Sucrose (JrSUT1) and hexose (JrHT1 and JrHT2 ... - Tree Physiology

Tree Physiology 28, 215–224 

© 2008 Heron Publishing—Victoria, Canada 

Sucrose (JrSUT1) and hexose (JrHT1 and JrHT2) transporters in 

walnut xylem parenchyma cells: their potential role in early events of 

growth resumption 

MÉLANIE DECOURTEIX, 1 GEORGES ALVES, 1 MARC BONHOMME, 2 MEDERIC PEUCH, 2 

KHAOULA BEN BAAZIZ, 1 NICOLE BRUNEL, 1 AGNÈS GUILLIOT, 1 RÉMY RAGEAU, 2 

THIERRY AMÉGLIO, 2 GILLES PÉTEL 1 and SOULAÏMAN SAKR 1,3 

1 

UMR 547-PIAF, site des Cézeaux, Université Blaise Pascal, 24 avenue des Landais, 63170 Aubière, France 

2 

UMR 547-PIAF, site INRA de Crouelle, 234 avenue du Brézet, 63100 Clermont-Ferrand, France 

3 Corresponding author (soulaiman.sakr@univ-bpclermont.fr) 

Received July 12, 2006; accepted April 23, 2007; published online December 3, 2007 

Summary In temperate woody species, the vegetative 

growth period is characterized by active physiological events 

(e.g., bud break), which require an adequate supply of soluble 

sugars imported in the xylem sap stream. One-year-old shoots 

of walnut (Juglans regia L. cv. ‘Franquette’) trees, which have 

an acrotonic branching pattern (only apical and distal vegetative 

buds burst), were used to study the regulation of xylem 

sugar transporters in relation to bud break. At the end of April 

(beginning of bud break), a higher xylem sap sucrose concentration 

and a higher active sucrose uptake by xylem parenchyma 

cells were found in the apical portion (bearing buds able 

to burst) than in the basal portion (bearing buds unable to burst) 

of the sample shoots. At the same time, xylem parenchyma 

cells of the apical portion of the shoots exhibited greater 

amounts of both transcripts and proteins of JrSUT1 (Juglans 

regia putative sucrose transporter 1) than those of the basal 

stem segment. Conversely, no pronounced difference was 

found for putative hexose transporters JrHT1 and JrHT2 (Juglans 

regia hexose transporters 1 and 2). These findings demonstrate 

the high capacity of bursting vegetative buds to import 

sucrose. Immunological analysis revealed that sucrose transporters 

were localized in all parenchyma cells of the xylem, including 

vessel-associated cells, which are highly specialized in 

nutrient exchange. Taken together, our results indicate that xylem 

parenchyma sucrose transporters make a greater contribution 

than hexose transporters to the imported carbon supply of 

bursting vegetative buds. 

Keywords: branching, bud break, cambium, influx, Juglans 

regia, vessel-associated cells, walnut tree. 

Introduction 

The bursting vegetative bud is a photosynthetically inactive 

sink, so it must import soluble sugars to meet its carbon and 

energy demands (Quinlan 1969, Kelner et al. 1993, Maurel et 

al. 2004). Before the formation of an efficient photosynthetic 

apparatus in spring, the vegetative bud grows mainly at the expense 

of carbohydrate reserves. Loescher et al. (1990) proposed 

that xylem sap is the main route by which reserve-derived 

soluble sugars are transported to different sink organs 

during the leafless period. This implies: (1) mobilization of 

carbohydrate reserves in different storage compartments of the 

tree (Loescher et al. 1990, Witt and Sauter 1994, Lacointe et 

al. 2004); (2) loading and long-distance transport of soluble 

sugars into xylem vessels (Bollard 1960, Sauter 1980, Lacointe 

et al. 2001); and (3) unloading into the parenchyma 

cells near the recipient sink. Hence, soluble sugars must be actively 

absorbed from xylem sap by vessel-associated cells 

(VACs) before delivery to recipient organs. The presence of 

VACs with sugar transporters can, thus, determine the intensity 

of carbon supply to sink organs. 

Despite the need for soluble sugars imported from the xylem 

sap stream for early events of bud break (Sauter 1980, 

1981, Sauter and Ambrosius 1986, Lacointe et al. 2001, 

Maurel et al. 2004), direct information about soluble sugar 

transporters in xylem tissue is lacking. In Robinia pseudoacacia 

L., study of the physiological characteristics of sugar 

influx in xylem parenchyma cells indicated the involvement of 

an H + /sucrose co-transporter during the resumption of vegetative 

growth (Fromard 1990). In contrast, in the xylem parenchyma 

cells of Populus, the operation of an H + /hexose cotransporter 

has been proposed (Himpkamp 1988). Few sugar 

transporters have been cloned from woody species to date. 

Some, such as BpSUC1 from birch root (Betula pendula Roth; 

Wright et al. 2000), SUT1 and 2 from citrus root (Citrus sp.; Li 

et al. 2003) and VvSUTs from berry grape (Vitis vinifera L.; 

Davies et al. 1999, Ageorges et al. 2000), share characteristics 

with those identified in herbaceous species. Others, such as 

VvHT1 from berry grape (Fillion et al. 1999, Vignaut et al. 

