- Email: [email protected]
Influence of increased zinc levels on phloem transport in wheat shoots
! Pi4nt PhysioL WlL 150. pp. 228-231 (1997)
Short Communication
Influence of Increased Zinc Levels on Phloem Transport in Wheat Shoots THOMAS HERREN
and URS
FELLER*
Institute of Plant Physiology; University of Bern, Altenbergrain 21, CH-3013 Bern, Switzerland Received April 12, 1996 . Accepted June 10, 1996
Summary
Elevated zinc levels may cause various symptoms in plants by interfering with ion uptake in the roots, transport processes within the plant or metabolic activities. It has been reported previously that the symplastic transport via the phloem is inhibited under zinc toxicity. In general, an increased zinc supply causes higher zinc contents in the vegetative plant parts of wheat, while the zinc content in the grains is not or only slightly affected. Zinc can be transferred from the xylem to the phloem in the peduncle. In the work reported here, the influence of high zinc levels on phloem transport in maturing wheat was investigated by feeding increasing zinc concentrations via a stem flap below the flag leaf node of field-grown plants. Simultaneously fed strontium and rubidium served as markers for xylem and phloem transport, respectively. At the highest zinc quantities fed (above 1 J.lmol per plant in l'mL), dry matter accumulation in the grains was markedly, and rubidium redistribution to a lesser extent, affected in this system. Our results led to the conclusion that the phloem transport was strongly inhibited above a critical zinc level and that this effect was most likely due to interference with phloem loading or with the mass flow in the sieve tubes and not primarily by affecting phloem unloading or metabolism in the sinks.
Key words: Triticum aestivum L., maturation, phloem, transport, zinc. Introduction
The mobility of zinc within the plant is generally considered to be intermediate (Bukovac and Wittwer 1957; Marschner 1995). The plant species, the age of the plant or the organ of interest may be relevant for the evaluation of zinc mobility (Kochian 1991). Zinc has been reported to be translocated in the phloem in the form of complexes with organic acids (van Goor and Wiersma 1976), and it is not yet clear to which extent zinc is present in the xylem sap as a free cation (Tiffin 1972) or complexed with organic acids (White et al. 1981). Zinc has been found to be easily mobile in the phloem of maturing wheat (Herren and Feller 1994; Herren and Feller 1996; Pearson and Rengel 1995). It has been reported previously that zinc can be transferred from the xylem to the phloem in the peduncle of wheat (Herren and Feller 1994) similar to potassium or rubidium (Haeder and Beringer 1984; Feller 1989). In wheat, a high zinc supply caused no
* Correspondence. © 1997 by Gustav FISCher VerJag. Jena
major increase in the zinc content of the grains in intact plants (Herren and Feller 1996) or detached shoots (Herren and Feller 1994), while the zinc levels in the vegetative parts of these plants were markedly higher than in control plants. High levels of zinc can cause toxicity symptoms in nontolerant plants (Chaney 1991). Effects often observed are chloroses due to an interference of zinc with iron (Rosen et al. 1977; Woolhouse 1983) or manganese utilization (Boardman and McGuire 1990). High concentrations of zinc, nickel or cobalt in the nutrient medium of bean plants inhibited the loading of sucrose into the phloem in cut leaf discs (Rauser and Samarakoon 1980). These results indicate that elevated zinc levels may interfere with phloem loading or transport. Toxic effects of zinc on the phloem transport in wheat are the focus of the work presented here. Increasing zinc quantities were fed via a stem flap below the flag leaf node into intact wheat plants in the field to detect effects on dry matter accumulation in the maturing grains and on rubidium redistribution. The aim of the work presented here was to elucidate inhibitory effects of zinc on phloem transport in intact
Influence of zinc on phloem transport
229
wheat plants and to identify the Zinc levels causing such effects.
weight at later stages of maturation. but this effect was only significant for the final harvest. Visual senescence symptoms in the flag leaf lamina were visible at the highest zinc level already 2 days after the beginning of the feeding period. whereas the lower zinc concentrations did not affect the seMaterial and Methods nescence pattern as compared to untreated plants. The highly mobile rubidium accumulated initially mainly Winter wheat (Triticum IUstivum L.. cv. <
2d
7d
14d
28d
Control (not fed) 0.000 0.333 1.000 3.333
7.5±OA 7.7±1.4"' 7.5±1.2"' 7.9±0.2"' 5.2±0.3"""
14.7±O.8 13.2± 1.314.5±2.2"' 11.7±2.5"' 9.5 ± 2 6"" .
