Structure of Hair Roots in Lysinema ciliatum R. Br. and its Implications for their Water Relations
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1 Annals of Botany 77: , 1996 Structure of Hair Roots in Lysinema ciliatum R. Br. and its Implications for their Water Relations W. G. ALLAWAY* and A. E. ASHFORD * School of Biological Sciences, The Uni ersity of Sydney, NSW 2006, and School of Biological Science, The Uni ersity of New South Wales, Sydney, NSW 2052, Australia Received: 1 February 1995 Accepted: 11 May 1995 The fine lateral roots of Lysinema ciliatum R. Br., an epacrid from habitats subject to periodic drought in Western Australia, are hair roots resembling those of Ericaceae. The finest (ultimate) hair roots have a cortex consisting only of an endodermis and an exodermis. Both layers have Casparian strips on the radial walls. The exodermis develops to state III very close to the root tip, showing wall thickening and a suberized lamella encircling each cell. In many roots collected after tip-growth had ceased and the tip had fully differentiated this suberized exodermis completely encircled the apex. In older hair roots the epidermis collapses or is sloughed off leaving the suberized exodermis as the outermost layer. The very fine hair roots have a very small stele containing only one xylem tracheid, and phloem consisting of a single sieve element with companion cell. The very small diameter of the single tracheid indicates a high resistance to water flow along the hair roots. This may tend to conserve soil moisture in the region of the hair roots, leading to improved survival and prolonged function of mycorrhizas in the field Annals of Botany Company Key words: Lysinema ciliatum R. Br., endodermis, exodermis, hair root, water, xylem. INTRODUCTION The roots of Epacridaceae and Ericaceae lack root hairs but carry very fine hair roots that form ericoid mycorrhizal associations (Read, 1983; Reed, 1987). Australian environments where Epacridaceae are characteristically found are dry for long periods of the year. Hair roots are very small, fragile and possibly ephemeral, and it is not clear how they relate either structurally or functionally to the larger roots, how they acquire water or how they survive dry periods. We examined root structure and xylem dimensions of Lysinema ciliatum R. Br., an epacrid from habitats subject to periodic drought in Western Australia, to begin an approach to these questions. MATERIALS AND METHODS Lysinema ciliatum cuttings in perlite: sand: Australian peat (1:1:1) in 7 5 cm plastic pots were kept very wet but freely draining in the glasshouse (method of G. Nielssen, pers. comm.). About 30% survived, producing adventitious roots from the base of the cut stem. Plants were harvested after 9 12 months $ Morphology and measurement of the root system The root system was carefully excavated under continuous observation with a dissecting microscope to ensure that roots were not damaged or lost, by sliding away the pot, rinsing away the potting mixture using a gentle flow of reverse-osmosis purified water, and finally gently teasing away any remaining potting mixture under water. Adventitious roots were severed at their junction with the stem with a razor blade. For morphology and measurement of the root system, each adventitious root and its entire branching system was placed in a Petri dish in dilute phosphate-buffered glutaraldehyde ph 6 8. For each adventitious root ten of the first order of hair roots and ten of the second order of hair roots were randomly selected, rejecting any with broken tip, and width at the base and tip and total length were measured. If there were fewer than ten hair roots in one of the orders, all intact hair-roots in that order were measured. Microscopy Individual hair roots were transferred to reverse-osmosis water on a microscope slide and examined whole, unstained or stained. Selected roots were transferred to fixative and processed for light or electron microscopy. Fixation, embedding and light microscopy were as in Ashford, Allaway and Reed (1996). For electron microscopy long pieces of the first and second order of hair roots were placed in 2 5% glutaraldehyde in M PIPES buffer plus 1% caffeine, ph 7 4 (Allen et al., 1989), at 4 C. The distal 2 3 mm of each was cut under fixative and transferred to fresh fixative; proximal lengths were discarded. After about 7 h, samples were given three buffer rinses, post-fixed in buffered 2% osmium tetroxide at room temperature for 2 h, dehydrated in an ethanol series from % with 10% increments for 15 min each, infiltrated in increasing concentrations of resin (Spurr, 1969) over 6 d, and flat-embedded at 60 C for 24 h. Sections µm thick were mounted on formvar-coated single-slot copper grids, stained with 1996 Annals of Botany Company
2 384 Allaway and Ashford Hair Roots in Lysinema FIG. 1. Roots of Lysinema ciliatum cuttings. A, Part of the root system with some of the potting mixture removed, showing pale ochre-coloured adventitious and branch roots and whitish hair-roots. Tapering adventitious roots emerge from the base of the cutting (top) and produce a few similar branches as well as very many hair roots, themselves also producing laterals. Bar 1 mm. B, Transverse section (TS) of a hair root stained with toluidine blue shows five epidermal cells (ep), one of which is thick-walled; exodermis (ex) with thickened outer tangential and radial walls stained blue with toluidine blue; and endodermis with its cells in radial alignment with those of the exodermis. The stele has only five cell profiles: a very small tracheid, a small sieve element, a companion cell, and two other cells. Bar 10 µm. C, TS of hair root stained with PAS: the wall thickening in epidermis (ep) and exodermis (ex) is well stained, but the Casparian strip in the exodermal (arrows) and endodermal radial walls did not stain. Bar 10 µm. D, Autofluorescence of TS of hair root using blue-violet excitation: in the outer region of the radial walls of the exodermis there is a particularly bright region identical to the endodermal Casparian strip. Bar 10 µm. E, TS of a hair root stained with toluidine
