Original article
The effects of ectomycorrhizal status
on carbon dioxide assimilation capacity,
water-use efficiency and response to transplanting
in seedlings of Pseudotsuga menziesii (Mirb) Franco
JM Guehl J Garbaye
1 INRA Centre de Recherches de
Nancy,
Laboratoire deBioclimatologie
et
d’Écophysiologie Forestières,
54280Champenoux;
2
INRA Centre de Recherches de
Nancy,
Laboratoire deMicrobiologie Forestière,
F 54280Champenoux,
France(Received
30 March1990; accepted
5 December1990)
Summary —
Oneyear-old Douglas
firseedlings, mycorrhizal
with Laccaria laccata or with Thele-phora
terrestris and grown at two levels ofphosphorus
in the nutrient solution(10
and 40mg·l -1 P),
were
compared
for water relations and gasexchange
before and aftertransplanting
innon-limiting
water conditions. The results show
that i),
L laccata is more efficient than T terrestris inincreasing photosynthesis
and water useefficiency, ii), phosphorus deficiency
reducesphotosynthesis
and wa-ter use
efficiency, iii),
thestimulating
effect of L laccata onphotosynthesis
and water useefficiency is,
at leastpartly,
due to theimprovement
ofphosphorus nutrition, iv),
thephotosynthesis
reductionresulting
fromtransplanting
is due to a non-stomatalmechanism,
andv),
the recovery ofphotosyn-
thesis involves the
regrowth
of the externalmycelium
ofmycorrhizas.
These results are discussed from theviewpoint
of theplant-fungus relationships.
ectomycorrhizae
/phosphorus
nutrition /CO 2
assimilation / water-useefficiency
/transplant- ing
Résumé — Effets du statut
mycorhizien
sur lacapacité
d’assimilation deCO 2 ,
l’efficience d’utilisation de l’eau et laréponse
à latransplantation
de semis dePseudotsuga
menziesii(Mirb)
Franco. Des semis de 1 an dedouglas, mycorhizés
par Laccaria laccata ouThelephora
ter-restris ont été élevés durant une saison de croissance à 2 niveaux de
phosphore
dans la solution nutritive(10
et 40mg·l -1 P)
et ont étécomparés
dupoint
de vue des relationshydriques
et deséchanges
gazeux avant etaprès transplantation (à
2 datesdifférentes,
en octobre et enfévrier)
enconditions
hydriques
non limitantes. A faible niveau dephosphore,
lesplants
inoculés par L laccata avaient une surface foliaireplus importante
que lesplants mycorhizés
par T terrestris(tableau 1) et
étaient
également
caractérisés par des taux d’assimilation deCO 2
et d’efficiencephotosynthétique
d’utilisation de l’eau
plus
élevés(tableau
II etfig 1).
La carence enphosphore
réduit laphotosyn-
thèse et l’efficience d’utilisation de l’eau
(tableau II, fig 1).
L’effet stimulant de L laccata sur l’effi- cience de l’eau estdû,
au moins enpartie,
à l’amélioration de la nutrition enphosphore (fig
7 et9).
La réduction de la
photosynthèse
consécutive à latransplantation (fig 2),
bienqu’accompagnée
par une fermeturestomatique (fig 3),
est dûe essentiellement à un mécanisme nonstomatique (fig 4)
etn’est pas liée à une altération de l’état
hydrique
et nutritionel(fig
7et 8)
desplants.
Le rétablissement de laphotosynthèse après transplantation
est concomitant à larégénération
racinaire(fig 5),
mais sondéterminisme
implique également
lareprise
d’activité duchampignon (fig 6).
