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Plant Physiology 132:2218-2229 (2003) © 2003 American Society of Plant Biologists Fructans, But Not the Sucrosyl-Galactosides, Raffinose and Loliose, Are Affected by Drought Stress in Perennial RyegrassUnité Mixte de Recherche Institut National de la Recherche Agronomique-Université de Caen-Basse Normandie, Laboratoire de Physiologie et Biochimie végétales, Institut de Recherche en Biologie Appliquée, Université, 14032 Caen cedex, France (V.A., A.M.-B., J.-P.B., C.H., M.-P.P.); and Institute of Plant Biology, University of Zurich, Zollikerstrasse 107, CH–8008 Zurich, Switzerland (F.K.)
The aim of this study was to evaluate the putative role of the sucrosyl-galactosides, loliose [  -D-Gal (1,3)
-D-Glc (1,2)  -D-Fru] and raffinose
[-D-Gal (1,6) -D-Glc (1,2)
-D-Fru], in drought tolerance of perennial ryegrass and to
compare it with that of fructans. To that end, the loliose biosynthetic
pathway was first established and shown to operate by a UDP-Gal: sucrose (Suc)
3-galactosyltransferase, tentatively termed loliose synthase. Drought stress
increased neither the concentrations of loliose and raffinose nor the
activities of loliose synthase and raffinose synthase (EC 2.4.1.82). Moreover,
the concentrations of the raffinose precursors, myoinositol and galactinol, as
well as the gene expressions of myoinositol 1-phosphate synthase (EC 5.5.1.4)
and galactinol synthase (EC 2.4.1.123) were either decreased or unaffected by
drought stress. Taken together, these data are not in favor of an obvious role
of sucrosyl-galactosides in drought tolerance of perennial ryegrass at the
vegetative stage. By contrast, drought stress caused fructans to accumulate in
leaf tissues, mainly in leaf sheaths and elongating leaf bases. This increase
was mainly due to the accumulation of long-chain fructans (degree of
polymerization > 8) and was not accompanied by a Suc increase.
Interestingly, Suc but not fructan concentrations greatly increased in
drought-stressed roots. Putative roles of fructans and sucrosyl-galactosides
are discussed in relation to the acquisition of stress tolerance.
One of the strategies employed by plants to survive drought stress includes the synthesis of protective compounds, which may act by stabilizing membranes and proteins or mediating osmotic adjustment (Bohnert et al., 1995  ;
Hare et al., 1998;
Hoekstra et al., 2001).
Included among these protective compounds are the water-soluble carbohydrates
(WSCs), Glc, Suc, raffinose, myoinositol, and fructans.
Raffinose family oligosaccharides (RFOs) such as raffinose and stachyose
accumulate during seed development and are thought to play a role in the
desiccation tolerance of seeds (Blackman et
al., 1992
In addition to GolS, myoinositol 1-phosphate synthase (INPS; EC 5.5.1.4) is
another enzyme that may control the levels of galactinol and raffinose. It
represents the point of entry into the RFO biosynthetic pathway because it
diverts carbon from Glc-6-phosphate to myoinositol-1-phosphate, which is then
used by inositol monophosphatase to produce myoinositol, the galactinol
precursor. When potato (Solanum tuberosum) antisense INPS
transformants were analyzed, they showed strongly reduced levels of
myoinositol, galactinol, and raffinose in their leaves
(Keller et al., 1998
Fructans (polyfructosyl-Suc) are a further group of reported candidates for
drought protectants. In several species, fructans are either accumulated
(Volaire and Lelièvre,
1997
Suc:fructan 6-fructosyltransferase (6-SFT, EC 2.4.1.10) is one of the
enzymes involved in grass fructan biosynthesis
(Sprenger et al., 1995
Temperate forage grasses such as Dactylis glomerata, Festuca
arundinacca, or perennial ryegrass (Lolium perenne) cannot
maintain growth and development under prolonged and intense drought, but must
be able to remain alive during a limited water deficit period to recover
actively after rehydration (Volaire and
Lelièvre, 1997
Under non-stressed conditions, perennial ryegrass plants accumulate small
amounts of raffinose and loliose (Pavis et
al., 2001
Loliose Tissue Localization and Loliose Synthase Characterization Loliose was not homogeneously distributed in perennial ryegrass plants (Fig. 1A). The highest concentration was found in seeds where it amounted to almost 2% of the dry weight, and 80.5% of the WSC, the other sugars being Suc, Glc, and Fru. In vegetative tissues, loliose was found exclusively in leaf sheaths and the upper part of the roots. In leaf sheaths, the highest concentration was found in the middle internal sheaths. Loliose was neither detected in leaf blades nor in immature growing leaves.
