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Effect of Inoculation Sequence on the
Interaction between Glomus Intraradices
and Fusarium Oxysporum f. sp. RadicisLycopersici in Tomatoes
M. Caron
a b c
, J.A. Fortin
a b c
& C. Richard
a b c
a
Experimental Farm, Agriculture Canada , P.O. Box 1070, L
'Assumption, Quebec, JOK 1G0
b
Centre de Recherches en Biologie Foreslière , Université Laval ,
Quebec, G1K 7P4
c
Research Station, Agriculture Canada , 2560, Boul. Hochelaga, SainteFoy, Quebec, G1V 2J3
Published online: 29 Dec 2009.
To cite this article: M. Caron , J.A. Fortin & C. Richard (1986) Effect of Inoculation Sequence on the
Interaction between Glomus Intraradices and Fusarium Oxysporum f. sp. Radicis-Lycopersici in Tomatoes,
Canadian Journal of Plant Pathology, 8:1, 12-16, DOI: 10.1080/07060668609501835
To link to this article: http://dx.doi.org/10.1080/07060668609501835
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CANADIAN JOURNAL OF PLANT PATHOLOGY 8: 12-16, 1986
Effect of inoculation sequence on the interaction between
Glomus intraradices and Fusarium oxysporum f. sp. radicis-lycopersici in tomatoes
M. Caron, J.A. Fortin, and C. Richard
Experimental Farm, Agriculture Canada, P.O. Box 1070. L 'Assumption, Quebec JOK I GO (Contribution No. J-1005, Saint-Jean
Research Station); Centre de recherches en biologie foreslière, Université Laval, Quebec (Quebec) Gl K 7 P4; and Research
Station, Agriculture Canada, 2560, boul. Hochelaga, Sainle-Foy, Quebec, GIV2J3 (Contribution No. 285, Sainte-Foy Research
Station). Present address of M. Caron: Centre de recherches, Les Tourbières Premier Ltée, Chemin Témiscouata, C. P. 482,
Rivière-du-Loup (Quebec) G5R3Z1.
Downloaded by [North Carolina State University] at 15:29 09 March 2015
Accepted for publication 1986 02 03
To determine if the decrease caused by Glomus intraradices, a vesicular-arbuscular mycorrhizal (VAM) fungus, in root rot of
tomatoes and in the population of Fusarium oxysporum f.sp. radicis-lycopersici varies with the sequence of inoculation of
the two fungi, tomato plants were inoculated with Glomus 4 weeks before, simultaneously with, and 4 weeks after the
inoculation with Fusarium. Reductions in root rot and in the population of F. oxysporum were observed in all treatments
and were not influenced by the sequence of inoculation with the two microorganisms. Root colonization by G. intraradices
was significantly increased when F. oxysporum was inoculated simultaneously with or 4 weeks before the VAM fungus.
Plant dry mass was not increased by the presence of G. intraradices alone, but compensation for dry mass loss due to F.
oxysporum occurred when the VAM fungus was inoculated after the Fusarium.
Caron, M., J.A. Fortin, and C. Richard. 1986. Effect of inoculation sequence on the interaction between Glomus intraradices and
Fusarium oxysporum f. sp. radicis-lycopersici in tomatoes. Can. J. Plant Pathol. 8; 12-16,
Afin d'établir si la diminution de la pourriture des racines de tomate et de la population de Fusarium oxysporum f.sp. radicislycopersici associée a la presence du Glomus intraradices, champignon mycorhizien a vésicules et arbuscules, varie en
fonction de l'ordre d'inoculation des deux champignons, des plants de tomate ont été inoculés avec le Glomus 4 semaines
avant l'inoculation avec le Fusarium, en même temps, et 4 semaines après. Une diminution du niveau de pourriture des
racines et de la population fusarienne a été observée pour tous les traitements, mais n'a pas été influencée par la sequence
d'inoculation des deux micro-organismes. La colonisation des racines par le G. intraradices a été augmentée de fagon
significative lorsque le F. oxysporum a été inoculé simultanément ou 4 semaines avant le champignon mycorhizien. La masse
sèche des plantes n'a pas été augmentée en presence du G. intraradices inoculé seul bien qu'il y ait eu compensation pour la
perte en masse sèche due au Fusarium en presence du G. intraradices lorsqu'inoculé après le Fusarium.
