Plant Physiol. (1998) 117: 183–188
Fruit Development in Trillium1
Dependence on Stem Carbohydrate Reserves
Line Lapointe*
Département de Biologie, Université Laval, Ste-Foy, Québec, Canada G1K 7P4
Leaves are the main source of carbon for fruit maturation in most
species. However, in plants seeing contrasting light conditions such
as some spring plants, carbon fixed during the spring could be used
to support fruit development in the summer, when photosynthetic
rates are low. We monitored carbohydrate content in the rhizome
(a perennating organ) and the aboveground stem of trillium (Trillium erectum) over the entire growing season (May–November). At
the beginning of the fruiting stage, stems carrying a developing fruit
were harvested, their leaves were removed, and the leafless stems
were maintained in aqueous solution under controlled conditions
up to full fruit maturation. These experiments showed that stem
carbohydrate content was sufficient to support fruit development in
the absence of leaves and rhizome. This is the first reported case, to
our knowledge, of complete fruit development sustained only by a
temporary carbohydrate reservoir. This carbohydrate accumulation
in the stem during the spring enables the plant to make better use of
the high irradiances occurring at that time. Many other species
might establish short-term carbohydrate reservoirs in response to
seasonal changes in growing conditions.
Carbon allocation in plants changes over the course of
the season. In most herbaceous perennials there are large
changes in underground biomass at the end of the growing
season, reflecting the accumulation of carbohydrates for
the next year’s growth (Bradbury and Hofstra, 1977;
Chapin et al., 1986; Cyr et al., 1990). However, spring
ephemerals that senesce with the closing tree leaf canopy
show a rapid accumulation of carbohydrates early in the
season (Risser and Cottam, 1968), indicating that carbohydrate reserves can be quickly replenished and that the
timing of carbohydrate accumulation might be related to
growing conditions. Spring plants that senesce late in the
summer experience two types of contrasting light conditions. Photosynthetic rates are high at the beginning of the
growing season under the high light conditions before
the tree canopy closes and much lower over the rest of the
growing season, which is over by July or August (Sparling,
1967; Taylor and Pearcy, 1976). Under such conditions,
plants might accumulate carbohydrates much earlier than
plants growing under constant low (understory) or high
(field) light conditions. The first goal of this study was to
determine the pattern of carbohydrate accumulation and
1
This work was supported by a grant from the Natural Sciences
and Engineering Research Council of Canada.
* E-mail [email protected]; fax 1– 418 – 656 –2043.
use in trillium (Trillium erectum L.), a spring herb with a
long growing season.
Despite the fact that T. erectum produces only one fruit
per plant, with a biomass of 2 to 8% of total plant biomass,
fruit abortion is frequent (L. Lapointe, personal observation). Aerial parts of the plant senesce quickly when the
plant aborts its fruit, most frequently in late June, whereas
nonaborting plants keep their leaves up to the time of
complete fruit maturation, suggesting that leaves are required to support fruit development. We completely defoliated plants at different times during fruit development to
determine if fruit abortion could be induced later in the
season, and to what extent carbohydrate reserves would be
used to support the fruit during its development in the
absence of leaves (L. Lapointe and A. Deslauriers, unpublished data). Contrary to our original expectations, complete defoliation during fruit development did not induce
fruit abortion. Furthermore, carbohydrate analysis showed
that there was no loss of reserves from the rhizome in
defoliated, fruiting plants. These results suggested that
there may be a temporary carbohydrate reservoir in the
stem that can support fruit development and maturation.
Stems have been shown to act as temporary reservoirs of
carbon in some species, but usually contribute less than
50% to fruit development (Wardlaw, 1990; Schnyder, 1993).
