Journal of Experimental Botany, Vol. 52, No. 361, pp. 1731-1738,
August 1, 2001
© 2001 Oxford University Press
Original Papers |
Boron supply into wheat (Triticum aestivum L. cv. Wilgoyne) ears whilst still enclosed within leaf sheaths
1 School of Environmental Science, Murdoch University, Murdoch, Perth, WA 6150, Australia
2 School of Biological Sciences and Biotechnology, Murdoch University, Murdoch, Perth, WA 6150, Australia
Received 1 February 2001; Accepted 9 April 2001
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Abstract |
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The present study investigates whether there is significant remobilization of 10B previously loaded in the flag and penultimate leaves into the young, actively growing ear enclosed within the sheaths of flag and penultimate leaves. It also explores whether B transport into the enclosed ear declines when air humidity in the shoot canopy increases. After 5 d 10B labelling during the period from early to full emergence of the flag leaf, the plants were transferred into nutrient solutions containing either 10 µM 11B or no added B for 3 d. Regardless of the subsequent B supply levels to the roots, 10B contents in the ear continued to increase by up to 5-fold 3 d after the end of 10B supply in the nutrient solution. During these 3 d, the ear experienced a rapid increase in biomass. However, the majority of B in the ear during the 3 d treatment period was from the newly acquired 11B from root uptake, rather than retranslocation of 10B previously deposited in the leaves. By comparing the relative distribution of 10B, Rb (xylem-to-phloem transfer marker) and Sr (xylem-marker) in the ear and the flag leaf, the distribution of 10B resembled that of Rb more than Sr. Canopy cover treatment greatly suppressed leaf transpiration and decreased the amount of newly acquired 10B in the flag leaf and the ear, but not in the upper stem segments. The results suggest that whilst the young ear was still fully enclosed within the leaf sheaths without any significant transpiration activity, B transport into the ear is predominantly dependent on the long-distance B transport in the xylem driven by leaf transpiration and, therefore, on concurrent B uptake from the roots.
Key words: Wheat, Triticum aestivum cv. Wilgoyne, 10B/11B, Rb, Sr, xylem.
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Introduction |
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Previous studies have demonstrated that deficient B supply during reproductive growth resulted in sterile florets and low grain set in wheat (Huang et al., 1996
, 2000; Rawson, 1996b). These studies have identified critical periods for the whole ear (5–7 d) or a single floret (2–3 d), during which B deficiency caused acute sterility and low grain set. During these short periods, there is a rapid increase in ear biomass and therefore sink expansion for B while the young ear is still fully enclosed within the 1–2 layers of sheaths of the flag/penultimate leaves.
The full enclosure of the ear within the sheath of flag and penultimate leaves implies that transpiration through the young ear is minimal considering the high humidity in the atmosphere surrounding the enclosed ear. It is well known that B transport into shoot parts exposed to the atmosphere is predominantly driven by transpiration flow in the xylem (Brown and Shelp, 1997). However, it is unclear how B is transported into the enclosed, rapidly growing ear during its early growth phase and whether there is a significant remobilization of B previously deposited in the leaves to the young ear, in response to the depletion or interruption of B supply to the roots.
Wheat stem possesses a unique vascular system in which xylem and phloem transfer cells are located in vegetative and spikelet nodes (Zee and O'Brien, 1970; O'Brien and Zee, 1971; Busby and O'Brien, 1979). This vascular structure in the nodes provides the routes for solute exchange between xylem and phloem (Pate, 1975). Apart from the xylem transport mechanism, other mechanisms may also be involved in the transport of B into the enclosed young ear, such as phloem transport after rapid xylem-to-phloem exchange/transfer (Shelp et al., 1998; Marentes et al., 1997). However, if B-remobilization and phloem-B transport are possible in wheat plants, it might be expected that the ear B status would be unaffected by a short-term B withdrawal from the roots and by factors suppressing transpiration, such as high ambient air humidity and temperature.
As a result, it is hypothesized that (1) the B previously deposited in the leaves may be retranslocated into the non-transpiring organ—the young ear enclosed within flag/penultimate leaf sheath, in response to the interruption of B supply in the roots; and (2) B transport into the enclosed ear may not be sensitively depressed by lowered leaf transpiration resulting from increasing temperature and humidity in the canopy air.
