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Influence of Salt concentration on infectivity and development
of Meloidogyne incognita on tomato
Ezarug A. EDONGALI
*, Larry DUNCAN,and Howard FERRIS
Department of Nematology, University of California Riuerside, C A 92521, U . S . A .
SUMMARY
I n greenhouse studies, infectivity and development of M . incognita on tomato was impaired by’increasing soil
solution concentrations (ECe 1.5, 2.5, 3.5, 5.0
mmhos/cm) of NaCl,CaCl, or combinations of both salts. In two
experiments, reduced infectivity was pronounced on a susceptible cultivar (Hunts) a t al1 salt concentrations, while
infectivity was reduced primarily a t higher Salt concentrations on a moderately resistant host (Beefmaster). Development of entrant juveniles was significantly depressedby both salts on cv. Hunts, but
merely delayed on cv.Beefmaster. Impaired infectivity and development resulted in population reduction to
23% and 39% of controls on
Beefmaster and Hunts, respectively, six
weeks after infection.
RÉSUMÉ
Influence de la concentration en sels sur l’infectivité et ’le développement de Meloidogyne incognita sur tomate
Au cours d’étudeseffectuées en serres, I’infectivité et le développement M.
de incognita sur tomate ont été d’autant
plus affectés que les solutions de NaCl, de CaCl, ou de ces d e u s sels dans le sol étaient plus concentrées (ECe 1,5 ;
2,5 ; 3,5 ; 5,O mmhoslcm). Au cours des deux expériences, l’infectivité a été réduite à toutes les concentrations sur
un cultivar sensible (Hunts) alors que la réduction de l’infectivité n’a débuté qu’aux concentrations élevées sur un
cultivar modérément résistant (Beefmaster). Le développement des juvéniles ayant pénétré a été réduit significativement par les deux sels sur le cv. Hunts mais seulement retardé
sur le cv. Beefmaster. Six semaines après
l’infection, les altérations causées à l’infectivité et au développement ont amené une réduction de la population par rapport aux témoins de 23 y. sur Beefmaster et 39 y. sur Hunts.
.
Root-knot nematodes (Meloidogyrze spp.) are
worldwide indistributionandareimportant
parasites of a wide range of economically
important plants. Mostspecies of Meloidogyrze
areseriousplantpathogens
in aridand semiarid regions. These regions are characterized by
high evapotranspiration rates, due to high temperature and low relative humidity, which may
result in tremendous accumulationof salts in the
root zone. The chemical composition of the soil
solutiondirectly affects plants(Bernstein,1964)
and nematodes (Bird, 1977). Saline soils contain
variable amounts of cations and anions a t different
concentrations
and
complexities.
The
commondominantanionsarechlorides
(Cl-),
sulfates ( S O P ) , bicarbonates (HC03-),and sometimesnitrate(NOs-).Thecationsarecalcium
(Ca2+),sodium(Na+),magnesium
(Mg2+), and
sometimes potassium (K+).These elements can
exist individually or in combination with otbers
to form complex compounds.
The influence of suchcompoundsonnematode infectivity is unclear. Na+, Cl-, and boron
a t excessive amounts might have specific toxic
effects onplants(Bernstein,1964
; Mengel &
Kirby,1978).
Egg hatching of M . ju.uarzica
decreasedas theconcentration of the electrolytes (NaCl, CaCl,,KC1) increased in the solution media (Dropkin, Martin & Johnson, 1958).
Wallace (1966) studied egg hatch, survival and
’ Present address : Department of Plant Pathology, Faculty
13538, Tripoli, Libya.
Revue Nématol. 5 (1) : 111-127 (1982)
of Agriculture, University
of El-Fateh, P.O. Box
111
E . A . Edongali, L. Duncan di. H . Ferris
developmentunderdifferentmoistureregimes
in which various electrolyte concentrations were
obtained.