Along with carbohydrate content of the rhizome, that of
the stem was also measured during the entire growing
season in fruiting plants of T. erectum. Previous work
showed that at the end of the growing season, T. erectum
rhizomes contained high levels of starch. Considering the
large size of the rhizome and the small biomass of the fruit,
it was possible that fruit maturation in defoliated plants
would not reduce the level of rhizome carbohydrates to
any great extent (Primack and Hall, 1990). The aim of this
study was to determine whether the stem was capable of
supporting fruit development by itself. Stems carrying a
developing fruit were harvested, defoliated, and maintained under controlled conditions in liquid medium. If
complete fruit maturation occurred this would show that
the stem of T. erectum had accumulated sufficient carbohydrates to support the development of fruit in the absence of
rhizome and leaves. Whereas some species use stems as
temporary carbon reservoirs (Pate et al., 1983; Yamagata et
al., 1987; Wardlaw, 1990), only Jerusalem artichoke (Helianthus tuberosus) appears to rely extensively on this tem-
Abbreviation: HQS, 8-hydroxyquinone.
183
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184
Lapointe
porary reserve for tuber formation at the end of the growing season (Incoll and Neales, 1970). Cereal plants rely on
stem carbohydrates for fruit development under severe
stress, which leads to reduced yields (Gallagher et al., 1976;
Schnyder, 1993). If the stem can support normal fruit development in T. erectum, this would be the first reported
case, to our knowledge, of a complete dependence on
temporary carbohydrate reserves for fruit development.
MATERIALS AND METHODS
Plant Harvests
Every week from May to August, and every 2 weeks
from September to November, 1994, eight reproductive
plants of trillium (Trillium erectum L.) were harvested from
a woodland area located near Québec city, Canada. The
plants were washed, separated into rhizomes, roots, stems,
leaves, and reproductive structures, dried (heat-killed at
100°C, dried at 70°C), and weighed. The rhizomes and
stems were then ground to a fine powder. Plants harvested
during the summer tended to be larger than plants harvested in the spring, so for size comparisons we also collected a series of fruits from smaller plants during the
summer. These fruits were also dried and weighed.
Carbohydrate Analyses
Carbohydrates were analyzed as described previously
(Lapointe and Molard, 1997), with the following modifications. Dry-ground tissues were reground with a polytron
homogenizer (model PT 3100, Kinematica AG, Littau, Switzerland) in a mixture of methanol, chloroform, and water
(12:5:3, v/v). The mixture was then left to macerate for 2 h
at 0°C before being centrifuged to separate soluble sugars
from nonsoluble residues. The supernatant was analyzed
before and after invertase digestion to estimate reducing
sugar and Suc content. The nonsoluble residues were first
heated at 100°C for 90 min to gelatinize starch, then incubated at 55°C for 1 h in presence of amyloglucosidase. All
reducing sugars were measured colorimetrically at 415
nm after reaction with p-hydroxybenzoic acid hydrazide.
Cut-Stem Experiment
Sixty T. erectum flowering plants were harvested in midJune, 1996. By this time, plants that would have aborted
their fruit had already started to senesce and only nonsenescing plants were chosen. Each stem was cut at the base
with a razor blade and immediately placed in water. Back
in the laboratory, the stems were measured, re-cut under
water, and all three leaves were removed. Each stem was
placed in a test tube containing 10 mL of one of the following: distilled water, nutrients, HQS, or nutrients and HQS.
The nutrient solution was made up of 5 mm Ca(NO3)2, 5
mm KNO3, 2 mm KH2PO4, and 1 mm MgSO4. The concentration of the HQS solution was 200 mg L21. Stems were
maintained in growth chambers (G30, Conviron, Win-
Plant Physiol. Vol. 117, 1998
nipeg, Canada) that simulated understory conditions in
July, with an irradiance of 25 mmol m22 s21 and a 14-h light
period at 25/15°C day/night temperatures. Stems were cut
every week and solutions were replaced twice a week.
Fruits were harvested when they reached maturity and
easily detached from the pedicel. Mature seeds (large seeds
bearing an eliaosome), aborted seeds (any seed larger than
the unfertilized ovule but smaller than mature seeds and
without an eliaosome), and unfertilized ovules were
counted for each harvested fruit. These three categories of
seeds were used to estimate the percent seed set and the
percentage of ovules fertilized.
Seed set ~%! 5
no. of mature seeds
3 100
total no. of ovules
(1)
Ovules fertilized ~%! 5
no. of mature seeds 1 no. of aborted seeds
3 100
total no. of ovules
(2)
Total dry fruit biomass, which included carpels, unfertilized ovules, and aborted seeds, and mature seed dry biomass were measured.
