Seasonal and cell type specific expression of sulfate transporters in the phloem of Populus reveals tree specific characteristics for SO4 2- storage and mobilization

The storage and mobilization of nutrients in wood and bark tissues is a typical feature of trees. Sulfur can be stored as sulfate, which is transported from source to sink tissues through the phloem. In the present study two transcripts encoding sulfate transporters (SULTR) were identified in the phloem of grey poplar (Populus tremula x P. alba). Their cell-specific expression was analyzed throughout poplar in source tissues, such as mature leaves, and in sink tissues, such as the wood and bark of the stem, roots and the shoot apex. PtaSULTR1;1 mRNA was detected in companion cells of the transport phloem, in the phloem of high-order leaf veins and in fine roots. PtaSULTR3;3a mRNA was found exclusively in the transport phloem and here in both, companion cells and sieve elements. Both sulfate transporter transcripts were located in xylem parenchyma cells indicating a role for PtaSULTR1;1 and PtaSULTR3;3a in xylem unloading. Changes in mRNA abundance of these and of the sulfate transporters PtaSULTR4;1 and PtaSULTR4;2 were analyzed over an entire growing season. The expression of PtaSULTR3;3a and of the putative vacuolar efflux transporter PtaSULTR4;2 correlated negatively with the sulfate content in the bark. Furthermore, the expression pattern of both PtaSULTR3;3a and PtaSULTR4;2 correlated significantly with temperature and day length. Thus both SULTRs seem to be involved in mobilization of sulfate during spring: PtaSULTR4;2 mediating efflux from the vacuole and PtaSULTR3;3a mediating loading into the transport phloem. In contrast, the abundance of PtaSULTR1;1 and PtaSULTR4;1 transcripts was not affected by environmental changes throughout the whole season. The transcript abundance of all tested sulfate transporters in leaves was independent of weather conditions. However, PtaSULTR1;1 abundance correlated negatively with sulfate content in leaves, supporting its function in phloem loading. Taken together, these findings indicate a transcriptional regulation of sulfate distribution in poplar trees.