1.
Journal of Horticllilural Science (1995) 70 (5)
m 1utrition and fruit load on the
.s17~.s2S
The influence of fruiting on the bud sprouting and flower
induction responses to chilling in Citrus
Amrican Society for Horticultural
an interpretation manual. (Reuter,
\ustralia,120-47.
By A. GARCIA·LUIS. M. KANDUSER and J. L. GUARDIOLA
Departamento de Biologia Vegetal, Universidad Politecnica, E-46022 Valencia, Spain
Maroochy Horticultural Research
on leaf analysis of fruit trees. 1.
National Institute of Agricultural
SUMMARY
The effect of chilling temperatures on bud sprouting and flower formation was
compared on fruiting and non-fruiting 'Owari' satsuma mandarin (Citrus tmshiu Marc)
trees. On non-fruiting trees, bud dormancy was weak, and a significant proportion of
buds were able to sprout at high temperatures without being chilled. Separate effects of
low temperatures on bud sprouting and flower induction were demonstrated. On fruiting
trees these two effects of low temperatures were also demonstrated on summer-flush
~af analYses of fruit trees. 6. Leaf
e Natio~al Institute of Agricultural
luaus fruits and nuts. Horticultural
buds, but not on older (spring-flush) buds. The spring-flush buds from fruiting trees
'ew of Plant Physiology, 13, 81-108.
md principles. In Plant analysis, an
'., Eds). Inkata Press, Australia, Idefoliation, and nutrient status of
:iety for Horticultural Science. 102,
leficiency in Japanese persimmons
I Experimental Station, 4. 31-41.
scarcely sprouted \vithout being chilled. These buds required a longer chilling period for
dormancy release than for flower induction, and it was not possible to separate the effect
of low temperature on flower induction from the effect on dormancy release. The
presence of fruit reduced flower formation by reducing bud sprouting. Furthermore,
fruit had a direct inhibitive effect on vernalization which resulted in increased formation
of vegetative shoots. The effect of fruit and low temperature on flowering was unrelated
to carbohydrate accumulation in the leaves or the roots.
i
I
!)
.
I
TE~lPERATURE
is the most important environ­
mental factor controlling Citrus flowering in
sublropical climates, where a main and usually
uni4ue bloom period occurs in spring after the
Irees have been subjected to low temperatures
for several months (Monselise, 1985; Daven­
pOri, 1990). Flower formation also results, or is
1 enhanced, when potted Citrus trees are
subjected to low-temperature conditions for
several weeks (Lenz, 1969; Moss, 1969; Gold­
schmidt et af.. 1985; Southwick and Davenport,
1986; Garcia-Luis et al.• 1992b). The threshold
temperature for enhancing flower formation
, has not been determined precisely, but is likely
to be below 19°C (Davenport, 1990).
The mechanism through which low-tem­
perature treatment enhances flower formation
has not been established. Low temperatures
have often been considered as inductive
IMonselise, 1985), but they also release bud
may increase flowering as a resul t of the
release of the dormancy of previously induced
buds rather than, or in addition to, an
inductive effect, and the published data do
not allow discrimination among these alter­
natives. As the first signs of flower morpho~
genesis occur during the early stages of bud
sprouting (Ayalon and Monselise, 1960; Iwa­
hori and Gahata, 1981; Guardiola, Monerri
and Agusti, 1982: Lord and Eckardt, 1985), no
information can be obtained from morpholo­
gical and/or anatomical examination of the
buds.
An inductive effect of low temperature has
been demonstrated using in vitro culturt:s of
buds (Garcia-Luis er al., 1992b), but this
demonstration has not been extended to
entire trees. Although the in vitro bud
cultures are considered a valuable tool for
the study of ftO\'ier induction (Bernier et al.,
~ dormancy and enhance bud sprouting (Moss,
1981; Dickens ,nd Van Staden, 1988) they may
1976; Southwick and Davenport, 1986).
also lead to artifacts, as they suppress the
influence of interorgan correlations which may
be an important component of flower forma­
i 1969,
;. This results in a positive relationship between
Shoot initiation and flower formation (Guar­
diola, 1981). Therefore. the low temperatures
1
tion in entire plants (Bernier. 1988). In the
SIS
Fruiring effects ill citrus
present repun, we presellt evide1lce for ar.
rnducrive effect of low temperature on flower­
ing using entire S(ltsum8 mandarin trees. We
also show that fruit reduces flower formatinr.
buth inhibiting bud sprouting and also redu­
cing the vernalizing response to low tempera­
ture. As positive relationships he tween
carbohydrate levels and flowl:ring hnve been
reported in Citrus (Davenporl, 1990), we also
examined wht:ther the effecl of the fruit and of
low temperatures on /lowering parallel
changes on the accumulation of carbohy­
dratt:~ in the roots and the leaves.