We labeled 34 T. erectum flowering plants in the same
woodland area in early spring. When the fruits were mature we recorded stem height and harvested the fruit.
Fruits were dissected and weighed as described above. The
plant height and fruit characteristics of cut-stem plants
(four treatment groups) and of understory plants were
compared using one-way analysis of variance.
RESULTS
Carbon Allocation during the Growing Season
Starch was the main carbohydrate in T. erectum rhizomes
year-round (Fig. 1). Starch concentrations were low at the
beginning of the season, but after 3 weeks growth rapidly
increased and reached maximum levels within 5 weeks.
The starch content of the rhizome then remained constant
throughout the summer until senescence of the aboveground parts (late August for the plants sampled). Starch
content decreased drastically throughout autumn and
reached early spring levels by mid-November. The levels
of Suc and reducing sugars did not show seasonal variations. Reducing sugar content was slightly but consistently
higher than Suc content.
The pattern of stem carbohydrate content was different
from that of the rhizome. In the stems, reducing sugars
were the most abundant carbohydrates throughout the
season (Fig. 2). For the first 3 weeks of growth, reducing
sugar content steadily increased, and then decreased
slowly over the summer until there was a rapid decrease
when fruit reached maturity. Starch and Suc content were
low in the stems. Starch content was highest from late May
to late June. Suc content gradually decreased throughout
the spring then increased slowly over the summer.
To compare changes in fruit biomass during development and changes in stem and rhizome carbohydrates, the
total carbohydrates (starch, Suc, and reducing sugars) in
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Fruit Development and Stem Reserves
185
Figure 1. Starch (), reducing sugar (F), and Suc (E) content (mg g21
dry mass) of T. erectum rhizome during the growth season and until
late November. Data are represented as mean 6 SE from eight
individuals.
the whole rhizome and in the whole stem were estimated
(Fig. 3). Rhizomes are large compared with stems and
contain more carbohydrates. Week-to-week variations in
rhizome total carbohydrates reflected large variations in
plant size. Variations in fruit dry mass or total stem carbohydrates were much less than for total rhizome carbohydrates. Until the beginning of July, carbohydrates in the
stem were equivalent to a higher biomass than the total
mass of the developing fruit. After this period, fruit dry
mass was higher than stem carbohydrate biomass, but both
showed similar weekly variations until fruit maturation.
The total amount of carbohydrates in the stem at the end
of spring was greater than that required for fruit development during the summer (Table I). Total leaf area, which is
a good estimate of plant size in T. erectum (r 5 0.74; P ,
0.001), was similar for plants harvested in the spring for the
carbon-allocation study (197.5 6 10.1 cm2) and for plants
Figure 3. Total carbohydrates contained in the rhizome (A) and stem
(B) of T. erectum during the growth season. Flower (from May to
mid-June) and fruit dry mass (E) are also presented in B for direct
comparison with total stem carbohydrate content (F). Data are represented as mean 6 SE from eight individuals.
harvested for fruit in late summer (206.1 6 13.8 cm2). Since
the bud for the following year’s flower has been formed by
the end of the season, the mean bud biomass was subtracted
from fruit biomass to estimate the cost of fruit development
for the current season. Fruit biomass amounted to about 100
mg or 65% of the stem total carbohydrates. These calculations
Table I. Total carbohydrates accumulated in the stem during the
spring compared with flower and fruit biomass in T. erectum
Total Carbohydratesa
Flowerb
Fruitc
61 6 3
161 6 20
mg
155 6 7d
a
Figure 2. Starch (), reducing sugar (F), and Suc (E) content (mg
g21 dry mass) of T. erectum stem during the growth season. Data are
represented as mean 6 SE from eight individuals.
Estimated from plants harvested from May 16 to June 27, when
b
sugar levels were stable in the stem (Fig. 3).
Estimated from
plants harvested from May 2 to June 14, when flower biomass was
c
stable and fruit development was not initiated yet (Fig. 3).
Estimated from 27 fruits harvested in the understory the same year
d
(1994).
Data are presented as mean 6 SE for 56 individuals
(stem sugar and flower biomass), and 27 understory plants (fruit
biomass).
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186
Lapointe
do not take into account growth and maintenance or fruit
respiration during development.