2005) and BpHEX1 and BpHEX2 from birch root (Wright et 

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216 DECOURTEIX ET AL. 

al. 2000), are highly homologous with the already isolated 

hexose transporters. 

To date, the only sugar co-transporter gene identified from 

xylem tissue of a woody species is the Juglans regia L. putative 

sucrose transporter (JrSUT1), which encodes a putative 

stem-specific sucrose transporter (Decourteix et al. 2006). Its 

role has been investigated only in the autumn–winter period, 

when it appears to mediate the influx of sucrose released into 

the xylem sap after freeze/thaw events (Decourteix et al. 

2006). Although the physiological significance of some sugar 

transporters has been investigated, their involvement in vegetative 

bud burst has not been studied. However, because the 

plasma membrane H + -ATPase (PM-H + -ATPase) energizes a 

large set of secondary transporters, such as sugar transporters, 

studies have focused mainly on this protein (Fromard et al. 

1995, Arend et al. 2002, 2004, Alves et al. 2004). Plasma 

membrane H + -ATPase is reported to be seasonally regulated in 

walnut xylem tissue, because its amount and activity are 

higher when bud break occurs at the end of April, than in February 

(Alves et al. 2004, 2007). These findings support the 

idea that PM-H + -ATPase contributes to the early events of bud 

break by permitting sugar uptake from xylem sap, presumably 

via H + /sugar co-transporters. 

Our study focused on the characterization of putative sugar 

transporters in xylem tissues during the first stages of the 

growing season, with particular attention to the early events of 

bud break. Walnut (J. regia) cv. ‘Franquette’ was chosen as the 

study species because it exhibits an acrotonic branching pattern 

(the apical part of the shoot bears buds that are able to 

grow, whereas the basal part of the shoot bears buds that do not 

normally grow). Because sucrose and hexoses (glucose and 

fructose) comprise 95% of the total soluble sugars in walnut 

xylem sap during bud break (Alves 2003), the possible involvement 

of their respective transporters was investigated 

based on their patterns of activity and accumulation during the 

study period. 

Materials and methods 

Plant material 

Thirteen-year-old walnut trees (J. regia) cv. ‘Franquette’ 

grown in an INRA orchard near Clermont-Ferrand (south-central 

France, 45° N, 3° E) were selected for study. One-year-old 

shoots were collected at the end of each month, from March 

(early spring) to June (acquisition of autotrophy for carbon by 

new shoots). Segments were sampled 10 cm below the apical 

vegetative bud (apical stem segment) and 10 cm above the 

lowermost portion of the shoot (basal stem segment), and the 

xylem tissue collected as described by Alves et al. (2007). 

Starch and soluble sugar in xylem parenchyma cells 

Soluble sugars were extracted from the xylem tissue with 

80:20 (v/v) hot (80 °C) ethanol:water and purified as described 

by Moing and Gaudillière (1992). Glucose, fructose 

and sucrose concentrations were determined spectrophotometrically 

at 340 nm after enzymatic assays (Boehringer 

TREE PHYSIOLOGY VOLUME 28, 2008 

1984). Starch concentration was determined by a hexokinasecatalyzed 

glucose-6-phosphate linked assay (Kunst et al. 

1984) after hydrolysis of the sample with amyloglucosidase 

(Boehringer 1984). 

Xylem sap sugar concentration 

Immediately after stem excision, xylem sap was collected separately 

from the apical and basal portions of the excised shoots 

by vacuum extraction, according to the method of Bollard 

(1953). To avoid contamination of extracted xylem sap by 

phloem sap, the bark was scraped to a distance of about 3 cm 

from each end of the shoots. Following extraction, the xylem 

sap was heated to 80 °C for 20 min, and its sugar content determined 

as described by Maurel et al. (2004). 

Uptake of sucrose and glucose by xylem parenchyma cells 

Twenty-cm-long segments were cut from the apical and basal 

ends of 1-year-old stems preconditioned at 15 °C for 48 h in a 

temperature-controlled chamber (Liebherr 650l). Tissues outside 

the cambium were scraped from the ends of the segments 

to prevent phloem constituents entering the xylem at the ends 

of the stem segments. Each segment was perfused with 3 ml of 

the control solution (0.1 mM MgCl2, 0.1 mM KCl, 0.1 mM 

CaCl2 and 10 mM MES adjusted to pH 5.5 with HCl) under 

moderate pressure (0.1 MPa), and then perfused with 2 ml of a 

radioactive solution (control solution supplemented with 

1mM 14 C-labeled sucrose (70 kBeq ml –1 ) or with 1 mM 

14 –1 

C-labeled glucose (70 kBeq ml ) (both from NEN Life Science) 

in the presence and absence of 1 mM HgCl2 to dissipate 

the electrochemical potential difference. After a 1-h incubation 

at 15 °C, xylem vessels were rinsed with 6 ml of control 

solution and the shoot segments immediately frozen and 

stored at –20 °C until lyophilized, ground and the sugar extracted 

and radioactivity determined. 

