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This file was created by scanning the printed publication. Errors identified by the software have been corrected; however, some errors may remain. 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 Cheatgrass (Bromus tectorum) dominates many acres (Chatterton and others 1988). Although photosynthetic ofpreviously disturbed rangeland, particularly in the processes remain quite functional at relatively cool tem­ Intermountain West where it successfully competes for lim­ peratures in many species, the rates of carbon metabolism ited moisture. Its success is due in large part to plant ad­ and the utilization of photosynthates are reduced when aptations that facilitate early and rapid growth. An im­ temperatures fall below about 20 °C. portant element of cheatgrass' early growth is a type of If temperatures are warm enough for photosynthesis metabolism that permits growth to occur at to continue but cold enough to reduce plant growth, sig­ relatively cool temperatures. That adaptation involves the nificant amounts of are often temporarily metabolism ofa class ofcarbohydrates called fructan. stored in leaf tissues. In many plants these carbohy­ Fructans are essentially polymers synthesized drates are stored as . Starch hydrolysis is rela­ from that contain one and from two to sev­ tively cool-temperature sensitive (Chatterton and others eral thousand fructose molecules. They are synthesized 1972; Garrard and Carter 1976; Pollock 1986a; West and metabolized within plant vacuoles thus minimizing 1969). Thus, ambient temperatures from just above freez­ the limitations and inefficiencies of starch metabolism that ing to about 20 oc result in an accumulation ofleaf starch. generally occur within chloroplasts. Cheatgrass main­ This is the case with species such as bermudagrass, com, tains its dominance on many disturbed areas by, among sorghum, and soybeans. If starch accumulation occurs for other adaptations, having a carbohydrate metabolism that very long, the internal structures of the chloroplast are permits photosynthesis and other growth processes to occur physically distorted by the starch grains and photosynthe­ at very cool temperatures. If moisture is available, cheat­ sis is reduced (Chatterton and others1972; West 1970). grass seeds germinate soon after fall rains. Plants then Plants that accumulate predominantly starch and have remain green over winter and have a head start on many no alternative mechanism for storing photosynthates as other species when temperatures begin to warm with the polymers are generally classified as warm-season plants. end of winter. In contrast, temperate plants have evolved other types of carbohydrate metabolism that are generally less well INTRODUCTION understood than that of starch (Pollock and Chatterton 1988; Pontis and del Campillo 1985). Alternative syn­ Considerable attention has focused on the ecology, thetic path ways involve oligo- or such management, and opportunities for restoration of annual as sucrosylsaccharides that contain multiple fructose rangelands in the Intermountain region. If progress is to molecules (Housley and Volenec 1986). be made in restoring these rangelands, by enhancing site The presence of alternative mechanisms for carbohy­ stability, increasing plant cover and production, and by drate storage has long been recognized, but only during reducing dominance by weedy annuals, it will be neces­ recent years have they been intensively studied. Within sary to understand how and why species such as cheat­ the grass family, C-4 photosynthesis is closely associated grass (Bromus tectorum) are so successful in maintaining with starch-type metabolism; C-3 type photosynthesis a tenacious hold on so many acres. This paper will dis­ is almost exclusively associated with sucrosylsaccharide cuss one physiological adaptation that provides cheatgrass or fructan-type metabolism (Bender and Smith 1973; with a competitive advantage. Chatterton and others 1989). In any case, these alternate Relatively high temperatures and low available soil mois­ pathways provide mechanisms by which carbohydrates ture are common occurrences during the summer months can be stored outside the chloroplast (in the cell vacuole, on many cheatgrass-dominated ranges. Most of the dry Wagner and Wiemken 1986), thereby avoiding possible matter produced by cheatgrass occurs during a few weeks problems caused by starch accumulation and chloroplast in spring when moisture is available and temperatures disruption. are favorable for growth. During a significant portion COOL-TEMPERATURE PLANTS

Paper presented at the Symposium on Ecology, Management, and Res­ The significance of a plant's ability to grow under cool toration of Intermountain Annual Rangelands, Boise, ID, May 18-22, 1992. temperatures is extremely important in the Intermoun­ N. Jerry Chatterton is Research Leader, U.S. Department of Agricul­ tain region. Plants capable of growth under cool tempera­ ture, Agricultural Research Service, Forage and Range Research Labora­ tory, Utah State University, Logan, UT 84322-6300. tures are positioned to exploit the use of available soil

