Whole-Plant Responses of Brassica campestris (Cruciferae) to Altered Sink-Source

Relations

Ann S. Evans

American Journal of Botany, Vol. 78, No. 3. (Mar., 1991), pp. 394-400.

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American Journal of Botany 78(3): 394-400. 1991.

WHOLE-PLANT RESPONSES OF

BRASSICA CAMPESTRIS (CRUCIFERAE) TO

ALTERED SINK-SOURCE RELATIONS1

ANNS. EVANS^
Department of Ecology and Evolution, The University of Chicago, Chicago, Illinois 60637

Plants may respond to developmentally or environmentally induced changes in the relation-

ship between source (assimilate exporting) and sink (assimilate importing) organs through a
number of regulatory mechanisms. The purpose of this work was to describe responses in leaf
physiology, organ biomass partitioning, and reproduction of Brasszca campestris L. to altered
sink-source relations. Partial defoliation early in ontogeny increased sink-source ratio after 1
day and was accompanied by a significant increase in area-based photosynthetic capacity.
Assimilate was preferentially partitioned to new leaf tissue at the expense of stem and repro-
ductive tissue so that sink-source ratio and photosynthesis returned to control levels within a
week. Bud excision at flower initiation decreased sink-source ratio; plants in this treatment
responded through altered biomass partitioning, but there were no detected changes in leaf
physiology. Plants that were hand-pollinated had decreased specific leaf weight, and within a
week, sink-source ratio increased. Plants that were pollinated and then completely defoliated
produced 40°/o as many seeds as plants that were not defoliated, presumably through stem and/
or fruit photosynthesis, and at the expense of flower production. Together these results illustrate
that regulation of sink-source relations can occur through complex responses at several levels
of organization over a wide range of time scales.

In addition to external (environmental) fac- The Boussingault (1868, quoted in Neales

tors such as light intensity, temperature, etc.,
internal factors such as assimilate partitioning
may regulate the rate of photosynthesis in plants
(see Sharkey, 1985 for review). The role of
internal factors is often examined and dis-
cussed in terms of a 'source and sink' model
of plant functioning (Neales and Incoll, 1968).
Organs that are net consumers of assimilate
are referred to as sinks; the capacity to import
assimilate is referred to as sink strength or de-
mand. Source organs are those that produce
excess assimilate for export. All plant organs
act, at some stage of development, as sinks,
either reversibly for utilization (e.g., leaves) or
irreversibly for storage (e.g., fruits) (Ho, 1988).
Hence sink or source strength may change with
ontogeny.
I Received for publication 3 July 1990; revision accepted
3 1 October 1990.
The author thanks the greenhouse staff ofThe University
of Chicago, B. McCarthy, W. Schroeder, and S. Yamins,
for assistance in caring for the plants; Dr. P. Williams of
the Crucifer Genetics Cooperative for providing infor-
mation about rapid-cycling Brassica campestris; Drs. J.
Teen and D. Schemske for discussions which prompted
the work; and Drs. J. Karron, D. Marshall, D. R. Geiger,
and M. J. Kasperbauer for helpful comments on the manu-
script. This research was supported by the Hinds Fund of
The University of Chicago and NIH-GM07 197 Training
Grant in Genetics.
Current address: Department of Biology, University
of New Mexico, Albuquerque, NM 87 131.
and Incoll, 1968) Hypothesis ". . . that the ac-
cumulation of assimilates in an illuminated
leaf may be responsible for a reduction in the
net photosynthesis rate of that leaf' implies
that growth (sink demand) may regulate the
rate of photosynthesis just as the rate of pho-
tosynthesis regulates growth. Tests ofthe Bous-
singault Hypothesis have typically involved
studies of the correlation between photosyn-
thesis rate and altered leaf assimilate levels or
altered sink-source relations which are pre-
sumed to alter leaf assimilate level. Many ex-
perimental treatments (such as defoliation) that
serve to explore the range ofpossible responses
are potentially disruptive of integrated plant
functioning, while others (such as pollination)
presumably are not (Geiger, 1976,1987). ('Dis-
ruptive' treatments [e.g., natural defoliation or
herbivory] may nonetheless be of ecological
and evolutionary significance.) Reviews of the
literature (King, Wardlaw, and Evans, 1967;
Neales and Incoll, 1968; Geiger, 1976, 1987;
Guinn and Mauney, 1980; Herold, 1980) re-
veal that a significant response of photosyn-
thesis rate to altered leaf assimilate levels and/
or sink-source relations depends on the species,
type and ontogenetic timing of treatment, and
time of measurement. Clearly a direct feedback
regulation by assimilate level in leaves is not
a universal phenomenon. (Metabolic control
mechanisms are not the focus of this study;
March 19911 EVANS -SINK-SOURCE RELATIONS 395