3 lead citrate and uranyl acetate (Daddow, 1983), examined in a Hitachi 7000 transmission electron microscope and photographed on Ilford Technical Pan EM cut film. RESULTS Morphology of the root system in pot-grown cuttings After 9 12 months the successful cuttings, although still quite small, had produced a root system that permeated the potting mixture (Fig. 1A). There were two to nine adventitious roots that gave rise to a hair-root system. The basal region of the adventitious roots (first-order roots) gave rise directly to hair roots, while more distally adventitious roots also produced branches like themselves. Thus a second-order root could either be a branch or a hair root. The branches gave rise to hair roots like those from the adventitious roots. The hair roots produced hair-root laterals which in turn occasionally produced laterals. Thus in proximal regions of the root system there were three (or rarely four) orders of root, while distally there were four (or rarely five) orders. In both cases the last two (or rarely three) orders were hair roots. Adventitious roots tapered obviously ( µm in diameter at the base tapering to µm; six roots of each kind measured, on two cuttings), developed a periderm, and apparently maintained the capacity for further growth at the apex. Hair roots narrowed only slightly towards their tip (Fig. 1A, Table 1). Many of the Lysinema ciliatum hairroots we examined lacked a group of undifferentiated meristematic cells at their tip and therefore presumably did not have the potential for further tip-growth. We often found small lateral hair-root initials, so further growth of these hair roots could occur via the production of laterals. Third-order, penultimate hair-roots were smaller than the roots they emerged from, averaging about 71 µm in diameter at the base tapering to 57 µm. The ultimate, fourth-order hair-roots (Fig. 2A) were smaller: about 55 µm in basal Allaway and Ashford Hair Roots in Lysinema 385 TABLE 1. Dimensions of epacrid roots diameter, tapering to 49 µm. The hair roots were by far the most numerous component of the root system (Fig. 1A). Although there were a few hyphae associated with the roots, no mycorrhiza was found in these glasshouse-grown, uninoculated cuttings. Anatomy of hair roots Intact hair-root tips had a small root cap with mucilage (Ashford et al., 1996), and the epidermis had four to five longitudinal rows of cells, some thick-walled (Fig. 1B). Beneath the epidermis were two cell-layers, the radial alignment of which indicated that they had arisen by periclinal division of the same initials during development (Fig. 1B). The outer of these two layers carried a suberized lamella around the cell walls (Fig. 2B, C), while the inner showed a distinct Casparian strip on the radial walls of each cell (Fig. 2D). These two cell layers are interpreted to constitute the whole of the cortex, being exodermis and endodermis, respectively. The exodermis commonly reached state III of development, whereas in the endodermis only state I was observed (see Peterson, 1989 for definition of states). The outer tangential and radial walls of the exodermis became thickened and showed a blue reaction with toluidine blue (Fig. 1B), characteristic of phenolics (O Brien and McCully, 1981). The middle-lamella region of the exodermal radial walls did not stain with PAS, while the wall thickening was well stained (Fig. 1C). Autofluorescence in this unstained part was especially bright, like that of the endodermal Casparian strip (Fig. 1D), indicating that this was also the position of a Casparian strip. The unstained part was bright between crossed polarizers (Fig. 1E, F), like typical endodermal Casparian strips, while other wall areas apart from the tracheids were dull. With Calcofluor white M2R the exodermal (and endodermal) Casparian strip regions were not stained (cf. Fig. 1G of Ashford et al., 1996). The Casparian strip of the endodermis could readily Mean no. Mean Mean diameter (µm) of roots Order of* length measured hair roots (mm) base tip per plant Reference Lysinema ciliatum first this paper second Lysinema ciliatum Hutton, Dixon and Sivasithamparam, 1994 Dracophyllum secundum R. Br. 47 Allen et al., 1989 Leucopogon par iflorus 46 Steinke, Williams and (Andr.) Lindl. Ashford, 1996 Leucopogon ericoides 54 Read, 1996 (Smith) R. Br. * The first order of hair roots were mostly third-order roots, and the second order of hair roots mostly fourth-order roots. Measured on micrographs published in the reference given. blue viewed between crossed polarizers. The Casparian strips in the radial walls of both exodermis and endodermis are bright; other wall areas apart from the tracheid and part of the epidermal wall-thickening are dull. Bar 10 µm. F, TS of a larger hair root stained with toluidine blue viewed between crossed polarizers: again the Casparian strips in exodermis and endodermis are bright. There are two small and one larger tracheid profiles. Bar 10 µm.
