Boron transport in plants: co-ordinated regulation of transporters

Abstract

Background: The essentiality of boron (B) for plant growth was established > 85 years ago. In the last decade, it has been revealed that one of the physiological roles of B is cross-linking the pectic polysaccharide rhamnogalacturonan II in primary cell walls. Borate cross-linking of pectic networks serves both for physical strength of cell walls and for cell adhesion. On the other hand, high concentrations of B are toxic to plant growth. To avoid deficiency and toxicity problems, it is important for plants to maintain their tissue B concentrations within an optimum range by regulating transport processes. Boron transport was long believed to be a passive, unregulated process, but the identification of B transporters has suggested that plants sense and respond to the B conditions and regulate transporters to maintain B homeostasis.

Scope: Transporters responsible for efficient B uptake by roots, xylem loading and B distribution among leaves have been described. These transporters are required under B limitation for efficient acquisition and utilization of B. Transporters important for tolerating high B levels in the environment have also been identified, and these transporters export B from roots back to the soil. Two types of transporters are involved in these processes: NIPs (nodulin-26-like intrinsic proteins), boric acid channels, and BORs, B exporters. It is demonstrated that the expression of genes encoding these transporters is finely regulated in response to B availability in the environment to ensure tissue B homeostasis. Furthermore, plants tolerant to stress produced by low B or high B in the environment can be generated through altered expression of these transporters.

Conclusions: The identification of the first B transporter led to the discovery that B transport was a process mediated not only by passive diffusion but also by transporters whose activity was regulated in response to B conditions. Now it is evident that plants sense internal and external B conditions and regulate B transport by modulating the expression and/or accumulation of these transporters. Results obtained in model plants are applicable to other plant species, and such knowledge may be useful in designing plants or crops tolerant to soils containing low or high B.

Fig. 1.

A schematic model of B transport in A. thaliana roots under B limitation. Cell layers of a cross-section of A. thaliana roots where the Casparian strip is developed in the endodermis (State I; White, 2001) are illustrated. It is likely that endodermal cells subsequently become suberized and unable to take up solutes directly from the root apoplast (Moore et al., 2002). Under B limitation, NIP5;1 increases the permeability of boric acid to cell membranes, and facilitates influx of B into root cells from the soil. BOR1 exports B out of the cells toward the xylem against the concentration gradient. It is likely that the co-ordinated expression patterns of BOR1 and NIP5;1 are essential for efficient transcellular transport of B as NIP5;1 possibly facilitates B influx, following the B concentration gradient that BOR1 generates. Under high levels of B supply, expression of both NIP5;1 and BOR1 is decreased by transcriptional and post-transcriptional regulation, respectively. The downregulation of NIP5;1 and BOR1 might be beneficial for avoidance of overloading of high concentrations of B to shoots.