however, recent work [see conference proceed- active radiation [PAR] ca. 1,300 pmol m-2
ings edited by Cronshaw, Lucas, and Giaquin- sec-l) was supplemented continuously by cool-
ta, 1986; Foyer, 1987; Ho, 19881 has empha- white fluorescent bulbs (150 pmol m-2 sec-'),
sized cellular biochemistry and the role of and temperature was regulated between 17 C
translocation in sink-source relations.) and 27 C. Water with fertilizer was supplied
The Boussingault Hypothesis describes only ad libitum. Flats containing individual pots
one potential response of the whole plant to were rotated on a daily basis and moved se-
altered sink-source relations. Responses may rially every 4 days.
also occur through altered patterns of assimi-
late export and/or altered partitioning of ex- Experimental manipulations and measure-
ported assimilate (Geiger, 1976, 1979, 1987), ments-Plant responses to altered sink-source
leading, for example, to changes in the number relations-Three different experimental ma-
or size of organs (e.g., leaves). Plant responses nipulations were designed to alter sink-source
may occur at various functional levels and over relations (operationally defined as the ratio of
a range of time scales. Consequently, under- stem and reproductive biomass to leaf bio-
standing sink-source relations requires char- mass), and thus, presumably, leaf assimilate
acterization of whole-plant responses. levels. A rapid change in sink-source relations
The purpose of this work was twofold. First, was effected by tissue excision (treatments a
to characterize whole-plant responses to al- and b below) while agradual change was brought
tered sink-source relations by asking whether about by manipulating development (treat-
organ biomass partitioning and reproduction, ment c). The three treatments were adminis-
as well as leaf physiology, change in response tered at three different stages of ontogeny, so
to experimental manipulations. And second, the effects of type and timing of treatment are
to quantify the role of leaf assimilate in fruit not separable. According to the Boussingault
and seed production. Hypothesis, photosynthetic rate should in-
crease with increased sink-source ratio. Changes
MATERIALS AND METHODS in other physiological traits, as well as biomass
partitioning and reproductive characters, may
Plant material- Brassica campestris L. (syn also occur in response to altered sink-source
rapa) is a weedy, annual mustard that is also ratio.
of agricultural importance. The flowers are her- a. Defoliation-Sink-source ratio was in-
maphroditic, with a sporophytic self-incom- creased by decreasing source tissue. At day 15
patibility system. Rapid-cycling populations of after planting, most plants had, in addition to
Brassica species are the result of artificial se- viable cotyledons, two partially expanded true
lection for reduced reproductive time (Wil- leaves and another emerging leaf or leaves. The
liams and Hill, 1986). I obtained seeds of rap- oldest partially expanded true leaf of treatment
id-cycling B. campestris from the Crucifer plants was excised, and the other was used to
Genetics Cooperative (Department of Plant measure leaf physiological characteristics.
Pathology, University of Wisconsin at Madi- b. Bud excision-Sink-source ratio was de-
son). The base population is characterized creased by decreasing sink demand. At day 20,
(Williams and Hill, 1986) by rapid germination when about half the plants had commenced
(as few as 48 hours from planting), petite habit, flowering, all reproductive tissue of treatment
rapid onset of flowering (as few as 14 days from plants was excised. Leaf physiological mea-
planting), high female fertility, and rapid seed surements were made on the most recent fully
maturation (20-30 days from pollination). expanded leaf.
Phenotypically, the population responds c. Pollination-Sink-source ratio was in-
strongly to various environmental parameters creased by increasing sink demand. For 1 week
and shows considerable isozyme (Williams and beginning at day 18 all flowers of treatment
Hill, 1986) and quantitative genetic (Evans, in plants were pollinated. Plant characteristics
press) variation. were first measured the day after the last pol-
Seeds were planted in early March 1988. To linations were performed. Again, leaf physio-
minimize the effect of variable phenology on logical measurements were made on the most
the results of experimental manipulations, I recent fully expanded leaf.
selected seedlings that germinated within 24 For each of these three experiments there
hours of one another (on day 3 after planting). were 42 treatment and 42 control plants. Half
Seedlings were transplanted 2 days after ger- the plants were destructively sampled 1 day
mination to 3-inch pots and maintained in The after manipulations were administered, while
University of Chicago greenhouse. Ambient the remaining 21 treatment and 2 1 control
light (maximum midday photosynthetically plants were sampled 1 week after manipula-
396 AMERICAN JOURNAL OF BOTANY [VO~.
78

