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FRUCTAN METABOLISM AND
COOL-TEMPERATURE GROWTH
IN CHEATGRASS
N. Jerry Chatterton
ABSTRACT
of the winter when soil moisture is often most plentiful,
temperatures are too cold for significant plant growth
(Chatterton and others 1988). Although photosynthetic
processes remain quite functional at relatively cool temperatures in many species, the rates of carbon metabolism
and the utilization of photosynthates are reduced when
temperatures fall below about 20 °C.
If temperatures are warm enough for photosynthesis
to continue but cold enough to reduce plant growth, significant amounts of carbohydrates are often temporarily
stored in leaf tissues. In many plants these carbohydrates are stored as starch. Starch hydrolysis is relatively cool-temperature sensitive (Chatterton and others
1972; Garrard and Carter 1976; Pollock 1986a; West
1969). Thus, ambient temperatures from just above freezing to about 20 oc result in an accumulation ofleaf starch.
This is the case with species such as bermudagrass, com,
sorghum, and soybeans. If starch accumulation occurs for
very long, the internal structures of the chloroplast are
physically distorted by the starch grains and photosynthesis is reduced (Chatterton and others1972; West 1970).
Plants that accumulate predominantly starch and have
no alternative mechanism for storing photosynthates as
polymers are generally classified as warm-season plants.
In contrast, temperate plants have evolved other types
of carbohydrate metabolism that are generally less well
understood than that of starch (Pollock and Chatterton
1988; Pontis and del Campillo 1985). Alternative synthetic path ways involve oligo- or polysaccharides such
as sucrosylsaccharides that contain multiple fructose
molecules (Housley and Volenec 1986).
The presence of alternative mechanisms for carbohydrate storage has long been recognized, but only during
recent years have they been intensively studied. Within
the grass family, C-4 photosynthesis is closely associated
with starch-type metabolism; C-3 type photosynthesis
is almost exclusively associated with sucrosylsaccharide
or fructan-type metabolism (Bender and Smith 1973;
Chatterton and others 1989). In any case, these alternate
pathways provide mechanisms by which carbohydrates
can be stored outside the chloroplast (in the cell vacuole,
Wagner and Wiemken 1986), thereby avoiding possible
problems caused by starch accumulation and chloroplast
disruption.
Cheatgrass (Bromus tectorum) dominates many acres
ofpreviously disturbed rangeland, particularly in the
Intermountain West where it successfully competes for limited moisture. Its success is due in large part to plant adaptations that facilitate early and rapid growth. An important element of cheatgrass' early growth is a type of
carbohydrate metabolism that permits growth to occur at
relatively cool temperatures. That adaptation involves the
metabolism of a class of carbohydrates called fructan.
Fructans are essentially fructose polymers synthesized
from sucrose that contain one glucose and from two to several thousand fructose molecules. They are synthesized
and metabolized within plant vacuoles thus minimizing
the limitations and inefficiencies of starch metabolism that
generally occur within chloroplasts. Cheatgrass maintains its dominance on many disturbed areas by, among
other adaptations, having a carbohydrate metabolism that
permits photosynthesis and other growth processes to occur
at very cool temperatures. If moisture is available, cheatgrass seeds germinate soon after fall rains. Plants then
remain green over winter and have a head start on many
other species when temperatures begin to warm with the
end of winter.
INTRODUCTION
Considerable attention has focused on the ecology,
management, and opportunities for restoration of annual
rangelands in the Intermountain region. If progress is to
be made in restoring these rangelands, by enhancing site
stability, increasing plant cover and production, and by
reducing dominance by weedy annuals, it will be necessary to understand how and why species such as cheatgrass (Bromus tectorum) are so successful in maintaining
a tenacious hold on so many acres. This paper will discuss one physiological adaptation that provides cheatgrass
with a competitive advantage.
Relatively high temperatures and low available soil moisture are common occurrences during the summer months
on many cheatgrass-dominated ranges. Most of the dry
matter produced by cheatgrass occurs during a few weeks
in spring when moisture is available and temperatures
are favorable for growth. During a significant portion
COOL-TEMPERATURE PLANTS
The significance of a plant's ability to grow under cool
temperatures is extremely important in the Intermountain region. Plants capable of growth under cool temperatures are positioned to exploit the use of available soil
Paper presented at the Symposium on Ecology, Management, and Restoration of Intermountain Annual Rangelands, Boise, ID, May 18-22, 1992.
