* ' ION UPTAKE IN RELATION TO THE '''-'"u.n v DEVELOPMENT OF A ROOT HYPODERMIS
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1 New Phytol. (igj6) JJ, '-^ ^^ ' '''-: ^i'i^ J i.. * ' ION UPTAKE IN RELATION TO THE '''-'"u.n v DEVELOPMENT OF A ROOT HYPODERMIS :?m::,^^ BY I. B. FERGUSON* AND D. T. CLARKSON '" ' 'I ARC Letcombe Laboratory, Wantage 0X12 gjt, U.K. ' A^^fi'"*^'-1975) *- SUMMARY The suberization of the outer cortical cells in the basal zones of maize roots to form a hypodermis reduced the radial movement of phosphate towards the stele. Suberization of these cells appeared to place a far greater restriction on the translocation of phosphate to the shoot than the suherization of the endodermis. Under the same conditions as were used for growing maize, barley roots did not develop a hypodermis, and phosphate movement from the basal zones of the root axes was not restricted. ; ' "' ;' - INTRODUCTION ", ' ' -"'\ ' ' Suberization of the root endodermis has been shown to have little or no effect on the movement of phosphate across maize or barley roots (Clarkson and Sanderson, 1971; Ferguson and Clarkson, 1975). This finding is compatible with the view that there is a pathway for ion movement through the symplast, the continuity of which is maintained by the plasmodesmata, and which passes through the walls of the endodermis. However, in an earlier paper (Ferguson and Clarkson, 1975), we found that there was very little transport of phosphate to the shoots from the extreme basal region of maize roots. We suggested that this decline in transpoi-t might be due to the suberization of the outer cortical cells to form a hypodermis or exodermis. This view is supported by evidence, in the present paper, on the distribution of ^^P in root tissues obtain by microautoradiography. **"''' ' METHODS ' ' Maize seedlings (Zea mays cv. Giant White Horsetooth) were grown for 10 days in a culture solution of the following composition: (mm): Ca(NO3)2^ 1.5, KNO3 5, KH2PO4 I, MgS04 1-5, NaNO3 2; together with minor nutrients including iron (Fe EDTA) at o. i mm. The seedlings were subjected to 16 h illumination each day from fiuorescent lamps which gave an intensity of 2 x 10* lux, at a temperature of 2o C and at 70% R.H. Roots of intact seedlings were sealed into slits cut across the diameter of a polyethylene tube as described by Ferguson and Clarkson (1975), allowing a root segment 3.5 mm long to be exposed to a nutrient solution containing o.oi mm phosphate labelled with -^^P (5 A'Ci ml"'). The remaining part of the root system was in a similar but non-radioactive solution. The regions investigated were 12 cm from the apex (on the apical side -' * Present address: Plant Diseases Division, D.S.I.R., Private Bag, Auckland, New Zealand. ": II
2 12 I. B. FERGUSON AND D. T. CLARKSON of the emerging lateral roots), 20 cm from the apex (in the lateral root zone), and the root base (approximately 30 cm from the apex). After 4 h, the segments were washed, removed from the apparatus, dipped into a 15% methyl cellulose solution (at approximately 2 C), and immediately frozen in liquid nitrogen. The subsequent procedures for mounting the material, cutting sections (10 ^m at 2o C), preparation of Kodak AR 10 stripping film, and mounting the sections on the emulsion, have all been fully described by Sanderson (1972). After 8 days' exposure at 25 C, the film was developed for 5 min at i8 C in D-19 developer, followed by fixing for 5 min in 'Amphix'. To prepare permanent mounts, the sections, after development, were passed through an alcohol series and mounted in 'Euparal' (Gurr). The procedure allowed the autoradiograph to be viewed with the emulsion above the section as described by Sanderson (1972). The distribution of ^^P in the sections was determined by measuring the density of silver grains in successive 100 ^m'^ fields lying across the diameter of the section using a Leitz microscope photometer.,^i,;,,..,, ^,.,._ 50 (a) 1 ' -Iti i-. ri' -. ^1 30 I - ( "h 0 S 50 e g 30.., 10 ' -a o V 1 50 I fi A ' ' (b) (c) n nil n 1 vl B- n ** y *- - J.,.oJ..._ o.3?.s: -o <i> -o "C -o ' -i'jt».^ ccujo S.^ujQ- S ^ -Olii?'; Fig. I. Radial distribution of ^^P in different regions of seminal axes of maize roots, (a) Base, endodermis and hypodermis suberized; (b) 20-em region, endodermis completely suberized; (c) 12-cm region, endodermis incompletely suberized. The segment located 12 cm from the apex was from the unbranched part of the axis while the segment located at 20 cm was from the lateral root zone (but did not include any lateral roots). The basal zone was approximately 30 em from the apex. Eaeh profile is constructed from the mean value from a minimum of ' i ten transects from several sections. uijimst'. i,'i 'niif.r '1 1 > 1."';: n ii'^-: -jii.'