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Frequencies of Plasmodesmata in Allium Cepa L. Roots: Implications for Solute Transport Pathways

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Frequencies of Plasmodesmata in Allium Cepa L. Roots: Implications for Solute Transport Pathways Journal of Experimental Botany, Vol. 52, No. 358, pp. 1051±1061, May 2001 Frequencies of plasmodesmata in Allium cepa L. roots: implications for solute transport pathways Fengshan Ma1 and Carol A. Peterson2 Department of Biology, University of Waterloo, Waterloo, Ontario N2L 3G1, Canada Received 21 August 2000; Accepted 27 December 2000 Abstract Introduction Plasmodesmatal frequencies PFs) were analysed Intercellular transport between living plant cells is medi- in Allium cepa L. roots with a mature exodermis ated by plasmodesmata PD). These cytoplasmic channels 100 mm from the tip). For all interfaces within the provide a low-resistance pathway that is available for a root, the numbers of plasmodesmata PD) mmÀ2 wall wide range of ions and molecules typical size exclusion surface Fw) were calculated from measurements of limit -1kDa). PD are dynamic structures that can be 60 walls on ultrathin sections. For tissues ranging regulated by a number of internal and external factors from the epidermis up to the stelar parenchyma, the Overall and Blackman, 1996; Ding et al., 1999). When frequencies were also expressed as total PD num- dealing with symplastic transport across a tissue, what À1 bers mm root length Fn), which is most instructive is observed is the collective, rather than the individual, for considering the radial transport of ions and photo- functioning of PD on that particular interface. Therefore, synthates because the tissues were arranged in the frequency of functional PD is the most important concentric cylinders). The Fn values were constantly parameter that will determine the direction, extent and high at the interfaces of exodermis±central cortex, rate of symplastic transport under given conditions. Data central cortex±endodermis and endodermis±pericycle regarding plasmodesmatal frequencies PFs) must be 5 5 5 4.05 3 10 , 5.13 3 10 , and 5.64 3 10 , respectively). If obtained with transmission electron microscopy TEM); the plasmodesmata are functional, a considerable the time required for this approach has largely con- symplastic transport pathway exists between the strained efforts to perform large-scale surveys. Available exodermis and pericycle. Two interfaces had espe- frequency information has been principally produced for 4 cially low PFs: epidermis±exodermis Fn 8.96 3 10 ) leaves from decades of painstaking endeavour to elucid- 4 and pericycle±stelar parenchyma Fn 6.44 3 10 ). This ate photosynthate transport processes Gamalei, 1991; suggests that there is significant membrane transport Van Bel, 1993; Van Bel and Oparka, 1995; Turgeon, across the interface of epidermis±exodermis through 1996). Also, exciting advances have been made, yet again, short cells) and direct transfer of ions from pericycle in leaves, in the structural and functional regulation of to protoxylem vessels. In the phloem, the highest PD during macromolecule transport Ding et al., 1999; PF was detected at the metaphloem sieve element± Lucas, 1999; Oparka and Santa Cruz, 2000). In compar- companion cell interface Fw 0.42), and all other ison, PD in root systems have received limited attention. interfaces had much lower PFs around 0.10). In the In a recent study of the Arabidopsis thaliana L. root apical pericycle, the radial walls had a high PF Fw 0.75), a meristem, a tissue-speci®c pattern of PD distribution feature that could permit lateral circulation of solutes, was observed, and dye-coupling experiments established a thus facilitating ion inward) and photosynthate correlation between this pattern and the potential for outward) delivery. symplastic diffusion of small molecules Zhu et al., 1998). For root tissues proximal to the root tip, only a very Key words: Allium cepa L., phloem unloading, plasmo- few species have been examined and in these, PFs were desmata, plasmodesmatal frequency, root, symplastic measured only for selected interfaces Robards et al., transport, transmission electron microscopy. 1973; Robards and Jackson, 1976; Warmbrodt, 1985a, b, 1 Present address: Department of Plant Biology and Plant Biotechnology Centre, The Ohio State University, Columbus, Ohio 43210, USA. 2 To whom correspondence should be addressed. Fax: q1 519 746 0614. E-mail: [email protected] À1 À2 Abbreviations: Fn, number of plasmodesmata mm root length 5at individual tissue interfaces); Ft, number of plasmodesmata mm tissue interface; À2 Fw, number of plasmodesmata mm wall surface; PD, plasmodesmata; PF, plasmodesmatal frequency; TEM, transmission electron microscopy. ß Society for Experimental Biology 2001 1052 Ma and Peterson 1986a; Kurkova, 1989; Wang et al., 1995). To date, a types.) Most authors have assumed that ions are trans- complete picture of symplastic connections in any root ported from the cortex to the stelar parenchyma from has been lacking. whence they are ®nally transferred into the vessels Special consideration is needed for some plants that Sanderson, 1975; Stelzer et al., 1975; Robards and have an exodermis in