MATERIALS AND METHOl)S
Orchard and potted trees of 'Owari' satsuma
mandarin (Citrus unshill Marc) were used in
the experiments. On each case, the sprouting
und Rowering behaviour of the buds were
compared for fruiting and non-fruiting trees.
The 40 year okI orchard trees used in the
experiments were grafted on sour orange
(Citrus aurantium L) rootstock. Four uniform
trees were defrultcd by hand immediately after
the natural drop of fruitlds (4 June) 2nd used
as non-fruiting (defruiled) trees. An additional
four trees which were harvested at fruit
maturity (14 October) served as fruiting
trees. Each tree served as a sampling unit tor
flowering measurements and carbohydrate
determinations. Leaf sampling and car bollY­
drate analyses were performed as described by
Garda-LUIS el ul. (1995). Bud sprouting and
flower formation were mC<isured during the
summer flush of growth and the following year
spring flush of growth, on four branches having
2,700 to J,100 buds less lhan one year old.
Separate records were obtained for bud
behaviour according to bud age. The shoot.s
developed tram the~~ buds were classified
according to Sauer (1951) as vegetative.
gen-:rativc and mixed-type. Only single [lowcr
intlorescenc~s formed in these trees. The
results are presented as number of shoots!
flowers per 100 nodes.
All potted trees u<;ed in the experirnt:nts
were grafted unto Carrizo citrange (Poncirus
tn/ohara X Cicrus sinensis) rootstock and
grown outdoor~ under shade in 15 I pots in a
mix of 1 peat: 1 sand: 1 soil. Ambient
temperatures wert:: in the range of 24-31'"C
1
,,
(maximum daily temperatures) and 14-18cC
effective
(minimum). These temperatures may have at
in~ucing A
most a marginal effect on flower indUCtion iJ1
regime (de
Cimls (Moss. 1969, 1976).
lf~cS, 12 1
One group of 54 trees was three years old i treZltment.
when used in the experiments. These trees had
tree> werE
flowered anu set frui t during the spriGg Hush of
menlo In
ero\\'th (April) and ranged in height fmm 1.0
wer..: defn
to 1.2 ffi. They bore 6--7 fruits (mean fruit fresh
rooms to (
weight at the start of the experiment was 49 g)
during ch
and 203-215 Je::lves per plant. Th~se trees
fio\\'erillg.
scarcely sprouted m summer, and most of the
dev~lopin!
buds whose flowering behaviour was man. ) tha~ were
itared (see below) were formed during the
beginning
seldom sp
spring flush ot growth.
The 24 trees of the second group were two
pruning 0
!990). Wit
years old when used, r~l1ged in height from O'9
of three t
to l.2 m and bUle 170-210 leaves per plant
ieavcs aBC
when used. Flowering was prevented in spring
by IJruning the distfll 10 em of the shuuts, j min;ltions
where the Dowers ure usually formed, and I derea sam
made vigorous growth during the slimmer I vVhtrc
dfects w(
flush of growth.
test In 1h
The f1uwering behaviour of these tre~s was
effects
of
determined on 26 September (fruiting-trees)
mertts and
and on 2q October(non-fruiling trees). In each
using com
case, the trces were forced to sproUl by
root tran
transferring them to a growth room at a high
hetcrogen
temperature regime (26/13 ~ lOC for fruiting
trees and 26120 ::: 1°C for non-fruiting trees;
day and night respectively) under a daily 16 h
light period with a photosynthetic photorl flux
Chilling t)
density of 600 M-mol m-~ S-I at plant level,
Only ("
prOVIded by a mixture l1f fluorescent (SylVania
cool white f48Tl2'CW/WHO) and incandes·
E//t:( I 'J/ chI!
cent lamps. The trees werc placed either
growlll rt)OlJl
directly into the high temperature regime
ourl/uur f<!fJI{
(unchillecJ trees) or after being kept iii
inductive cold conditions (chilled trees). The
non-fruiting t.rees were chilled for 60 d at lS/lO
:::!:: l"C (day and night temperature respec·
Cr)IHJ"llrre~
tively) at the same photoperiodic regime
WillI fruit
described above. In the fruiting trees, one
Dl'lruited
group of trees was chilled for S3 d at 15/100('
Chjl!nllnn
Wl(/' fruit
as describeu for non-fruiting trees. A second
Ddnn(cd
group of trees was chilled outdoors for 56 d al
Chi,'f<"l!