Ces résultats sont discu- tésdu point de
vue des relationsplante-champignon.
ectomycorhize
/ nutritionphosphatée
/ assimulation deCO 2
/ efficience de l’eau /transplanta-
tion
INTRODUCTION
Ectomycorrhizal symbiosis is essential for nursery-grown conifer seedlings and is de-
terminant for plant
survivaland growth af-
ter
outplanting (Marx
etal, 1977; Le
Tacon etal, 1988). It is also known that different
fungal associates
do notprovide
the samebenefit
in thisrespect, through
mecha-nisms as
diverse
asimproving
mineral ab-sorption
andassimilation affecting hormo-
nal balance in the plant, enhancing the
contact
between
roots andsoil,
and pro-tecting
rootsagainst
disease(Chalot et al, 1988). This paper describes and discuss-
es
the physiological
status of oneyear-old Douglas
firseedlings, associated with
two differentectomycorrhizal fungi
and grown at twophosphorous levels,
beforethey
were
lifted. The behaviour of the
sameseedlings transplanted in controlled condi- tions
wasalso considered.
The results presented
here arepart of
aproject which
isaimed
atunderstanding
the role played by the fungal
associatesduring
thetransplanting shock
sufferedby
forest plants when outplanted,
even innon-limited water
supply
conditions(Guehl
et
al, 1989).
Gasexchange parameters (CO
2 assimilation rate, transpiration rate,
water-useefficiency)
wereused
asphysio- logical
criteria formonitoring
the behaviour ofplants
with differentectomycorrhizal
status.
MATERIALS AND METHODS
Plant material
Douglas
fir(Pseudotsuga
menziesii(Mirb)
Fran-co) seedlings
were grown in the summer in aglasshouse,
in 95 ml containers filled with 1/1(v/
v) vermiculite-sphagnum peat
mix inoculated with theectomycorrhizal fungus
Laccaria lacca- ta or non-inoculated. Inoculum wasmycelium aseptically
grown for two months inglass jars,
ina
vermiculite-peat
substrate moistened with nu- trient medium.Twenty
per cent(v/v)
inoculumwas mixed with the
potting
mix beforefilling
thecontainers. Each inoculation treatment was wa-
tered with a
complete
nutrient solution contain-ing
either 10 or 40mg·ml -1 phosphorus
asNa
2 PO 4
.
Eachfungus-phosphorus
level treat-ment involved 120
seedlings.
At the end ofSep- tember,
whengrowth stopped
and buds were set up, a randomsample
of 6seedlings
per treatment was observed formycorrhizas
with astereomicroscope
aftergently washing
the rootsystems. Ectomycorrhizal development
was rat-ed
according
to a four-level scale(0:
no mycor-rhiza;
1: raremycorrhizas;
2: severalconspicu-
ous
mycorrhizal
clusters and/ormycorrhizas
disseminated
throughout
the rootsystem;
3: my- corrhizas abundant in allparts
of the root sys-tem).
Three treatments were chosen for subse-quent
measurements andanalysis:
- Tt low
phosphorus level,
noninoculated,
my- corrhizal with contaminantThelephora
terrestris(mycorrhizal rating: 1.6);
-TtP:
high phosphorus
level,non-inoculated, mycorrhizal
with T terrestris(rating: 2.4); ]
- LI: low
phosphorus level,
inoculated with Lac- carialaccata, predominantly mycorrhizal
with Llaccata
(rating: 2.6)
andslightly
contaminated with T terrestris.Sampling
andexperimental set-up
The
seedlings
werekept
in a frostlessglass-
house
during winter,
withoutfertilization,
under conditions such that aerialgrowth
wasstopped
from October to March. Two sets of measure- ments were
performed:
in November and in Feb- ruary. At eachdate,
20plants
per treatmentwere
randomly picked
among the 50% tallestones. Before
transplanting,
6-8 of theseplants
were used for gas
exchange
measurements and fordetermining
thephosphorus
andnitrogen
content of the needles. The 12
remaining plants
were used for gas
exchange
measurements andtransplanted
as follows:they
wereimmediately lifted,
their rootswashed,
andmycorrhizal
devel-opment
wasquantified.