Heterodera rostochiensis egg hatching (Ellenby
& Gilbert,,1958),andreproduction
of freeliving nematodes (Everard, 1960), were decreased when exposed to saline media. Prot ( 1 9 7 8 ~ ~
b ; 1979a, b ) observedeffects of moistureand
Salt gradients on movementandbehavior
of
M . jauunica and four other plant-parasitic nematodes.A low soil moisturecontent,combined
with a highertemperatureinthepresence
of
root-knotnematode,increasedthenumber
of
galls in proportion t o t.he size of the root system
(Jones, 1932).
In the absence of a host plant, many plant.
nematodes,
including
Meloidogyne spp.,
can
remain alive for several months
o r even years
(Bergeson, 1959). Survival of citrus nematode in
saline soil has been studied (Kirkpatrick & Van
Gundy, 1966), and under
field conditions more
citrusnematodes
wererecoveredfromcitrus
roots subjected to high salinity (6.5 mmhos/cm)
t h a n fromcitrusgrowing
a t lowersalinity
levels (2.5 mmhos/cm). There is no information
on how long Meloidogyne spp. juveniles survive
and remain infective in saline soils.
The influence of salinity on development of
Meloidogyne species has not been investigated.
Development of Meloidogyne was studied b y
Godfreyand
Oliveira(1932)
on cowpea and
pineapple.Thelength
of timeelapsingfrom
initial inoculation to the first egg development
wasnineteendaysincowpeaand
35 daysin
pineapple.Bird (1959) studieddevelopment of
r o o t - h o t ( M .jauanica and M . hapln) on tomato.
Studies of environmental influence on development includeeffects of temperatxre(Daulton
& Nusbaum, 1966 ; Godfrey & Oliveira, 1932 ;
Jones, 1975 ; Jones, 1932 ; Tyler, 1933b), moisture (Jones, 1975 ; Wallace, 1966) and nutrients
(Oteifa,1953).Thepresentexperimentswere
undertaken to study the influence of increasing
concentrations of varioussaltsoninfectivity
anddevelopment of Meloidogyneincognita on
resistant and susceptible tomato cultivars.
Materials and Methods
-
Thirty-five-day-old tomato seedlings (Lycopersicon esculenturn
.
Mill) of cultivars : Hunts
~.
~
2580 (WessonFood Co.), Beefmaster(Burpee
Seed Co.), and Ronita (PetoSeed Co.) were sown
in vermiculite and grown in a greenhouse. After
35 days,theseedlings
were transplanted t o
insulated styrofoam cups filled with blow Sand
(78%Sand, 14% silt, and 8% Clay). Each cup
was lined with a polyethylene bag
t o prevent
Salt leakage. Plants were then treated according
t o the objectives of the study.
INFECTIVITY
STUDIES
Tendaysaftertransplanting,asolution
of
either sodium chloride (NaCl), calcium chloride
(CaCl,) or a combination of a 1 : 1 ratiowas
added to the cups at different concentrations t o
obtain desired salinity levels. The range of levels
did not exceed those which occur in agricultural
soils. Three days after salinization, 400 freshlyhatched
second-stage
M . incognita juveniles
from greenhouse populations were either inoculated directly or gradually preconditioned to salttreated or untreated soil.
Direct inoculation
Freshlyhatchedjuveniles
were inoculated
direc,tly to salt-treated soil a t ECe levels of 0.0,
1.5, 2.5,
3.5,
and
5.0 mmhos/cm. Inthese
experiments either NaCl, CaCl,, or combinations
of thetwosalts
wereused as salinizers, and
Hunts 2580 andBeefmastertomatoseedlings
were used as hosts. Each Salt and ihe combination treatment were tested in separate experimentswhenBeefmasterwashost,andwere
combined in a singleexperiment when Hunts
was the host. Treat,ments were replicated fifteen
times.Fiveplants
were destructivelysampled
24 hr, 48 hr, and 1 wk after inoculation. Roots
were washed with water and stained in
boiling
acid/fuschin-lactophenol for 2 min. The stained
rootswerewashedunderrunningwaterfor
2-3 min t o remove t.he excessstain, and transferred to lactophenolfordestaining
for a t least
two days. The destained roots were cut free of
the root stub and spread over
glass plates, in
which 3-4 drops of glycerinwereadded,and
pressed
firmly
to
another
glass plate.