28.8±O.9 26.7±1.I" 26.6±O.8" 22.7±5.3'" 14.6±6's**
42.9± 2.1 42.0± 2.338.5± 4.0'" 37.5± 3.2" 21.4± 11.2""
4.6±O.7
Dry weight per grain [mg]
Discussion At the lowest -.inc levels applied, the maturation of the wheat plants was not affected as compared to the untreated control plants. When the zinc concentration in the feeding
230
THOMAS HERREN and DRS FELLER
o 3
2
2
o
Q.
0.5
0 ~-r~~~-r~~
4
1? o C
C
Q.
Q.
Q.
~ 2
~ 2
•
o
o E
o
o
o 3
E
~ 0 ~-r~--~~-r-; ... en 4 J.J mM Zn
Q.
~ 0 ~~~~~-r~~ .Q
It:
1.0
...
Q.
Q.
1 mM Zn
-oJ
C
o 3
0.0
Q.
-oJ
-oJ
0.5
E
~ 0.0 .........,...--.--.,..-..,....-r-l C
4
N
1.0
3
3
2
o
5 10 1 5 20 25 30
mM Zn
1.0
3
1?
o
mM Zn
0.5
o
5 10 15 20 25 30
o
5 1 0 1 5 20 25 30
Time after feeding [d] FJg.l: Distribution of strontium, rubidium, and zinc in field-grown wheat plants fed with increasing zinc concentrations (0, 1 or 3.3 mmol/L) via a stem Oap below the flag leaf node. The feeding solution (1 mL) with the indicated zinc concentration contained 10 ~mol RbCI and 10~mol SrC12 • Shoots were harvested 0,2,7, 14, and 28 days after the treatment. Means and standard deviations of 4 plants are shown for the contents in the grains (0), in the peduncle (e), and in the Oag leaf lamina (\7).
solution (1 mL) was higher than 1 mmol/L, senescence symptoms were already visible after 2 days in the plant parts above the feeding position. This indicates that in our system 1 ~mol zinc was the critical toxicity level for the plants. Various physiological processes, including transpiration and solute losses from the leaves in the rain, may be affected by the accelerated senescence in plants fed with 3.3 ~mol zinc. Throughout the maturation' period the total strontium content in all shoot parts decreased slightly. These losses, as well as those observed for rubidium, can be explained by the leakage from senescing parts exposed to rain (Tukey 1970; Debrunner and Feller
1995).
Simultaneously fed rubidium was rapidly removed from the transpiration stream at all zinc levels applied, since no elevated rubidium levels were observed in the glumes and the flag leaf lamina 2 days after feeding. Such a removal from the xylem and a subsequent loading into the phloem has been reported previously (Haeder and Beringer 1984; Feller 1989). Zinc was also removed from the transpiration stream. Compared to rubidium, the removal of zinc was less efficient, since increasing amounts of zinc were detected in the organs with a high transpiration rate. The relatively constant zinc contents in the grains at all zinc levels applied are consistent with earlier reports indicating that zinc is removed from the xylem but that the transport to the grains via the phloem is
well regulated in wheat (Herren and Feller 1994; Herren and Feller 1996). From the rubidium transport to the grains (Fig. 1) and from the dry matter accumulation in the grains (Table 1) it is evident that the elevated zinc supply interfered directly or indirectly with phloem transport. Since the zinc contents in the grains were not elevated, it appears likely that the inhibitory effect of zinc on phloem transport was caused at the site of phloem loading (leaf veins or peduncle) or by affecting the mass flow in the phloem, and not primarily by interfering with phySiological processes in the sinks (grains). Acknowledgements We thank the Landwirtschaftliche Schule RUtti in Zollikofen for growing the wheat plants and Dr. Andrew J. Fleming for improving the English of the manuscript. This work was supported by the Swiss Federal Office of Environment, Forests and Landscape.
References BOARDMAN, R. and D. O. MCGUIRE: Forest Eco!. Manag. 37, 167205 (1990). BUKovAc, M. J. and S. H. WlTrWER: Plant Physio!. 22, 428-435 (1957).