Irees
ambient temperatures, follmved by 53 d in the
Wuh hUll
growth room at 15/l0°C. The forcing 01' trees
De!"Ul~et1
not included in the experiment after 56 d The <In,Jl~'si:;
outdoor chilling proved that the ambienl
~prQlI!iIlg, st
tntcri.lctlOn "
temperature at this time of the year waS ~
I
1
I
atures) and 14~18'C
may have at
n flower induction in
)
) was three years old
:lents. These trees had
ring the spring flush of
:ed in height from 1.0
'ruits (mean fruit fresh
experiment was 49 g)
:r plant. These trees
:lmef, and most of the
behaviour was mon­
re formed during the
~ratures
econd group were two
"ged in height from 0.9
1--210 leaves per plant
vas prevented in spring
10 cm of the shoots.
, usually formed. and
!l during the summer
A.
GARCIA-LuIS.
M.
KANDUSER
effective in releasing bud dormancy and
inducing flowering as the 15/10"C temperature
regime (data not shown). For the non-fruiting
trees, 12 trees served as replicates for each
treatment. In the fruiting treeS experiment, 18
trees were used on each temperature treat­
ment. In each treatment, half the trees (9)
were defruited at the transfer to the growth
rooms to determine if the presence of the fruit
during chilling and/or bud sprouting affects
flowering. Bud sprouting and the nature of the
developing shoots were measured in all nodes
that were less than one year old at the
beginning of the experiment; older buds
seldom sprout unless the tree is disturbed bj,'
pruning or excessive defoliation (Davenport,
1 1990). Within each treatment, random groups
of three trees were formed for sampling of
\! leaves and fibrous roots. Carbohydrate deterI minations were performed on the dry, pow­
dered samples, as indicated above.
'
Where appropriate, significant treatment
effects were determined using Student's t­
test. In the potted fruiting trees experiment,
effects of the main variables (chilling treat­
ments and presence of fruit) were determined
using complete analysis of variance. A square
root transformation was used to reduce
heterogeneity of the variance.
I
and J. L
GUARDIOLA
819
when forced directly at 26113°C without prior
chilling. The perc~ntage of bud sprouting in
these unchilled trees was very low, and v~ry
few flowers were formed (Table I).
No budburst occurred during the low
temperature treatments. After 53 d of chil­
ling, a significant number of buds became
uninhibited and sprouted upon transfer of the
trees to the warm conditions. This resulted in
an increaSe in the number of all type of shoots.
particularly the vegetative and generative
ones. A longer duration of the low tempera­
ture treatment (for 109 d) further increased
the percentage of bud sprouting upon transfer
to the warm conditions and the number of
mixed-type and generative shoots formed, but
had no additional effect on the number of
vegetative shoots. The increase in the number
of flowering shoots was greater (P<0.05) than
the increase in bud sprouting, and resulted
mainly from the development of several shoots
in a single node.
Defruiting the trees before the low tem­
perature (15110'C) incubation (chilled trees)
or upon transfer to the warm conditions
(unchilled trees) had no significant effect on
bud sprouting nor in flower formation (Table
I).
Carbohydrate accumulation in the leaves
was not affected by temperature and was
increased by the removal of the fruit (Table
IT). Differences in starch content accounted for
most of the differences in total leaf carbohy­
'jour of these trees was
)tember (fruiting-trees)
,-fruiting trees). In each
forced to sprout by
growth room at a high
!6/13 :': l'C for fruiting
: for non-fruiting trees;
vely) under a daily 16 h
RESULTS
::>tosynthetic photon flux Chilling effects Oil fruiting potted trees
m" S·I at plant level.
Only 60'% of the fruiting trees sprouted
of fluorescent (Sylvania
T"HLI:. 1
N/WHO) and incande,­
EJJ('(/ of chillmg treatments Oll fmd sprvlllmg and jiowering III fruiling ported stl!swna trees. Trees were forced to sprow in (/
~es were placed either grow//( room at 26/13"C, eitherdirl:'ctfy Of! 26 September (control/rees). afler 53 Ii at l5/life (chilled Irees, 53 Ii) or after 56 d ar
by 53 d at 15/life (chilled Irees, 56 + 53 dJ. in each treatment, a hal/fJflhe trees werc defnlllcd at
,,h temperature regime. (Jurd, 'or temperaturethefollowed
(ramIer t<J the growth room (defruited Irees). ~'allles are means of nine IfC!!." ::':: SE
after being kept 111
Shoots formed (No.ll00 nodes)
ions (chilled trees). The
Nodes
e chilled for 60 d at 15/10 Treatment
Vegetative
Mixed
Generative
No. flower/tOO node~
sprouting %
,ht temperature respec­
COlllro{ trees
; photoperiodic regime
With fruit
} ::':: 1
4::1
1.6 ::!: 0.9
2 ::':: 1
9 ~ 3
Ddnilled
:; ::':: 2
} ::':: fl.6
1O~ 3
1.8 :!:: 0.3
l ::':: D.S
the fruiting trees, onc
'illed for 53 d at 151\0'( [hilled trees (53 d.)