Soluble sugar flux from xylem to vegetative buds 

During vegetative bud break (April), total fluxes of soluble 

sugars from xylem vessels to buds were determined by a 

method based on that of Valentin et al. (2001). Five-cm-long 

segments were cut from the apical and basal ends of 1-year-old 

shoots preconditioned at 15 °C for 48 h. Each segment was 

perfused first with 3 ml of control solution (1 mM KCl and 

NaCl and 0.2 mM CaCl2 adjusted to pH 6 with HCl) under 

moderate pressure (0.1 MPa) of nitrogen gas, and then with 

0.5 ml of a radioactive-sugar solution (control solution supplemented 

with 10 mM 14 C-labeled sucrose (70 kBeq ml –1 ), or 

10 mM 14 C-labeled glucose (70 kBeq ml –1 ), or 200 mM 3 H-labeled 

mannitol (400 kBeq ml –1 ) (Sigma). Because a mannitol 

transporter has not been described in walnut, and mannitol has 

never been found in the xylem sap of this species, mannitol 

was assumed to be a non-permeating osmoticum. 

A mannitol concentration of 200 mM was chosen to match 

the osmolarity of walnut xylem sap. After a 30-min incubation 

at 15 °C, xylem vessels were perfused (0.1 MPa) with 3 ml of 

unlabeled-sugar solution (10 mM sucrose or 10 mM glucose, 

200 mM mannitol). After 8 h, the solution was expelled from 



SUCROSE AND HEXOSE TRANSPORTERS IN WALNUT XYLEM PARENCHYMA 217 

the perfused vessels with nitrogen gas. The solution was collected 

for measurement of 14 C/ 3 H ratio at equilibrium and the 

bud immediately frozen in liquid nitrogen and stored at –20 °C 

until lyophilized, ground and the sugar extracted and its radioactivity 

determined. 

The sugar content of cells of vegetative buds was obtained 

by correcting the total 14 C radioactivity in the bud by the 

apoplasmic 14 C radioactivity ( 14 C cells = total 14 C– 14 C apoplasm, 

where 14 C apoplasm = ( 14 C/ 3 H)( 3 H in vegetative bud)). 

Total RNA extraction, and construction and screening of a 

xylem-derived cDNA library 

Total RNA was extracted from xylem, bark, source leaf, fine 

root and flowers (male and female) as described by Gévaudant 

et al. (1999). The RNA was quantified spectrophotometrically 

and its quality assessed by gel electrophoresis. 

A xylem hexose transporter probe was obtained by reverse 

transcription polymerase chain reaction (RT-PCR). Reverse 

transcription was carried out with 1 µg of total RNA extracted 

from xylem tissue in May and the Ready To Go T-primed 

First-Strand kit (Amersham). For the PCR, the following degenerate 

primers were used: Hex1, 5′-G(C/T)(T/G/C)AT- 

(T/C)ATGTT(C/T)TA(C/T)GC(A/C/G)CCTGT-3′; and 

Hex2, 5′-CCA(T/A)ACTT(C/G)A(T/A)(A/C/G)CT(G/C)- 

(A/C)CA(C/A)(C/A)AGCAT-3′; which were deduced from 

conserved regions of plant hexose transporter cDNAs (EMBL 

data library). 

Amplification was carried out in a thermal cycler (Gene 

Amp PCR system, Perkin Elmer) according to standard protocols. 

The amplified fragment (460 bp) was sequenced and 

used as a hexose transporter homologous probe to screen a xylem 

cDNA library (Sakr et al. 2003) under low stringency conditions. 

Two clones were obtained, completely sequenced and 

named JrHT1 and JrHT2 for Juglans regia hexose transporter 

1 and 2, respectively. The sequences of JrHT1 and JrHT2 have 

EMBL/Genbank/DDBJ Accession nos. DQ026508 and 

DQ026509, respectively. 

Semi-quantitative RT-PCR 

One µg of total RNA, extracted from xylem tissues as described 

above, was reverse transcribed. Three µl of the synthesized 

first-strand cDNA was amplified by PCR. Amplification 

of JrHT1 and JrHT2, JrSUT1 and JrAct (J. regia actin) was 

performed with the following specific primers: Hex11 (sense), 

5′-AGGAGATGAACAGAGTATGGAAGACC-3′ and Hex12 

(antisense), 5′-AGGHAAAACTAAAGAGCAAGGTCCC-3′ 

for the amplification of JrHT1 and JrHT2; Sut11 (sense), 

5′-AGATGCAATATCCGCAGTTCCC-3′ and Sut12 (antisense), 

5′-GCATGGHCTTTTGTAGCATTGGG-3′, for the 

amplification of JrSUT1; Act11 (sense), 5′-GATGAAGCCC- 

AATCAAAGAGGGGT-3′ and Act12 (antisense) and 5′-TGT- 

CCATCACCAGAAATCCAGCAC-3′ for the amplification of 

JrAct; JrEF1A (sense), 5′-TGG(A/T/C)GG(A/T)ATTGA- 

(T/C)AAGCGTG-3′ and JrEF1B (antisense), 5′-CAAT- 

(T/C)TTGTA(A/G)ACATCCTGAAG-3′ for the amplification 

of JrEF1 (J. regia Elongation Factor 1 alpha). Each PCR 

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was carried out as follows: 2 min at 94 °C for denaturation, 