Influence of zinc on phloem transport CHANEY, R. L.: In: ROBSON, A. D. (ed.): Zinc in soils and plants, pp. 135-150. Kluwer Academic Publishers, Dordrecht, The Netherlands (1991). DEBRUNNER, N. -and U. FELLER: J. Plant Physiol. 145, 257-260 (1995). FELLER, U.: J. Plant Physiol. 133,764-767 (1989). VAN GOOR, B. ]. and D. WIERSMA: Physiol. Plant. 36. 213-216 (1976). HAEoER, H.-E. and H. BERINGER: Physiol. Plant. 62, 439-444 (1984). HERREN, T. and U. FELLER: J. Plant Nun. 17. 1587-1598 (1994). - - J . Plant Nutr. 19,379-387 (1996). KOCHlAN, L. Y.: In: MORlVEDT, J. J.,F. R. Cox, L. M. SHUMAN, and R. M. WELCH (eds.): Micronutrients in agriculture, 2nd edition, pp. 229-296. Soil Science Society of America Inc., Madison, Wisconsin, USA (1991). MAR.sCHNER, H.: Mineral nutrition of higher plants, second edition. Academic Press, London (1995).
231
PEARSON, J. N ., Z. RENGEL, C. F. JENNER, and R. D. GRAHAM: Physiol. Plant. 95,449-455 (1995). RAUSER, WE. and A. B. SAMARAKOON: Plant Physiol. 65,578-583 (1980). ROSEN, J. A., C. S. PIKE, and M. L. GOLDEN: Plant Physiol. 59, 1085-1087 (1977). SCHENK, D. and U. FELLER:]. Plant Physiol. 137. 175-179 (1990). TIFFIN, L. 0.: In: MORlVEDT, J. ]., P. M . GIORDANO, and W L. LINDSAY (eds.): Micronutrients in agriculture, pp. 199-229. Soil Science Society of America Inc., Madison, WISCOnsin, USA (1972). TUKEY, H . B.:Annu. Rev. Plant Physiol. 21, 305-324 (1970). WHITE, M. c., F. D. BECKER, R. L. CHANEY, and A. M. DECKER: Plant Physiol. 67, 292-300 (1981). WOOLHOUSE, H. W: In: LANGE, O. L. (ed.): Physiological plant ecology III: Responses to the chemical and biological environment, pp. 246-300. Springer Verlag, New York (1983).
Short Communication
Influence of Increased Zinc Levels on Phloem Transport in Wheat Shoots THOMAS HERREN
and URS
FELLER*
Institute of Plant Physiology; University of Bern, Altenbergrain 21, CH-3013 Bern, Switzerland Received April 12, 1996 . Accepted June 10, 1996
Summary
Elevated zinc levels may cause various symptoms in plants by interfering with ion uptake in the roots, transport processes within the plant or metabolic activities. It has been reported previously that the symplastic transport via the phloem is inhibited under zinc toxicity. In general, an increased zinc supply causes higher zinc contents in the vegetative plant parts of wheat, while the zinc content in the grains is not or only slightly affected. Zinc can be transferred from the xylem to the phloem in the peduncle. In the work reported here, the influence of high zinc levels on phloem transport in maturing wheat was investigated by feeding increasing zinc concentrations via a stem flap below the flag leaf node of field-grown plants. Simultaneously fed strontium and rubidium served as markers for xylem and phloem transport, respectively. At the highest zinc quantities fed (above 1 J.lmol per plant in l'mL), dry matter accumulation in the grains was markedly, and rubidium redistribution to a lesser extent, affected in this system. Our results led to the conclusion that the phloem transport was strongly inhibited above a critical zinc level and that this effect was most likely due to interference with phloem loading or with the mass flow in the sieve tubes and not primarily by affecting phloem unloading or metabolism in the sinks.