4 ex C ex G F. 2. For legend see facing page. H F D E B Allaway and Ashford Hair Roots in Lysinema 386 A
5 be located in the electron microscope but a Casparian strip could not clearly be demonstrated in the exodermis by electron microscopy although a suberized lamella was clearly shown (Fig. 2C, D). Regardless of the chemical fixation used the roots were always poorly fixed and embedded; despite this it was clear that the exodermis and endodermis often differentiated up to and around the apex (Fig. 2E). In larger hair roots, cell division had occurred in the endodermis and cells of the underlying intermittent pericycle (Fig. 1F); new endodermal walls could be distinguished by their lack of suberization. There was no evidence of division in the exodermis. Older hair roots generally lost their epidermal cells (cf. Ashford et al., 1996) and the suberized and thickened exodermis became their outermost layer (Fig. 2F). Transverse sections of the stele of the smallest roots showed only five cell profiles: a single tracheid, a small sieve element, a companion cell, and two other cells that were presumably phloem parenchyma (Figs 1B, C, D, E and 2B). The tracheids were very small (lumen commonly about 2 4 µm in diameter, Figs 1B, C, D, E and 2A, B) and generally had a long overlap at their pointed ends (Fig. 2G), where the common wall carried a large number of pits. In the larger hair roots there were often three or four tracheids, mostly small like those in the smallest roots, but with one larger tracheid with lumen often about 7 5 µm in diameter (those in Figs 1F, 2H are about 5µm across the lumen). Intact larger hair roots generally had about seven rows of epidermal cells (Fig. 1F). Suberization of the exodermis and endodermis was clearly visible with Sudan black B (Fig. 2H), as were the Casparian strips in both these tissues with crossed polarizers (Fig. 1F). DISCUSSION The hair roots of Lysinema ciliatum and other epacrids [Dracophyllum secundum, Leucopogon ericoides and Leucopogon par iflorus (Table 1); Epacris impressa Labill. (McLennan, 1935); Leucopogon juniperinus R. Br., Lysinema elegans Sonder and Woollsia pungens (Cav.) F. Muell. (our unpubl. res.)] do not differ fundamentally in morphology and anatomy from those of Ericaceae. Epacrid hair-root diameters (Table 1) were within the range of ericaceous hairroots (cf., e.g. between 20 and 151 µm incalluna ulgaris Allaway and Ashford Hair Roots in Lysinema 387 measured on published micrographs of Read and Stribley, 1975; Bonfante-Fasolo and Gianinazzi-Pearson, 1979, 1982; Berta and Bonfante-Fasolo, 1983; Read, 1983; Berta et al., 1988). Epidermis and cortex In both Ericaceae and Epacridaceae the outermost cell layer of intact hair-roots is clearly an epidermis, and the cortical layers arise from initials that are distinct from those of the epidermis and those of the central stele (see Ashford et al., 1996). Just proximal to the apex the single layer of cortical initials gives rise to two cortical cell-layers by periclinal division. In L. ciliatum both cell layers beneath the epidermis become suberized in the manner typical of an endodermis and exodermis, confirming that they are indeed the inner and outer cortical layers, respectively. The endodermis develops only Casparian strips and in larger roots shows further divisions. The outer of these two layers shows the suberin lamella and Casparian strips characteristic of an exodermis (see Peterson, 1989) and a thickened, phenolic-impregnated deposit on the outer tangential and radial walls. The data to hand indicate that the finest roots in the Ericaceae also possess an exodermis (Burgeff, 1961, Calluna ulgaris; Nieuwdorp, 1969, Vaccinium macrocarpon). The presence of an exodermis is unsurprising since it is widespread in angiosperms (Perumalla, Peterson and Enstone, 1990). It is noteworthy that in the finest epacrid and ericaceous roots the exodermis and endodermis are both retained while other cortical layers are absent. Perumalla et al. (1990) suggested that the exodermis would have similar permeability properties to the endodermis, but reported that possession of an exodermis did not obviously relate to water availability. Nevertheless, if the layers function as predicted, uptake from soil through apoplast to symplast would be limited to the epidermis. Radial transfer of substances into the root either directly from the soil, or via the mycorrhizal fungus, would be strongly dependent on symplastic movement from the epidermis through the exodermis via plasmodesmata. When the epidermal cells collapse