to the nontreated controls (F2,44 = 40.4;P < 0.00005), (F2,44 = 5.9; P = 0.006) (Table 1). When M.

chitwoodi was inoculated into treated soil and controls, sig-nificantly fewer nematodes were found in the roots and soilin comparison to the control plants (F2,44 = 34.4;P < 0.00002) (Table 1). In addition, there was a significantdifference between the two M. albus treatments, 1.0% w/wM. albus caused higher mortality to M. chitwoodi than the0.5% w/w M. albus treatment (F1,28 = 10.1; P = 0.0036)(Table 1). Similarly, there was a significant differencebetween the two M. albus treatments with respect to num-bers of nematodes found in the soil; 1.0% w/w M. albus

treatment resulted in less M. chitwoodi juveniles in the soilthan the 0.5% w/w M. albus treatment (F1,28 = 15.5;P = 0.0005). Meloidogyne hapla was not detected insideinoculated pepper roots or in the soil around the pepperroots treated with 0.5% w/w and 1.0% w/w M. albus com-pared to control plants (F2,44 = 14.5; P = 0.0007) and(F2,44 = 13.5; P = 0.001) (Table 1).

3.3. Meloidogyne hapla motility test and greenhouse assay

In the greenhouse assay, M. hapla juveniles that dis-played reduced movement due to M. albus exposure in thechamber study were found at 0.16 + 0.04 per g pepper root,and 0.3 + 0.2 nematodes per 100 g soil around the pepperroots, while the control peppers had higher nematode num-bers, 9.8 + 0.7 nematodes per g root and 43 + 15 nematodesper 100 g soil (F2,44 = 25; P < 0.00009) (F2,44 = 10.7;P = 0.004), respectively.

4. Discussion

This is the first report on the nematostatic properties ofM. albus against the root-knot nematode, M. hapla. Theobserved nematostatic properties of M. albus did not killM. hapla nematodes within the incubation period usedfor all nematode species tested but caused paralysis. Inaddition, in this study M. albus proved to be an effectivenematicidal treatment by causing mortality to the mosteconomically important plant-parasitic nematodes in

ratylenchus penetrans, Meloidogyne chitwoodi, and M. hapla, to Muscodor

# Nematodes/1 g roota

trol 0.5% M. albus 1.0% M. albus Control

± 1.4 — — —± 0.6 0 0 10.4 ± 2.9± 10.0 65.9 ± 9.6 20.5 ± 0.1 436 ± 35.3± 30.0 0 0 11.8 ± 3.1

than the controls.us.

384 E. Riga et al. / Biological Control 45 (2008) 380–385

Washington State, M. chitwoodi, M. hapla, P. allius, and P.

penetrans. Nematode reductions were observed both in therhizosphere soil and the roots of potato, pepper, tobaccoand bean.

There has been limited work on the effect of M. albus onplant-parasitic nematodes. Recently, Grimme et al. (2007)reported that a biorational mixture of M. albus volatiles(a synthetic mixture of key antimicrobial gases producedby M. albus), protected tomatoes from the root-knot nem-atode, M. incognita. Grimme et al. (2007) reported that aM. albus biorational mixture, contained the following com-pounds: 1-butanol, 2-methyl, 1, butanol, 2-methyl acetate;propanoic acid; and 2-methyl-, 2-methyl propyl ester,whereas Strobel et al. (2001) reported that the most biolog-ically inhibitory group of compounds derived from M.

albus against bacteria and fungi was 1-butanol, 3-methyl-acetate. Mercier and Jimenez (2007) showed a time courseproduction of the main antifungal volatiles, isobutyric acid,2-methyl-1-butanol and isobutanol, produced by M. albus.

However, the specific M. albus compound or mixture ofvolatile organic compounds responsible for mortality inplant-parasitic nematodes has not yet been characterized.

Lacey et al. (2008) reported the fumigation ability of M.

albus to control potato tuber moth in stored potatoes andhypothesized that plant-parasitic nematodes that damagepotato tubers in storage could be controlled, as well. How-ever, this hypothesis needs to be tested.

The plant-parasitic nematodes used in our study are ofmajor economic importance to the agricultural industryof Washington State and the PNW. Muscodor albusappears to offer promise as a synthetic fumigant replace-ment. Therefore, further studies are needed to evaluatethe fumigant properties of M. albus under field conditionsin the presence of the plant-parasitic nematodes used in ourlaboratory and greenhouse tests.

Acknowledgments

E. Riga is supported by the College of Agricultural, Hu-man, and Natural Resource Sciences Agricultural ResearchCentre, PPNS No. 0451, Department of Plant Pathologyand IAREC WSU-Prosser, Project No. WNP00542, Wash-ington State University, Pullman, WA 99164-6430, USA.Many thanks to AgraQuest, Davis, California, for provid-ing the Muscodor albus inoculum and Debra Inglis, DonHostetter and Steven Arthurs for their editorial comments.

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