Interaction studies in which a host plant is
inoculated with a vesicular-arbuscular mycorrhizal
(VAM) fungus prior to its inoculation with a fungal
root pathogen have indicated various effects by the
VAM fungi on the development of the pathogen
and on the severity of diseases induced in the host
plants (Baath & Hayman 1983, Davis et al. 1978,
Kaye et al. 1984). A few studies have been
conducted in which a VAM fungus and a fungal
root pathogen were inoculated simultaneously but
none where the pathogen was inoculated prior to
the VAM fungus. When inoculated simultaneously, a decrease (Krishna & Bagyaraj 1983,
Zambolim & Schenck 1983), an increase (Davis et
al. 1979, Ross 1972), or no effect (Schönbeck &
Dehne 1977) of the VAM fungi on the development
of the pathogen or the severity of disease induced in
the host plants was observed.
In previous studies (Caron et al. 1985, 1986a,
1986b), we have demonstrated that the presence of
the VAM fungus Glomus intraradices Schenck &
Smith can decrease both root rot of tomatoes
{Lycopersicon esculentum Mill.) and the development of the pathogen Fusarium
oxysporum
Schlecht. f.sp. radicis-lycopersici
Jarvis &
Shoemaker. The objective of this work was to
determine if such effects are influenced by the
sequence of inoculation of the two fungi.
Materials and methods
Seeds of tomato (cv. Vendor) were surfacesterilized for 1.5 min in 3% sodium hypochlorite,
blotted dry on sterilized filter papers and
germinated for 5 days at 26°C on potato dextrose
agar (PDA, Difco) in petri dishes. Germinated
seeds without contaminants were then planted in
sand, grown in a greenhouse, watered as needed
with demineralized distilled water (DDW), and, 2
weeks after planting, fertilized with a Long Ashton
solution (Hewitt 1966) modified by adding 300 mg
of KC1 per L (Plenchette et al. 1982).
Three-week-old seedlings were carefully
removed from the seedbeds and the root system
gently washed free of sand with DDW. The
seedlings were transplanted to 18-cm-diameter pots
containing pasteurized calcined montmorillonite
clay (Turface, IMC Imcore, Mundelein, Illinois
60060) (Caron et al. 1985). The initial available P
content of Turface as determined by extraction in
0.1 NHCl +0.3 7VNH4F and analysed by the
12
Downloaded by [North Carolina State University] at 15:29 09 March 2015
CARON ET AL.:TOMATO/FUSARIUM/GLOMUS
vanadomolybdophosphoric yellow color method
in nitric acid system (Jackson 1958) was 115 /ug'g';
the initial pH was 6.1. One hour prior to
transplanting the seedlings, the substrate in each
pot was watered with 500 mL of DDW followed by
100 mL of modified Long Ashton solution.
The pathogen F. oxysporum f.sp. radicislycopersici (MC-27) was grown on PDA.
Macroconidia were harvested in sterilized-distilled
water from 26-day-old cultures incubated at 26° C
under fluorescent lights (40 /xE-s'-nr2) and the
conidial suspension was sieved (45 /xm). The
concentration of the inoculum was approximat i v e ^ 5.4 x 104 macroconidia/mL for both
inoculation periods.
At the time of transplanting, a set of seedlings
was inoculated with G. intraradices (G+) only, by
placing 1 g (fresh mass) of mycorrhizal leek roots
{Allium porrum L. cv. Alaska) 5 cm below the soil
surface. To introduce into the nonmycorrhizal
treatment (G ) the microflora usually associated
with pot culture inoculum, 1 mL of a spore-free
washing, obtained by wet sieving mycorrhizal roots
through a 45 /xm mesh sieve, was added to the
control pots together with 1 g of autoclaved
mycorrhizal leek roots. A second set of seedlings
was inoculated with F. oxysporum f.sp. radicislycopersici (F+) by spreading 1 mL of the conidial
suspension onto the roots using a calibrated
pipette. Uninoculated control (F~) plants received
1 mL of sterilized distilled water. A third set of
seedlings was transplanted and kept for subsequent
inoculation.