333 moisture in the fall, winter, and spring when soil mois­ FRUCTAN ture is most plentiful. Many range plants, classified as weedy species, have an alternate carbohydrate metabolism that involves fructan. Fructan is a polymer built on sucrose and consists C~O~H primarily of fructose moieties (Pollock and Chatterton 1988}. Dandelion (Taraxacum o(ficinale}, a widely dis­ 0/~'CH20H persed weed, is a cool-temperature adapted plant that IHO H reaches maturity early:in the spring and is just one ex­ . ~HCHaOH 0 ~CHa0 H ample of many Compositeae that metabolize fructan. HO H H H HOH Other fructan-accumulating weeds include burdock HO CH20H (Arctium minus}, ragweed (Ambrosia artemisiaefolia}, H OH 0 HO H Canada thistle (Cirsium arvense), knapweed (Centaurea repens), and hawkweed (Hieracium scouleri). Cheatgrass, as well as wild oats (Avena fatua) and quackgrass (Elytri­ 1-Kestose gia 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 primar­ ily of fructose. Fructan can also be in either linear or branched forms (Pontis and del Campillo 1985). Starch 6·Kestose 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 syn­ thesis in that the substrate is phosphorylated in starch but not in fructan synthesis (Pollock 1986b). 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 fruc­ Neokestose tan structures in representative species including cheat­ grass. Fructan metabolism and structures differ widely Figure 1-Chemical structures of 1-kestose, among species. One-kestose is the most common simple 6-kestose, and neokestose. Although each fructan in Gramineae species (Housley and others 1989; consists of sucrose (one glucose Pontis and del Campillo 1985). It is synthesized by the and one fructose) plus one additional fructose addition of one or more fructose molecules from sucrose molecule, the manner in which the second fruc­ onto another sucrose. Thus, one sucrose is split into fruc­ tose is attached onto sucrose varies among the tose and glucose (Scott and others 1966). The fructose is three molecules. attached to a second sucrose to form the fructan molecule and the glucose is used in the synthesis of another su­ crose. Each fructan moiety contains one glucose and from two to several thousand fructose moieties (Grotelueschen Although there are only three possible ways of attach­ and Smith 1968; Shiomi and others 1976). Degree of poly­ ing a second fructose onto sucrose, there are nine possible merization (DP) is used to describe fructan size. For ex­ DP4 structures if one adds a fructose to a DP3 fructan. ample, a fructan containing three is Considering the many possible structures with increasing DP3. Fructans involve bonds between carbons 2 and 1 DP, the complications of synthesis are obvious. Much of and between carbons 6 and 2 (Pontis and del Campillo the early work on fructans was done using Jerusalem ar­ 1985). There are three possible DP3 fructan structures tichoke (Helianthus tuberosus) (Edelman and Jetrord (fig. 1). They are 1-kestose, 6-kestose, and neokestose 1968). Figure 2 shows a separation of all the water sol­ (Pollock and Chatterton 1988). Only in the case of neo­ uble carbohydrates (fructans) from kestose is glucose not in a terminal position (Gross and tubers. Each peak represents a different size fructan. others 1954).

334 w (/) 100 structures, but because procedures have not been avail­ z Jerusalem Artichoke able that adequately separate and purify the various 0 0.. kinds of fructan (Pollock and Chatterton 1988). (/) w 75 Figure 4 is a chromatogram of a mixture of the extracts 0:: (fructans) from cheatgrass and orchardgrass (Dactylis glo­ 0:: 0 merata). The shaded peaks are those from orchardgrass. f- u 50 It remains to be determined how the different families of w w fructans affect metabolism and plant adaptation. 0 f-z 25 w CHEATGRASSADVANTAGES u 0:: w In summary, fructan biosynthesis is a type of carbohy­ 0.. 0 0 5 10 15 20 25 30 drate metabolism that facilitates carbohydrate storage away from the chloroplast (Wagner and Wiemken 1986) RETENTION TIME (MINUTES) and provides a significant advantage to plants in environ­ ments such as the Intermountain region where moisture Figure 2- Anion exchange chromatogram of the water-soluble carbohydrates from Jerusalem is generally most available when temperatures are cool. Fructan metabolism, combined with other adaptations, artichoke (Helianthus tuberosus) tubers. Each peak differs from its neighbor by one fructose including excellent seedling vigor, allows cheatgrass to molecule. Retention ti mes increase with mo­ become established in the fall when adequate moisture lecular weight. 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 w (/) 100 leaves is often maintained over winter, cheatgrass is able z CF' R Bromus tector~m (C) 0 to fix significant amounts of C02 and to grow under very 0.. n (/) -K cool temperatures. Thus, cheatgrass gets a head start on w 75 0:: many other Great Basin taxa. Such early growth may 0:: s INI allow cheatgrass to more efficiently utilize limited soil 0 8·K f- moisture, thereby allowing it to out-compete other plants u 50 w ~ for available resources. The early spring growth and very w short life cycle of cheatgrass permit the production of 0 25 _J f-z \t w u ~~ 0:: w 0 0.. r 0 5 10 15 20 25 30 ...... 1200 RETENTION TIME (MINUTES) > E 1000 Figure 3-Anion exchange chromatogram of w the water-soluble carbohydrates, primarily l/) z 800 fructans, from cheatgrass (Bromus tectorum) 0 leaves. 0.. l/) w 600 0:: 0:: 400 0 f- u Thus, each peak represents a fructan that differs from the w 200 peak on either side by a single fructose molecule. Note f-w 0 how relatively simple and symmetrical the pattern is for 0 Jerusalem artichoke. It turns out that J erusalem arti­ choke tubers contain only one isomer or structure for each 0 5 10 15 20 25 30 polymer size. MINUTES Cheatgrass contains multiple forms or isomers for each DP (fig. 3) and therefore contains a much more complicat­ Figure 4-A chromatogram of a mixture ed family offructan structures than Jerusalem artichoke. of the fructans from cheatgrass (Bromus Relatively little is known about either the structures or tectorum) and orchard grass (Dactylis glomerata). The anion exchange separation the enzymology of fructan biosynthesis. Advances have clearly shows the presence of different and come slowly, not only because of the complexity of the distinct families of fructans in the two species.