The
plates were viewed under
a dissecting microscope
t- o determine
number
of juveniles
- - - thetotal
_ .- -~
.- - __ . _ _ - . .
-
112
,
Revue Nématol. 5 ( 1 ) : 111-117 (1982)
Salt concentration and Meloidogyne incognita
that had penetrated into the root system. The
infectivity percentage was determined by dividing the number of juveniles in the roots by the
total nematodes inoculated.
Precondition treatment
Since sudden exposure to saline soil solutions
might constitute an unnatural shock
t o nematodes, a population of M . incognita juveniles
calibrated at 400 per cup we’re gradually preconditionecl in a Salt gradient (i.e., 1.5, 2.5, 3.5,
and 5.0 mmhos/cm) for 4 hr at every salinity
,levelbeforeinoculation
toeithertreated(5.0
mmhos/cm)oruntreatedsandy
soil. Atthe
same Lime, an equal number of juvenileswas
exposed to distilled water for the same period
and inoculated to treated and untreated
soils.
Inthesetests,threetomatocultivarswere
used
as
indicators
of nematode
survival
:
Beefmaster,Hunts
2580, andRonita.Each
treatment was replicated five times and harvested 1 week after inoculation. Roots were processed and infectivity determined as above.
’
DEVELOPMENTAL
STUDY
Ten days after transplanting,
NaCl or CaC1,
were added to the soil in solution t o establish
an ECe of O, 3.5 and 5.0 mmhos/cm a t equilibrium.Nematodes were inoculatedasbefore.
Soi1 andairtemperatureswererecordedfor
theduration of theexperimenh.Plantswere
washed from five pots every weelt for six weeks
from each treatment and cultivar. Roots were
prepared and examined as before and developmental stages of the nematodes were recorded.
Time and temperature relations were expressed
in heat units (hu): each centigrade degree above
10.5for
1 hourcontributing
1 effective unit
(Tyler,
1933b).
Summation
of these
units
provide a measure of the heat unit requirements
for a given stage of life history exposed to any
Salt type and concentration. The stages recorded
were : ( i ) second-stage juvenile (J,) ; ( i i ) thirdandfourth-stage
(JJ,) combinedbecause
of
the difflculties in ’ differentiating them ; (iii)
mature females ( 9 ) ; and (iu) number of egg
masses (E.M.) produced.
Revue Némaiol. 5 (1) : 111-117 (1982)
Results
INFECTIVITY
Direct inocula,tion
Nematode infectivity was lower on non-Salt
treatments of Beefmaster than those of Hunts
(Tab. 1 & 2). Underpresentconditions, however, Beefmaster did not show strong resistance
t o nematode penetration. The trend
of al1 Salt
treatments on Beefmaster was for
lower infectivityas EC, increased.Thistrendwasstatistically
significant
only
inthe
CaC1, and
c,ombination t.reatments. CaC1, treatments generally showedsignificantreductionsonly
at
the higher Salt concentrations, but combination
of thetwosaltshadasynergistic
effect on
penetration during the first day. Infectivity
on
subsequent daysshowed little difference between
effects of CaC1, and combination Salt treatments.
Whenthemoresusceptiblecultivar,Hunts,
was used asan indicator ilost, (Tab.
2), increased
ECe againtended t o reduceinfectivity.Salt
effectswere generallymorepronouncedearly
intheexperimentandeachtype
of Salt as
well as the combination treatment significantly
reducedinfectivity.Althoughthecombination
treatmentsgavesomewhat
lower infectivity
after 24 hours than the other treatments, the
differences were not as strilting as those obtained
on Beefmaster.