20 s at 94 °C, 20 s at 59 °C and 45 s at 72 °C for 35 (JrHT1, 

JrHT2 and JrSUT1), and 25 cycles (JrAct) followed by 10 min 

at 72 °C for the final extension. The amplification of JrEF1 

was carried out as follows: 2 min at 94 °C for denaturation, 

20 s at 94 °C, 30 s at 57 °C and 45 s at 72 °C, for 35 cycles. The 

optimal numbers of PCR cycles were established to generate 

unsaturated (linear phase) but detectable signals. All PCRs 

were performed in parallel on the same cDNA under the same 

conditions. 

Preparation of the affinity-purified anti-JrHTs antibody 

Anti-JrHT1 and anti-JrHT2 antiserum was raised in rabbits 

(Eurogentec, Herstal, Belgium) against a synthetic peptide 

(PKVEMGKGGRAIKNV) coupled to a carrier protein 

(KLH). This sequence was derived from the C-terminal region 

of JrHT1 and JrHT2, but is not conserved in all hexose transporters 

from other species. Antibodies were affinity-purified 

against the synthetic peptide and checked for cross-reaction 

against the C-terminal region of JrHT1. The proteins cross-reacting 

with anti-JrHT1 and anti-JrHT2 antibodies are called 

JrHT1 and JrHT2. 

The affinity-purified anti-JrSUT1 antibody was raised 

against a synthetic peptide (MEVESANKDMRAAQR) chosen 

from the N-terminal region of JrSUT1 (Decourteix et al. 

2006). As in Decourteix et al. (2006), the proteins cross-reacting 

with anti-JrSUT1 antibody are called JrSUT1. 

Microsomal fraction and analysis by SDS-PAGE and 

Western blot 

Xylem microsomal fractions from the apical and basal segments 

of the sample shoots were isolated as described by 

Alves et al. (2004). Protein samples (30 µg) were subjected to 

sodium dodecyl sulfate polyacrylamide gel electrophoresis 

(SDS-PAGE) according to Laemmli (1970). The gel system 

consisted of a 5% stacking gel and a 10% resolving gel. After 

electrophoresis, polypeptides were transferred to a nitrocellulose 

membrane (Transfer Membrane, BioTrace NT) by 

electroblotting. Membranes were probed with either anti- 

JrHT1 and anti-JrHT2 (1/500 dilution) or anti-JrSUT1 

(1/3000 dilution) primary antibodies and anti-rabbit IgG 

(H + L) (P.A.R.I.S., Compiègne, France) peroxidase-labeled 

secondary antibody (1/10,000 dilution). The protein–antibody 

complex was detected with the ECL Western blotting 

analysis system (Amersham Pharmacia Biotech). 

JrSUT1, JrHT1 and JrHT2 immunolocalization in xylem 

parenchyma cells 

Immunolocalization of JrSUT1 and JrHT1 and JrHT2 was 

performed on apical and basal segments of 1-year old stems as 

described by Decourteix et al. (2006). Briefly, each stem segment 

of about 4 mm in length was fixed for 45 min at 4 °C in 

1.5% (v/v) formaldehyde and 0.5% (v/v) glutaraldehyde in 

0.1 M phosphate buffer (pH 7.4) containing 0.5 % (v/v) dimethylsulfoxide 

and then washed in 0.1 M phosphate buffer 

(pH 7.4) followed by phosphate buffered saline (PBS, pH 7.2). 




Fifteen-µm sections were rinsed in PBS (pH 7.2) and bathed 

for 15 min in PBS containing 0.1% (v/v) Triton X-100 and 

0.2% (w/v) glycine (pH 7.2). After saturation of nonspecific 

sites, sections were incubated overnight with either 1/100 diluted 

antibody against JrSUT1, 1/5 diluted antibody against 

JrHT1 and JrHT2 or the same antibodies saturated with the 

KLH-coupled synthetic peptide. After washing, sections were 

incubated for 3 h with goat anti-rabbit antibodies conjugated 

to alkaline phosphatase (Sigma) diluted in blocking solution. 

Tissue sections were washed with Tris buffered saline and incubated 

with the chromogenic substrates nitro-blue tetrazolium 

chloride and 5-bromo-4-chloro-3′-indolyphosphate p-toluidine 

salt (BioRad). Color development was carried out at 

room temperature and was stopped by washing in H2O. 

Statistical analysis 

Means and standard errors were calculated from replicates. 

Date and sugar effects were evaluated by analysis of variance 

(ANOVA) and by rank and Duncan tests (at 5%). 