Thegrowing
white roottips
weresectioned,
and theseedlings
wereplanted
insphagnum peat
in flat(3
cmthick)
containers with a
transparent
wallallowing
ob-servation of the roots. These containers were
placed
in a climate chamber under thefollowing
environmental conditions:
photoperiod,
16h;
airtemperature,
22 ± 0.2°C(d)
and 16.0 ± 0.2°C(night); photosynthetic photon
fluxdensity (400-
700
nm),
400μmol
m-2s-1provided by
fluores-cent
tubes;
relative airhumidity,
60%(day)
and90%
(night);
ambientCO 2
concentration(C a ),
420 ± 30
μmol·mol -1 . They
were watered twicea week with the 10
mg·l -1
P nutrient solution in order to maintain the moisture of thepeat
near fieldcapacity.
Water status, gas
exchange,
root regenera-tion
(number
ofelongated
whitetips),
and re-growth
ofmycorrhizal
extramaticalmycelium (quantified according
to the samerating
scaleas
above)
were assessed 4, 11 and 18 d aftertransplanting.
At the end of each
experiment,
theseedlings
were
processed
fordry weight
and leaf area de-termination. Needles were then oven-dried
(60°C
for 48h)
and mineralanalyses
were per- formed(February only).
Water status and gas
exchange
measurements
Predawn needle water
potential (ψ wp )
was deter-mined on one needle per
seedling prior
to thegas
exchange
measurementsby
means of aScholander pressure bomb
specifically
devisedfor measurements on individual conifer needles.
For the November
experiment,
theplants
were taken from the climate room to a laborato- ry where gas
exchange
measurements weremade
by
means of an opensystem consisting
ofthree assimilation chambers connected in
paral-
lel in which the environmental factors could be controlled. Measurements were made at 22.0 ± 0.5°C air
temperature,
10.6 ± 1.0 Pa·kPa-1leaf- to-air water vapour molar fractiondifference,
400
μmol·m -2 ·s -1 photosynthetic photon
fluxdensity (400-700 nm)
and 350 ± 5μmol·mol -1
ambient
CO 2
concentration(C a ).
For the
February experiment,
gasexchange
measurements were made in the climate room
with a
portable gas-exchange
measurement sys- tem(Li-Cor 6200, Li-Cor, Lincoln, NE, USA).
The
CO 2
concentration in the climate room waskept
constant(C a
= 425 ± 15μmol·mol -1 ).
Gas
exchange parameters (CO 2
assimilation rate,A;
leaf conductance for water vapour, g; in- tercellularCO 2 concentration, C i )
were calculat-ed with the classical
equations (Caemmerer
andFarquhar, 1981) taking
into account simultane-ous
CO 2
andH 2 O
diffusionthrough
the stomatal pores. IntercellularCO 2
concentration(C i )
calcu-lations were
performed
in order to assesswhether differences for A between treatments and A
changes
in response totransplanting
were due to
chloroplastic
or to stomatal factors(Jones, 1985).
Previous measurements madeon conifers
(unpublished data)
did not show anypatch pattern
in stomatalclosure,
so that relia- bleC i
calculations can beperformed
from leafgas
exchange
data. Moreprecisely, CO 2
assimi-lation rate was considered in an
(A, C i ) graph
asbeing
at the intersection of two functions:i),
thephotosynthetic CO 2
demand function(D)
whichdefines the
mesophyll photosynthetic capacity
and, ii),
thephotosynthetic CO 2 supply
function(Su) defining
the diffusional limitation toCO 2
as-similation. For
determining
the(D) functions, C a
was varied
stepwise
and A andC i were
calculat-ed for each
step.
The Su function is a line withan x-axis
intercept approximately equal
toC a
and a
negative slope approximately equal
to -g(Guehl
andAussenac, 1987).
Water-use effi-ciency (WUE)
was determined as theA/g
ratio.At the end of the
experiment,
theseedlings
were harvested and
plant
material wasseparat-
ed into differentcompartments (needles,
stemsand root
systems).
Eachcompartment
was oven-dried at 60°C for 48 h andweighed.
Thedried needles were
kept
for mineralanalysis.