It is unclear if B withdrawal for several days could damage the vascular systems within the tissues of the young ear. If so, solute transport efficiency into the ear may be depressed in -B plants. To separate this structural impairment in the transport system from the B supply issue, Rb and Sr which do not have metabolic roles in plants were fed to the plant roots (Feller, 1989; Kuppelwieser and Feller, 1991). In wheat, Sr is carried via the transpiration stream into flag leaves and maturing ears (actively transpiring); in contrast, Rb is rapidly transferred from xylem into the phloem and reaches the ear via phloem transport (Feller, 1989; Kuppelwieser and Feller, 1991). The distribution patterns of Sr and Rb in the ear and leaves are therefore compared with the distribution of pre-loaded B and newly acquired B in the young ear and flag and penultimate leaves, to estimate differences/similarities in transport behaviour.
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Materials and methods |
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Plant culture
General methods for preparing and culturing wheat (cv. Wilgoyne) plants in the present experiments were described earlier (Huang et al., 2000
). Briefly, after germination and acclimatization, plants were grown in a full-strength basal nutrient solution containing (µM): NH4NO3 2000, KNO3 2800, Ca(NO3)2 1600, MgSO4 1000, KH2PO4 100, K2HPO4 100, FeEDTA 100, NaCl 8, ZnSO4 2, MnSO4 2, CuSO4 0.5, and Na2MoO4 0.08. Aliquots of nutrients were added into each pot during the experiments by programmed nutrient addition as described previously (Huang et al., 1996). Solution pH was maintained in the range of 5.5–6.5. Analytical grade chemicals were used to make up stock solutions of these nutrients to which was added acid-cleaned B-specific resin (IRA-743, Sigma Chemical Co.) (5 g moist resin l-1) to adsorb trace amounts of B contamination possibly present in solution. Water used for making up all chemical and nutrient solutions was purified by passing through a column packed with B-specific resin. Boron isotopes were supplied as boric acid enriched with 10B (99.47% wt) or 11B (99.34% wt) (Eagle Picher, USA). The plants were supplied with enriched 11B from the post-germination stage onwards until the start of the 10B treatment periods specified in each experiment described below. Each pot had four plants initially and was successively thinned to two just before applying the B-isotope treatments. Before transfer into the treatments, plant roots were rinsed with double-deionized water and then three changes of triple-deionized water (purified with acid-cleaned B-specific resin) containing 2 mM CaSO4, to remove surface-adsorbed B.
Sample preparation and chemical analyses
At harvest, plants were separated into six parts: ear (including stem segment above the flag leaf node), flag leaf (FL), penultimate leaf (PL), the leaf immediately older than PL (PL+1), stem segment between nodes subtending FL and PL (SS-FP), and stem segment between PL and PL+1 nodes (SS-PP). They were dried at 70 °C to constant weight, finely ground, and dry-ashed at 180 °C for 1 h and then at 500 °C for 12 h as described previously (Brown et al., 1992). Sample ash was taken up in 10 ml 1% nitric acid solution and the mixture was warmed at 60 °C for 30 min. Beryllium (Be) was added as an internal standard to all sample and standard solutions for the analysis of 10B and 11B ratios by inductively coupled plasma-mass spectrometry (ICP-MS, Perkin Elmer, Elan 6000, USA). Total B, Rb and Sr concentrations in the digest solutions were determined by the ICP-atomic emission spectrometry (ICP-AES, Varian).
Data analysis
The distribution of 10B, Sr and Rb in plant parts was calculated as the ratio of the content in a plant part to the total content per plant and expressed as a percentage. The data were analysed by analysis of variance for treatment effects and differences among mean values were determined by the Duncan's multiple range test (P
0.05) with the SPSS statistical package (SPSS, vs 6.0, SPSS Inc., 1993).
Experiment 1: Contribution of previously loaded B to B in the enclosed ear
The objective of this experiment was to investigate whether 10B previously loaded in the plants was a significant source of B supply for ear growth and development before ear emergence (i.e. when the ear was still enclosed by two layers of leaf sheath), in particular, when root B supply was limited. The plants were loaded with Sr and Rb and the distribution patterns of Sr and Rb were compared to that of 10B.
