Lateral Transport of Organic and Inorganic Solutes

Abstract

Organic (e.g., sugars and amino acids) and inorganic (e.g., K⁺, Na⁺, PO₄^2-, and SO₄^2-) solutes are transported long-distance throughout plants. Lateral movement of these compounds between the xylem and the phloem, and vice versa, has also been reported in several plant species since the 1930s, and is believed to be important in the overall resource allocation. Studies of Arabidopsis thaliana have provided us with a better knowledge of the anatomical framework in which the lateral transport takes place, and have highlighted the role of specialized vascular and perivascular cells as an interface for solute exchanges. Important breakthroughs have also been made, mainly in Arabidopsis, in identifying some of the proteins involved in the cell-to-cell translocation of solutes, most notably a range of plasma membrane transporters that act in different cell types. Finally, in the future, state-of-art imaging techniques should help to better characterize the lateral transport of these compounds on a cellular level. This review brings the lateral transport of sugars and inorganic solutes back into focus and highlights its importance in terms of our overall understanding of plant resource allocation.

Keywords: inorganic solutes; lateral transport; organic solutes; phloem; xylem.

Figure 1

Organic and inorganic solutes take several paths to enter and exit the plant vascular system. This scheme is based on the Arabidopsis thaliana anatomy. (A,C,E) Schematic representation of a source organ (source leaf) (A), a transport organ (floral stem) (C), and a sink organ (root) (E). (B,D,F) Schematic representation of the possible transport pathways taken by the organic and inorganic solutes between the different cell types in each organ ((B): leaf; (D): floral stem; and (F): root). 1. Loading of carbohydrates, organic acids, and amino acids in the sieve tubes. 2. Water flow between xylem and phloem. 3. Lateral transfer of amino acids from xylem to phloem. 4. N metabolism and N remobilization. 5. Leakage and retrieval of carbohydrates, amino acids, and ions between the phloem and the surroundings tissues. 6. Unloading of carbohydrates, organic acids, amino acids, and ions for the supply of metabolic precursors for cell division and expansion. 7. Uptake, efflux, and influx of inorganic solutes (e.g., NO₃⁻, PO₄³⁻, K⁺, SO₄²⁻) and nitrogen to the xylem. 8. Absorption and flow of water to the xylem. 9. Unloading of carbohydrates, organic acids, and amino acids that will later be used as precursors for cell division and expansion. The light blue, pale yellow, pink, and green arrows represent the water, inorganic solutes, nitrogen, and sugar movement, respectively. The circles represent the transporter-mediated movement of organic and inorganic solutes. BS: bundle sheath; CC: companion cell; En: endodermis; PD: plasmodesmata; Ph: phloem; pP: phloem parenchyma cell; PPP: phloem–pole pericycle; Px: protoxylem; MC: mesophyll cell; Mx: metaxylem; SE: sieve element; xV: xylem vessel; xP: xylem parenchyma cell; XPP: xylem-pole pericycle.

Figure 2

Model for sugar and ion transport in the Arabidopsis floral stem. The upper panel shows a vascular bundle transversal section stained with alcian blue/safranin O. The primary cell walls appear in different shades of orange and the secondary cell walls appear in red. The lower panel is a sketch showing a longitudinal view of the different cell types present in a vascular bundle. The white bridges between two cells represent the plasmodesmata. The model was based on current knowledge of the spatial distribution of sugar and ion transporters in the Arabidopsis floral stem. Known locations of members of the sugar and ion transporters in other Arabidopsis organ or in woody stem have been added as putative locations in Arabidopsis floral stem (question marks). pPC: phloem parenchyma cell; CC: companion cell; SE: sieve element; SUC: SUCROSE TRANSPORTER; SWEET: SUGAR WILL EVENTUALLY BE EXPORTED TRANSPORTERS; xV: xylem vessel; xF: xylary fiber; xPC: xylem parenchyma cell.