Cut-Stem Experiment
None of the cut stems in aqueous solutions, but 21% of
the labeled plants in the understory, aborted their fruit
(data not shown). The plants chosen for the cut-stem experiment tended to be larger (higher stem height), but on
average produced somewhat smaller fruits compared with
plants in the understory; however, these differences were
not statistically significant (Table II; P 5 0.069). The proportion of fertilized ovules, the proportion of fertilized
ovules that matured into seeds, and the total number of
seeds per fruit were not significantly different for any of
the treatments or growing conditions. Mean seed mass was
lower in treatments in which HQS was included in the stem
maintenance solution. Otherwise, there were no significant
differences in mean seed mass of fruit developed on cut
stems compared with mean seed mass of fruit developed
on control plants. Carpel dry mass, which included all
parts of the fruit except mature seeds, showed that the
slightly lower fruit biomasses from cut stems were mainly
due to lower mean seed mass; carpel dry masses were
similar across all groups (P 5 0.140). Fruits developed on
cut stems were more fleshy, as was reflected by their lower
ratio of dry to fresh mass. This parameter was also influenced by the presence of nutrients in the solution that
tended to reduce the amount of water in the fruit.
DISCUSSION
The present study strongly suggests that stems are used
as temporary carbohydrate reservoirs for fruit maturation
in T. erectum. A complete defoliation treatment during fruit
maturation under natural conditions has already suggested
the possibility of carbohydrate accumulation in the stem (L.
Lapointe and A. Deslauriers, unpublished data). Stem tissue was previously found to be a temporary carbon reservoir in cereals (Schnyder, 1993) and other agricultural
plants (Incoll and Neales, 1970; Pate et al., 1983; Yamagata
et al., 1987); however, in most species stored carbohydrates
support only part of the fruit development (Rawson and
Evans, 1971; Bonnett and Incoll, 1992). In the current study
Plant Physiol. Vol. 117, 1998
of T. erectum it appeared that stem carbohydrate content
was sufficient to support complete fruit development. Establishing a temporary carbohydrate reservoir would allow
spring ephemerals to maximize photosynthesis when irradiances are high in early spring and to develop mature
fruit more often or to produce larger fruit than plants
relying on low summer light for photosynthesis to support
fruit development.
Rhizome carbohydrate reserves were replenished
quickly in the spring and leaves did not translocate significant amounts of carbohydrate to the rhizome over the
summer. In many other perennials, carbohydrate accumulation in underground parts occurs much later, in August
or September (Bradbury and Hofstra, 1977; Cyr et al., 1990;
Zasada et al., 1994). In some arctic plants, rhizome starch
contents are replenished quickly (early July), well before
the end of the growing season (Fonda and Bliss, 1966;
Chapin et al., 1986). But there are other arctic plants with
typical late-season starch accumulation (Chapin et al.,
1986). The accumulation of carbohydrate reserves early in
the season might reflect the short spring period, when
ephemerals can photosynthesize at a maximum rate before
conditions change. Sixty percent of the rhizome reserves
was replenished by current photosynthesis, the rest appeared to be long-term carbohydrate reserves. Long-term
reserves may only be used after a catastrophe such as fire,
severe defoliation, or freezing (Whigham, 1984), or may be
used to allow fruit set in perennial species (Stephenson,
1981).
Buds in T. erectum were visible at the end of the growing
season and contained partly developed leaves and flowers.
A large fraction of the rhizome starch content appeared to
be translocated to the bud throughout autumn, and by
mid-November, rhizome starch content was the same as in
early spring. Only a small fraction of the autumn decrease
in starch content may be attributed to the increased Suc
content (23%) and rhizome respiration. Soil temperature
decreased rapidly in the autumn (data not shown), which
would minimize carbon respiration losses. Early carbon
translocation to the bud probably accelerates shoot growth
in the spring, which then only requires water uptake for
cell elongation.
Sugar accumulated in stem tissue of T. erectum in the
spring. Cereals also accumulate maximum carbohydrate in
Table II. Characteristics of the fruits harvested from cut stems maintained in different aqueous solutions and from control plants growing in
the understory
Stem height is an indication of plant size. One-way analysis of variance results are presented for all parameters. Data are presented as mean 6
SE for 15 individuals per treatment and 27 understory plants. Statistical differences (P # 0.05) after a multiple comparison procedure was
performed (Tukey test) are indicated by different letters (a, b, and c).