Projected
needle areas of theseedlings
were
determined
with a video cameracoupled
to an
image analyser (ΔT area
meter; ΔT devic- es,Cambridge, UK).
Mineral analyses
The total
nitrogen
content of the dried andground
needles was determined with a C/Nanalyser (Model 1500;
CarloErba, Italy).
Thevalues obtained with this
technique
are about10%
higher
than those obtained with theKjel-
dahl method. The
phosphorus
concentrationswere determined after pressure
digestion
of theground
material with 100%HNO 3 ,
at 170°C for6 h
(Schramel
etal, 1980)
with a direct currentplasma
emissionspectrometer (Model Spectro Span 6;
BeckmanInstruments, USA).
RESULTS
Plant
size
and biomassData relative
tothe size and biomass of the February seedlings (before transplant- ing)
aregiven
in table I. Stemheight
washighest
inthe
TtP andLI
treatments.Root
collar diameter and totaldry weight
weresignificantly higher
in TtP than in the othertreatments,
whereas there was nosignifi-
cant
difference
inthe root/shoot ratio be-
tweenthe different
treatments.Needle
area was
significantly higher
inTtP and
LIthan in
Tt. The seedlings of the different
treatmentsdid
notexhibit significant differ-
ences in
their specific leaf dry weight (ratio
of needle dry weight
toneedle area).
Gas exchange and
water-useefficiency
Table
IIgives the
meanvalues
ofCO 2
as-similation
rate(A), stomatal conductance
(g) and
water-useefficiency (WUE
=A/g)
in the different treatments
before
trans-planting,
inthe
2experiments.
TtP and LIexhibited
Avalues significantly higher than
those in Tt both in November and in Febru- ary. A
washigher
inTtP than in LI in No-
vemberbut
not inFebruary.
InNovember, TtP
was characterizedby g
valuessignifi- cantly higher
thanthose in the other
treat-ments, while in February there
was nosig-
nificant difference for this parameter.
Water-use efficiency in TtP and LI
wassignificantly higher than that in Tt in both
experiments. There
was nosignificant dif-
ferences between TtP and
LI.For
agiven treatment,
theWUE values
wereidentical for the
twoexperiments.
Figure
1gives
aninsight into the WUE
regulation
at the individual levelprior
totransplanting. The regression
lines wereforced through the origin
sothat their
slopes (water-use efficiency) could be compared. In November
aswell
as inFeb- ruary, the invididual variability of the plots
relative
to treatmentsTtP and
LI was or-dered along the
samelinear relationship expressing proportionality between A and g and thus constancy of WUE both for the
individualplants
and the twodates.
In con-trast,
treatment Ttdid
notexhibit such
acontrol of WUE
atthe individual level since
no
significant (P
<0.05) correlation be- tween A
andg
wasobserved for this
treat- ment.Moreover,
theplots of the latter
treatmentoccupied
alower position
inthe (A, g) graphs, thus indicating lower WUE.
Transplanting resulted in
amarked de-
crease
of A between day
0and day
4in all
treatments
and for
the 2 measurement pe-riods (fig 2).
InFebruary,
thedecrease of A continued until
18 d aftertransplanting for
treatment
LI, while
aslight recovery of A
was
observed
fromd
4 in treatments Tt and TtP. Such a recovery was not appar- ent inNovember,
when the decrease in Awas more
pronounced in the TtP seedlings
than
it
was inthe LI seedlings, since the A values of these
treatments weresignifi- cantly different
atday 0, but
were notdif- ferent
18d after transplanting (fig 2). In February,
avery different pattern
wasob- served with the decrease of A being the
most
pronounced
in LI.Transplanting also affected g (fig 3) in
amanner
approximately identical with
the ef-fects
onA. However,
thedecrease
ofg
was less
pronounced
than that ofA, partic- ularly during the first
4d
aftertransplant- ing. In February, the recovery
ofg
in treat- mentsTtP and Tt took place only from d 11, and
arecovery of g
wasalso observed
in treatmentLI.