Four weeks after transplanting, all plants were
carefully uprooted. Tomato plants previously
inoculated only with G intraradices, and their
corresponding controls, were then inoculated with
Fusarium following the procedure previously
described, viz., G + F , G+F+, G F+, G F . Similarly,
tomato plants previously inoculated only with the
Fusarium, and their corresponding controls, were
inoculated with G. intraradices a previously
described, viz., G+F , G+F+, G~F+, G~F~. Tomato
plants which had not been inoculated with either of
the two microorganisms at the time of transplanting were inoculated simultaneously (G+F+) with
both microorganisms, and appropriate controls
(G~F , G+F , G F+) were added. Regardless of the
time of inoculation with Glomus and Fusarium, the
interaction between the two fungi in the tomato
plants was for a 5-week period for each set of
seedlings. Each treatment was replicated eight
times. All plants were harvested at week 12, 5 weeks
after the second inoculation.
For each plant, the percentage of root necrosis
was visually assessed on the basis of the proportion
13
of the root system showing surface necrosis at
harvest. Root pieces of each plant, with and
without necrosis, were plated on sucrose nutrient
agar (Nirenberg 1981) to detect the presence of F.
oxysporum f.sp. radicis-lycopersici.
Survival of F. oxysporum
f.sp. radicislycopersici was evaluated in each pot by placing 2 g
of substrate free of plant material in 100 mL of
water agar (0.12%) in a 125-mL flask and shaking
for 1 h; subsequently, the substrate was allowed to
settle for 10 min, after which 1 mL of the
supernatant was diluted in 9 mL of water agar
(0.12%). From each flask and each subsequent
dilution, 1 mL of the suspension was spread on
each of four petri dishes containing Komada's
selective medium for F. oxysporum Schlecht.
(Komada 1975). The petri dishes were incubated in
the dark for 10 days at 24°C, after which period F.
oxysporum colonies were counted, and the number
of propagules per gram of dry mass of substrate was
determined.
Root samples from each plant were cleared and
stained according to Phillips and Hayman (1970)
using acid fuchsin instead of cotton blue (Berch &
Kendrick 1982). A root endomycorrhizal colonization (REC) index (Plenchette et al. 1982) for each
plant was established from an examination of three
sites 3 mm apart on each of 40 1-cm-long root
segments randomly sampled. The dry mass of the
tomato plants was determined after drying at 65°C
for 24 h.
The experimental design was a randomized
complete block design (8 blocks). The variances of
the percent of root necrosis, the number of F.
oxysporum propagules, the REC index, and the
dry mass were analysed following a 3 * 2 * 2
factorial.
Results
The sequence of plant inoculation with F.
oxysporum
f.sp. radicis-lycopersici
and G.
intraradices significantly influenced (P= 0.05) the
effect of Fusarium on colonization of the root by G.
intraradices (Table 1). An analysis of variance of
the REC index for each sequence of inoculation
indicated that the presence of Fusarium inoculated
4 weeks after G. intraradices had no effect
(P=0.05) on root colonization by the VAM
fungus, while the presence of Fusarium inoculated
simultaneously or 4 weeks before the inoculation
with G. intraradices resulted in significant increases
(P=0.0l) in the REC index of 6.2% (8.1-14.3%),
and 17.1% (8.3-25.4%), respectively.
The presence of G. intraradices resulted in
significant reductions (P=0.0\) in root necrosis
caused by Fusarium independently of the sequence
of inoculation of the two fungi, as indicated by the
14 CANADIAN JOURNAL OF PLANT PATHOLOGY, VOLUME 8, 1986
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Table 1. Analysis of variance of the root endomycorrhizal colonization (REC) index, the percent of root necrosis, the number of F,
oxysporum propagules and the dry mass of tomato plants inoculated with G. intraradices 4 weeks before, simultaneously with, or 4
weeks after inoculation with F. oxysporum f.sp. radicis-lycopersici
Sum of squares
Mean square
Source of variation
d.f.