With fruil
19 :!:: S
13 ::':: 5
33 :: 7
3.3 ::':: 1.2
LO ::':: 3
-fruiting trees. A second
20 ::!: 7
Delruited
16 :!:: 4
5.4 ::':: 1.8
15 1: 4
37 ::':: 6
lilled outdoors for 56 d al
Outler! trees (56 + 53 d.)
S, followed by 53 d in the
Wtlhfruit
H::'::lO
12::'::4
7.D::,::3
47::'::3
54::'::6
O'C. The forcing of trees
Dclruiled
53::!: 5
20 :::::: 6
[J.O ::':: 4
40 ::':: 3
53 ::':: 6
, experiment after 56 d The analYSIS of variance of the
transformed data revealed significant effects (P>SO.Ol) of the chillmg treatments on bud
'oved that the ambienl sproullng. shoot formation and llower formation. Neither the effect of the fruit (with frUlt vs. defrUltcd) nor the first-order
time of the year was ~ Ihleracllon were significant.
vx
820
Fruiting effects in
1
cifrUS
TABLE II
The inflllence of temperature on carbohydrate contents in {eaves and roots of jmllms pOlled trees. Samples were picked after
53 d of IncubatiOIl III ellner 26/13U C or is/lOoe from trees wah fruit or wah the fruit removed at the begin.ning of the inCllbatio n
(defrwted frees), Values. In % on dry-mailer basis, are means of three n:pflcates ::':: SE
T Tees wlth fruit
Plant part and
IS/ID
carbohydrate fractlon
c
e
DefrUlted trees
26/13"C
15/1O"C
11.1
0.2
ILl ::':: 0.8
22.2 ::':: 0,9
22.0 ::':: 0.5
Roots
Soluble sugars
Starch
Total carbohydrates
4.8 :::: 0.1
4.6 ::':: 1.3
9.4 ::':: 1.3
3,8::,:: 0.2
4,3 ::':: U.S
15.7 ::':: 0.2
20.0 ::':: 0.3
4.2 ::':: 0.2
3.2 ::':: D.I
7.4 :':: 0.1
10.5 ::':: U.3
11.5 ::':: D.5
SldTC
Tc>tal
RaNI
S(llut
SldfC
Tlltal
II
.>'i:
TABLE ((I
Effect of chilling treatmems on bud sprouting andfiowulIIg in non-fmiting pofted Sa!sumll trees. Trees were forced II' sprollf'ti-i
a growth room at 20!2(fC either directly (contraltrees) or after 00 d at 15/](/'C (chilled trees). Vallles lire meallS pf 12 t~A'
~SE
.~
1!'
Shoots formed (No.JlOO nodes)
Control trees
Chilled trees
29
48
~
~
6
2
- - -
VegetatIve
24
4
~
~
Lca' es
I
Chilling effects on non-fruiting poued trePs
All the non-fruiting trees sprouted readily
when forced directly at 26/20'C. Mainly
vegetative shoots were formed, and the
number of flowers formed was very low
(Table III).
No visible budburst occurred during the 151
10°C temperature treatment, but the swelling
Treatment
t
1 veg..:t(
of the buds and some opening of the prophYlls,
marl'
which are the first signs of bud sprouting, were
forme
evident in some of the distal buds at the end of
nodeS
this treatment. The low temperature treatment
set a
markedly increased (P<O.O!j the number of
reml)\
buds which sprouted upon transfer to the
contr~
warm conditions. Most of the shoots formed in
II fruitin
the chilled trees were generative, while the
The
formation of vegetative shoots was almost
these
suppressed by chilling. The number of mixed­
folln"
type shoots increased slightly (Table Ill).
to 10
Starch accumulated in both the leaves and
preSe!
the roots during the low temperature incuba~
highcl
tion. Under warm conditions (26/20°C) only:.
tree;.,
small changes \vere found in the carbohydrate'
p~rccl
concentrations (Table IV).
spring
bud,.
The effect of the fruil on bud sprouting and· SprOll'
flowering in adult trees
form..:
In early July a flush of growth occurred both
Rq
in the control and in the de fruited trees.:
fiOWCT
Percentage of bud sprouting during this flus~,.: (P<l).l
of growth was higher in the defruited than iD:~·. trees
the fruiting trees (2.1 % vs. 0.7%, P<O.OS),··
Nearly 35% of the shoots formed in th(
defruited trees were of the mixed type, with:,~' The e.(I1
Irer's II!