Results 

Starch and sugar in xylem parenchyma cells 

From March to May, mean starch concentration was 1.8- to 

2.5-fold higher in apical stem segments than in basal stem segments 

of 1-year-old shoots, but there was no difference in June 

(Figure 1). The seasonal pattern in starch concentration was 

similar in the apical and basal stem segments. Starch concentration 

increased by a factor of two in early spring (March– 

April), reached a maximum in April and decreased to a minimum 

in June. Starch concentration was around ten- and fourfold 

higher in April than in June, in the apical and basal stem 

segments, respectively. Except in June, starch concentrations 

were higher than soluble sugar concentrations. In March and 

April, mean soluble sugar concentration in xylem parenchyma 

cells was at a maximum, and was 1.7-fold higher in apical stem 

segments than in basal stem segments (Figure 1). 

Xylem sap sugar concentrations and uptake at bud break 

Mean total concentrations of sucrose and hexose in the xylem 

sap were 2.5-fold higher in apical stem segments than in basal 

stem segments of the 1-year-old shoots (2.3 versus 0.9 mg 

ml –1 , respectively; P < 0.05) (Figure 2A). Mean sucrose concentration 

was about 4-fold higher in apical stem segments 

than in basal stem segments, whereas hexose concentrations 

were similar in both (Figure 2A). 

Active sucrose uptake was estimated at +15 °C by subtracting 

passive sugar uptake (in the presence of HgCl2 ) from total 

sugar uptake (in the absence of HgCl2 ). At the start of bud 

break, mean active sucrose uptake in apical stem segments was 

4.3-fold higher than in basal stem segments (9.5 versus 

2.2 nmol g DM –1 h –1 ; P < 0.001) (Figure 2B). In contrast to sucrose, 

there was little active glucose uptake under the same experimental 

conditions. 


Figure 1. Changes in starch and soluble sugar (GFS = glucose + fructose 

+ sucrose) concentrations in xylem parenchyma cells of the apical 

and basal segments of 1-year-old walnut shoots. Values are means 

± SE of at least three replicates. 

JrHT1 and JrHT2: putative hexose transporters 

To obtain putative hexose transporter cDNA from xylem tissue, 

conserved domains of known hexose transporter sequences 

from different species were used to design degenerate 

primers for RT-PCR. An amplified cDNA fragment of about 

460 bp was sequenced and found to be homologous to hexose 

Figure 2. (A) Xylem sap sucrose (filled bars) and hexose (glucose + 

fructose; open bars) concentrations in apical and basal segments of 

1-year-old walnut shoots at the end of April (onset of bud break). Values 

are means ± SE of five replicates. (B) Active sucrose uptake by 

parenchyma cells in the apical and basal segments of 1-year-old walnut 

shoots estimated by subtracting passive uptake (in the presence of 

HgCl2 ) from total uptake (in the absence of HgCl2 ) of sucrose. Values 

are means + SE of at least three replicates. 




transporters from other species. Thus, it has been used as a homologous 

probe to screen a xylem-tissue-derived cDNA library 

(Sakr et al. 2003). Two full-length cDNA clones encoding 

putative hexose transporters, JrHT1 and JrHT2, were isolated. 

The complete nucleotide sequences of the clones JrHT1 

and JrHT2 contained an open reading frame of 1563 and 1524 

bp, respectively, and had 98% sequence similarity. JrHT1 and 

JrHT2 encode 521 and 508 amino acid polypeptides, respectively. 

The putative amino acid sequence of JrHT1 was aligned 

with the deduced protein sequences of known hexose transporters 

(Figure 3A). The identity between JrHT1 and other 

hexose transporters ranges from 51 to 85%, and the closest 

identity was found with the RcSCP from Ricinus communis L. 

(Weig et al. 1994). 

Expression analysis of these putative hexose transporters in 

different organs was carried out by a semi-quantitative RT- 

PCR approach, with RNAs extracted from leaf, fine root, xylem, 

bark and flowers (male and female). Because the primer 

pair (Hex11/Hex12) is common to JrHT1 and JrHT2, the amplified 

band was named JrHT1 and JrHT2. JrHT1 and JrHT2 

transcripts were detected in all of the tested organs, including 

the xylem tissue (Figure 3B), contrasting with the sink-specific 

expression of a cDNA encoding a putative sucrose transporter 

isolated by Decourteix et al. (2006) from walnut xylem 

tissue (JrSUTs; Figure 3B). No significant difference in transcript 

abundance of JrHT1 and JrHT2 was found between 

source leaf and sink organs (xylem, fine root and bark). The 

lowest abundance of JrHT1 and JrHT2 was in male flowers. 

Transcript patterns of JrSUT1 and JrHT1 and JrHT2 during 

the growing season 

The relative transcript abundance of JrHT1 and JrHT2 and a 

putative sucrose transporter JrSUT1 previously isolated from 

walnut xylem tissue by Decourteix et al. (2006) was examined 

by semi-quantitative RT-PCR as previously applied to walnut 

xylem tissue (Sakr et al. 2003, Decourteix et al. 2006). As 

shown in Figure 4A, the apical and basal stem segments exhibited 

a contrasting pattern of JrSUT1 transcript abundance. In 

the apical segment, JrSUT1 transcripts were abundant in 

March and April, whereas they were undetected in May and 

June. In the basal segment, the transcript level of JrSUT1 was 

high in April and June and low in March and May. 