Precorzdition treatrnent
Penetration by unpreconditioned larvae was
not suppressed in Salt treated soils to levels as
low as in the previous experiment. Nematodes
whichweregraduallypreconditioned
t o high
Salt levelsbefore inoculationpenetratedroot
systems of both varieties as well in salt-treated
soilsas
inuntreated
soils. Unpreconditioned
larvaepenetratedroots
of plants in al1 treatments at a
significantlyhigher ratethandid
preconditionedlarvae.
In severaltreatments,
unpreconditionedlarvaehadhigherrates
of
penetration in soils of EC, 5.0 mmhos/cm t h a n
inuntreated soils incontrast t o theprevious
experiment.
113
E. A . Edonqali, L . D u n c a n dl- H . Ferris
Table 1
Effect of different salinizers on M . incoqnita second stage juveniles infectivity
t o Beefmaster tomato seedlings.
N a Cl
CaCl,
NaCl
DaY
12.8a
mmhoslcm
1
0.0
1.5
2.5
3.5
5.0
10.8a
15.2a
14.4~1
12.8a
2
7
I
2
7
22.4a
22.5a
21.4a
22.7a
20.5a
26.4a
24.8a
21.5a
21.0a
21.5a
12.5b
11.3b
10.3b
8.8b
4.3a
15.9b
14.8b
15.8b
7.9a
9.la
15.8b
15.6b
18.8b
17.8b
10.7a
+ CaC1,
DaY DaY
2
1
7
22.4~
16.4b
13.5b
12.lb
3.6a
21.lb
O.Oa
O.Oa
O.Oa
O.Oa
26.2~
18.8b
14.8a
11.Sa
11.2a
Table 2
Effect of different salinizers on M . incoqnita second stage juveniles
infectivity t o Hunts 2580 tomato seedlings
ECe
mmhoslcm
1
0.0
1.5
2.5
3.5
5.0
19.8~
13.2b
12.6b
9.8b
2.0a
NaCl
CaCl,
NaCl f CaCl,
DaY
Day
DaY
2
Y
1
26.5~
16.3b
15.6b
‘14.5b
9.8a
37.0b
23.la
19.5a
21.3a
18.8a
19.8b
Y
2
12.la
9.9a
10.4~1
8.3a
26.533
18.3a
15.1~1
14.la
13.3a
37.0b
24.3~1
23.3~1
20.2~1
19.la
1
2
Y
19.8~
7.5b
8.9b
6.2b
0.3a
26.513
15.6a
17.2a
14.2a
10.3a
37.0b
21.3~1
17.9a
20.2a
19.7a
Table 3
Effect of NaCl and CaCl, as salinizers on development of root-knot nematodc (Meloidoqyne incoqnita)
on Lycopersiconesculentum cv.Beefmaster
,
Physioloqical
ECe
time of exposure (mmhoslcm)
( h u > 10.5 OC)
2 092
4 O00
6 380
8 060
10 268
13 054
A =
-
-.
B =
114
NaCl as salinizer
CaCl,
as salinizer
. -_
- -_
52
47b
49b
14a
4a
la
3a
O
3.5
5.0
O
3.5
5.0
O
3.5
5.0
O
3.5
5.0
O
3.5
5.0
O
3.5
5.0
3
-
309b
42a
2%
__
- -
Stage of Development
J3/J4
9
A
E.M.
52
Stage of Development
53/54
9
E.M.