.urj RESULTS AND DISCUSSION.?.'.j j The radial distribution of ^^P in transverse sections cut from segments taken from different parts of the seminal root axis is shown in Fig. i. Whilst considerable amounts of ^^P were found in the stele in the 12-cm and 20-cm regions (the latter being the lateral root zone), very little reached the stele in the basal region (see also Plate 2, Nos. 3 and 4). There was a marked accumulation of ^^P at the root surface in the basal zone; the exact location of this accumulation cannot be defined, but the density of silver grains was greatest over the single epidermal layer (Plate i, Nos. i and 2). Much of the phosphate at the root surface may have been associated with external microflora, particularly in the
3 Ion uptake and hypodermis development 13 basal zone, where discrete zones of high intensity labelling can be seen (Plate i. No. 2). These results allow us to consider the relative significance of suberization of the endodermis and of the outer cortical cells. The development of the endodermis under the conditions in which our maize plants were grown in the present work has been described by Ferguson and Clarkson (1975), and a more detailed account of endodermal development in Zea mays has been published recently by Haas and Carothers (1975). In the 12- cm region, where lateral roots are being initiated, and in some cases are emerging from the pericycle, suberin lamellae have been laid down in some, but not all, endodermal cells. This process, however, is complete in the lateral root region (20 cm) and at the root base. Uptake experiments have shown that this extensive suberization of the endodermis in maize does not affect radial phosphate movement (Ferguson and Clarkson, 1975), and similar conclusions have been reached with barley (Clarkson and Sanderson, 1971). The distribution of ^^P on either side of the endodermis in microautoradiographs shown in Fig. I is consistent with these earlier results. The cells of the outer cortex form suberin lamellae in their walls at a much greater distance from the root tip than those of the endodermis. However, in regions apical to the emerging lateral roots (10-12 cm from the apex), we have observed a positive reaction to the stain Sudan IV in the walls of the outer cortical cells. Electron microscopic examination has revealed that this material is not organized into the characteristic suberin lamellae; these can be observed only at the extreme base of the root axis. As noted by Ferguson and Clarkson (1975), the lamellae are not deposited in the single layer of epidermal cells, but are visible in the walls of the underlying cortical cells. The hypodermis appears to be continuous in that there are no gap cells; such cells have Ijeen found in some species (Van Fleet, 1950). There are similarities between the endodermis and hypodermis in their responses to histochemical tests for fats and suberin, and in their common possession of suberin lamellae and Casparian bands. It is interesting to note that according to Williams (1947), the epidermis, hypodermis and endodermis all have a common meristematic origin. But the deposition of suberin lamellae is complete in the endodermis of both lateral root and basal regions, whereas it is only at the base of the root axis that lamellae are present in the outer cortical cells. The correlation between the appearance of the lamellae and the restriction of the radial movement of phosphate in the basal zone may well be due to a reduction of the effective absorbing surface of the root caused by the presence of a layer of low ionic permeability between the plasmalemmata of the cortical cells and the free space of the walls. This would restrict entry into the symplast. In contrast, barley roots do not form a suberized hypodermis under our growing conditions. We attempted to induce suberization by exposing the basal 2 cm of growing barley roots to the air for several days. However, no extra wall thickening was detectable and there was no difference in the amount of phosphate transported across the root between these roots and controls. Uptake studies (Clarkson and Sanderson, 1971) and micro-autoradiography (Figure 4 in Clarkson, Robards and Sanderson, i97i)have shown that while cortical cells remain alive, there is no restriction on radial phosphate movement in the basal zones of barley roots. v ACKNOWLEDGMENTS We wish tothank Mr J. Sanderson for his helpful advice on micro-autoradiography and Mr S. Young for assistance with the microscopy.