The pattern of JrHT1 and JrHT2 transcripts differed from 

that of JrSUT1 and between the apical and basal stem segments 

(Figure 4B). In the apical segment, JrHT1 and JrHT2 

transcripts were slightly more abundant in April and May than 

in March and June. In the basal segment, JrHT1 and JrHT2 

transcripts increased from March to May, but decreased in 

June. 

Accumulation and localization of sugar transporters during 

the growing season 

The affinity-purified anti-JrSUT1 antibody labeled a single 

band of 54 kDa on immunoblots, which is consistent with the 

molecular mass of several sucrose transporters (Lemoine 

2000). In the apical segment, band intensity was highest in 


Figure 3. (A) Comparison of the deduced amino acid sequence of 

JrHT1 with those of other hexose transporters from mono- and dicotyledonous 

plants. The dendrogram was generated by comparison 

of the sequences by the CLUSTAL W 1.74 software (Higgins et al. 

1994). VvHT2 (Accession no. AAT77693); AtSTP1 (CAA39037); 

AtSTP4 (BAB01308); VfSTP1 (CAB07812); AtSTP9 (NP175449); 

AtSTP5 (CAC69071); AtSTP6 (CAC69073); AtSTP11 (CAC- 

69075); tMST2.1 (CAG27605); tMST2.2 (CAG27609); tMST3.1 

(CAG27606); ZmMST1 (AAT90503); PaMST1 (CAB06079); PMT1 

(AAC61852); LeHT2 (CAB52689); VvHT1 (CAA04511); RcSTC 

(AAA79761); OsMST3 (BAB19864). Percentage identity is noted on 

the right. (B) Expression patterns of JrHTs and JrSUTs in various organs 

of walnut tree. Semi-quantitative reverse transcriptase polymerase 

chain reactions (RT-PCRs) were performed with either 

Sut1A/Sut1B for JrSUTs, Hex11/Hex12 for JrHTs or Act11/Act12 

for JrAct. At least four RT-PCRs were conducted on each of the two 

biological replicates. All yielded similar results to those shown. 

March (early spring) and April (beginning of bud break), 

whereas no labeled band was found in May and June (Figure 

5A). In the basal segment, the band increased in intensity 

from March to April and disappeared in May and June. In 

March and April, there was more JrSUT1 protein in xylem parenchyma 

cells of the apical than of the basal stem segments 

(Figure 5A). 




Figure 4. Expression patterns of JrSUT1 and JrHT1 and JrHT2 in xylem 

parenchyma cells in apical and basal segments of walnut stems 

harvested from March to June. Semi-quantitative reverse transcriptase 

polymerase chain reactions (RT-PCRs) were performed with either 

(A) Sut11/Sut12 for JrSUT1 or (B) Hex11/Hex12 for JrHT1 and 

JrHT2. (C) JrEF1 was used as control. At least four RT-PCRs were 

conducted on each of two biological replicates, yielding similar results 

to those presented here. 

The affinity-purified anti-JrHT1 and JrHT2 antibody 

yielded only a single band of 52 kDa, which is comparable to 

the molecular mass of other hexose transporters (Williams et 

al. 2000, Vignault et al. 2005). The protein pattern of JrHT1 

and JrHT2 contrasted with that of JrSUT1 (Figure 5B). In the 

apical xylem parenchyma cells, JrHT1 and JrHT2 were barely 

detectable in March, and only a faint signals were observed in 

April and June. The greatest amount of JrHT1 and JrHT2 was 

found in May, coinciding with a period of intense radial 

growth in walnut (Daudet et al. 2005). In the basal xylem parenchyma 

cells, no significant signal was found, except in 

May, when JrHT1 and JrHT2 were abundant. In May, JrHT1 

and JrHT2 were more abundant in the basal than in the apical 

stem segment. 

Immunolocalization analysis of the hexose transporters was 

performed in sections harvested from apical and basal stem 

segments of 1-year-old stems at the end of April (beginning of 

bud break). No signal was detected when the immunolocalization 

was performed either with the saturated primary antibody 

(data not shown) or in the absence of the primary antibody 

(Figures 6B, 6D, 6F and 6H). For JrSUT1, immunolabeling 

was limited to the living cells of the xylem in both apical 

(Figure 6A) and basal (Figure 6C) stem segments. It was 

strongly detected in VACs, which are highly specialized in nutrient 

transports, and in both axial and ray parenchyma cells 

(Figures 6A and 6C). Similar patterns were found for JrHT1 

and JrHT2. The immunolabelling was detected in living cells 

including axial and ray parenchyma cells and VACs (Figures 

6E and 6G). 

Total transport of sucrose and glucose from xylem vessels to 

bud cells 

The sucrose transporter JrSUT1 accumulated preferentially in 

the apical segment of the walnut shoot and was more highly 

expressed than the glucose transporters JrHT1 and JrHT2 

(Figures 4 and 5) at the beginning of bud break in April. 