their roots. The exodermis is an Clarkson, 1976; Clarkson, 1993). This idea gained outermost cortical layer that develops Casparian bands support from experiments in which stelar parenchyma Peterson and Perumalla, 1990) and suberin lamellae cells proved to be capable of actively accumulating ions Kroemer, 1903; Von Guttenberg, 1968). The Casparian from the cortex in Z. mays LaÈuchli et al., 1971a, b, bands, since they are in the anticlinal walls, do not affect 1974a, b). However, studies on Hordeum vulgare L. roots the roots' symplastic transport in the radial direction. The suggested that the pericycle might play a major role in suberin lamellae, lying all around the cells' protoplasts, xylem loading Vakhmistrov et al., 1972; Kurkova et al., may or may not affect the symplastic connections within 1974; Vakhmistrov, 1981). In the latter species, the the root, according to the type of the exodermis. In the pericycle±stelar parenchyma interface had a much lower uniform exodermis all cells elongate), as seen in Zea PF than the pericycle±endodermis interface, and it was mays L. the only species of this category examined envisaged that the majority of ions would proceed from by TEM), suberin lamellae do not interfere with the the pericycle directly to the xylem vessels, rather than symplastic continuity of the layer Wang et al., 1995). through the stelar parenchyma cells Vakhmistrov et al., However, in the dimorphic exodermis with long and 1972; Kurkova et al., 1974; Vakhmistrov, 1981). In the short cells alternating along the axis of the root), as present study, the relative signi®cance of these two tissues in Citrus sp. Walker et al., 1984) and Allium cepa L. stelar parenchyma and pericycle) at this critical point of Ma and Peterson, 2000), suberin lamella deposition in radial ion transport will be examined in Allium cepa L. long cells severs all their PD. Accordingly, the short cells roots. without suberin lamellae) must play a paramount role in Phloem unloading in roots is another ®eld that is the symplastic ¯uxes of ions and photosynthate-derived poorly understood. In the root tip, symplastic transport nutrients). In an earlier paper, an overall view of PD phloem unloading and post-phloem transport) is intens- relationships but not details of frequencies) of A. cepa ive to sustain cell division and growth Dick and ap Rees, roots was provided Ma and Peterson, 2000). A closer 1975; Oparka et al., 1994; Zhu et al., 1998). More mature examination of PD distribution in the exodermis short zones proximal to the tip) are apparently weaker sinks cells), as well as in all other tissues, will provide further for photosynthates but here all the living cells still need insights into the symplastic connections in mature roots. a continuous supply of photosynthates for their normal There are some other major issues that remain unclari- respiratory activities. Phloem unloading and post-phloem ®ed, one of which concerns xylem loading. Are the xylem transport of photosynthates in mature zones could be vessels loaded by stelar parenchyma cells intervening accomplished by a symplastic pathway in several species between the xylem and phloem strands) or by pericycle or examined Giaquinta et al., 1983; Warmbrodt, 1985a, b, by both? See Fig. 1for locations of these and other cell 1986a, b). However, in A. thaliana, no symplastic phloem unloading was observed under normal conditions of root growth Wright and Oparka, 1997). In the present study, it was noted whether or not the PD associated with the phloem were structurally normal, and what the related PFs may imply for solute transfer. There are several ways of expressing PFs, three of which were used in the present study. 1) The number À2 of PD mm wall surface Fw). This is the basic and most commonly used value as in most of the studies cited above). Fw is most useful for a comparison of cell inter- faces to predict their relative capacity for symplastic transfer and, thus, is applicable to the phloem region of the root where the paths concerned are very short. 2) The number of PD on a tissue interface over a unit root length Fn). This treatment is more instructive than the previous Fig. 1. Diagram of a cross-section of Allium cepa L. root showing cell one for predicting symplastic transport capacity for and tissue interfaces studied for plasmodesmatal frequencies. For the tissues ranging from epidermis to pericycle. This is simply À2 measurement of PD mm wall surface Fw), cell walls are marked with À1 because all the tissues except for the central cortex) are short, thick lines. For PD mm root length Fn), tissue interfaces are drawn in circles of thin lines numbered 1through 5). The boxed area organized into concentric cylinders; the interface areas indicates the location of Fig. 3A. of which are determined by their radii Fig. 1). The Frequencies of plasmodesmata in onion roots 1053 À1 interfaces will be traversed by both ions in the inward PD mm root length 1 Fn ) direction moving from the soil solution to the stele) and The interfaces measured were: 1) epidermis±exodermis, 2) photosynthates in the outward direction moving from exodermis±central cortex, 3) central cortex±endodermis, 4) the stele to the cortex and epidermis).
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