Key words: Triticum aestivum L., maturation, phloem, transport, zinc. Introduction
The mobility of zinc within the plant is generally considered to be intermediate (Bukovac and Wittwer 1957; Marschner 1995). The plant species, the age of the plant or the organ of interest may be relevant for the evaluation of zinc mobility (Kochian 1991). Zinc has been reported to be translocated in the phloem in the form of complexes with organic acids (van Goor and Wiersma 1976), and it is not yet clear to which extent zinc is present in the xylem sap as a free cation (Tiffin 1972) or complexed with organic acids (White et al. 1981). Zinc has been found to be easily mobile in the phloem of maturing wheat (Herren and Feller 1994; Herren and Feller 1996; Pearson and Rengel 1995). It has been reported previously that zinc can be transferred from the xylem to the phloem in the peduncle of wheat (Herren and Feller 1994) similar to potassium or rubidium (Haeder and Beringer 1984; Feller 1989). In wheat, a high zinc supply caused no
* Correspondence. © 1997 by Gustav FISCher VerJag. Jena
major increase in the zinc content of the grains in intact plants (Herren and Feller 1996) or detached shoots (Herren and Feller 1994), while the zinc levels in the vegetative parts of these plants were markedly higher than in control plants. High levels of zinc can cause toxicity symptoms in nontolerant plants (Chaney 1991). Effects often observed are chloroses due to an interference of zinc with iron (Rosen et al. 1977; Woolhouse 1983) or manganese utilization (Boardman and McGuire 1990). High concentrations of zinc, nickel or cobalt in the nutrient medium of bean plants inhibited the loading of sucrose into the phloem in cut leaf discs (Rauser and Samarakoon 1980). These results indicate that elevated zinc levels may interfere with phloem loading or transport. Toxic effects of zinc on the phloem transport in wheat are the focus of the work presented here. Increasing zinc quantities were fed via a stem flap below the flag leaf node into intact wheat plants in the field to detect effects on dry matter accumulation in the maturing grains and on rubidium redistribution. The aim of the work presented here was to elucidate inhibitory effects of zinc on phloem transport in intact
Influence of zinc on phloem transport
229
wheat plants and to identify the Zinc levels causing such effects.
weight at later stages of maturation. but this effect was only significant for the final harvest. Visual senescence symptoms in the flag leaf lamina were visible at the highest zinc level already 2 days after the beginning of the feeding period. whereas the lower zinc concentrations did not affect the seMaterial and Methods nescence pattern as compared to untreated plants. The highly mobile rubidium accumulated initially mainly Winter wheat (Triticum IUstivum L.. cv. <
2d
7d
14d
28d
Control (not fed) 0.000 0.333 1.000 3.333
7.5±OA 7.7±1.4"' 7.5±1.2"' 7.9±0.2"' 5.2±0.3"""
14.7±O.8 13.2± 1.314.5±2.2"' 11.7±2.5"' 9.5 ± 2 6"" .
28.8±O.9 26.7±1.I" 26.6±O.8" 22.7±5.3'" 14.6±6's**
42.9± 2.1 42.0± 2.338.5± 4.0'" 37.5± 3.2" 21.4± 11.2""
4.6±O.7
Dry weight per grain [mg]
Discussion At the lowest -.inc levels applied, the maturation of the wheat plants was not affected as compared to the untreated control plants. When the zinc concentration in the feeding
230
THOMAS HERREN and DRS FELLER
o 3
2
2
o
Q.
0.5
0 ~-r~~~-r~~
4
1? o C
C
Q.
Q.
Q.
~ 2
~ 2
•
o
o E
o
o
o 3
E
~ 0 ~-r~--~~-r-; ... en 4 J.J mM Zn
Q.
~ 0 ~~~~~-r~~ .Q
It:
1.0
...
Q.
Q.
1 mM Zn
-oJ
C
o 3
0.0
Q.
-oJ
-oJ
0.5
E
~ 0.0 .........,...--.--.,..-..,....-r-l C
4
N
1.0
3
3
2
o
5 10 1 5 20 25 30
mM Zn
1.0
3
1?
o
mM Zn
0.5
o
5 10 15 20 25 30
o
5 1 0 1 5 20 25 30
Time after feeding [d] FJg.l: Distribution of strontium, rubidium, and zinc in field-grown wheat plants fed with increasing zinc concentrations (0, 1 or 3.3 mmol/L) via a stem Oap below the flag leaf node. The feeding solution (1 mL) with the indicated zinc concentration contained 10 ~mol RbCI and 10~mol SrC12 • Shoots were harvested 0,2,7, 14, and 28 days after the treatment. Means and standard deviations of 4 plants are shown for the contents in the grains (0), in the peduncle (e), and in the Oag leaf lamina (\7).
solution (1 mL) was higher than 1 mmol/L, senescence symptoms were already visible after 2 days in the plant parts above the feeding position. This indicates that in our system 1 ~mol zinc was the critical toxicity level for the plants. Various physiological processes, including transpiration and solute losses from the leaves in the rain, may be affected by the accelerated senescence in plants fed with 3.3 ~mol zinc. Throughout the maturation' period the total strontium content in all shoot parts decreased slightly. These losses, as well as those observed for rubidium, can be explained by the leakage from senescing parts exposed to rain (Tukey 1970; Debrunner and Feller
1995).