6-8 leaves and a flower in the apex (233 :'.: lQ,~
flowers per tree). The remaining 65% we~::
drates.
Starch accumulation in the roots was
enhanced by the removal of the fruit, particu­
larly in trees kept at low temperatures. The
highest starch content (15.7%) was found in
the defruited trees kept at 15/lO°C. Starch was
nearly absent (1.7%) in the roots of trees with
fruit which were kept at high temperature (26/
13'C).
At the time the outdoor trees were trans­
ferred to the growth room the fruit was nearly
mature and had ceased to grow. Accordingly, it
had a minor effect on carbohydrate accumula­
tion. The starch levels in the de fruited trees at
the end of 53 d at 15/10'C low temperature
incubation were 7.8% (leaves) and 16.7%
(roots). In the trees with the fruit on the
corresponding values were 8.2% and 11.7%
(leaves and roots respectively).
Nodes
sprouting, %
~arroh)
S,'iut
12.0 ::':: 0.2
2.5 ::':: 0.1
14.5 :': 0.1
.
I~
,
26/13 C
10,0::':: 0.6
3,8 ::':: 0.3
13.8 ::':: 0.4
1.7 '" DJ
5.5 ::':: 1).5
Infl
c
Leaves
Soluble sugars
Starch
Total carbohydrates
=
The
; ,,'ere' pl(
7
1
Mixed
::
~
1
4::':: 1
Generative
3
57
:t.
~
1
6
Tree
1\
Fmilil/(
Spri;,
Sumr
Over
Defnlll
Spnr
Sumr
Over
-
1,
A.
rees. Samples were pIcked afler
'Ihe beginning vf Ihe incubatlOll
lieales ± SE
DefrUlted trees
:: 0,2
;.:. 0.8
10.5 ::': 0.3
11.5 ± 0.5
::': 0.9
22.0 ::':: 0.5
:::': 0.5
± 0.2
4,2 :::': 0.2
3.2 :::': 0.1
::': 0.3
7.4 .:::': 0.1
opening of the prophylls,
TIS of bud sprouting, were
, distal buds at the end of
IW temperature treatment
(P<O.01) the number of
d upon transfer to the
st of the shoots formed in
re generative. while the
l.tive shoots was almost
g. The number of mixed~
j slightly (Table 11\).
d in both the leaves and
low temperature incuba·
:onditions (26/20°C) only
~ound in the carbohydrate
.e IV).
.lit on brld sprouring and
~es
h of growth occurred both
in the defruited trees.
.prouting during this flush
~r in the defruited than in
2.1 % vs. 0.7%, P<0.05).
e shoots formed in the
, of the mixed type, with
Ner in the apex (233 :': 10
[he remaining 65 % were
"ees. Trees were forced 10 sprout in
ees). Values are means of 12 trees
~rative
~ 1
~6
No. flower/IOO nodes
5 ::':: 1
61 ± 5
GARClA~LuIS,
M.
KANDl:SER
and J. L.
821
GUARDIOLA
TABLE IV
The mIll/eriC" of tempera/lire of inCllblllion on carbohydrate cOlllellls l!l leaves (lnd rools of non-frUiting palled trees. Samples
were pwked IJlter 60 d of Iflcubation at either 261200C or 15/11fC. Values, in ~.;, on dry-matter basis, are means of fOLlr replicates
:::': SE
Pi~,nt part and
cjrbohydrate fraction
Day 0
values
lncuhated
at 15/10~C
Incubated
at 26/20~C
6.1 :::': 0.2
5.2 ::':: 0.8
11.3 ~ 0.7
L,·c/ves
Soluble sugars
Starch
Total carbohydrates
6.2
5.5
11.7
0.2
0.3
0.4
5.7 ::: 0.3
10.6 ::!: 2.2
16.3 ::!: 2.1
Roots
Soluble sugars
Starch
lotal carbohydrates
2.6
66
9.2
0.1
0.8
0.7
13.7
180
vegetative shoots. These vegetative shoots had
more nodes (12.9) than vegetative shoots
formed during the spring flush of growth (5.6
oodes per shoot). Most of the flowers formed
set a fruit. These fruits were immediately
removed to keep the trees fruitless. By
contrast, only vegetative shoots formed in the
fruiting trees.