Plants were cultured as described above, under glasshouse conditions with: mean air temperature 23.6 °C (range: 32–18); mean relative humidity 57% (range: 35–71%); mean PAR (photosynthetic active radiation) 694 µmol m-2 s-1 (range: 322–1028) (natural sunlight in the glasshouse from 10.00–16.00 h). The plants were supplied with 10 µM 11B-enriched boric acid from the post-germination stage until 32 d after germination (DAG) when the penultimate leaf reached 90–100% full emergence (the appearance of the ligules) and the flag leaf was at early emergence (5–10% emergence). By this stage, each plant had 6–8 tillers.
On 32 DAG, the 10B loading treatment was applied to the plants by transferring them into fresh, full-strength nutrient solution containing 10 µM 10B, 0.5 mM SrCl2 and 0.5 mM RbCl for 5 d during which flag leaves developed from 5–10% emergence to near full-emergence. At transfer, all tillers except for the main shoot were trimmed off with stainless steel razor blades at their stem base (without removing any roots), to achieve uniformity among plants, to maximize loading of 10B in the flag leaf, to minimize the shading effects of tillers on each other and to simplify the quantification of B contents and distribution in plant parts (in particular: the ear, the flag leaf and the penultimate leaf).
After being loaded with 10B, Rb and Sr for 5 d, the plants with fully emerged flag leaves were subsequently transferred into two levels of B treatments for 3 d: (1) control, fresh nutrient solutions with 10 µM 11B and (2) B withdrawal (-B), fresh nutrient solutions without B supply. About 4 g moist, acid-cleaned B-specific resin (Amberite-743) was placed in the -B nutrient solutions to absorb any B released out of roots. Boron concentrations in the -B nutrient solutions were below the detection limit of the ICP-AES (0.01 µg B l-1). This period coincided with the development of anthers from late premeiotic/early meiosis stage to around mitosis-I in the primary florets of the central spikelets of the ear. At the end of the B treatment period, the ear was still enclosed by the flag leaf sheath.
The plants were harvested just before transfer into the B treatments on 37 DAG, 1 d and then 3 d after transfer, respectively. Three replicates of each treatment were harvested at each harvest. They were dissected into plant parts as described above and oven-dried at 70 °C for their dry weights and analyses of 10B and 11B.
Experiment 2: Effects of transpiration on B status in the ear
The purpose of this experiment was to investigate the long-distance transport of B by manipulating canopy transpiration activity. If B transport into the enclosed ear is dependent on the long-distance transport of B in the transpiration flow in the xylem, B status in the enclosed ear would be decreased by the reduction of canopy transpiration under warm and humid conditions.
Wheat plants were cultured in the same way as Experiment 1 and were thinned to two per pot. Plants were cultured as described above under glasshouse conditions with: mean air temperature 24.1 °C (range: 18–33); mean relative humidity 55% (range: 34–70%); mean PAR 715 (range: 352–1046) µmol m-2 s-1 (natural sunlight in the glasshouse from 10.00 –16.00 h). The maximal air temperature inside the canopy cover at midday was about 5 °C higher than the ambient. On 41 DAG, 12 pots of plants were transferred from nutrient solutions containing 10 µM 11B into those with 10 µM 10B, 0.5 mM SrCl2 and RbCl. At transfer, 6–8 tillers per plant (except for the main shoot) were trimmed off with stainless steel razor blades to maximize the loading of 10B in the remaining main shoot. Transpiration and B treatments started on 41 DAG for 3 d, by the end of which ears were still enclosed by the flag leaf sheath.
Transpiration treatments applied were control (no cover) and cover (entire canopy was covered within a 30 l clear plastic bag over the two plants of each pot). Plant roots were rinsed before transfer as in Experiment 1. Three pots of each treatment were harvested on days 1 and 3 after transfer, for the analyses of 10B, 11B, Sr, and Rb in plant parts as described in Experiment 1.