TABLE 1. Plant responses to defoliation (day 15). For each characteristic within each sampling period, control and
treatment means were compared by a t-test. Sample size for each group was 21

Mean 1 day response Mean I week response

Characteristic Control Treatment Control Treatment

Leaf production (number)

3.1 3.0 3.5 3.0
Leaf area (cm2)
15.7 **a 11.7 45.1 37.3
Leaf biomass (g)
0.035 ** 0.026 0.100 0.079
Stem biomass (g)
0.010 0.010 0.054 * 0.042
Reproductive biomass (g)
0.006 0.005 0.061 * 0.051
Total aboveground biomass (g)
0.050 ** 0.041 0.216 * 0.172
Sink-source ratio (g:g)
0.45 * 0.56 1.26 1.30
Flowering time (days)
nab na 19.1 19.4
Flower production (number)
na na 6.6 5.7
Fruit production (number)
na na na na
Specific leaf weight (g m-,)
23.6 23.8 28.8 27.9
Area-based photosynthetic rate (pmol CO, rn-, sec-')
20.1 ** 22.8 27.2 28.2
Area-based transpiration rate (mol H,O mc2 seccl)
12.6 12.8 13.8 13.1
Water-use efficiency (pmol CO, : mmol H,O)
1.6 1.8 2.1 2.2
a Significance levels: P < 0.05, *; P < 0.01, **.

na = not applicable.