The biosynthesis of galactosyl-Suc trisaccharides has been shown to proceed
by pathways involving either UDP-Gal (for planteose and umbelliferose
synthesis) or galactinol (for raffinose synthesis) as galactosyl donors, with
Suc being always the galactosyl acceptor (for review, see
Keller and Pharr, 1996
The water content of the soil was measured to determine the drought rate. Under control conditions, the water content of the soil remained fairly constant. Under stress conditions, the soil water content dropped from 3 to 1.2 g g-1 dry soil during the first 7 d of drought and still decreased during the 7 following d to reach almost zero (Fig. 2). By contrast, the leaf water potential did not change during the first week of drought but started to decrease sharply afterward from -0.4 to less than -1.6 MPa. During the rewatering period, the soil water content increased immediately from 0.1 to 2.6 g g-1 dry soil in 3 d and reached the same value as the control soil (3.3 g g-1 dry soil) 11 d later. The leaf water potential increased also sharply in parallel with the soil water content during the early period of rewatering from -1.6 to -0.7 MPa but remained stable afterward.
Under control conditions, the water content of the leaf tissues and the roots remained fairly constant (Fig. 3). Under stress conditions, the water content of elongating leaf bases and leaf sheaths showed a 25% to 30% decrease during the 14 d of drought, whereas that of leaf blade and roots declined only by 16% and 6%, respectively. However, no significant difference was found on a dry weight basis between control plants and drought-stressed plants. During the rewatering period, the water content in each tissue of drought-stressed plants increased again progressively to reach values that were not significantly different from those in control plants. The dry weight of drought-stressed plant tissues remained stable after rewatering, whereas it increased in control plants, leading to 30% to 45% differences in dry weight between drought-stressed plants and control plants at the end of the rewatering period. The number of tillers per plant increased progressively during the experiment but was always similar between droughtstressed and control plants (data not shown).
Under stress conditions, fructan concentrations increased significantly in all leaf tissues. The most pronounced increase was observed in elongating leaf bases where a 2-fold higher concentration was reached at the end of the drought period (amounting to 60% of the dry weight) as compared with control plants (Fig. 4A). During the rewatering period, fructan concentrations first increased (in mature leaves) or remained stable (in elongating leaf bases) before declining in all leaf tissues of drought-stressed plants to come back to values similar to those in control plants. In roots, fructan concentrations did not change significantly during the experiment, neither in control nor in drought-stressed plants.
To determine whether the fructan accumulation in leaf tissues during drought was due to low or high degree of polymerization (DP) fructans, WSC samples were analyzed by high-performance anion-exchange chromatography with pulsed amperometric detection (HPAEC-PAD; Fig. 5). To compare the relative proportions of low and high DP fructans, the same amounts of total fructan were injected for each type of tissue. At the beginning of the experiment (d 0), elongating leaf bases contained a higher proportion of low DP fructans, whereas in leaf sheaths and in leaf blades, high DP fructans were predominant. During drought, the proportion of low DP fructans decreased strongly in elongating leaf bases and only weakly in leaf sheaths, leading to a greater proportion of high DP fructans after drought stress (d 14) in those tissues. By contrast, the proportion of low DP fructans increased slightly in leaf blades. After rewatering (d 28), the proportion of low DP fructans increased again in elongating leaf bases, whereas it remained unchanged in leaf sheaths and leaf blades.
Contrary to fructans, Suc levels were not significantly affected in leaf tissues, whereas they almost doubled in roots from d 7 to 14 of drought stress and declined again after rewatering (Fig. 4B). Glc concentrations did not change significantly in elongating leaf bases of drought-stressed plants (Fig. 4C). Fru concentrations, however, declined by 50% during drought stress and increased after rewatering (Fig. 4D). In leaf sheaths, both Glc and Fru concentrations remained unchanged throughout the experiment. In leaf blades and in roots, hexose concentrations increased by at least 2-fold during drought and decreased after rewatering.
