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Keywords:

  • zinc;
  • xylem;
  • Thlaspi caerulescens;
  • apoplastic transport;
  • heavy metal tolerance;
  • hyperaccumulation

White et al. (2002) recently proposed that apoplastic transport of zinc to xylem could significantly contribute to the extreme levels of foliar zinc accumulation found in Thlaspi caerulescens. But do these proposals really stand up? Their main arguments are: the rate of Zn translocation to the shoot increases linearly with the external Zn concentration, rather than showing saturation kinetics; at elevated external Zn concentrations (> 27 µM), the rate of Zn translocation to the shoot exceeds the apparent Vmax of the saturable component of the net Zn influx into the roots; observed foliar Zn concentrations are usually in excess of model predictions based on the apparent Vmax for saturable Zn influx into the roots, except when unrealistically low parameter values for the shoot to root fresh weight ratio and the relative growth rate are used.

First, as admitted by the authors themselves, the apparent unsaturable component of Zn uptake in roots might in part represent low-affinity uptake into the symplast, rather than apoplastic accumulation. For example, overexpressing the T. caerulescens ZNT1 zinc transporter in yeast confers considerable low-affinity Cd uptake with approximately linear kinetics (Pence et al., 2000). Likewise, it is possible that some transporters mediating high affinity transport of cations other than Zn would be capable of mediating low-affinity Zn transport in T. caerulescens. If so, then the unsaturable component of Zn translocation to the shoot might result from low-affinity symplastic, rather than apoplastic transport to the xylem, at least to some degree. This possibility has been acknowledged by the authors, but it is crucial to determine the precise contributions of both pathways to the unsaturable component of Zn uptake. As yet there is no direct evidence at all, and interpretations favoring the apoplastic pathway over the symplastic one are premature.

Second, the apparent discrepancies between observed foliar Zn concentrations in T. caerulescens and the maximum predictions based on the models developed by the authors might in part result from unrealistic assumptions. In particular, the assumption of a constant foliar Zn concentration during plant development is disputable. The Zn concentration in individual leaves increases during ageing (Macnair & Smirnoff, 1999), suggesting that the total rosette Zn concentration should increase throughout at least some part of the growing season. Also, the shoot to root fresh weight ratio might be subject to ontogenetic change at least throughout the juvenile stages of the life cycle (Ernst, 1968). In general, the relative foliar Zn accumulation rate might be conceived to differ, albeit temporarily, from the relative growth rate of the rosette, which could greatly impact on foliar Zn concentrations.

Third, as pointed out by the authors, an apoplastic xylem metal loading pathway should not exhibit cation selectivity. Also, competitive interactions between cations would be expected to be less pronounced, or less skewed at least, than in the case of a common symplastic pathway (White, 2001). These conditions do not seem to be met, however, as shown by several case studies. Assunção et al. (2001) compared foliar Ni and Zn concentrations in a Ni-hyperaccumulating serpentine T. caerulescens ecotype after three weeks of growth at factorial combinations of 1-, 10-, and 100-µM concentrations of Zn and Ni in the nutrient solution. Raising external Zn from 1 to 100 µM caused a 78% decrease of the foliar Ni concentration (from 107 to 24 µmol g−1 d. wt) in plants growing at 100 µM external Ni. Even 10 µΜ Zn was sufficient to cause a 67% decrease in foliar Ni. Conversely, raising Ni from 1 to 100 µΜ in a 100-µΜ Zn background only caused a 15% decrease in foliar Zn (from 107 to 91 µmol g−1 d. wt). Moreover, the sum of foliar Ni and Zn was approximately the same in the reciprocal treatment permutations and barely higher in the 100-µM/100-µM Zn/Ni combination (114 µmol g−1 dw) than in the 100-µM/1-µΜ Ni/Zn and Zn/Ni treatments (110 µmol g−1 d .wt, on average). Obviously, these phenomena are compatible with a common, but Zn-preferent saturable symplastic pathway, rather than with nonselective apoplastic xylem loading. One might argue that the asymmetric competitive interaction of these metals tended to be stronger in the lower concentration range (Assunção et al., 2001), suggesting that xylem loading might become less selective as the external metal concentrations increase. This may be true, but a 78% inhibition of the foliar Ni accumulation by a mere equimolar Zn addition to the nutrient solution suggests that the contribution of apoplastic xylem loading, whenever present, is not even substantial at external metal concentrations as high as 100 µM. A comparable argument can be derived from a similar factorial experiment with Cd and Zn (A. G. L. Assunção, unpublished), using the Cd-hyperaccumulating Ganges ecotype of T. caerulescens (Lombi et al., 2001). Foliar Cd accumulation was not suppressed by Zn at low external Cd concentrations, in conformity with recently published results of Zhao et al. (2002). Moreover, the inhibiting effect of Cd on foliar Zn accumulation was negligible at low external Zn, suggesting a highly selective high-affinity transport of both metals. However, at the highest external concentrations applied (50 µM) the foliar accumulation rates were decreased by 80% (Zn), or 35% (Cd), when the other metal was supplied at equimolar concentration. These results clearly argue in favor of a common, but Cd-preferent low-affinity symplastic transport to the xylem, rather than an apoplastic pathway. In general, interecotypic differences with regard to the metal-specificity patterns of foliar accumulation seem to be largely maintained under under high metal exposure. For example, even when compared at 50-µM external metal concentrations, we still found a strongly disproportional variation, up to fourfold (Cd), threefold (Zn), or eightfold (Ni), in foliar accumulation among T. caerulescens ecotypes (A. G. L. Assunção, unpublished). This would be difficult to reconcile with a substantial nonselective component pathway in xylem loading.

Fourth, to substantially contribute to foliar Zn accumulation in a Zn hyperaccumulator, the rate of apoplastic xylem loading should be orders of magnitude higher than in shoot excluder metallophytes growing at the same site. Such a dramatic increase would be expected to require major changes in the ontogenetic patterns of Casparian strip development and lateral root formation. However, such changes have never been noticed. Moreover, too much loss in cation selectivity might be expected to cause major cation nutrient imbalances.

In conclusion, the precise contribution of apoplastic xylem loading in Zn hyperaccumulation in T. caerulescens remains elusive. As pointed out by White et al. (2002), cation selectivity and competition between cations are the most obvious clues to the problem. However, the circumstantial and experimental evidence available thus far clearly argues against, rather than in favor of, a substantial role for apoplastic xylem metal loading in the heavy metal hyperaccumulation syndrome.

References

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  2. References
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