tions were administered. For each plant, the
sampling procedure was as follows. When ap-
plicable, the day of first flower and the numbers
of flowers and fruits were noted. Area-based
photosynthetic and transpiration capacities
(close to maximal rates) were estimated from
CO, uptake and H,O loss, respectively, at sat-
urating PAR (2,300 pmol m-2 sec-') and am-
bient temperature (20-25 C) with a Model
LCA-2 infrared gas analyzer (Analytical De-
velopment Co., Ltd, Hoddesden, UK). Water-
use efficiency was calculated as the ratio of
photosynthesis to transpiration. Specific leaf
weight was estimated by measuring the mass
and area (LI-3 100 area meter, Li-Cor, Lincoln,
NE, USA) of the tissue used for gas exchange.
Leaves were counted and removed, and total
leaf area of each individual was measured. The
remaining aboveground biomass was parti-
tioned into stem and reproductive parts. Re-
productive biomass included all tissue (except
leaves) distal to the first bud or flower of each
raceme. Biomass samples were dried and later
weighed. The ratio of stem and reproductive
biomass to leaf biomass was calculated to es-
timate sink-source relations.
The role of leaf assimilate in fruit and seed
production -The purpose of this experiment
was to evaluate the role of leaf assimilate in
fruit and seed production. For 1 week begin-
ning at day 18 all flowers of 42 plants were
pollinated. Three days after the last pollina-
tions had been performed (day 28), 21 treat-
ment plants were completely defoliated and the
remaining 21 plants were used as a control.
After 2 1 days (day 46) the experiment was ter-
minated and the following characteristics were
measured: day of first flower, numbers of flow-
ers and fruits, and numbers of developed and
aborted seeds per fruit. Since plants were al-
lowed to completely senesce, leaf physiological
characteristics and biomass partitioning were
not measured.
Statistical analyses -Comparisons of treat-
ment and control means within each sampling
period were performed using Procedure TTEST
of SAS Institute, Inc. (1985). An adjusted t-sta-
tistic was calculated for groups of unequal vari-
ance.
RESULTS
Plant responses to altered sink-source rela-
tions -Defoliation -As intended, the leaf re-
moval treatment significantly decreased total
aboveground biomass and significantly in-
creased sink-source ratio after 1 day (Table 1).
In accord with the Boussingault Hypothesis,
area-based photosynthetic capacity was greater
in treatment than control plants. However,
control and treatment groups measured 1 week
after defoliation showed no differences in sink-
source ratio or area-based photosynthetic ca-
pacity. Although total aboveground biomass
was still greater in control than treatment plants,
leaf biomass and area were not; the difference
in total aboveground biomass was due to dif-
ferences in stem and reproductive biomass.
Presumably, the rapidly increased photo-
synthetic rate in treatment plants led to greater
leaf assimilate which was preferentially par-
titioned to new leaf tissue at the expense of
stem and reproductive tissues. As a result, al-
though total aboveground biomass remained
March 19911 EVANS -SINK-SOURCE RELATIONS 397

TABLE2. Plant responses to flower bud excision (day 20). For each characteristic within each sampling period, control
and treatment means were compared by a t-test. Sample size for each group was 21

Mean 1 day response Mean I week response

Characteristic Control Treatment Control Treatment

Leaf production (number) 3.9 3.9 13.5 ***a 19.1

Leaf area (cm2) 3 1.O 30.7 72.9 ** 102.3
Leaf biomass (g) 0.066 0.073 0.176 ** 0.238
Stem biomass (g) 0.038 0.042 0.109 * 0.137
Reproductive biomass (g) 0.036 *** 0.001 0.129 *** 0.064
Total aboveground biomass (g) 0.141 * 0.115 0.415 0.439
Sink-source ratio (g:g) 1.17 *** 0.58 1.41 *** 0.88
Flowering time (days) 19.3 19.0 19.3 ** 18.7
Flower production (number) 3.0 ** 1.1 32.1 *** 3.1
Fruit production (number) nab na 0.4 ** 0
Specific leaf weight (g m-2) 25.8 26.0 29.8 30.4
Area-based photosynthetic rate (pmol CO, rn-, sec-I) 24.5 23.8 19.3 18.3
Area-based transpiration rate (mol H 2 0 rn-, sec-') 7.4 7.5 10.2 10.4
Water-use efficiency (pmol CO, : mmol H,O) 3.4 3.2 1.9 1.8
a Significance levels: P < 0.05, *; P < 0.01, **; P < 0.001, ***.
na = not applicable.