Loliose and raffinose concentrations were determined at the beginning and the end of drought and rewatering, respectively. In roots, the concentrations were below the detection limit, so only data from leaf tissues are presented. The RafS activities were measured in elongating leaf bases and in leaf sheaths (Table I). Raffinose was barely detectable in elongating leaf bases, representing less than 0.1% of the dry weight. In leaf sheaths and leaf blades, it represented 0.2% and 0.4% of the dry weight, respectively, at the beginning of the experiment. At the end of the drought stress, raffinose concentrations declined more in mature leaf tissues of stressed plants than those of control plants. Concomitantly, RafS activity decreased in leaf sheaths under both conditions. Neither raffinose concentrations nor RafS activities were significantly affected by the rewatering treatment in mature leaf tissues. In elongating leaf bases, however, where raffinose concentrations and RafS activities were the lowest, raffinose concentrations were significantly affected by rewatering because it was higher in drought-stressed plants than in control plants. These higher raffinose concentrations in elongating leaf bases at the end of the rewatering period probably resulted from the higher RafS activities detected in this tissue at the end of the drought period compared with those in control plants. Among mature leaf tissues, loliose was specifically located in the sheaths. Loliose did not accumulate in this tissue during drought stress (Table I). Loliose synthase activity was detected in leaf sheaths but at an extremely low level (<0.1 nkat mg-1 protein) and did not show any significant change during drought stress (data not shown).
On the basis of known INPS and GolS sequence data, specific DNA primers
were designed and used for reverse transcription-PCR amplification of
homologous sequences from perennial ryegrass leaf sheaths. The deduced amino
acid sequence of INPS (EMBL accession no. AY154382) is highly homologous to
known INPS sequences from monocotyledonous species
(Yoshida et al., 1999 INPS and GolS expression as well as myoinositol and galactinol concentrations were determined in leaf tissues during drought stress and rewatering (Fig. 6). INPS expression was not affected by drought and rewatering in elongating leaf bases, whereas it decreased in leaf sheaths and in leaf blades, compared with that in control plants where it was rather stable. At the end of the rewatering period, INPS expression in leaf blades and leaf sheaths was lower than in plants grown under normal conditions. The concentration of myoinositol did not change significantly in these two leaf tissues throughout the experiment. It increased in elongating leaf bases during the first 7 d of drought stress and declined thereafter.
GolS gene expression was much less affected by drought stress in elongating leaf bases than in leaf sheaths and leaf blades where it was strongly down-regulated. In all tissues, rewatering caused an increase in GolS expression. The galactinol concentrations correlated positively with the changes in GolS expression; no significant change in elongating leaf bases and a decrease in leaf sheaths and leaf blades were observed.
Loliose Biosynthetic Pathway and Its Role in Drought Tolerance of Perennial Ryegrass
The in vitro synthesis of loliose was obtained by incubation of desalted
enzyme extracts from perennial ryegrass leaf sheaths with UDP-Gal and Suc
proceeding according to the reaction: UDP-Gal + Suc
In perennial ryegrass, loliose does not act as a transport carbohydrate
because it was not detected in the phloem sap collected by the aphid
stylectomy technique (unpublished data). It does not seem to represent a
carbon storage compound either, which could be mobilized after defoliation to
sustain regrowth (Pavis et al.,
2001
The fact that transgenic plants, which overexpressed AtGolS cDNAs
and accumulated galactinol and raffinose, showed improved drought tolerance
provides direct evidence that the stress-inducible GolS gene controls the
level of RFOs and that galactinol and raffinose play important roles in
drought stress tolerance (Taji et al.,
2002
The increased carbohydrate concentrations in shoots and roots of perennial
ryegrass subjected to water deficit can easily be explained by the fact that
growth is limited to a much higher extent than photosynthesis
(Arcioni et al., 1985
It is well known that drought stress induces a shift in the partitioning of
photosynthetic products in favor of Suc
(Hare et al., 1998
A recent study showing homologous expression patterns for 6-SFT and INPS
genes in barley leaves led to the proposition that the Glc produced from
fructan synthesis may stimulate INPS gene activity
(Wei et al., 2001
On the basis of current knowledge, RFO metabolism operates in families
(Cucurbitaceae, Lamiaceae, and Scrophulariacea) where fructans do not
accumulate (Keller and Pharr,
1996
Plant Material and Drought Stress Conditions
Perennial ryegrass (Lolium perenne L. cv Bravo) plants were grown
in a greenhouse with a photoperiod of 16 h of natural light supplemented by a
photosynthetic photon flux density of 110 µmol m-2
s-1 (Phyto tubes, Claude, GTE, Puteaux, France). The thermoperiod
was 24°C (day) and 18°C (night). Seeds were germinated on water and
transferred to plastic pots filled with perlite (three plants per pots) after
2 weeks. Nutrient solution, previously described by Gonzalez et al.