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Results |
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Contribution of previously loaded 10B to the total B in the ear and flag leaf
By the end of 5 d 10B supply, 10B was present in all plant parts and 80% of the 10B taken up by the plants was present in the shoot (data not shown). The loading intensity of 10B (µg 10B plant part-1) decreased with increasing age of leaves, with the highest in the flag leaf (about 4 µg 10B plant-1) and the lowest in the bulked old leaves (about 2 µg 10B plant-1) (data not shown). At the end of 10B labelling, the 10B content was greater in the FL than the PL (Fig. 1
). This means that more B was transported into the newly fully expanded FL than the PL which was already fully expanded at the start of 10B labelling.
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The results showed that B in the enclosed ear was mainly from the concurrent 11B uptake from the roots (Fig. 1
). By day 3, the amount of 10B in the ear contributed only a small proportion to the total B content, compared to the total amount of B acquired by the rapidly growing young ear. Nevertheless, the amount of 10B in the ear continued to increase during the 3 d after the end of 10B supply in the nutrient solution, regardless of concurrent levels of B supply in the nutrient solutions (Fig. 1).
Distribution of 10B, Rb and Sr
In general, B withdrawal after the 10B loading period did not affect the subsequent distribution of 10B, Rb and Sr in the plant parts sampled.
Over the 3 d after the end of 10B supply in the nutrient solution, the distribution of 10B into the ear increased from about 1–5% of the total 10B previously taken up by the plants (Fig. 2). On day 1, there was a transient increase of 10B distribution in the stem segment between the flag and penultimate leaf nodes (SS-FP), which was actively elongating during the treatment period. In contrast, there was no significant change in 10B distribution in the flag leaf, penultimate leaf and the stem segment SS-PP. There was about 4% reduction in 10B distribution in the roots by day 3, though statistically it was not significant (Fig. 2).
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The distribution of Rb (xylem-to-phloem transfer marker) in the ear, flag leaf and penultimate leaf was similar to that of 10B in these parts (Fig. 3
). Rb distribution in the ear increased from about 0.4% to almost 4% by day 3 after the end of Rb supply. There was a significant continual increase in Rb distributed to the youngest stem segment sampled (SS-FP) (but not the SS-PP), over the 3 d after the end of Rb supply to the roots. The proportion of Rb distributed to the roots declined from about 59% to 49% of the total Rb uptake.
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The distribution of Sr (xylem marker) in the plant parts behaved differently from those of 10B and Rb. The proportion of Sr distributed to the ear had only a small net increase, from about 0.3% to 1% by day 3 (Fig. 4.
). There was a continual increase in the proportion of Sr distributed to the flag and penultimate leaves over the 3 d after the end of Sr supply. The proportion of Sr distribution in the youngest stem segment, SS-FP, transiently increased on day 1, then significantly decreased on day 3; and in the stem segment of SS-PP continued to decline, in response to the end of Sr supply to the roots. In particular, there was a big decrease of the proportion of Sr distributed in the roots even 1 d after the end of Sr supply from about 21% to 4% and remained at that level on day 3.
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To compare the distribution of B, Rb and Sr in the ear (non-transpiring organ) relative to the flag leaf (actively transpiring organ), content ratios were calculated between the ear and the FL. The ratios of 10B contents between ear and flag leaf increased up to 6–7-fold over the 3 d period in both the control and -B treatments (Table 1
). The Rb content ratios between ear and FL increased up to 8–9-fold by day 3 (Table 1). In contrast, Sr content ratios between the ear and FL only increased by a factor of 2–3 by day 3.
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There was no effect of B treatments on plant growth (Fig. 5
). Ear dry weights increased by 10-fold in both the control and -B treatments during the treatment. As the active stem elongation occurs concurrently with the ear growth, the dry weights of the stem segments SS-FP and SS-PP also significantly increased during the treatment period.
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Effects of canopy cover on the uptake of 10B, Rb and Sr in plant parts
Canopy cover strongly suppressed the transpiration activity in the shoots. By the end of the 3 d period, water use by the plants were 403±14 and 75±23 ml under the control and cover, respectively.