48b
67b
20a
198b
118a
l21a
60a
40a
85b
4
2
137b
67a
55a
194b
145a
I38a
200a
182a
175a
19%
172a
165a
26a
50a
38a
142c
60b
39a
156c
60b
39a
199b
113a
lOla
15a
49b
42b
2
10a
2a
2a
38 1
144
-
1
5
16
8
60a
56a
68a
202c
144b
112a
182b
186b
137a
183a
184a
150a
29 a
35a
Ila
104b
41a
37a
173b
60a
56a
Salt concentration and Meloidogyne incognita
Table 4
Effect of NaCl and CaCI, as salinizers on development of root-knot nematode ( M . incognita)
on Lycopersicon esculentum cv. Hunts 2580
Physiologieal
ECe
time of exposure (mmhoslcm)
( h u > 10.5 O C )
2 092
4 O00
380
6
8 060
10 268
13 054
0.0
3.5
5.0
0.0
3.5
5.0
0.0
3.5
5.0
0.0
3.5
5.0
0.0
3.5
5.0
0.0
3.5
5.0
J2
Stage of Development
J3/J4
P
105b
75ab
70a
5ab
10a
16b
3
-
-
-
-
-
-
240c
202b
110a
27a
1.18b
140b
-
6
-
-
-
690c
250b
153a
.52
-
4
-
(l)
E.M.
-
-
-
-
-
96b
102b
25 a
209c
134b
89a
250c
19413
153a
250c
201b
155a
-
-
122c
63b14a
1Oa
49b
62b
20a
110b
80ab
69a
J 3 / J 4J 2
Stage of Development (,)
0
E.M.
106b
64a
55a
la
1l b
1Ob
-
-
88a
85a
8
-
-
69b
1077b
237a
218a
-
-
-
-
244c
77b
45a
29a
10a
50b
-
-
1
21
-50b
-20a
-
ll0b
73a
74a
149b
216b
98a
1 86a
: 22633
8a
109a
l a40a 104a
-
-
78b
8a
Oa
115b
22a
= NaCl as salinizer
(z) = CaCl, as salinizer
(l)
DEVELOPMENT
Discussion
Larval penetration of roots of both cultivars
showed the same trends of suppression a t high
Salt concentrations as .in the direct penetration
experiment(Tab. 3 & 4).Developmentup t o
and including the fourth stage (J4)required a t
least 4 O00 hu. 'Total numbers of J3/J4 were
significantlydepressed
bythe two Salt types
andconcentrationsonHunts,
while on Beefmaster,development
wasmerelydelayed.
A
similartrendwasnotedwithdevelopment
of
mature females. At 6 380 hu most Salt treated
plantshadsignificantly
fewer mature females
than
control
plants.
This
trend
remained
throughout the experiment on Hunts (Tab. 4),
but differencesbetween
treatmentsgradually
became non-significant on Beefmaster (Tab. 1).
Production of eggmasseswasdepressed
by
increasedsalinity on bothcultivars,although
the differenceswere
not significant on Beefmaster until 10 268 hu. Reflecting this trend,
initial penetration by second generation larvae
(13 054 hu) was significantly depressed in Salt
treated plants.
Thecharacteristics of thenematodewhich
increase its chances of invasionare important
because of the limited time available for infection.
Wallace
(1966b) suggested t h a t newly
hatchedjuvenilesremainactive
for alimited
time of about 4-8 days. We found inal1 cultivars
tested,thatinfectivity
was maximum by the
7thdayafterinoculation.Wallace(1966a,
b)
considered that the probability that juveniles
will invade a root depends on many factors
:
(i) the presence of a host root ; (i;) the proximity
of the root ; (iii) the speed of the nematode ;
(iv) the tortuosity of the track the nematode
takes in reaching the root
; and ( u ) the speed
of penetration.The
presence of highlysusceptible hosts increases the chance of the nematode to invade the roots. This
was true when
Hunts2580 wasusedasanindicator.The
soil environment around a host root is also very
important in determining the fateof nematodes.