REC index
Blocks(B)
Sequence of inocu lation (I)
Glomus (G)
Fusarium (F)
IxG
1xF
G» F
\ *G*F
Error
Total
7
2
1
1
2
2
1
2
77
95
210.96
132.90
4030.04
570.38
172.77
157.69
459.37
227.31
2038.54
7999.96
30.14
66.45
4030.04
570.38
86.39
78.84
459.37
113.66
26.47
Root necrosis
Blocks (B)
Sequence of inoci lation (I)
Glomus (G)
Fusarium (F)
1 xG
1 xF
G» F
l«G»F
Error
Total
7
2
1
1
2
2
1
2
77
95
314.46
5390.39
8855.04
65000.04
1650.39
5390.39
8855.05
1650.39
8307.79
105413.96
44.92
2695.20
8855.04
65000.04
825.19
2695.19
8855.05
825.19
107.89
Number of F. oxysporum propagules
Blocks(B)
Sequence of inoci lation (I)
Glomus (G)
Fusarium (F)
Ix G
Ix F
G» F
1 x Gx F
Error
Total
7
2
1
1
2
2
1
2
77
95
Dry mass of tomato plants
Blocks(B)
Sequence of inoci lation (I)
Glomus (G)
Fusarium (F)
1 x G
1 xF
Gx F
lx Gx F
Error
Total
7
2
1
1
2
2
1
2
77
95
1161938.7
6205245.8
36298532.0
137465896.0
339631.2
7729573.4
34422135.7
898571.5
69889703.1
294411227.4
84.22
195.73
26.78
51.19
11.32
7.04
0.01
7.21
166.84
580.33
165991.2
3102622.9
36298532.0
137465896.0
169815.6
3864786.7
34422135.7
449285.8
907658.5
12.03
97.87
26.78
51.19
5.66
18.52
0.01
3.60
2.17
F. ratio
1.14 n.s.
2.51 n.s.
152.22**
21.54**
3.26*
2.98 n.s.
17.35 **
4.29*
0.42
24.98
82.07
602.45
7.65
24.98
82.07
7.65
n.s.
**
**
**
**
**
**
**
0.2 n.s.
3.4*
40.0 **
151.5**
0.2 n.s.
4.3 *
37.9 **
0.5 n.s.
5.55**
45.17**
12.36**
23.62 **
2.61 n.s.
8.55 **
0.002 n.s.
1.66 n.s.
d.f. Degrees of freedom.
n.s. Not significant.
5% level of significance.
1% level of significance.
analysis of variance of the percent of root necrosis
for each sequence of inoculation. However the
differences of the percent of root necrosis between
the presence and the absence of G. intraradices
indicated a greater reduction (58.8%) when G.
intraradices was inoculated 4 weeks after the
inoculation with Fusarium, than when it was
inoculated simultaneously (38.3%) or 4 weeks
before (18.1%) the inoculation with Fusarium.
Similarly plant inoculation with G. intraradices 4
weeks before, simultaneously with, or 4 weeks after
inoculation with Fusarium resulted in significant
reductions (P - 0.01) in the number of propagules
of Fusarium of 2749, 2021, and 2513, respectively;
these variations in the population of Fusarium in
the presence and absence of G. intraradices were
independent of the sequence of inoculation of the
two fungi (Table 1). Plant mortality (25% of the
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CARON ET AL.: TOMATO/FUSARIUM/GLOMUS
plants) occurred only in plants inoculated with
Fusarium but not followed by inoculation with G
intraradices.
There were significant differences
(P-0.0\)
between blocks (Table 1) for the dry mass of tomato
plants; these differences were not related to the
treatments but to the position of the blocks in the
greenhouse. There was a significant interaction
(Z5 = 0.01) between the time of inoculation with
Fusarium and its effect on the dry mass of plants
(Table 1). The differences between the means of the
dry mass of plants in the presence (F+) and the
absence (F ) of Fusarium were obtained by using
the following equation: (G+ mean - G~ mean) for
F+ - (G+ mean - G mean) for F~. This calculation
indicated no effect on plant dry mass either in the
presence or in the absence of Fusarium when
Glomus was inoculated 4 weeks before Fusarium.
When Glomus and Fusarium were inoculated
simultaneously, the difference between the means
for F+ and F" (-1.3) showed that Glomus had a
greater effect on plant dry mass in the absence of
Fusarium. Similarly the difference between the
means for F+ and F~ indicates that Glomus had an
effect (+1.3) on plant dry mass in the presence of
Fusarium only when the later was inoculated 4
weeks before the inoculation with Glomus.
Discussion
The observation that the presence of G.
intraradices resulted in a decrease in root necrosis
and in the population of F. oxysporum f.sp. radicislycopersici when inoculated prior, simultaneously
or after the pathogen clearly indicates that this
effect of G. intraradices on root rot and on the
population of F. oxysporum
f.sp. radicislycopersici is independent of the sequence of
inoculation with the two microorganisms.