N. Jerry Chatterton is Research Leader, U.S. Department of Agriculture, Agricultural Research Service, Forage and Range Research Laboratory, Utah State University, Logan, UT 84322-6300.
333
FRUCTAN TRISACCHARIDES
moisture in the fall, winter, and spring when soil moisture is most plentiful.
Many range plants, classified as weedy species, have an
alternate carbohydrate metabolism that involves fructan.
Fructan is a sugar polymer built on sucrose and consists
primarily of fructose moieties (Pollock and Chatterton
1988}. Dandelion (Taraxacum o(ficinale}, a widely dispersed weed, is a cool-temperature adapted plant that
reaches maturity early:in the spring and is just one example of many Compositeae that metabolize fructan.
Other fructan-accumulating weeds include burdock
(Arctium minus}, ragweed (Ambrosia artemisiaefolia},
Canada thistle (Cirsium arvense), knapweed (Centaurea
repens), and hawkweed (Hieracium scouleri). Cheatgrass,
as well as wild oats (Avena fatua) and quackgrass (Elytrigia repens), is also a fructan accumulator. Obviously
fructan metabolism occurs in many of the world's most
dreaded temperate weeds.
To understand how fructan metabolism may offer a
competitive advantage, it is enlightening to consider some
differences between starch and fructan. While starch is
comprised of glucose molecules attached to form either
linear or branched chains, fructan is comprised primarily of fructose. Fructan can also be in either linear or
branched forms (Pontis and del Campillo 1985). Starch
and fructan are strikingly different in their solubility.
Fructan is much more water soluble and is hydrolyzed
into fructose without the energy (ATP) requirement of
starch (Edelman and Jefford 1968; Henry and Darbyshire
1980; Pollock 1986b; Shiomi and others 1979a,b). Fructan
synthesis may be slightly more efficient than starch synthesis in that the substrate is phosphorylated in starch
but not in fructan synthesis (Pollock 1986b).
C~O~H
0/~'CH20H
IHO
H
~H
CHaOH 0
~CHa
0
H
.
HO
H
H
H
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HO
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1- Kestose
6·Kestose
CHEATGRASSFRUCTANS
Inasmuch as cheatgrass is the current focus of interest,
I will discuss relationships of cheatgrass fructans with
those of other species. Recent efforts in my laboratory
have focused on the purification and identification of fructan structures in representative species including cheatgrass. Fructan metabolism and structures differ widely
among species. One-kestose is the most common simple
fructan in Gramineae species (Housley and others 1989;
Pontis and del Campillo 1985). It is synthesized by the
addition of one or more fructose molecules from sucrose
onto another sucrose. Thus, one sucrose is split into fructose and glucose (Scott and others 1966). The fructose is
attached to a second sucrose to form the fructan molecule
and the glucose is used in the synthesis of another sucrose. Each fructan moiety contains one glucose and from
two to several thousand fructose moieties (Grotelueschen
and Smith 1968; Shiomi and others 1976). Degree of polymerization (DP) is used to describe fructan size. For example, a fructan containing three monosaccharides is
DP3. Fructans involve bonds between carbons 2 and 1
and between carbons 6 and 2 (Pontis and del Campillo
1985). There are three possible DP3 fructan structures
(fig. 1). They are 1-kestose, 6-kestose, and neokestose
(Pollock and Chatterton 1988). Only in the case of neokestose is glucose not in a terminal position (Gross and
others 1954).
Neokestose
Figure 1-Chemical structures of 1-kestose,
6-kestose, and neokestose. Although each
trisaccharide consists of sucrose (one glucose
and one fructose) plus one additional fructose
molecule, the manner in which the second fructose is attached onto sucrose varies among the
three molecules.
Although there are only three possible ways of attaching a second fructose onto sucrose, there are nine possible
DP4 structures if one adds a fructose to a DP3 fructan.