or are sloughed off, it would appear that this avenue for transfer would be lost and this region of the root would be more isolated from the immediate environment. In the L. ciliatum hair roots we examined in which extension growth had evidently ceased, the exodermis and endodermis FIG. 2. Roots of Lysinema ciliatum cuttings. A,B,G,H, Light micrographs; C F, electron micrographs. A, Longitudinal section of an ultimate, fourth-order hair-root about 40 µm in diameter shows the epidermal layer, the cortex consisting only of exodermis and endodermis, both distinguishable from other tissues by their darkly-stained phenolic contents, and a single file of very narrow tracheids. The root was curved so the section is not median at the extreme tip. Bar 25 µm. B, TS of an ultimate, fourth-order hair-root treated with Sudan Black B. The epidermis and most cells of the stele, which are Sudan Black-negative, show only as ghosts in the micrograph. The exodermis has thick Sudan blackpositive outer tangential and radial walls and a thin Sudan black-positive inner wall. Small Sudan Black-positive regions in radial walls indicate the Casparian strips in the endodermis. The tracheid is Sudan Black-positive. Bar 10 µm. C, Suberized lamellae in radial cell-walls of the exodermis. The thickened tertiary walls are quite electron-lucent and the cell contents are coagulated and electron-opaque, presumably because of their high phenolic content. TS, bar 0 5 µm. D, Casparian strip in radial walls of the endodermis is more electron-opaque than the rest of the wall and shows thin electron-opaque borders where the plasmalemmas are tightly appressed to it. The suberized region of the adjacent exodermal cell is visible at the extreme right of the picture. TS, bar 0 5 µm. E, The exodermis (ex), distinguishable by its suberized lamellae (thin electron lucent region in the walls) and dense coagulated contents, is differentiated up to and around the apex in this slightly non-median longitudinal section. Bar 10 µm. F, In an older hair-root from which the epidermal cells have been lost, the thick-walled exodermis is the outermost layer. There are three tracheid profiles. TS, bar 25 µm. G, The pointed ends of overlapping tracheids are visible in this living hair root under Nomarski optics. Bar 10 µm. H, A larger hair root treated with Sudan Black B, showing suberization of the exodermis and endodermis, two small tracheids like those in the smallest roots and one larger tracheid. TS, bar 10 µm.
6 388 Allaway and Ashford Hair Roots in Lysinema were often fully differentiated up to and around the root apex, indicating that this potential permeability barrier extends around the entire hair-root. This modification could reduce desiccation and enhance survival of these fine roots. Western Australia, and the Biomedical Electron Microscope Unit, the University of New South Wales, for facilities; and the Australian Research Council, the Society for Growing Australian Plants North Shore Group and the Australian Flora Foundation for research grants. Structure of the root xylem and its significance for water transport For a given pressure difference volume flow in tubes depends on the fourth power of the radius. Hair-root tracheids are very small: the lumen of the largest tracheid in the larger hair roots is about 3 8 µm radius while the smaller tracheids are only about 1 2 µm radius. In a typical larger hair root, therefore, about 100 times as much water will flow along the large as in each of the three smaller tracheids. In the smallest hair roots with only a single tracheid there will be a very high resistance to longitudinal water-flow. This can be understood in a resistance model of the root system. The main (adventitious and branch) roots have low resistance. Most of the roots are hair roots, the larger of which are up to 17 mm long and have fairly high resistance, and the smaller 6 mm long with very high resistance. Since so much of the root system consists of hair roots there are very many of these resistances, mostly connected in parallel. Parallel resistances sum up by a reciprocal rule, so although each individual resistance is high, there are so many in parallel that overall the total resistance is low. As a result, the hair root system should exploit the soil uniformly, drawing water from a large soil volume, but not excessively depleting any part of that volume. In nature the hair roots would be mycorrhizal, and the special root water-relations described above would have the advantage of maintaining favourable water status for the longest