335 mature seed before soil moisture is either lost to evapora­ Housley, T. L.; Volenec, J. J. 1986. The synthesis offruc­ tion or used by other species. tans in tissues of tall fescue. Current Topics in Plant Biochemistry and Physiology. 5: 198. Pollock, C. J. 1986a. Environmental effects on sucrose and REFERENCES fructan metabolism. Current Topics in Plant Biochemis­ Bender, M. M.; Smith, D. 1973. Classification of starch­ try and Physiology. 5: 32-46. and fructosan-accumulating grasses as C-3 or C-4 spe­ Pollock, C. J.1986b. Fructans and the metabolism of su­ cies by carbon isotope analysis. Journal of the British crose in vascular plants. New Phytologist. 104: 1-24. Grassland Society. 28:97-100. Pollock, C. J.; Chatterton, N.J. 1988. Fructans. In: Chatterton, N. J.; Carlson, G. E.; Hungerford, W. E.; Lee, Preiss, J., ed. The biochemistry of plants. New York: D. R. 1972. Effect of tillering and cool nights on photo­ Academic Press: 109-140. synthesis and chloroplast starch in pangola. Crop Sci­ Pontis, H. G.; del Campillo, E. 1985. Fructans. In: Dey, ence. 12: 206-208. P.M.; Dixon, R. A, eds. Biochemistry of storage carbo­ Chatterton, N.J.; Harrison, P. A; Bennett, J. H.; Asay, hydrates in green plants. New York: Academic Press: K. H. 1989. Carbohydrate partitioning in 185 accessions 205-227. of Gramineae grown under warm and cool tempera­ Scott, R. W.; Jefford, T. G.; Edelman, J. 1966. Sucrose tures. Journal of Plant Physiology. 134: 169-179. fructosyltransferase from higher plant tissues. Bio­ Chatterton, N.J.; Thornley, W. R.; Harrison, P. A.; chemical Journal. 100: 23-24. Bennett, J. H. 1988. Dynamics of fructan and sucrose Shiomi, N.; Yamada, J.; Izawa, M. 1979a. A novel biosynthesis in crested wheatgrass. Plant and Cell pentasaccharide in the roots of (Asparagus Physiology. 29: 1103-1108. officinalis L.). Agricultural Biological Chemistry. Edelman, J.; Jefford, T. G. 1968. The mechanism of fruc­ 43: 1375-1377. tosan metabolism in higher plants as exemplified in Shiomi, N.; Yamada, J.; Izawa, M. 1979b. Synthesis of Helianthus tuberosus. New Phytologist. 67:517-531. several fructo- by asparagus fructosyl­ Garrard, L. A; Carter, J. L. 1976. Leaf assimilate level tansferases. Agricultural Biological Chemistry. 43: and photosynthesis of Digitaria decumbens Stent. Soil 2233-2244. and Crop Science Society of Florida. 35:6-10. Wagner, W.; Wiemken, A 1986. Properties and subcellu­ Gross, D.; Blanchard, P. H.; Bell, D. J. 1954. A trisaccha­ lar localization of fructan hydrolase in the leaves of bar­ ride formed from sucrose by yeast invertase. Journal of ley (Hordeum vulgare L. cv. Gerbel). Journal of Plant the American Chemical Society: 1727-1730. Physiology. 123:429-439. Grotelueschen, R. D.; Smith, D. 1968. Carbohydrates in West, S. H. 1969. Carbohydrate metabolism in tropical grasses. III. Estimations of the degree of polymerization plants subjected to low temperatures. Soil and Crop of the fructosans in the stem bases of timothy and bro­ Science Society of Florida. 29: 264-272. megrass near seed maturity. Crop Science. 8: 210-212. West, S. H. 1970. Biochemical mechanism of photosynthe­ Henry, R. J.; Darbyshire, B. 1980. Sucrose:sucrose fruc­ sis and growth depression in Digitaria decumbens when tosyltransferase and fructan:fructan fructosyltrans­ exposed to low temperatures. Physiology of pasture and ferase from Allium cepa. Phytochemistry.19: 1017-1020. forage plants. In: Florida Agricultural Experiment Sta­ Housley, T. L.; Kanabus, J.; Carpita, N. C. 1989. Fructan tion Journal Series. 3328:514-517. synthesis in leaf blades. Journal of Plant Physiol­ ogy. 134: 192-195.

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