Juvenile penetration was affected by tlle concentration and perhaps the type
of Salt in the
soil solutions. Prot (1978u, b ; 1 9 7 9 ~ )observed
Reuue Néinatol. 5 (1) : 111-117 (1982)
115
E . A . Edongali, L. D u n c a n & H . Ferris
~
__
.
t h a t juvenile r o o t - h o t nematodes
migrate
towardlower Salt concentrationsregardless of
the presence of a host. Present findings do not
indicate whether high Salt concentrations interfere with nematode sensory perceptionor reduce
its ability t o penetratebyothermechanisms.
Depletion of body contents in juveniles occurred when exposed t o gradua1 increases in salts,
possiblyawounting forlowerinfec,tivitydue
to reduc,ed metabolicactivityandmovement
in the soil, which c.ould inhibit the search for
infection sites.
At liigher Salt concentration,calciumtranslocat,ion in the xylem is reduced, which in turn,
may depress the growth of meristematic tissues
(Mengel & Kirlcby,1978). Thiscould-lead t o
fewer roots available for infection. Mengelancl
Kirkby (1978) also reported that NaCl salinity
affects theincorporation
of inorganic N and
thus
depresses
prot,ein synthesis
in
young
plants.
This
leads
t o growt.11 inhibition
in
youngrootmeristematictissues,whichwas
observed in Hunts, but not Beefmaster.
However, sincepreconditionedjuvenilesdisplayed
markedly
reduced
penetration
of roots
in
untreated soil, it is unlikely that direct alteration of plants or plant attractants by high Salt
levels is a sole cause of reduc,ed penetration.
It is unknown whet,her Salt-aclapted populat.ions evolve in saline field situations, however,
simple
preconditioning
treatments
had the
effect of reducing and even reversing penetration trends noted in direct inoc.ulation experiments. Such results may indicate that sudden
osmoticsbock c.aused reduc.ed penetrationin
the direct inoc,ulation series. These data suggest
t h a t reducedpenetrationmaynotoccurin
response t o salinityinnaturallycondit.ioned
field populations. However, reduced penetration
in response t o salinity .was noted in the direct
inoculation studies and the development studies,
while inthe preconditioningseriesevennonpreconditioned larvae exhibited greatly reduced
penetmtion in al1 treatments. For this reason,
it is
unclear
whether
unidentified
variables
confounded theresults of prec,onditioning on
penetration.
Alterat,ion in plantgrowihdue
t o excess
salinity suc.11 as those citecl abovearemore
likely t o influenc,e development of established
parasites, Tyler- (1933a),~and GtlIe_rs &_ve sug-
116
gested t h a t a healthycondition of thehost
plant is important for the development of its
parasite,s. Greater numbers of J,, J, and adult
parasites were observed than infective J, stages.
This is due to difflculty in observing the slender
J, stage and perhapssuggests t h a t infectivity
test,s can be delayed until entrant larvae undergo
furtherdevelopmentand
bec.ome moreeasily
visible.Theinfluences
of saltsonnematode
development
appeared
more
pronounc.ed on
Hunts than Beefmaster. Developmentt o mature
females in Beefmasterwasdelayedby
salt.
treatments,butby
13 054 hu there wereno
significant differencesbetween treatments.Numbers of egg masses a t 13 054 hu remained significantlydifferentfromcontrolplants,although
newly mature females inSalt treated plants may
have been capable of further egg production.
Whetherdevelopment
is
merely
delayed.
or
permanently impaired on these cultivars, plants
will be subjected t o fewer total nematodes and
populations a t t h e end of the season should be
reduced.Suchfindingshaveimplimtionsin
terms of development of plantdamage Eunctions
and
nematode
population
models
for
plantsgrownunderhighsalinityconditions.
Areas of related
interest
are
plant
grow!h
responses to sa1init.y which may interact, with
nematode
pathogenesis,
and
the
ability
of
nematode eggs andlarvaetosurviveinthe
absence of hosts in saline soils.
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L. (1964). Salt tolerance of crop plants.
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__
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R. W.
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