During the 3 d period, plant biomass continued to increase in both the control and cover treatments, but canopy cover decreased biomass of the growing plant parts—ear, FL and upper stem segments, compared to that of the control (Table 2). The new growth—the young ear and stem segments of SS-FP was significantly slowed by the canopy cover. By day 3, the dry weights of the FL and newly emerged tillers were also depressed by the canopy cover. By day 3, there was about 40% reduction in ear dry weight in the cover treatment, compared to the control.
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Cover treatment significantly decreased the concurrent uptake of 10B in the ear and all leaves sampled, but had little effect on 11B contents previously deposited in the plant parts (Table 3
). By day 3, cover treatment decreased 10B content in the FL by more than 50%, compared to the control, but did not affect 10B contents in the stem segments.
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Cover treatment significantly decreased the contents of Rb and Sr in the ear, Similar trends were also observed with Rb and Sr distribution in the plant parts, except that cover treatment decreased Rb (but not Sr) contents in the stem segments by day 3 (Table 4
).
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Discussion |
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Overall, the results demonstrated that B status in the ear enclosed within the sheath of flag and penultimate leaves, was dependent on the concurrent B uptake from the roots (Experiment 1) and the long-distance B transport in the xylem driven by leaf transpiration activity (Experiment 2). Boron withdrawal for 3 d did not change the distribution of the non-metabolic elements Sr and Rb in plant parts, suggesting that the transport efficiency of the developing vascular systems in the young ear was not impaired by the short period of B deficiency.
Notwithstanding the conclusion that B transport into the enclosed ear was predominantly determined by the concurrent B uptake from the roots, there was a continual increase in 10B distribution into the ear even by day 3 after the end of 10B supply in the roots. However, the net amount of B retranslocated into the ear after the end of 10B supply in the roots was far from adequate for the rapidly growing B sink. Comparatively, it has been found that, in broccoli and lupin, B acquired by concurrent uptake during inflorescence development was the main source of B for the reproductive structures (exposed to the atmosphere) as the retranslocation of B acquired before inflorescence emergence only accounted for less than 2% of the total B in the plant parts (Marentes et al., 1997). As a result of limited retranslocation of B, wheat is prone to male sterility in the florets if there was an interruption to B supply to the roots during the early growth phase of the ear (Rawson, 1996b; Huang et al., 2000).
Nevertheless, a continual increase in 10B distribution into the ear was observed even by 3 d after the end of 10B supply to the roots. On the basis of the present results, it is difficult to attribute this increase to any particular source of B retranslocation. Dannel et al. found that B concentrations in root cell sap of sunflower were 56 µM when plants were supplied with 100 µM B in the nutrient solution and only as little as 3 µM with 1 µM B in the nutrient solution (Dannel et al., 2000). Therefore, in the present experiment, the 10B in the apoplastic and symplastic spaces of roots at the end of 10B supply may be partially available for further transport into the shoots as plants had been continuously cultured in adequate B supply. In addition, there was a large root-to-shoot ratio as the tillers were removed and this may enhance the residual availability of B in the roots after the end of 10B supply. This pool of B may have been transported up the stem and partially contributed to the initial increase in 10B distribution into the enclosed ear after the end of 10B supply to the roots. Indeed, on day 1 after the end of 10B supply, there were increases in 10B distribution in the upper stem segments just below the flag leaf node, but not on day 3. This suggests the transient flux of an immediately available pool of B from the roots.
However, the available pool of 10B in the root apoplastic and symplastic pools is reported in previous studies with sunflower, to diminish significantly when plants are transferred from adequate/abundant B levels into deficient levels (Pfeffer et al., 1997). Hence, the fact that the preferential increases in 10B distribution in the ear relative to the flag leaf occurred in both the control and B withdrawal treatments of wheat suggests that there may be some other sources of 10B retranslocated into the ear by day 3, apart from the roots.