depressed a week later, area-based photosyn- Pollination -Since all flowers of treatment
thetic capacity and sink-source ratio returned plants were hand-pollinated during the week-
to control levels. long treatment period, there was a significant
increase in the number of developing fruits 1
Bud excision -Bud removal, resulting in de- day later (Table 3). However, at that time there
creased flower production and reproductive were no differences in the number of flowers
biomass, had the desired effect of causing an produced, reproductive biomass, or sink-source
immediate decrease in total aboveground bio- relations. Although differences in leaf biomass
mass and sink-source ratio (Table 2). Neither and area were not significant,specific leafweight
photosynthetic capacity nor any other plant was significantly lower in treatment than con-
characteristic displayed a response after 1 day. trol plants. No other leaf physiological char-
Reproductive biomass and flower and fruit acteristics exhibited a response to the polli-
production were still significantly lower in nation treatment. For the plants sampled 1
treatment plants measured 1 week after treat- week after the last pollinations, differences in
ment, but leaf production, biomass and area, fruit production led to differences in repro-
as well as stem biomass, were significantly ductive biomass and sink-source relations.
greater in treatment than control plants. Con- Again, the only leaf physiological response was
sequently, although total aboveground bio- a decreased specific leaf weight in plants with
mass was as great in treatment plants as in developing fruits.
control plants, sink-source ratio of treatment In contrast to the defoliation and bud ex-
plants was still depressed relative to control cision treatments, alterations in sink-source
plants. The decreased mean flowering time of relations were evident only after a week. In-
the treatment group is of note; this anomalous creased fruit production did not lead to sig-
result was not a function ofthe treatment, which nificantly decreased leaf or stem biomass or
was applied after most of the plants com- flower production. Whether fruit abortions oc-
menced flowering. The low level of fruit pro- curred is unknown.
duction in the control group was a result of
natural pollination in the greenhouse. The role of leaf assimilate in fruit and seed
Since bud excision eliminated the repro- production -Treatment plants, which were
ductive sink, assimilate was directed to alter- completely defoliated after the week-long pol-
native sinks, leading to an increase in leaf and lination period, had reduced flower, fruit, and
stem production after 1 week. Short- or longer- seed production (Table 4). However, despite
term responses in leaf physiological character- the lack of leaf assimilate, treatment plants
istics were presumably not involved in the were able to produce ca. 40°/o as many seeds
changes in biomass partitioning. Also in con- as control plants. Seed maturation presumably
trast to the defoliation treatment was the in- occurred via stem and/or fruit photosynthesis,
adequacy of changes in biomass partitioning and at the expense of allocation to new flowers.
to adjust sink-source relations to control levels. The lower fruit production of treatment plants
398 AMERICAN JOURNAL OF BOTANY [Vol. 78

TABLE3. Plant responses to flower pollination (days 18-24). For each characteristic within each sampling period,
control and treatment means were compared by a t-test. Sample size for each group was 21

Mean 1 day response Mean 1 week response

Characteristic Control Treatment Control Treatment

Leaf production (number)

Leaf area (cm2)
Leaf biomass (g)
Stem biomass (g)
Reproductive biomass (g)
Total aboveground biomass (g)
Sink-source ratio (g:g)
Flowering time (days)
Flower production (number)
Fruit production (number)
Specific leaf weight (g m-2)
Area-based photosynthetic rate (pmol CO, m-2 sec-')
Area-based transpiration rate (mol H 2 0 m-2 sec-I)
Water-use efficiency (pmol CO, : mmol H 2 0 )
a Significance levels: P < 0.05, *; P < 0.01, **; P < 0.001, ***.
na = not applicable.

may have been a result of fruit abortions in response of photosynthesis. In rapid-cycling B.