Treatment
Stem Height
Distilled water
HQS
Nutrients
HQS 1 nutrients
Understory
Analysis of
variance results
27.8 6 0.7
27.6 6 0.8
27.3 6 0.6
27.1 6 0.9
24.0 6 1.0
P 5 0.336
Seed No.
Ovules
Fertilized
31.7 6 5.2
31.5 6 4.1
32.1 6 5.3
32.9 6 4.6
28.3 6 3.4
P 5 0.782
74.2 6 4.5
71.5 6 3.1
64.6 6 5.1
76.3 6 3.0
71.8 6 2.9
P 5 0.305
cm
Seed Set
Dry Mass
Total fruit
Mean seed
mg
Carpel
Fruit Dry-to-Fresh
Mass Ratio
99.3 6 12.3
84.8 6 10.3
101.0 6 9.6
90.2 6 11.7
149 6 21
P 5 0.069
2.39 6 0.20 ab
1.86 6 0.12 a
2.36 6 0.18 ab
1.87 6 0.15 a
3.73 6 0.30 b
P , 0.001
30.3 6 3.5
28.4 6 3.5
33.7 6 3.2
29.7 6 3.2
43.1 6 5.3
P 5 0.140
0.109 6 0.005 ab
0.106 6 0.007 a
0.153 6 0.014 bc
0.125 6 0.010 ab
0.202 6 0.017 c
P , 0.001
%
52.0 6 5.6
52.3 6 4.2
54.4 6 5.6
62.3 6 4.3
57.8 6 3.8
P 5 0.536
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Fruit Development and Stem Reserves
stems under high irradiance. Shaded cereals (30% of full
sunlight) could only accumulate about one-half of the carbohydrates accumulated by full-sun plants (Judel and
Mengel, 1982). In this study irradiance in the understory
over summer, 1% of full sunlight (data not shown), was
much lower than that used in a previous study (Judel and
Mengel, 1982). We found no increase in stem carbohydrate
content in T. erectum over the summer, suggesting that the
carbohydrates had accumulated in stems only during the
conditions allowing high photosynthetic rates.
The idea that the stem in T. erectum was used as a
temporary carbohydrate reservoir was supported by several observations. First, we found more carbohydrate in the
stem than is required for stem tissue respiration. Second,
most of these carbohydrates were reducing sugars and not
Suc, which suggests that carbohydrates were not mobile
sugars that shifted from the leaves to the rhizome, but
rather were stored carbohydrates. Third, when irradiances
decreased in early June (Vézina and Grandtner, 1965), stem
sugar content did not decrease, acting as a temporary
carbon reservoir and not actively translocated between
leaves and rhizome. There is evidence from sequential 14C
labeling in wheat (Bell and Incoll, 1990) for separate carbohydrate pools for transport and storage in stems. The
total amount of carbohydrates stored in the stem was low
compared with that in the rhizome, but was sufficient to
allow complete fruit development (Table I). The percentage
of biomass in the stem slowly decreased during fruit maturation (L. Lapointe and A. Deslauriers, unpublished data),
which suggests that, similar to wheat (Bell and Incoll,
1990), the decrease in stem dry biomass during fruit maturation in trillium is a reflection of source and sink exchanges.
The cut-stem experiment confirmed that the carbohydrate reserves in the stem were sufficient to support fruit
development. Seeds were slightly smaller than seeds matured on complete plants (rhizome and leaves present), but
all cut stems matured a fruit. In defoliation experiments
using double-stem T. erectum plants, the leafless stem produced smaller seeds when the nondefoliated stem senesced
early compared with when it senesced late (A. Deslauriers
and L. Lapointe, unpublished data). Therefore, leaves may
play a role during fruit maturation, but are not essential for
fruit development. Very low irradiances in the understory
mean leaf photosynthetic rates are low during the summer
(L. Lapointe and A. Deslauriers, unpublished data). Stem
photosynthesis is likely to be limited, since the stem is
vertical and shaded by the leaves. The fruit is always dark
red and cannot fix carbon. A major source of carbon for
fruit development in T. erectum must be the carbohydrates
stored in the stem during spring.