In
figure
4 thegas exchange
data offig-
ures 2 and 3 are
presented
in A vsC i graphs. For both
measurementperiods
and in all
treatmentsthe decline of A in
re-sponse
totransplanting
wasaccompanied by increasing C i , and
wasprimarily due
toalterations
inthe photosynthetic demand
for
CO 2 while the supply function (related
to
stomatal conductance)
wasaffected only
to a minor extent.Root and mycorrhizal regeneration
Root (fig 5) and mycorrhizal (fig 6) regener-
ation of thetransplanted seedlings
oc-curred from d 11 after
transplanting
in No-vember,
and fromd
4 inFebruary. Root regeneration
wasthe highest
in treatmentTtP for both periods and
wasmarkedly
lower
in the other treatments(fig 5). The
seedlings of
treatmentTtP also had the
highest mycorrhizal regeneration
inFebru-
ary
(fig 6),
but not inNovember. Mycorrhi-
zal
regeneration in
the LI treatment wasidentical
tothat
in TtPand superior
tothat
in Tt
inNovember, but
wasnoticeably low-
er
than that in the other
treatmentsin Feb- ruary.
Water
and nutrient statusNo significant alteration in
ψ
wp
wasob-
served after
transplanting
in any of the treatmentsand
all treatmentshad similar
ψ
wp values ranging
from -0.8 to -0.6MPa (data
notshown).
Before transplanting, needle P
concen-tration was
significantly higher
inthe TtP seedlings than
inthe other
treatments(fig 7). Treatments Tt and
LIhad identical
nee- dle Pconcentrations
inNovember,
while inFebruary the needle P
concentration wasslightly
butsignificantly higher
in LI than inTt. In February, transplanting significantly
reduced
the
needle P content inTtP,
whilethis concentration remained
unchanged
inthe other
treatments.Needle
Nconcentration
inthe LI
treat- ment wassignificantly lower than those of
treatmentsTt and TtP in November and lower than
inTtP
inFebruary (fig 8). The seedlings
of treatmentTt had higher
Nconcentrations
inFebruary (fig 8). The seedlings
of treatment Tt hadhigher
Nconcentrations in
February
than in Novem-ber,
while noseasonal changes
occurredin
the other
treatments.Transplanting had
no
significant effect
onneedle
N concen-tration
inany of the
treatments.Gas exchange parameters
ofthe indi- vidual plants
wereexamined
withrespect
to
their needle nutrient
status.There
wasno
relationship
between theseparameters
and the
needle
N concentrations. Therewas a
significant correlation between A and needle
Pconcentration only
in treat-ment Tt
(fig 9a),
inthe other treatments A
was not
related
to P.Stomatal conduc-
tance wassignificantly correlated with P
via
aparabolic function (fig 9b), with the
minimum of g
occurring
at about 2000μg·g
-1 P in the needles. The clearest pic-
ture of
limiting
effect due to P was ob- servedrelative
tothe WUE data shown
infigure
9c:there
was aclose linear
relation-ship between
WUE in treatmentTt, while the plots relative
to treatmentsLI and TtP
occupied
thenon-limiting
Pregion (P
con-centration
superior to
700μg·g -1 )
of thegeneral relationship.