The sprouting and flowering behaviour of
these trees during the spring flush of the
following year (after they had been subjected
to low temperature winter conditions) is
presented in Table V. Bud sprouting was
higher in the defruited than in the control
trees. In the defruited trees, the same
percentage of sprouting was found in the
spring-formed than in the summer-formed
buds. In the fruiting trees, the percentage of
sprouting was higher (P<0.05) in the summer­
lormed than in the spring-formed buds.
Regardless of bud age, the number of
flowers formed per 100 nodes was higher
(P<O.Ol) in the defruited than in the fruiting
trees (Table V). In the spring-flush buds, the
4.3
~
:!:
~
0.1
0.6
0.5
46 :::': 0.2
7.3 :!: 0.8
11.9:::': 1.0
removal of the fruit increased the number of
generative shoots but had no effect on the
number of vegetative and mixed-type shoots
formed. In the summer-flush buds, the removal
of the fruit reduced the number of vegetative
shoots and increased the number of mixed­
type and generative shoots formed (Table V).
Both in fruiting and in defruited trees, more
leafy shoots formed (vegetative plus mixed­
type) in the summer flush than in the spring­
flush buds. In relative terms (per 100 nodes)
flower formation in the fruiting trees was
higher in the spring-flush buds than in the
summer-flush buds (Table V). In the defruited
trees, total flower number per 100 nodes was
similar in both bud types, but there were
marked differences in the nature of the
inflorescences (Table V). In the spring-flush
buds 80% of the flowers were in generative
inflorescences, while in the summer flush buds
76% of them were in mixed-type shoots.
Defruiting had a minor effect on the
carbohydrate contents of the leaves. Starch
contents were slightly higher in the leaves of
TABLE V
The effeci of the fwit on natural bud sprouting and flowering. In defwited trees the fruitlets were removed on -I June; in frui!ing
rref~ the fmit were harvested on 16 October. BLld sproUling and flowering were measured Ihe following spring. Values are
means of four trees:::': SE
Shoots formed (NoJl00 nodes)
Tree type and bud age
Fruillflg frees
Spring-flush buds
Summer-flush buds
Overall mean
Defmited trees
Spring-flush buds
Summer-flush buds
O\erall mean
Nodes
sprouting, %
54 :::': 5
66 : :': 2
55 ± 5
Vegetative
3
36
4
Mixed
1
28
1
6
29
3
07
28
75 ::': 2
1
76 .± 3
75 :::': 2
8
0.2
2
20
74
1
0.4
26
Generative
1
28
1
27
7
1
7
5
3
4
82
23
75
10
5
8
No. flowerllOO nodes
56
31
55
7
4
7
102
97
101
7
5
7
c·.1
"d
"it
d
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,d
822
Fruiting effects in citrus
TABLE V[
The
eff~ct of ~h.e frllli vI! wrbo~ydrale contents In
In
the spnng-.flll5h leaves. In de/rtl/ted (lees [he frlllilets were removed on 4 lUll
[rwllng trees the frill! were harvested on 16 October htilleJ, in % drv matter, ilre means of fOllr trees -I- 5£
e;
Date of sampling
Tree type and
4 July
carbohydrate fraction
16 June
Frwllng trees
Soluble sllgar~
Starch
Total carbohydrates
9.1 ~ 0.2
6.6 '" 0.2
15.8 ::<: 0.2
9.3
5.3
14.6
::+::
8.4 ::!:: 0.2
7.5 ::<::: 0.2
8.6
6.4
15.2
:!:
4 October
14 December
02
0,2
D.2
6.2 ::+:: 0.2
2.5 ::':: 0.3
8.7 ::':: 0.5
8.9 2:: 0.1
12.4 ::':: III
OA
0.6
0.8
6.2 :!:: 0,2
10.1
~
3.1
13.2
­
~
Defruired trees
Soluble sugars
Starch
15.9 :::':: 0,2
Total carbohydrates
::<:::
::<:::
::+::
::<:::
2.6
8.9
+
0.1
0.2
35
:'.: 0.2
A further
\ of the: fruit
;'hiJIing was (
I ~en ts~ In
, ,r
i
Ii
::: 0.6
-=
~
1).3
1).7
DISCUSSIQI':
Although the enhancement of flower forma­
tion in Citrus by chilling has been referred to as
an inductive effect (MonseIi5e, 1985; Daven­
port (1990); the precise mechanism has not
been ascertained. An inductive effect results in
the transformation of a vegetative meristem
into a flowering meristcm, and it is easily
demonstrable in herbaceous species in which
the unchi]]ed plants continue vegetative growth
(Thomas, 1993). In Cirrus, as in other perennial
trees, chilling releases bud dormancy. Flower
formation parallels bud sprouting and shoot
initiation (see references in the Introduction),
which makes it difficult to demonstrate the
inductive nature of chilling on flowering.