Transport pathways for B into the enclosed ear were explored by comparing 10B, Rb and Sr distribution in the ear and other plant parts. The distribution of 10B in the shoot parts and roots resembled that of Rb (the xylem-to-phloem transfer marker) more than Sr (the xylem-transport marker). The distribution of Rb in the ear and the stem segment SS-FP continued to increase significantly by day 3 after the end of Rb supply to the roots, while a significant reduction of Rb distribution occurred in the roots. In contrast, Sr distribution in the ear only increased up to 1% by day 3 after the end of Sr supply, while Sr distribution in the upper stem segments and the roots declined significantly. This proportion of Sr may have been redistributed into the flag and penultimate leaves through xylem-transport as Sr distribution in these leaves significantly increased. By contrast, there were little changes of 10B and Rb distribution in the leaves. By comparing content ratios of 10B, Rb and Sr in the ear relative to the FL, it was also shown that 10B and Rb were preferentially distributed into the ear even after the end of supply in the nutrient solutions, but Sr was preferentially distributed towards the transpiring leaves, the FL and PL.
These results suggest there may be a certain degree (less than Rb, though) of xylem-to-phloem transfer of B in wheat plants while being transported from roots into shoot parts, followed by phloem transport into the non-transpiring new growth such as the enclosed young ear. In wheat, there are well-developed xylem/phloem transfer cells in the vegetative and spikelet nodes of the stem (Zee and O'Brien, 1970; O'Brien and Zee, 1971; Busby and O'Brien, 1979). This physical structure in the nodes provides efficient routes for solute exchange between xylem and phloem (Pate, 1975). Rubidium is efficiently transferred from the xylem to the phloem in the stem nodes and reaches the ear via the phloem. The vascular connection between the flag leaf and the ear, through the node, is not an essential bridge for Rb flux into the ear, but significantly contributes to the redistribution of Rb from the flag leaf into the ear (Feller, 1989; Kuppelwieser and Feller, 1991). The same may apply to the case of B. Nevertheless, further research is needed to understand exact transport pathways for B into the enclosed ear.
In dicot species such as broccoli and lupin, significant levels of B in phloem sap have been reported by Shelp and colleagues (Shelp et al., 1998; Marentes et al., 1997). Retranslocation of B into the inflorescence occurred with some of the B acquired before and during inflorescence emergence, but B status in the reproductive organs was very much dependent on the newly acquired B during inflorescence growth. This is because the amount of B transported in the phloem stream depends on the xylem-to-phloem transfer of newly acquired B by roots, which in turn is determined by the concurrent B uptake by roots and transport in the xylem (Shelp et al., 1998). The level of B in the phloem sap in response to the change of B supply in roots remains unknown.
Although there may be minimal transpiration through the young ear enclosed within the sheath of the flag and penultimate leaves, the transport of B into this organ is still very much dependent on the long-distance transport of B from the concurrent B uptake which is driven by leaf transpiration activity. Even when there was no limitation in B supply in the nutrient solution, B uptake into the leaves was severely restricted, due to the low transpiration activity induced by high humidity effects of the cover treatment. By day 3, plants in the cover treatment transpired about 400 ml less water than those in the control (data not shown). This may be the reason that floret sterility usually occurs in wheat plants grown in the subtropics under the conditions of high temperature and air humidity (as reported by Rawson, 1996a).
The flag leaf seems to play an important role in regulating B flux into the ear during its early growth, as it is usually the most actively photosynthesizing and transpiring organ at that stage. The flag leaf is a strong competing sink for B against the ear. This competition may lead to an inadequate B supply into the ear when B supply in the rooting medium is limited. As a result, water use efficiency in wheat cultivars may be related to the variation in their B efficiency as suggested earlier (Rerkasem and Jamjod, 1997).
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Acknowledgments |
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The present study was funded by the Australian Research Council small grant in 1999. We thank Dr Brenda Rohl and Mr Michael Smirk at the University of Western Australia, for their invaluable help in the analyses of B isotopes by the ICP-MS (PE, Elan 6000).
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Notes |
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3 To whom correspondence should be addressed. huang{at}central.murdoch.edu.au
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References |
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Brown PH, Shelp BJ. 1997. Boron mobility in plants. Plant and Soil 193, 85–101.
Busby CH, O'Brien TP. 1979. Aspects of vascular anatomy and differentiation of vascular tissues and transfer cells in vegetative nodes of wheat. Australian Journal of Biology 27, 703–711.
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Huang L, Pant J, Dell B, Bell R. 2000. Effects of boron deficiency on anther development and floret fertility in wheat (Triticum aestivum L. ‘Wilgoyne’). Annals of Botany 85, 493–500.
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