DISCUSSION
The seedlings
associatedwith
T terrestrisand supplied with
anon-limiting (40
mg·
l
-1 (P)
nutrientsolution
weretaller and
had ahigher
biomass thatthe seedlings
associated with
Tterrestris
butsupplied
with a 10
mg· l -1 (P) solution. Seedlings
mycorrhizal with
Llaccata and grown
un-der limiting
P conditions(10 mg· l -1 P)
were taller than the
seedlings infected with T terrestris and supplied with the
same so-lution (table I). However, both
root collardiameter
and totalplant
biomass were notsignificantly different between the
twolat-
ter treatments.Harley and Smith (1983) and Guehl et al (1990) have reported simi-
lar results
indicating i), that the
extent towhich
growth
wasaffected by ectomycor-
rhizal infection will
depend
onthe fungal species and
strain used asmycobiont
andii), that there
maybe
adiscrepancy
be-tween
effects
ofmycorrhizae
on stem el-ongation
on the one hand and ondiameter
and
weight growth
onthe
other.Tyminska
et
al (1986) observed higher biomass growth
in Pinus silvestrisseedlings
infect-ed with
Llaccata than in seedlings
infect-ed with
Tterrestris
over awide range of
Pconcentrations
innutrient solution (0.1-31
mg·
l -1
). These
authorsalso observed
thatthe difference in biomass
between the two treatments was notaccompanied by
asig-
nificant
difference
in needle P concentra-tion,
andsuggested the stimulating
effectof
Laccaria laccata -
evenobserved in
seedlings
with alow percentage of mycor- rhizal
roots - tobe related
tothe capacity
of this fungus
toproduce growth regulators
such as
indole
acetic acid(IAA). They
sup-ported this assumption by the work of Ek
etal (1983) who found that the
same strain of Llaccata produced large quanti-
ties of
IAA. Inthe present study
withPseu- dotsuga menziesii
asthe host plant, significant differences
inneedle
Pconcentrations
werefound between Tt and
LI(figs
7 and9). Furthermore,
needle Pconcentration
in LI wasintermediate
be- tween those in Tt andTtP.
Thatthe growth stimulating effect
ofLaccaria
laccata ismediated,
at leastpartially, by
a P nutri-tional effect
cannot beprecluded here.
In the present study, the superiority of
Llaccata
ascompared
to Tterrestris
wasalso
observed
relative to theCO 2 assimila-
tion
characteristics
of theseedlings
atthe
end of the first
growing
season. As com-pared with
the Ttseedlings,
needlesurface
area
(table I)
andCO 2 assimilation
rates(table II)
of theLI seedlings
were about 42and 48%
higher, respectively,
thusconfer- ring
tothe
LIseedlings
awhole plant CO 2
assimulation capacity
about 2.1 timesthat
in the Ttseedlings
andapproximately equivalent
to that in the TtPseedlings.
Several
authors(Jones and Hutchinson, 1988; Guehl
etal, 1990) have reported
similar modulations
ofhost plant CO 2
as-similation
capacity
due to the nature ofthe mycobiont. CO 2
assimilation rate wasclearly
Plimited
in treatment Tt(fig 9a).
Using 31 P
nuclearmagnetic
resonance,Foyer
andSpencer (1986) studied the ef- fects of reduced phosphate supply
on in-tracellular orthophosphate (Pi) distribution and photosynthesis
in Hordeumvulgare
leaves.
They observed
thati),
over awide
range of leaf Pi, the cytoplasmic
Pilevel
ismaintained
constant,
while thevacuolar
Pi is allowed to fluctuate inorder
tobuffer the
Piin the cytoplasm and ii), that
anoverall
minimum
cytoplasmic Pi concentration of between
5-10mmol· l -1 is required
to sus-tain
optimal
ratesof photosynthesis
in thelight. Despite
therelatively high
P concen-trations found in
ourstudy
inall the LI and TtP seedlings,
someseedlings of these
treatments
exhibited
verylow
Avalues (fig 9a). Thus, other limiting
factors arelikely
tobe involved.
Water-use efficiency
washigher and
less variable
in LI than inTt (table II, fig 1).
Guehl
et al (1990)
observed thatPinus pin-
ea
seedlings associated with different
ec-tomycorrhizal fungi
werecharacterized by higher and less variable
WUE valuesthan
non-mycorrhizal plants. This result is
ofgreat importance, since it indicates that
ec-tomycorrhizal
infection mayconfer
en- hanceddrought adaptation
tothe
hostplant,
notonly by improving
wateruptake (Druddridge
etal, 1980)
andplant
waterrelations (Boyd
etal, 1985), but also through higher WUE. In the present study,
the data of
figure
9csuggest that
the im-provement of
WUE in the L laccariainfect- ed seedlings
ascompared
tothe
T terres-tris seedlings is mediated by
anutritional P effect involving both
effects onA (fig 9a)
and
g (fig 9b). It is worth noting that there
was a
clear tendancy
forg
to beincreased
when totalleaf
P was lower than 2 000μg·g -1
.