There was an increase in bud sprouting and
in flower formation in response to chilling both
in fruiting (Table I) and non-fruiting (Table
Ill) potted trees, but with different time-course
responses. In fruiting trees the formation of
vegetative shoots was enhanced initially by
chilling: 17.5% of the nodes formed vegetative
shoots after 53 d of low~temperature treat­
ment. These buds could not be induced to
flower by a longer duration of chilling, which
enhanced flower formation but did not reduce
significantly the number of vegetative shoots
formed (16 :!: 4 per 100 nodes after 109 d of
chilling: Table I). Hence. there was no clear
evidence for an inductive effect of low
temperature. Our results could be explained
assuming that low temperature releases the
dormancy of buds previously induced and that
the chilling requirements are lower for vege_
tative than for flower buds (Garcia-Luis et al
1992b). In non-fruiting trees, 24% of the node;
formed vegetative shoots when forced to
sprout un chilled. In these trees, the number
of vegetative shoots formed was drastically
reduced (down to 4 :!: 1 per 100 nodes) after
60 d of low-temperature: treatment, and
simultaneously there was an increase in the
number of generative shoots formed (Table
III). This behaviour demonstrat~s an inductive
effect of low temperature on those buds which
were able to sprout unchilled.
A similar inductive effect is likely in all cases
in view of the reported behaviour of the buds
in vitro. Up to 53% of the buds from unchilled
fruiting trees could be cold-induced to flower
in vitro, but they formed vegetative shoots
only when forced to sprout unchilled (Garcia·
Luis el aI., 1992b). Further, when buds
sampled at different times along the winter
were cultured in vitro under non-inductive
conditions, they sprouted readily, demonstrat·
ing that bud dormancy is determined mainly
by correlative effects of other organs (para·
dormancy), but the number of buds flowering
in culture increased with the duration of
exposure of trees to the winter inductive
conditions (Garcia-Luis el aI., 19923) Garda­
Luis and Kanduser, unpublished). This induc­
tive effect was not shown in vivo since more
chilling seems necessary for the release of bud
dormancy than for flower induction. More
than 100 d of chilling were needed to cause the
sprouting of 49% of the buds of the fruiting
trees (Table I), while 15 d of incubation at 171
10 0 e sufficed to induce flowering in 53 % of
these buds in vilro (Garcia-Luis et al., 1992b).
vi
j
al.. 1986)
removal enh,
thi: !nhibitivE
fruit on flow(
,xpo::iUre ane
si~nl!icant (1
and previ.
al 1986) i
during the pt
lhe ftowerin
chilling seve]
lion has be
evergreen \\
chilling (Hal
and Martin,
oi fruitlets (
(Stulle and r
i.e. some f
period, redu
The defru
also showed
flower form,
spring-flush
ing was rna
bud sprouti
marc buds:
the control
effect of fru'
inRul'nce on
number of 5
were vegeta
sprouting w:
buds, as the
slightly low,
However, il
fruit on flo\}
induction. I
developed s
7.6% in th,
contrasts w
few flower
Spring-flush
Kanduser,
1992b). It
cultures v,'e
SIX weeks)
'I"
defruited trees during June. but no differences
in carbohydrate composition were detectable
after July (Table VI).
31
j (Goldschmid
,
1
-i
the !rlll(lets were removed on 411111 /'!.
Ire m<!On5 of to/u trees:::':: SE
.
October
14 December
--------,.2 :!: 0.2
8.9 ::':: (j.l
..5 :!: 0.3
.7 , 0.5
3.5 ::':: 0.2
12.4 ~ 0.1
1.2
:.6
10.1 ::':: 0.6
3.1 :::':: OJ
13.2 :::':: 0.7
:!:
:!:
0.2
0.1
:.9:::':: 0.2
iements are lower for vege_
wer buds (Garcia-Luis et at
liting trees, 24 % of the node'~
'e shoots when forced to
In these trees, the number
)Qts formed was drastically
, 4 ± I per 100 nodes) afler
:rnperature treatment, and
lere was an increase in the
·ative shoals formed (Table
ur demonstrates an inductive
)erature on those buds which
lut unchilled.
:tive effect is likely in all cases
)orted behaviour of the buds
% of the buds from unchilled
Id be cold-induced to flower
'y formed vegetative shoots
I to sprout unchilled (Garcia­
92b). Further, when buds
rent times along the \vinter
1 vitro under non-inductive
;prouted readily, demonstrat­
mancy is determined mainly
'fects of other organs (para­
he number of buds flowering
ased with the duration of
es to the winter inductive
ia-Luis et af., 1992a) Garcia­
er, unpublished). This induc­
ot shown in vivo since more
cessary for the release of bud
for flower induction. More
ling were needed to cause (he
, o(the buds of the fruiting
fhile 15 d of incubation at ]71
induce flowering in 53 % of
'0 (Garcia-Luis et al., 1992b).