Figure 5. Immunoblot analyses of microsomal fractions of xylem parenchyma 

cells in the apical and basal segments of walnut stems harvested 

from March to June and incubated with either (A) the 

affinity-purified anti-JrSUT1 antibody or (B) the affinity–purified 

anti-JrHT1 and anti-JrHT2 antibody. Four independent experiments 

yielded similar results to those presented here. 

Therefore, we checked whether the accumulation pattern of 

sugar transporters in xylem tissues and the import of sugar into 

vegetative buds was coordinated. At the beginning of bud 

break, sucrose influx was more than 14-fold higher into buds 

of the apical stem segment than the basal stem segment (1453 

and 104 nmol g DM –1 h –1 , respectively) and was more than 

70-fold higher than glucose influx for both locations (18.7 and 

1.39 in buds of the apical and basal stem segments, respectively; 

Table 1). 

Discussion 

In temperate woody species, bud break marks the beginning of 

vegetative growth, which is characterized by intense physiological 

activity that creates a high demand for soluble carbohydrates 

(Maurel et al. 2004). Based on a double-labeling experiment 

with walnut trees, Lacointe et al. (2004) reported that the 

greatest consumption of labeled reserves occurred in spring 

between the onset of bud break (end of April) and the acquisition 

of autotrophy for carbon by new shoots (mid-June). In 

keeping with these findings, our data show that starch stored in 

stem xylem parenchyma cells was hydrolyzed during the same 

period (Figure 1). In poplar, a strong and rapid mobilization of 

starch reserves has been reported during bud break and has 

been related to activation of amylases (Witt and Sauter 1994). 

In parallel with the breakdown of starch, soluble sugar concentrations 

(sucrose, glucose and fructose) in xylem parenchyma 

cells declined significantly (Figure 1). These findings differ 

from those reported for the rest period (Sauter and Kloth 1987, 

Sauter 1988, Améglio et al. 2000) and are consistent with increased 

consumption of starch-derived carbohydrates during 

early vegetative growth. 

Recently, JrSUT1, a putative stem-specific sucrose transporter, 

has been characterized in walnut xylem parenchyma 

cells, and has been implicated in sucrose retrieval from xylem 

sap during winter (Decourteix et al. 2006). To identify hexose 

transporters expressed in the xylem tissue, we screened a xylem 

cDNA library with a homologous probe and isolated two 

putative hexose transporters designated JrHT1 and JrHT2 

(Juglans regia hexose transporters 1 and 2). These transporters 

cluster only with plant hexose or monosaccharide transporters 




(Figure 3A), and the highest identity (85%) was with RcSCP 

(Weig et al. 1994). JrHT1 and JrHT2 had all the characteristics 

of monosaccharide transporters including 12 transmembrane-spanning 

domains and the conserved V/ LPETK or 

Table 1. Capacities of buds of apical and basal stem segments of 

1-year-old walnut stems to import sucrose and glucose during bud 

break. Values are means ± SE of at least five replicates. 

Stem segment Sucrose import Glucose import 

(nmol g DM –1 h –1 ) (nmol g DM –1 h –1 ) 

Apical 1453.5 ± 217.8 18.7 ± 8.1 

Basal 103.7 ± 23.9 1.4 ± 0.4 


Figure 6. Transverse sections showing the 

general distribution of JrSUT1 and JrHT1 

and JrHT2 in the xylem parenchyma cells 

of walnut stem. Immunolabeling of 

JrSUT1 in living cells of the (A) apical 

and (C) basal stem segments and 

immunolabeling of JrHT1 and JrHT2 in 

living cells of the (E) apical and (G) basal 

stem segments. No labeling was detected 

in the controls (B, D, F, H). Abbreviations: 

A, axial parenchyma cell; F, fiber; R, ray 

parenchyma cell; V, vessel; and VAC, vessel 

associated cell. Scale bars equal 

25 µm. 

(R/K)XGR(R/K) motifs, and JrHT1 and JrHT2 transcripts 

were found in both source and sink organs, as is the case for 

other hexose or monosaccharide transporters (e.g., LeHT2, 

Gear et al. 2000; AtSTP4, Trüernit et al. 1996; or PaMST1, 

Nehls et al. 2000). 

During early spring, walnut xylem sap is considered the primary 

route by which soluble sugars are transported from exporting 

organs to recipient sinks, mainly the buds and possibly 

the cambium (Lacointe et al. 2001, 2004). This was verified by 

our experiments, which showed a large amount of radiolabeled 

sugar, perfused into xylem vessels, moved to vegetative bud 

cells (Table 1). At bud burst, bud vascular tissue includes only 

protoxylem, so that, to reach the meristematic zone, sugars 

must pass by the VACs, which control nutrient exchanges between 

xylem vessels and parenchyma cells (Fromard et al. 




1995, Sakr et al. 2003, Decourteix et al. 2006). Sucrose and 

hexose co-transporters were immunolocalized in VACs at the 

onset of bud break, indicating that active sugar absorption 

from xylem vessels can be mediated by VAC-localized transporters. 