possible period of time, allowing the mycorrhizas to remain active over the whole root system. This presupposes that there will be longitudinal flow in these tiny tracheids. For water to be drawn along, there has to be a substantial pressure differential. From values given by Canny (1991) for pressure difference required to draw water along xylem tubes of various dimensions we estimate that to get essentially any flow along the finest roots would require a water potential difference of 3 bars per 6 mm, while larger hair roots with a larger tracheid would require only 0 1 bar approximately. To function at all the finest hair-roots must be short (as indeed they are). Since there is likely to be a high longitudinal resistance there may be a greater tendency to draw water radially inwards across the hair-root in basal regions, rather than longitudinally through the tracheid from the apex. Perhaps a benefit of the suberized exodermis endodermis complex is to increase the resistance of this radial pathway and thus protect soil and mycorrhiza in basal regions from drying out. ACKNOWLEDGEMENTS We thank Suzanne Bullock for root measurements and electron microscopy; Kings Park and Botanic Garden, Perth, for the cuttings; the Botany Department and the Centre for Microscopy and Microanalysis, the University of LITERATURE CITED Allen WK, Allaway WG, Cox GC, Valder PG Ultrastructure of mycorrhizas of Dracophyllum secundum R. Br. (Ericales: Epacridaceae). Australian Journal of Plant Physiology 16: Ashford AE, Allaway WG, Reed ML A possible role for the thick-walled epidermal cells in the mycorrhizal hair roots of Lysinema ciliatum R. Br. and other Epacridaceae. Annals of Botany 77: Berta G, Bonfante-Fasolo P Apical meristems in mycorrhizal and uninfected roots of Calluna ulgaris (L.) Hull. Plant and Soil 71: Berta G, Gianinazzi-Pearson V, Gay G, Torri G Morphogenetic effects of endomycorrhiza formation on the root system of Calluna ulgaris (L.) Hull. Symbiosis 5: Bonfante-Fasolo P, Gianinazzi-Pearson V Ultrastructural aspects of endomycorrhiza in the Ericaceae. I. Naturally infected hair roots of Calluna ulgaris (L.) Hull. New Phytologist 83: Bonfante-Fasolo P, Gianinazzi-Pearson V Ultrastructural aspects of endomycorrhiza in the Ericaceae. III. Morphology of the dissociated symbionts and modifications occurring during their reassociation in axenic culture. New Phytologist 91: Burgeff H Mikrobiologie des Hochmoores mit besonderer Beru cksichtigung der Erikazeen-Pilz-Symbiose. Stuttgart: Gustav Fischer Verlag. Canny MJ The xylem wedge as a functional unit speculations on the consequences of flow in leaky tubes. New Phytologist 118: Daddow LYM A double lead stain method for enhancing contrast of ultrathin sections in electron microscopy: a modified multiple staining technique. Journal of Microscopy 129: Hutton BJ, Dixon KW, Sivasithamparam K Ericoid endophytes of Western Australian heaths (Epacridaceae). New Phytologist 127: McLennan EI Non-symbiotic development of seedlings of Epacris impressa Labill. New Phytologist 34: Nieuwdorp PJ Some investigations on the mycorrhiza of Calluna, Erica and Vaccinium. Acta Botanica Neerlandica 18: O Brien TP, McCully ME The study of plant structure: principles and selected methods. Melbourne: Termarcarphi Pty Ltd. Perumalla CJ, Peterson CA, Enstone DE A survey of angiosperm species to detect hypodermal Casparian bands. I. Roots with a uniseriate hypodermis and epidermis. Botanical Journal of the Linnean Society 103: Peterson CA Significance of the exodermis in root function. In: Loughman BC, ed. Structural and functional aspects of transport in roots. Dordrecht: Kluwer, Read D The biology of mycorrhizas in the Ericales. Canadian Journal of Botany 61: Read DJ The structure and function of the ericoid mycorrhizal root. Annals of Botany 77: Read DJ, Stribley DP Some mycological aspects of the biology of mycorrhiza in the Ericaceae. In: Saunders FE, Mosse B, Tinker PB, eds. Endomycorrhizas. London: Academic Press, Reed ML Ericoid mycorrhiza of Epacridaceae in Australia. In: Sylvia DM, Hung LL, Graham JH, eds. Mycorrhizae in the next decade. Practical applications and research priorities. Gainesville: Institute of Food and Agricultural Sciences, University of Florida, 335. Spurr AR A low-viscosity epoxy resin embedding medium for electron microscopy. Journal of Ultrastructural Research 26: Steinke E, Williams PG, Ashford AE The structure and fungal associates of mycorrhizas in Leucopogon par iflorus (Andr.) Lindl. Annals of Botany 77:
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