InZea mays, Wong
etal (1985)
observed
adramatic decrease
inA without
any effect on WUE(A/g ratio)
when P inthe nutrient
solution wasdecreased
from 41 to 1.2mg·l -1 . However,
inPinus radia- ta, Conroy et al (1988) found
lowerWUE
inP deficient
plants (needle
Pconcentration
700-800μg·g -1 )
than in non deficientplants (needle
Pbetween
1 000 and 1 500μg·g -1
). Thus,
their critical value(800 ug·g
-1
)
was the same as in ourexperi-
ments.
Harris et al (1983) found that
inleaf
discsof Spinacia oleracea,
lowP i led
to aloss of stomatal
control and
widestomatal apertures, while high
Pi inducedstomatal closure.
Inthe
samespecies, Herold (1978) observed that
mannose anddeoxy- glucose induced wilting by metabolically sequestering
Pi.Feeding
Pi deficientHor-
deumvulgare and Spinacia
oleracea cutleaves with Pi
through
thexylem transpira-
tion
flow, Dietz
andFoyer (1986) observed
a
short-term (5 min)
increase inCO 2
as-similation
and a concurrentdecrease
intranspiration, resulting in
amarked
in-crease
of WUE.
Transplanting markedly reduced A in all
treatments inboth experimental periods (fig 2). Analysing gas exchange data in A
vs
C i graphs (fig 4) clearly established that this
declineof A occurred while the diffu- sional CO 2 supply
to thechloroplasts
wasenhanced (C i increased), thus indicating
that the
changes
in A wereprimarily
due toalterations of the mesophyll photosynthetic capacity. Guehl
etal (1989) reached
thesame
conclusions
withtransplanted Ce-
drus atlantica seedlings. Our results also indicate
that thedecline
inA
cannot be ac-counted for
by alterations
inplant
waterstatus
and
inneedle nutrient
status(N and P). The only significant effect of transplant- ing
onneedle nutrient
status wasthe
de- creasefound
forP in the TtP seedlings
inFebruary,
inwhich the
recoveryof A
aftertransplanting
wasmost marked. The
na- tureof the factor triggering
thedecline of A remains unknown. In
aprevious study (Guehl
etal, 1989) it
has beenestablished
fortransplanted Cedrus atlantica seedlings
that the
recoveryof A, following the initial
phase of decline,
wasconcomitant with
rootregeneration. The results obtained
here(figs 2, 5, 6) suggest
thatthe
recovery of A wasrelated
to the recoveryof mycor-
rhizalactivity
ratherthan regeneration
ofelongating non-mycorrhizal white
roottips.
Two mechanisms could
beinvolved: pro-
ductionof growth regulators by
thegrow-
ing fungus, and/or improvement
of waterand mineral uptake through
the re-establishment of mycelial connections be-
tweenthe
rootand the soil. Our results also
showthat the ability of the plants
toregenerate mycorrhizae
aftertransplanting
is affected
by seasonal parameters
aswell
as
their ability
toregenerate
roots(Ritchie
and
Dunlap, 1982).
ACKNOWLEDGMENTS
This work was
supported by
agrant
from the Of- fice National des Forêts. The authors aregrate-
ful to R Zimmermann from theUniversity
ofBay-
reuth(FRG)
for mineralanalyses. They
wish tothank JL
Churin,
BClerc,
JMDesjeunes,
PGross and F
Willm,
INRANancy,
for their techni-cal assistance and JL Muller for
drawing
thefig-
ures.
They
aregrateful
to Pr B Dell(Murdoch
university, Perth, Australia)
forreviewing
themanuscript.
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