Assays of respiratory and phosphatase enzymes have shown 

that VACs are metabolically highly active during the growth 

period (Alves et al. 2001). However, JrSUT1 and JrHT1 and 

JrHT2 are not confined to VACs, but are located in axial and 

ray xylem parenchyma cells (Figure 6). This differs from the 

distribution observed in winter, when JrSUT1 is located 

mainly in VACs (Decourteix et al. 2006). It is possible that parenchyma-localized 

transporters participate in the transport of 

soluble sugars after xylem uptake, either by accelerating the 

transfer of soluble sugars from VACs to vegetative buds or by 

retrieving sugars leaked to the apoplasm during their symplasmic 

passage from VACs to bud. 

In herbaceous species, many studies have shown that the expression 

of sucrose and hexose transporters in sink organs is 

developmentally regulated in a way that is often related to sink 

carbon demand (Weber et al. 1997, Ylstra et al. 1998, Trüernit 

et al. 1999, Weschke et al. 2000, Scholz-Starke et al. 2003, 

Schneidereit et al. 2003). For instance, the accumulation of 

VfSUT1 (Vicia faba L. sucrose transporter), which is limited 

to the sites of sugar exchange between maternal and filial tissues, 

coincides with storage activity of the endosperm parenchyma 

in developing cotyledons (Weber et al. 1997). We 

found that the contribution of JrSUT1 to the supply of soluble 

sugars to bursting vegetative buds can be deduced from comparisons 

of both activity and accumulation of sugar transporters 

between apical and basal stem segments of 1-year-old walnut 

shoots. At the end of April (bud break), parenchyma cells 

in apical segments exhibited high sucrose concentrations (Figure 

2A), rapid sucrose absorption (Figure 2B) and elevated 

quantities of JrSUT1 transcripts (Figure 4A) and proteins 

(Figure 5A) compared with basal segments. This spatial upregulation 

of JrSUT1, together with its localization in xylem 

parenchyma cells (Figure 6) before and at the time of bud 

break, indicate that JrSUT1 can mediate active absorption and 

radial transport of xylem-imported sucrose from xylem vessels 

to vegetative bud cells when cambial growth is low 

(Améglio et al. 2002). In summary, JrSUT1 participates in the 

supply of sucrose to bursting vegetative apical buds, which exhibit 

a high capacity for sucrose import (Table 1). 

Up-regulation of JrSUT1 in the apical xylem parenchyma 

cells started before bud break (in March). Because the bursting 

bud is a net importer of sugar and acts as a strong sink by competing 

for nutrients with other sink organs (Maurel et al. 

2004), carbon supply to the breaking bud can be governed by 

the relative ability of xylem parenchyma cells to transport xylem-imported 

sugars. In this context, enrichment of xylem parenchyma 

cells of upper stem segments with JrSUT1 in early 

spring indicates the importance of sucrose to support of physiological 

activities preceding bud break in walnut trees. 

Compared with JrSUT1, JrHT1 and JrHT2 may make a limited 

contribution to bud carbon supply at the time of bud break. 

Xylem parenchyma cells were poorly enriched in both tran- 

scripts and proteins of JrHT1 and JrHT2 at bud break. Even if 

JrHT1 and JrHT2 were localized in VACs (Figure 6), the 

scarcity of both transcripts (Figure 4B) and proteins (Figure 

5B) of these transporters precluded detectable uptake of 

glucose under our experimental conditions. The limited role of 

hexoses at the start of bud break in walnut accords with the 

limited capacity of buds to import glucose (Table 1). Differential 

regulation of sucrose and hexose transporters suggests that 

the role of sucrose cannot be extended to all xylem sap-imported 

soluble sugars, and that hexoses contribute less to the 

carbon supply at bud break than sucrose. This finding contrasts 

with our earlier observations indicating the possible importance 

of glucose in early bud break in peach tree vegetative 

buds (Maurel et al. 2004). This apparent discrepancy may reflect 

differences in carbon metabolism between peach and 

walnut. For example, peach is a polyol-producing plant, 

whereas walnut is not. 

The greatest quantities of JrHT1 and JrHT2 transcripts and 

proteins were found in May (Figures 4B and 5B), coinciding 

with intense radial growth (Daudet et al. 2005). It is possible 

that these hexose transporters are involved in the carbon demand 

required for radial growth of walnut stems. 

We have demonstrated spatial and temporal regulation of 

putative sugar transporters in xylem parenchyma cells during 

the period of vegetative growth. These findings are comparable 

with those previously obtained for fava bean (Vicia faba 

L.) seeds in showing that sucrose and hexose co-transporters 

have different temporal and spatial patterns (Weber et al. 

1997). Our results suggest that sucrose transporter(s) 

(JrSUT1) contributes to the carbon supply of bursting vegetative 

buds, thereby participating with other physiological factors 

in the acrotonic branching pattern of walnut. 

Acknowledgments 

This work was supported by the Ministère de la Recherche et de 

l’Education Nationale and the INRA (Environment and Agronomy 

department). We thank Brigitte Saint-Joanis, Sylvaine Labernia and 

Marc Vandame for contributions, and Professor Alan Schulman (Institute 

of Biotechnology, Helsinki) for comments on the manuscript. 

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