(1989
Measurements were made just before the light period on one excised laminae
(the youngest mature leaf) per plant (three measurements for each triplicate),
using a Scholander-type pressure chamber following the procedure described by
Turner (1981
For each time point, triplicate pots containing three plants each were harvested. Plants were divided into four parts: roots, sheaths of mature leaves, blades of mature leaves together with the emerged part of the elongating leaf, and elongating leaf bases. One part of the harvested tissues was used immediately for enzyme extraction, whereas the remainder was frozen, stored at -80°C for RNA extraction, or freeze-dried for soluble carbohydrate extraction.
Soluble carbohydrates were extracted from 100 mg of freeze-dried tissues as
described previously by Morvan-Bertrand et al.
(2001
Freshly harvested tissues (300 mg) were ground in 840 µL of extraction buffer (50 mM MES, pH 6.3, 1 mM EDTA, 0.01% [v/v] Triton X-100, and 1 mM phenylmethylsulfonyl fluoride) at 4°C. After centrifugation (12,000g, 5 min), samples were desalted by gel filtration on Sephadex G-50 equilibrated with incubation buffer (75 mM HEPES, pH 8.5, and 5 mM dithiothreitol).
The loliose synthetic pathway was determined by testing different
galactosyl donors, galactinol (purified from cucumber [Cucumis
sativus] according to Pharr et al.
[1987
Enzyme activities were determined at 30°C and pH 8.5 with 50 mM Suc and 5 mM UDP-Gal or 5 mM galactinol for loliose synthase and RafS, respectively. Assays were stopped after 24 h by boiling. For control reactions, UDP-Gal or galactinol was omitted. Products of the reactions were quantified by HPAEC-PAD as described above.
Plant tissues were ground in liquid nitrogen and suspended in warm (80°C) solution consisting of 750 µL of phenol and 750 µL of extraction buffer (0.1 M LiCl, 100 mM Tris-HCl, 10 mM EDTA, and 1% [w/v] SDS, pH 8.0). After shaking, 750 µL of chloroform:isoamylalcohol (24:1, v/v) was added, and the solution was centrifuged for 5 min (4°C) at 20,000g. Total RNA was precipitated with LiCl (final concentration 2 M) overnight at 4°C. After centrifugation for 30 min (4°C) at 20,000g, the pellet was suspended in 250 µL of DEPC-water and 250 µL of phenol:chloroform:isoamylalcohol (25:24:1, v/v), mixed, and centrifuged for 5 min. RNA in the supernatant was precipitated again with 1 mL of absolute ethanol and 50 µL of sodiumacetate buffer (3 M; pH 5.6) overnight at -20°C. After centrifugation for 20 min (4°C) at 20,000g, the pellet was washed with 75% (v/v) ethanol, and total RNA was suspended in 50 µL final buffer (25 mM EDTA and 0.1% [w/v] SDS).
Poly(A+) RNA was purified from total RNA isolated from leaf
sheaths and reverse transcripted with oligo(dT) using reverse transcriptase
(Invitrogen, Carlsbad, CA). cDNA was then amplified by PCR. Specific primers
for GolS sequence amplification were designed according to conserved amino
acid regions of known GolS sequences
(Sprenger and Keller, 2000
Total RNA, isolated as described above, was quantified according to A260 and loaded (20 µg lane-1) onto a 1% (w/v) agarose gel containing 2.2 M formaldehyde subjected to electrophoresis (80 V for 3 h). RNA was then transferred to a nylon transfer membrane (gene screen, PerkinElmer Life Sciences, Boston) by capillary blotting with 10x SSC buffer. Membranes were prehybridized for 3 h at 60°C in a Church buffer (0.25 M Na2HPO4, 7% [w/v] SDS, 2 mM EDTA, 20 mg mL-1 heparin, and 10 µg mL-1 salmon sperm denatured DNA). Membranes were hybridized with the INPS probe overnight at 60°C, and the INPS probe was removed from the blot. Finally, the blot was hybridized with the GolS probe.
The significance of the results was evaluated by Student's t test, where P < 0.05 was considered significant.
We thank the harvesting team for help and Dr. Jean-Louis Durand for the loan of the pressure chamber. Received February 19, 2003; returned for revision March 17, 2003; accepted April 22, 2003. * Corresponding author; e-mail prudhomme{at}ibba.unicaen.fr; fax 33–2–31–56–53–60.
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TOP
ABSTRACT
RESULTS
loliose + UDP. The
enzyme, tentatively termed loliose synthase, can therefore be classified as a
UDP-Gal:Suc 3-galactosyltransferase (EC 2.4.1.?). It exhibits a broad pH
optimum between 7.5 and 8.5, suggesting a cytosolic location. The biosynthesis
of the two other galactosyl-Suc, umbelliferose
(Hopf and Kandler, 1974
