The Proton Electrochemical Transmembrane Gradients Generated by the Transfer Cells of the Haustorium of Polytrichum formosum and Their Use in the Uptake of Amino Acids

Abstract

The epidermal cells of the sporophyte haustorium of Polytrichum formosum are modified into transfer cells. These cells are located in a strategic place allowing them to control the exchanges between the two generations. Their plasmalemma creates proton gradients (A# and ApH) which increase during the development of the sporophyte. As the sporophyte grows from 2 to 4 cm long, the pH of the incubation medium of the haustoria decreases from 5.2 to 4.3, and the transmembrane potential difference (PD) hyperpolarizes form -140 to -210 millivolts. These gradients become rapidly larger than that generated by the plasmalemma of the basal cells of the sporophyte. They are used to energize the uptake of the solutes present in the apoplast of the gametophyte, particularly the amino acids. Below 20 micromolar a-aminoisobutyric acid uptake in the transfer cells is mediated by a saturable system and is optimal at acidic pH (4.0 and 4.5). It is strongly inhibited by compounds dissipating both A/4 and ApH (10 micromolar carbonylcyanide-m-chlorophenyl hydrazone) or only A# (0.1 molar KCI). The absorption of a-aminoisobutyric acid and of the other neutral amino acids tested induces an alkalinization of the medium and a depolarization of membrane potential difference which is concentration dependent. These data show that the uptake of amino acids by the transfer cells of the haustorium is a secondary translocation (proton-amino acid symport) energized by a primary translocation (proton efflux). More particularly, they show that transfer cells possess a membrane enzymic equipment particularly efficient to achieve the uptake of the solutes leaked in the apoplast from other cell types.For 20 years, transfer cells, which are widely distributed in the plant kingdom, have held the attention of many researchers (12-14, 24, 26 and references therein). These cells, which result from the transformation of different cellular types, are characterized in particular by internal wall ingrowths that increase 5-to 10-fold the surface area of the plasmalemma and by numerous mitochondria. They are often found in contact with conducting cells (sieve-tubes or vessels), at the interface of the two generations (gametophyte-sporophyte), or at the plant-environment interface. Due to their structural particularities and their distribution, it has been suggested that they are involved in apoplast-symplast exchanges (13,26 (6,7,14), and in the latter case, they originate from the leaf apoplast (9). Consequently, the study of their functioning should yield important information on the properties of exchanges between the gametophyte and the sporophyte. Another interest of the transfer cells of the haustorium of bryophytes lies in the absence of symplastic connections with the gametophyte (8, 14): only the apoplastic pathway is operating. Consequently, the properties of exchanges between the two generations are highly dependent on the properties of the plasmalemma of this cell type. The transfer cells which mediate the loading of the sieve tubes in highe...

Immunolocalization of the Plasma Membrane H+ -ATPase in Minor Veins of Vicia faba in Relation to Phloem Loading

“…Transfer cells, which are widespread in the plant kingdom, generally occur at strategic locations: the interface between the plant and the environment, the interface between generations, and, in veins, the interface between vascular and parenchyma cells. From the location of this cell type, its anatomical features (the increase of the plasma membrane surface area and the abundance of mitochondria), and its physiological activity (a strongly negative transmembrane potential difference, at least in epidennal transfer cells [Renault et al, 1989;Bonnemain et al, 1991]), we may infer that this cell type plays an important role in apoplast-symplast exchanges (Pate and Gunning, 1972;Gunning, 1977;Kursanov, 1984;Bonnemain et al, 1991) and in the increased uptake of Suc from the phloem apoplast (Wimmers and Turgeon, 1991). The present work supports this hypothesis based on the differentiation of the plasma membrane of the phloem transfer cell, which is particularly rich in H+-ATPase.…”

Control of Vascular Sap pH by the Vessel-Associated Cells in Woody Species (Physiological and Immunological Studies)

“…The pH of the perfused solution was measured continuously with H + -selective liquid membrane microelectrodes prepared according to a method already described (Amman et al, 1981;Renault et al, 1989). Briefly, the H + -selective microelectrode and the reference micropipette (filled with 3 M KC1 in 1% agar) were connected to an electrometer amplifier (model FD 233; WP Instruments, Inc., New Haven, CT) and to a chart recorder (Kipp and Zonen, Delft, The Netherlands).…”

Physiological Aspects of Sugar Exchange between the Gametophyte and the Sporophyte of Polytrichum formosum

“…the part of the sporophyte that is embedded in the cavity of the upper part (vaginula) of the gametophyte. It was shown recently that the plasmalemma of epidermal transfer cells of P. formosum haustorium creates a proton motive force much larger than that of other cells of the sporophyte (30). This proton motive force is used to energize the absorption of amino acids released into the apoplast of the gametophyte (5,6,27,30).…”

“…It was shown recently that the plasmalemma of epidermal transfer cells of P. formosum haustorium creates a proton motive force much larger than that of other cells of the sporophyte (30). This proton motive force is used to energize the absorption of amino acids released into the apoplast of the gametophyte (5,6,27,30). The sporophyte is also dependent on the gametophyte for its carbon nutrition, despite 1815 …”