The absence of an effect of F. oxysporum f.sp.
radicis-lycopersici on root colonization by G.
intraradices when the former was added after the
VAM funguss, generally confirms our previous
results (Caron et al. 1985, 1986a), although in one
instance (Caron et al. 1986b) an increase was
obtained. Kaye et al. (1984) have reported a greater
colonization of roots of poinsettia by Glomus
fasciculatum (Thaxter sensu Gerd.) Gerd. &
Trappe Dn the presence of Pythium ultimum Trow.
inoculated after the VAM fungus than in the
absence of Pythium. On the other hand, Baath and
Hayman (1983) have observed a lower root
colonization of tomatoes by Glomus caledonium
(Nicol. & Gerd.) Trappe & Gerd. inoculated prior
to Verticillium albo-atrum Reinke & Berthold than
in the absence of the pathogen. When inoculated
simultaneously no effect of Fusarium on root
15
colonization by G. intraradices has been observed
in our study. Krishna and Bagyaraj (1983) have
observed a reduction in root colonization of peanut
by Glomus fasciculatum in he presence of
Sclerotium rolfsii Curzi inoculated simultaneously with the VAM fungus compared to absence
of the pathogen. A reduction in root colonization
of soybean by Glomus mosseae (Nicol. & Gerd.)
Gerd & Trappe was also reported by Zambolim
and Schenck (1983) when Macrophomina phaseolina (Tassi) Goid., Rhizoctonia solani Kuhn,
or Fusarium solani (Mart.) App. & Wr. emend.
Snyd. & Hans, were inoculated simultaneously
with the VAM fungus, compared to the amount
of root-colonization by Glomus obtained in their
absence. This supports the belief that the effect of
a root fungal pathogen on root colonization by a
VAM fungus may be consistent within a system
but could vary in different VAM fungus/root
pathogen/host plant systems under study.
The inoculation of G. intraradices after F.
oxysporum f.sp. radicis-lycopersici resulted in a
substantial increase in root endomycorrhizal
colonization. This phenomenon cannot be
explained at present but it clearly demonstrates
that G. intraradices can colonize roots extensively
despite its introduction 4 weeks after the Fusarium.
This is the first report of an increase in root
colonization by a VAM fungus when inoculated
after a pathogen.
The absence of an effect on plant dry mass when
G. intraradices is inoculated prior to the Fusarium
inoculation is not surprising since the interaction
between the two fungi was monitored for only 5
weeks. In a previous study under the same
experimental conditions (Caron et al. 1986a), G.
intraradices had no effect on plant dry mass over a
12-week period. On the other hand, Fusarium
significantly reduced plant dry mass only after a 10week period of interaction with Glomus. The
observation that the presence of G. intraradices did
not generally result in dry mass increase was also
expected (Caron et al. 1985, 1986a, Fairweather &
Parbery 1982). The inoculation with Fusarium 4
weeks before the inoculation with Glomus resulted
in more root necrosis and plant mortality, and
consequently more plant dry-mass loss, which in
turn enhanced the effect of Glomus on Fusarium.
While the effects of G. intraradices on root rot of
tomatoes and on populations of F. oxysporum f.sp.
radicis-lycopersici appear to be independent of the
sequence of inoculation with the two microorganisms, the effect of the Fusarium on root
colonization by G. intraradices is affected by the
sequence of inoculation. Similar results were
obtained by Kellam and Schenck (1980) in an
16 CANADIAN JOURNAL OF PLANT PATHOLOGY, VOLUME 8, 1986
Downloaded by [North Carolina State University] at 15:29 09 March 2015
interaction study on soybean (Glycine max (L.)
Merr.) between Glomus macrocarpus (Nicol. &
Gerd.) Gerd. & Trappe and the root-knot
nematode Meloidogyne incognita (Kofoid &
White) Chitwood.
This study demonstrates that we need to
investigate not only the mechanism by which VAM
fungi can reduce disease incidence and pathogen
development but also the means by which a fungal
pathogen can enhance root colonization by a VAM
fungus.
The authors thank M. Bernier-Cardou for assistance in
statistical analyses, D. LeQuéré for her technical assistance, and
M. Chartrand for typing the manuscript.
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