Considering the many possible structures with increasing
DP, the complications of synthesis are obvious. Much of
the early work on fructans was done using Jerusalem artichoke (Helianthus tuberosus) (Edelman and Jetrord
1968). Figure 2 shows a separation of all the water soluble carbohydrates (fructans) from Jerusalem artichoke
tubers. Each peak represents a different size fructan.
334
w
(/)
z
structures, but because procedures have not been available that adequately separate and purify the various
kinds of fructan (Pollock and Chatterton 1988).
Figure 4 is a chromatogram of a mixture of the extracts
(fructans) from cheatgrass and orchardgrass (Dactylis glomerata). The shaded peaks are those from orchardgrass.
It remains to be determined how the different families of
fructans affect metabolism and plant adaptation.
100
Je rusalem Art ich oke
0
0..
(/)
w
75
0::
0::
0
f-
u
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25
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CHEATGRASSADVANTAGES
0::
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0..
0
10
5
20
15
25
30
RETENTION TIME (MINUTES)
2- Anion exchange chromatogram of
the water-soluble carbohydrates from Jerusalem
artichoke (Helianthus tuberosus) tubers. Each
peak differs from its neighbor by one fructose
molecule. Retention times increase with molecular weight.
Figure
w
(/)
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CF'
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Bromus tector~m (C)
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-K
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In summary, fructan biosynthesis is a type of carbohydrate metabolism that facilitates carbohydrate storage
away from the chloroplast (Wagner and Wiemken 1986)
and provides a significant advantage to plants in environments such as the Intermountain region where moisture
is generally most available when temperatures are cool.
Fructan metabolism, combined with other adaptations,
including excellent seedling vigor, allows cheatgrass to
become established in the fall when adequate moisture
is available. It remains green during the winter months
and is then capable of immediate photosynthesis when
temperatures are only slightly above freezing.
Because cheatgrass can metabolize carbohydrates at
cold temperatures and the photosynthetic potential of its
leaves is often maintained over winter, cheatgrass is able
to fix significant amounts of C02 and to grow under very
cool temperatures. Thus, cheatgrass gets a head start on
many other Great Basin taxa. Such early growth may
allow cheatgrass to more efficiently utilize limited soil
moisture, thereby allowing it to out-compete other plants
for available resources. The early spring growth and very
short life cycle of cheatgrass permit the production of
......... 1200
RETENTION TIME (MINUTES)
>
E 1000
3-Anion exchange chromatogram of
the water-soluble carbohydrates, primarily
fructans, from cheatgrass (Bromus tectorum)
leaves.
Figure
w
l/)
z
0
800
0..
l/)
w
600
0::
400
0::
0
f-
u
w
w
Thus, each peak represents a fructan that differs from the
peak on either side by a single fructose molecule. Note
how relatively simple and symmetrical the pattern is for
Jerusalem artichoke. It turns out that J erusalem artichoke tubers contain only one isomer or structure for each
polymer size.
Cheatgrass contains multiple forms or isomers for each
DP (fig. 3) and therefore contains a much more complicated family offructan structures than Jerusalem artichoke.
Relatively little is known about either the structures or
the enzymology of fructan biosynthesis. Advances have
come slowly, not only because of the complexity of the
f-
0
200
0
0
5
10
15
MINUTES
Figure 4-A chromatogram of a mixture
of the fructans from cheatgrass (Bromus
tectorum) and orchard grass (Dactylis
glomerata). The anion exchange separation
clearly shows the presence of different and
distinct families of fructans in the two species.
335
20
25
30
mature seed before soil moisture is either lost to evaporation or used by other species.
Housley, T. L.; Volenec, J. J. 1986. The synthesis offructans in tissues of tall fescue. Current Topics in Plant
Biochemistry and Physiology. 5: 198.
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Pollock, C. J.1986b. Fructans and the metabolism of sucrose in vascular plants. New Phytologist. 104: 1-24.
Pollock, C. J.; Chatterton, N.J. 1988. Fructans. In:
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Pontis, H. G.; del Campillo, E. 1985. Fructans. In: Dey,
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West, S. H. 1969. Carbohydrate metabolism in tropical
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