A.
GA.RCIA-LuIS.
M.
KANDU~ER
A further characterization of the influence
of the fruit in the vernalizing response to
~ chilhng was obtained in the defruiting experi­
; ments. In agreement with previous reports
, (Goldschmidt and Golomb, 1982: Garcia-Luis
t[ ai.. 1986) we found that an early fruit
removal enhanced flowering (Table V), while
: the inhibitive effect exerted by the maturing
j fruit on flowering during the low-temperature
eXpusure and during bud sprouting was non­
,ignificant (Table I). From the present (Table
V) and previously publJshed data (Garcia-Luis
~. (I al .. 1986) it seems that the presence of fruit
I dunng the period lune-September determines
the /lowering response of satsuma buds to
. chilling several months later. A similar situa­
tion has been reported for olive, another
evergreen whose flowering is enhanced by
chilling (Hackel and Hartmann, 1967; Rallo
and Martin, 1991). In this species the presence
'I of fruitlets (Lavee el al., 1986) or their seeds
: (Stuttc and Martin, 1985) 40 d after flowering,
i l.e. some five months before the chilling
I period, reduces next year flowering.
1 The defruiting experiments with adult trees
) also showed differences in the way fruit affects
\ flower formation in relation to bud age. In the
spring-flush buds the effect of fruit on tlower­
ing was mainly determined by the effect on
bud sprouting (depth of bud dormancy), as
more buds sprouted in the defruited than in
Ilbe control trees (Table V). The inhibitory
\ effect of fruit on flower induction had a minor
Influence on flowering, as only 5C:~ of the total
num ber of shoots formed in the fruiting trees
were vegetative. Some effect of fruit on bud
sprouting was also evident in the summer-flush
bUd~, as the percentage of bud sprouting was
slightly lower in the fruiting trees (Table V).
'I However, in these buds, the major effect of
fruit on flowering occurred by affecting flower
induction. In the fruiting trees, 54% of the
developed shoots were vegetative, against only
7.6% in the defruited trees. This behaviour
Contrasts with that of the buds in culture, as
few flowers could be cold~induced using
spring-flush bud cultures (Garcia-Luis and
Kanduser, in preparation; Garcia-Luis er ai.,
1992b). It should be noted that the bud
cullures were chilled for a shorter time (up to
six weeks) than the trees in the present \....ork,
1
I
and J. L.
GUARDIOLA
823
which were subjected for more than 16 weeks
to inductive temperatures. Since the summer­
flush buds were easily induced to flower in
vitro under these conditions, they should have
a lower chitling requirement for flower induc­
tion than the spring-flush buds.
A relationship between carbohydrate levels
and flowering has been reported in Citrus, but
most of the evidence comeS from alternate­
bearing cultivars (Monselise and Goldschmidt,
1982). In many cases no consistent correlation
has been found (Lewis el aI., 1964; Goldschmidt
el al., 1985; Garcia-Luis
et al., 1988; 1995;
Lovatt el al., 1988), indicating that carbohydrate
levels are not always the limiting factor for
flowering of Citrus. Our present data for 'Owari'
satsuma support this view as no correlation
could be established between carbohydrate
reserves and flowering. Similar flowering levels
were obtained in trees differing markedly in
carbohydrate reserves (i.e. defruited trees and
trees with fruit; Tables I and 11), and marked
differences in flowering were found in trees with
similar carbohydrate contents (Tables V and
VI). The effect of chilling and the fruit on
flowering does not appear to be mediated
through carbohydrate availability.
In summary the experiments presented here
carried out with intact trees demonstrate
independent effects of low temperature on
flower induction and on the release of bud
dormancy. These effects may be demonstrated
in non-fruiting trees and young (summer-flush)
buds from fruiting trees, but not in older
(spring-flush) buds of the fruiting trees, as their
chilling requirement for flower induction
seems lower than for the release of dor­
mancy. The fruit increases the chiUing require­
ment for the release of bud dormancy and
hence reduces bud sprouting, and also reduces
the vernalization response to chilling. The
effect of the fruit and of chilling on flowering
are unrelated to carbohydrate accumulation.
Thanks are due to Mr M. Sanchez Perales
for technical assistance. M. K. was recipient of
a fellowship from Ministerio de Educacion y
Ciencia, Spain. This research was financed by
C1CYT (Grant PB88-0358).
824
Fruiting effects in citrus
~
I
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