In the cut-stem experiment we added HQS to control
bacterial growth (Rogers, 1973; Ketsa and Boonrote, 1990).
It appeared that HQS was slightly harmful to the fruit and
seed development. Cut stems fed with nutrients did not
produce larger seeds or fruits compared with stems maintained in distilled water. The only effect of the nutrient
treatments was on the ratio of dry to fresh mass of the fruit.
We noticed that the fruits produced by cut stems were
fleshier than the fruits harvested from the field. This could
187
have been because of higher RH in the growth cabinets and
the absence of wind. Since nutrients played such a minor
role in fruit and seed development, it may be that the stem
also accumulates nutrients during spring. Spring ephemerals may take advantage of the nutrient flushes right after
snow melt (Muller, 1978; Hicks and Chabot, 1985). T. erectum leaves contain high levels of nitrogen (L. Lapointe,
unpublished data). Under natural conditions these leaves
slowly senesce during fruit maturation, with the possibility
of translocation of nutrients from leaves to fruit, as has
been shown for wheat (Waldren and Flowerday, 1978).
However, this postulated translocation does not seem to be
important enough to affect seed biomass in leafless plants.
Stem nutrient content may be sufficient to allow normal
seed development to take place.
Stems have previously been shown to be a temporary
carbon reservoir in cereals (Schnyder, 1993) and other
grasses (Warringa and Kreuzer, 1996), in soybean (Yamagata et al., 1987), cowpea (Pate et al., 1983), Plantago major
and Urtica dioica (den Hertog et al., 1996), and Jerusalem
artichoke (Helianthus tuberosus; Incoll and Neales, 1970).
However, in tulips, the only other spring ephemeral in
which stem carbohydrate content has been investigated,
there was no accumulation of carbohydrates in stem tissues
(Ho and Rees, 1976). Stem contribution to ear growth in
cereals varies from 3 to 40% in unstressed plants (Rawson
and Evans, 1971; Austin et al., 1977; Bonnett and Incoll,
1992), but can reach 70 to 100% in stressed plants (Gallagher et al., 1976; Scott and Dennis-Jones, 1976). In T.
erectum, stem carbohydrate contribution to fruit development was high and resembled the situation in stressed
cereals. The period of carbohydrate accumulation is shortened in stressed plants and the importance of carbohydrates stored in stems may be related to the time the plant
had to accumulate carbohydrates during periods of high
photosynthetic rates before fruit development began.
In spring ephemerals the establishment of a temporary
carbon reservoir enables the plant to benefit from high
irradiances in the spring. The presence of a temporary
carbon reservoir may alleviate some of the sink limitations
present before fruit development in fast-growing species
such as cereals (Bell and Incoll, 1990). It seems probable
that the development of a temporary carbohydrate reservoir could alleviate some of the sink limitations of slowgrowing species as well, since their growth is often also
strongly restricted by sink activity. Carbohydrate accumulation in stems would not compete with rhizome carbohydrate storage in T. erectum as it does in cereals, where there
does not seem to be competition between grain filling and
stem carbohydrate accumulation (Schnyder, 1993). T. erectum leaves were capable of replenishing rhizome carbohydrate reserves within 3 weeks after full development, when
plants were still flowering, and accumulation of carbon in
the stem made better use of the high spring irradiances.
Stephenson (1981) suggested that perennial species may
use reserves accumulated in previous years to support fruit
maturation. In T. erectum, and probably in other species as
well (Sohn and Policansky, 1977), long-term carbohydrate
reserves are probably aimed at future growth and are not
used for fruit development. These plants develop a short-
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188
Lapointe
term carbohydrate reservoir that supports current-year
reproduction.
ACKNOWLEDGMENTS
The author thanks Marie-Hélène Laroche and Annie Tremblay
for their help in harvesting plants in 1994, and Michel Bergeron,
Olivier Facon, and Frédéric Salvi for carbohydrate analyses.
Received November 21, 1997; accepted February 2, 1998.
Copyright Clearance Center: 0032–0889/98/117/0183/06.
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