4 14 I- B. FERGUSON AND D. T. CLARKSON REFERENCES CLARKSON, D. T., ROBARDS, A. W. & SANDERSON, J. (1971). The tertiary endodermis in barley roots: Fine structure in relation to radial transport of ions and water. Planta {Berl.), 96, 292. CLARKSON, D. T. & SANDERSON, J. (1971). Relationship between the anatomy of cereal roots and the absorption of nutrients and water. Agricultural Research Council Letcombe Laboratory Annual Report, 1970, 16. FERGUSON, I. B. & CLARKSON, D. T. ("1975). Ion transport and endodermal suberization in the roots of Zea mays. New Phytol., 75, 69. HAAS, D. L. & CAROTHERS, Z. B. (1975). Some ultrastruetural observations on endodermal cell development in Zea mays roots. Amer. J. Bot., 62, 336. SANDERSON, J. (1972). Micro-autoradiography of diffusible ions in plant tissues: problems and methods. y. Microsc, 96, 245. VAN FLEE-F, D. S. (1950). A comparison of histochemical and anatomical characteristics of the hypodermis with the endodermis in vascular plants. Amer. J. Bot., yj, 721. WILLIAMS, B. C. (1947). The structure of the meristematie root tip and origin of the primary tissues in the roots of vascular plants. Amer.J. Bot., 34, 455. '']' ' ' ' " '' ""' ' EXPLANATION OF PLATES ' ' ' ' ' ^ ^" Micro-autoradiographs of ^^P in tissues of the root of Zea mays sectioned at different ""'' distances from the root apex. Both root zones were treated with nutrient solutions of similar ' >{ specific activity of ^^P and sections were exposed to the photographic emulsion for the same j length of time (8 days) direct comparison of grain density is, therefore, permissible. 1A PLATE I -.1 ii^. --i.sili, :-ii'!-: ;;>: nir: No. I. Root periphery 20 cm from the root apex; at this point cortical cells do not have i suberin lamellae in their walls and are rather uniformly labelled. No. 2. Root periphery at extreme base of root where a suberized hypodermis is present. '' Note heavy accumulation of ^^P associated with the epidermis or its surface, many of the silver grains over the cortical cells may be derived by crossfire from the superficial spot., /^ PLATE 2 ''^ ' " No. 3. Detailed view of endodermal/stellar junction 20 cm from the root tip. Note the thick ' inner tangential wall (itw) of the endodermis and the similar grain densities in the cells on either side of it. 1 No. 4. Detailed view of endodermal/stellar junction at the base of the root. Note the greatly reduced density of grains in comparison with the 20 em zone (No. 3). 3 4
5 THE NEW PHYTOLOGIST, 77, i PLATE I U-. >C '. ' '. > * '20/im. C? O' s,....v '- /^_ /- '\'',-l 20/im I. B. FERGUSON AND D. T. CLARKSON /OiV UPTAKE AND HYPODERMIS DEVELOPMENT (facing p. 14)
6 THE NEW PHYTOLOGIST, 77, i PLATE 2 : < ( - ; ; : Itw 1- I. B. FERGUSON AND D. T. CLARKSON JOiV UPTAKE AND HYPODERMIS DEVELOPMENT
7
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