treatment plants and/or of increased natural campestris, growth appeared to regulate pho-
pollinations of control plants. The latter is like- tosynthesis only in extreme conditions early in
ly since natural pollinations did occur and con- development.
trol plants produced more flowers than treat- The only treatment to which photosynthesis
ment plants. Neither the number of seeds per responded as predicted by the Boussingault
fruit nor the number of aborted seeds per fruit Hypothesis was defoliation early in develop-
differed between treatment and control plants. ment. The increase in photosynthesis rate was
Hence, differences in total fruit production ac- rapid but short-lived, and changes in allocation
counted for the greater total seed abortion in were evident a week later. Geiger, Jablonski,
control plants. and Ploeger (1985) and Jablonski and Geiger
(1987) also reported changes in allocation in
DISCUSSION response to decreased source strength in sugar
beet: leaf area increased so that pho~osynthcsis
Regulation of sink-source relations can oc- on a whole-plant basis (but not an area basis)
cur through complex responses at several levels
was increased. In the present work, plants re-
of organization over a wide range of time scales.
sponded to decreased sink size (bud excision)
Sharkey (1985) noted that direct responses of
photosynthesis usually occur after drastic and increased sink size (pollinations) by alter-
treatments. Herold (1980) suggested that other ing allocation but not leaf physiology. Fondy
mechanisms, such as altered partitioning, may and Geiger (1980) likewise reported that re-
serve to buffer the system and preclude direct sponses to rapid changes in sink-source rela-
tions in sugar beet and string bean often in-
TABLE4. The role of leaf assimilate in fruit and seed
volve changes in the allocation of exported
production. For each characteristic, control and treat- assimilate but not necessarily changes in pro-
ment means were compared by a t-test. Sample size duction (photosynthesis) or export rate of as-
for each group was 21 similate.
Leaf assimilate certainly played a role in seed
Means
ripening, but stem and/or fruit photosynthesis
Characteristic Control Treatment
probably contributed to seed production in the
Days to first flower 19.7 20.0 absence of leaf assimilate. Mean seed produc-
Number of flowers 159 **= 82 tion in the absence of leaf assimilate was ca.
Number of fruits 29 *** 14 40°/o of the control mean, which suggests that
Number of seeds 356 *** 142
in the control treatment, the contribution of
Number of aborted seeds 34 * 11
Number of seeds per fruit 13 11 leaf assimilate to seed maturation was ca. 60%.
Number of aborted seeds Similar results have been consistently reported
~ e fruit
r 0.12 0.08 for Brassica species: contribution of leaf assim-
a Significance levels: P < 0.05, *; P < 0.01, **; P < ilate to seed maturation typically ranges be-
0.001, ***. tween 40% and 70% (Inanaga, Kumura, and
March 199 11 EVANS -SINK-SOURCE RELATIONS
Murata, 1979b; Thies and Brar, 1984; Biswas
and Mandal, 1987).
Ontogenetic changes in the status of organs
as source or sink also appear to follow a typical
pattern in Brassica species. Prior to flowering,
leaf photosynthesis is the primary source of
assimilate; once seed ripening commences, stem
and fruit photosynthesis become important
1868. Agronomie, chimie agricole
(Inanaga, Kumura, and Murata, 1979a; Chap-
man, Daniels, and Scarisbrick, 1984). (Con-
sequently, the accuracy with which sink-source
relations were estimated likely changed with
ontogeny.) Stem and fruit photosynthesis may
have played a role in plant responses to the
pollination experiment which was performed
in the 2 weeks after flowering commenced. The
lower specific leaf weight of pollinated plants
may have been a result of increased partition-
ing to developing fruits. In other work with
this population (Evans and Teeri, unpublished
data), specific leaf weight was positively cor-
related with both leaf carbon and nitrogen con-
tents as well as area-based photosynthetic ca-
pacity.
The response of flower production to altered
sink-source relations may also change with on-
togeny. Keiller and Morgan (1988) reported
that the duration of flowering in B. napus in-
creased when basal fruits were excised early in
flowering but not later. In the present work,
flower production did not differ between pol-
linated and nonpollinated plants early in flow-
ering. However, pollinated plants that were
subjected to a severe defoliation treatment lat-
er in development did produce fewer flowers.
Responses to given treatments may well have
been different if treatments had been applied
at alternative stages of development. For ex-
ample, photosynthesis increased in response
to defoliation early in ontogeny, but whether
the same response would follow defoliation
later in development was not examined. Fur-
ther experimentation is required to distinguish
the effects of type and timing of treatments on
type and timing of responses.
Nonetheless, the results reported here illus-
trate the potential interplay between life his-
tory (e.g., phenology, biomass allocation) and
physiological (e.g., photosynthesis, transpira-
tion) responses to altered sink-source relations.
A whole-plant approach to sink-source rela-
tions should prove useful for many areas of
plant research, ranging from the regulation of
photosynthesis for improvement of crop yield
(see Gifford, 1986; Stitt and Quick, 1989 for
reviews) to the ecology and evolution of her-
bivory (e.g., Maschinski and Whitham, 1989)
and reproduction (e.g., Bodson and Bernier,
1985; Lumbers and Lechowicz, 1989).
399
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