Simultaneously fed rubidium was rapidly removed from the transpiration stream at all zinc levels applied, since no elevated rubidium levels were observed in the glumes and the flag leaf lamina 2 days after feeding. Such a removal from the xylem and a subsequent loading into the phloem has been reported previously (Haeder and Beringer 1984; Feller 1989). Zinc was also removed from the transpiration stream. Compared to rubidium, the removal of zinc was less efficient, since increasing amounts of zinc were detected in the organs with a high transpiration rate. The relatively constant zinc contents in the grains at all zinc levels applied are consistent with earlier reports indicating that zinc is removed from the xylem but that the transport to the grains via the phloem is
well regulated in wheat (Herren and Feller 1994; Herren and Feller 1996). From the rubidium transport to the grains (Fig. 1) and from the dry matter accumulation in the grains (Table 1) it is evident that the elevated zinc supply interfered directly or indirectly with phloem transport. Since the zinc contents in the grains were not elevated, it appears likely that the inhibitory effect of zinc on phloem transport was caused at the site of phloem loading (leaf veins or peduncle) or by affecting the mass flow in the phloem, and not primarily by interfering with phySiological processes in the sinks (grains). Acknowledgements We thank the Landwirtschaftliche Schule RUtti in Zollikofen for growing the wheat plants and Dr. Andrew J. Fleming for improving the English of the manuscript. This work was supported by the Swiss Federal Office of Environment, Forests and Landscape.
References BOARDMAN, R. and D. O. MCGUIRE: Forest Eco!. Manag. 37, 167205 (1990). BUKovAc, M. J. and S. H. WlTrWER: Plant Physio!. 22, 428-435 (1957).
Influence of zinc on phloem transport CHANEY, R. L.: In: ROBSON, A. D. (ed.): Zinc in soils and plants, pp. 135-150. Kluwer Academic Publishers, Dordrecht, The Netherlands (1991). DEBRUNNER, N. -and U. FELLER: J. Plant Physiol. 145, 257-260 (1995). FELLER, U.: J. Plant Physiol. 133,764-767 (1989). VAN GOOR, B. ]. and D. WIERSMA: Physiol. Plant. 36. 213-216 (1976). HAEoER, H.-E. and H. BERINGER: Physiol. Plant. 62, 439-444 (1984). HERREN, T. and U. FELLER: J. Plant Nun. 17. 1587-1598 (1994). - - J . Plant Nutr. 19,379-387 (1996). KOCHlAN, L. Y.: In: MORlVEDT, J. J.,F. R. Cox, L. M. SHUMAN, and R. M. WELCH (eds.): Micronutrients in agriculture, 2nd edition, pp. 229-296. Soil Science Society of America Inc., Madison, Wisconsin, USA (1991). MAR.sCHNER, H.: Mineral nutrition of higher plants, second edition. Academic Press, London (1995).
231
PEARSON, J. N ., Z. RENGEL, C. F. JENNER, and R. D. GRAHAM: Physiol. Plant. 95,449-455 (1995). RAUSER, WE. and A. B. SAMARAKOON: Plant Physiol. 65,578-583 (1980). ROSEN, J. A., C. S. PIKE, and M. L. GOLDEN: Plant Physiol. 59, 1085-1087 (1977). SCHENK, D. and U. FELLER:]. Plant Physiol. 137. 175-179 (1990). TIFFIN, L. 0.: In: MORlVEDT, J. ]., P. M . GIORDANO, and W L. LINDSAY (eds.): Micronutrients in agriculture, pp. 199-229. Soil Science Society of America Inc., Madison, WISCOnsin, USA (1972). TUKEY, H . B.:Annu. Rev. Plant Physiol. 21, 305-324 (1970). WHITE, M. c., F. D. BECKER, R. L. CHANEY, and A. M. DECKER: Plant Physiol. 67, 292-300 (1981). WOOLHOUSE, H. W: In: LANGE, O. L. (ed.): Physiological plant ecology III: Responses to the chemical and biological environment, pp. 246-300. Springer Verlag, New York (1983).